Peptide signaling pathways in vascular differentiation › content › plantphysiol › early ›...

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Short title: Peptide signaling during vascular differentiation 1

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Peptide signaling pathways in vascular differentiation 3

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Hiroo Fukuda1 & Christian S. Hardtke

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1Department of Biological Sciences, Graduate School of Science, The University of 8

Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan 9

2Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 10

CH-1015 Lausanne, Switzerland 11

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One-sentence summary: 13

CLE peptide and related signaling pathways have been assigned prominent roles in the 14

development of both vascular tissues, xylem and phloem. 15

Author contributions: 16

H.F. and C.S.H. wrote the manuscript together. 17

Plant Physiology Preview. Published on December 3, 2019, as DOI:10.1104/pp.19.01259

Copyright 2019 by the American Society of Plant Biologists

www.plantphysiol.orgon July 27, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.

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The modern plant vascular system is a central feature of extant angiosperms and 18

consists of xylem, phloem, and the intervening procambium (Lucas et al. 2013). During 19

vegetative growth, the apical meristem serves as a continuous source of procambial 20

initial cells, which produce the primary xylem, the primary phloem, and the 21

procambium. In secondary growth, vascular cambium, which is derived from the 22

procambium, acts as a stem cell reservoir and continues to give rise to secondary xylem 23

and phloem cells. The formation of the vascular tissue is a well-organized plant 24

developmental process, whose central step is the regulation of vascular stem cell fates. 25

It is governed by cell-to-cell communication, and symplastic movement of signaling 26

molecules contributes to vascular development. Various secreted peptides as well as 27

plant hormones play crucial roles in cell-to-cell communication for regulating vascular 28

development (Fukuda and Ohashi-Ito, 2019). Among the peptides, several members of 29

the CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION (ESR) (CLE) family 30

act at different points of key processes in vascular development (Fukuda and 31

Ohashi-Ito, 2019; Hazak and Hardtke, 2016). The CLE family genes are conserved 32

among land plants. In the Arabidopsis (Arabidopsis thaliana) genome, there are 32 33

genes encoding 27 distinct CLE peptides (Yamaguchi et al. 2016). CLE precursor 34

proteins contain an N-terminal signal peptide and at least one conserved C-terminal 35

12-14 amino-acid CLE domain, from which a mature CLE peptide is produced through 36

proteolytic cleavage. The activity of some processed peptides is increased by 37

modifications such as hydroxylation on proline residues, and in some cases by 38

glycosylation with three arabinose residues (Ito et al. 2006; Ohyama et al. 2009; 39

Matsubayashi, 2011; Shinohara and Matsubayahi, 2013). During vascular development, 40

CLE41/CLE44, CLE45, and CLE9/CLE10 peptides function in distinct processes. In 41

addition, other peptides such as phytosulfokine and EPIDERMAL PATTERNING 42

FACTOR-LIKE (EPFL) peptides are thought to contribute to the regulation of vascular 43

development (Holzwart et al. 2018; Ikematsu et al. 2017). Crosstalk among peptides and 44

between peptides and plant hormones is an important current topic in vascular 45

development. In this update, we focus on recent advances in our understanding of the 46

regulation of vascular fate with an emphasis on peptide signaling. 47

The TDIF-TDR/PXY signaling pathway in xylem differentiation 48

TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF) is a 49



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CLE-family peptide composed of twelve amino acids including two hydroxylated 50

proline residues (Ito et al. 2006). TDIF was first isolated from zinnia (Zinnia elegans) 51

xylogenic culture medium as a factor inhibiting tracheary element differentiation (Ito et 52

al. 2006). The TDIF sequence is conserved in the genome of Euphyllophytes (Hirakawa 53

and Bowman, 2015) and encoded by the CLE41 and CLE44 genes in the Arabidopsis 54

genome (Hirakawa et al. 2008). The activity of TDIF in vascular development is also 55

conserved among extant Euphyllophytes (Hirakawa and Bowman, 2015). TDIF 56

RECEPTOR/PHLOEM INTERCALATED WITH XYLEM (TDR/PXY) was 57

demonstrated to be a TDIF receptor (Hirakawa et al. 2008). TDR/PXY belongs to Class 58

XI LEUCINE-RICH REPEAT RECEPTOR-LIKE KINASES (LRR-RLK), which 59

consist of an extracellular LRR domain, a single transmembrane domain for anchorage 60

in the plasma membrane, and a cytoplasmic kinase domain (Fisher and Turner, 2007; 61

Hirakawa et al. 2008). The extracellular domain of TDR forms a twisted right-handed 62

superhelical structure, comprising 22 LRRs and the N-terminus, and specifically 63

recognizes TDIF by its inner concave surface (Morita et al., 2016, Zhang et al., 2016a). 64

The crystal structure of TDR ectodomains contains N-linked glycans (Zhang et al., 65

2016b). The PXY (TDR) family (PXYf) is comprised of TDR (PXY), PXY-LIKE1 66

(PXL1), and PXY-LIKE2 (PXL2) (Fig. 1A). PXL1 and PXL2 also participate in vascular 67

development together with TDR, since TDIF binds the ligand binding pocket of both 68

PXL1 and PXL2 (Zhang et al., 2016b), and pxl1 and pxl2 mutations enhance the 69

vascular organization defects in tdr mutants (Etchells et al., 2013; Fisher and Turner, 70

2007). SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) family proteins 71

(SERK1 and others) act as co-receptors of TDR (Fig. 1A; Zhang et al., 2016b). In the 72

TDIF-TDR-SERK2 complex, TDIF mediates interactions between the LRRs of TDR 73

and SERK2. Similarly, the CLE42 peptide, the closest homolog of TDIF that also 74

displays TDIF activity (Ito et al., 2006), promotes an interaction between PXL2 and 75

SERK2 (Mou et al., 2017). Because SERK2 does not change the basic structure of the 76

TDIF-TDR complex, TDIF functions as a “glue” that joins TDR and a SERK, which 77

may contribute to phosphorylation of a cytoplasmic downstream factor (Zhang et al., 78

2016b). 79

In plants, the TDIF-TDR signaling module acts by inhibiting xylem 80

differentiation from procambial cells and promoting procambial cell proliferation, 81

which results in the maintenance of the procambial cell population (Hirakawa et al. 82



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2008). WOX4, which is a member of the WUSCHEL-RELATED HOMEOBOX (WOX) 83

gene family, is a downstream factor of TDR and promotes procambial cell divisions 84

(Fig. 1A; Ji et al. 2010; Hirakawa et al. 2010; Suer et al. 2011). Moreover, the SK1 85

[ARABIDOPSIS THALIANA SK11 (ATSK11), ATSK12, and ATSK13] and SK2 86

[BRASSINOSTEROID-INSENSITIVE2 (BIN2), BIN2-LIKE1 (BIL1), and BIL2] 87

subgroups of GLYCOGEN SYNTHASE KINASE3/SHAGGY-LIKE KINASE proteins 88

(GSK3s) contribute redundantly to suppress xylem differentiation downstream of TDR 89

(Fig. 1A). 90

Promotion of procambial/cambial cell proliferation by TDIF-TDR 91

TDR is expressed preferentially in procambium and cambium (Hirakawa et al. 2008; 92

Fisher and Turner 2007), while CLE41 and CLE44 are expressed specifically in phloem 93

and more widely in its neighboring cell files, respectively (Fig. 1A; Hirakawa et al. 94

2008). Defects in TDR or CLE41 cause the depletion of the procambial cells (Fisher and 95

Turner 2007, Hirakawa et al. 2008, 2010, Etchells and Turner 2010). Ectopic expression 96

of CLE41 under different promoters revealed that expression of CLE41 in or around 97

procambial cells is sufficient to drive vascular cell division, but localized expression of 98

CLE41 in the phloem is required for maintaining properly orientated cell divisions 99

(Etchells and Turner 2010). Thus, phloem-synthesized TDIF regulates the orientation of 100

procambial cell divisions in a non-cell-autonomous fashion. 101

TDIF upregulates WOX4 expression in a TDR-dependent manner (Hirakawa 102

et al. 2010). Genetic analyses showed that WOX4 is required to promote the 103

proliferation of procambial/cambial cells, but not for repressing xylem differentiation in 104

response to the TDIF signal. The WOX14 transcription factor may also function 105

redundantly in Arabidopsis to modulate procambial cell proliferations (Etchells et al., 106

2013). Moreover, WOX14 may act in xylem fiber differentiation through promotion of 107

gibberellin biosynthesis (Denis et al., 2017), consistent with the requirement of 108

gibberellin for xylem expansion (Ragni et al., 2011) (Fig. 1A). Although WOX4 was 109

shown to interact physically with the HAIRY MERISTEM (HAM) family protein 110

HAM4 (Zhou et al., 2015), it is still unknown how WOX4 regulates gene expression 111

with HAM proteins. 112

The cambium plays a central role in radial growth of woody plants. In the 113

poplar (Populus trichocarpa) genome, orthologs of CLE41, TDR/PXY, and WOX4 are 114



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conserved (Hirakawa and Bowman, 2015, Etchells et al., 2015, Kucukoglu et al., 2017), 115

and PttWOX4a and PttWOX4b are specifically expressed in the cambial region during 116

vegetative growth, but not after growth cessation and during dormancy (Kucukoglu et 117

al., 2017). A decrease in PttWOX4a/b levels achieved by RNAi treatment caused severe 118

reduction of the width of the vascular cambium and greatly diminished secondary 119

growth, although primary growth was not affected. 120

Because there is no homologous sequence to Arabidopsis WOX14 in poplar 121

or spruce (Picea) genomes, WOX4 is expected to be a major player of cambial 122

proliferation in woody plants. PtPP2::PttCLE41-PttANT::PttPXY double 123

overexpression lines, in which phloem-specific expression of PttCLE41 and 124

cambium-specific expression of PXY are induced, exhibited highly organized vascular 125

tissue, comparable to that of wild-type controls (Etchells et al., 2015). Because 126

orthologs of CLE41, TDR/PXY, and WOX4 are widely distributed in angiosperm and 127

gymnosperm tree species (Hirakawa and Bowman, 2015, Kucukoglu et al., 2017), the 128

TDIF-TDR/PXY-WOX4 pathway is an evolutionarily conserved program for the 129

regulation of the vascular cambium activity in wood formation. Recently two groups 130

identified bifacial, strongly proliferating cambial stem cells that feed both xylem and 131

phloem production during secondary growth in Arabidopsis (Shi et al., 2019, Smetana 132

et al. 2019). In fact, in the cambial stem cells, TDR/PXY and WOX4 genes were actively 133

expressed. Recently, Zhu and others found that PtrCLE20 is expressed in xylem cells 134

and represses cambium activity in poplar (Zhu et al. 2019). The molecular mechanism 135

underlying the xylem-producing CLE peptide-dependent regulation of cambium activity 136

should be analyzed further. 137

Interaction of the TDIF-TDR pathway with phytohormones 138

The role of auxin in the regulation of vascular cambium activity is well established and 139

the auxin concentration gradient peaks over the cambial region and decreases towards 140

the surrounding secondary tissues in hybrid aspen (Populus tremula L. x Populus 141

tremuloides Michx) (Tuominen et al., 1997). WOX4 has been shown to be necessary 142

both for the auxin responsiveness of the cambium cells and for the auxin-dependent 143

increase in the cambium cell division activity (Suer et al., 2011). Local auxin signaling 144

in TDR-positive stem cells stimulates cambium activity (Brackmann et al. 2018). An 145

analysis with a highly sensitive auxin response marker revealed a moderate auxin 146



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response in TDR-positive stem cells and a higher response in xylem and phloem tissues. 147

Whereas the auxin response factors (ARFs) ARF3 and ARF4 act redundantly as general 148

cambium activators, MONOPTEROS (MP)/ARF5 acts as an inactivator specifically in 149

cambium stem cells (Fig. 1A). Indeed, MP induction resulted in both WOX4 repression 150

and the induction of xylem- and phloem-related genes (Brackmann et al. 2018). 151

Recently, Smetana and others proposed that auxin-dependent WOX4 regulation occurs 152

in xylem precursor cells with an auxin maximum, which promotes division of vascular 153

stem cells in a non-cell autonomous manner (Smetana et al., 2019). This idea should be 154

verified from various viewpoints. 155

Periclinal and radial cell divisions in procambial cells of the root apical 156

meristem (RAM) are also regulated by two bHLH transcription factors, LONESOME 157

HIGHWAY (LHW) and TARGET OF MONOPTEROS 5 (TMO5) (Schlereth et al., 158

2010). In xylem precursor cells in the RAM, auxin induces TMO5 expression, which 159

allows the formation of heterodimers between LHW and TMO5 (Fig. 1B). The 160

heterodimers directly promote the expression of target genes involved in the final step 161

of cytokinin biosynthesis, LONELY GUY 3 (LOG3) and LOG4 (Ohashi-Ito et al., 2014, 162

De Rybel et al., 2014). Therefore, cytokinin was hypothesized to act as a mobile signal 163

from the xylem to trigger divisions in the neighboring procambium cells. DOF2.1 and 164

its closest homologs, TMO6 and DOF6, may be key transcription factors downstream of 165

cytokinin in terms of procambial cell proliferation (Smet et al., 2019, Miyashita et al., 166

2019). In xylem precursor cells, however, LHW-TMO5-induced HISTIDINE 167

PHOSPHOTRANSFER PROTEIN 6 (AHP6) represses cytokinin signaling to inhibit 168

cell proliferation (Ohashi-Ito et al., 2014, De Rybel et al., 2014). 169

Suppression of xylem differentiation from procambial cells 170

TDIF signaling releases BIN2 and BIL2, but not BIL1, from TDR, and then activates 171

these GSK3s, which results in the suppression of xylem differentiation (Fig. 1A; Kondo 172

et al., 2014). Conversely, the inhibition of GSK3s with a chemical inhibitor (De Rybel 173

et al., 2009), bikinin, induces xylem differentiation (Kondo et al., 2014, 2015). 174

Bikinin-dependent ectopic xylem differentiation is suppressed in loss-of-function 175

mutants for BRI1-EMS-SUPPRESSOR 1 (BES1) (Kondo et al., 2016, Saito et al., 2018), 176

a direct substrate of GSK3s in the brassinosteroid signaling pathway (Yin et al., 2002). 177

By contrast, constitutively active BES1 (bes1-D) promotes xylem differentiation 178



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(Kondo et al., 2014). The loss-of-function mutant of BRASSINAZOLE RESISTANT 1 179

(BZR1), the closest homolog of BES1, also shows a bes1-like phenotype, but a weaker 180

one (Saito et al., 2018). Thus, BES1 and BZR1, which are suppressed by GSK3s, act 181

redundantly in promoting xylem differentiation (Fig. 1A). Further analysis indicated 182

that the GSK3s-BES1/BZR1 signal not only regulates xylem but also phloem 183

differentiation (Kondo et al., 2016, Saito et al., 2018). This finding is consistent with a 184

previous report showing that both bes1-D and bzr1-D partially rescued the phenotype of 185

the octopus mutant, in which root protophloem differentiation is suppressed (Anne et al., 186

2015), and with a role of brassinosteroid signaling in phloem sieve element 187

differentiation (Kang et al., 2017). Nevertheless, whether the canonical brassinosteroid 188

pathway effectors also have a role in root protophloem development remains unclear 189

(Kang et al., 2017). Of SK1 and SK2 GSK3s, BIL1 may have a distinct role in vascular 190

development (Fig. 1A). Han and others suggested that BIL1 phosphorylates and 191

activates MP, and the activated MP promotes the expression of two A-type Arabidopsis 192

Response Regulators (ARRs), ARR7 and ARR15, which suppress cambial cell 193

divisions (Han et al., 2018). 194

The finding that bikinin induces ectopic xylem cell differentiation led to the 195

establishment of a useful tissue culture system for vascular cell differentiation named 196

VISUAL (Vascular cell Induction culture System Using Arabidopsis Leaves). In 197

VISUAL, mesophyll cells in cultured cotyledons or leaf disks differentiate at a high 198

frequency into tracheary elements and sieve elements via the procambial stage in the 199

presence of bikinin (Kondo et al., 2015, 2016). This system enabled the analysis of the 200

roles of various genes in vascular differentiation by using their mutants as starting 201

materials of VISUAL. 202

Brassinosteroid signaling may interact with the 203

TDIF-TDR-GSK3s-BES1/BZR1 signaling pathway, because GSK3s and BES1/BZR1 204

are among its key components (Fig. 1A). Indeed, brassinosteroid promotes xylem 205

differentiation (Yamamoto et al, 1997, Caño-Delgado et al., 2004, Kubo et al, 2005), 206

which suggests that brassinosteroid regulates procambial cell fates to counteract TDIF 207

signaling through the reverse regulation of GSK3s. BRASSINOSTEROID 208

INSENSITIVE 1 (BRI1) is the major receptor for brassinosteroid and the BRI1 gene is 209

expressed widely in plants, while its homologs, BRI1-LIKE 1 (BRL1) and 3 (BRL3), are 210

expressed predominantly in vascular tissues. In particular, BRL1 expression is 211



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associated with the procambial cells in inflorescence stems (Caño-Delgado et al., 2004). 212

In procambial cells, therefore, the TDIF and brassinosteroid signals may be balanced 213

via GSK3s to determine procambial cell identity. Because brassinosteroid biosynthesis 214

occurs in procambial cells, which is promoted by auxin and cytokinin (Yamamoto et al., 215

2001, 2007), brassinosteroid may act as an autocrine factor in xylem differentiation 216

from procambial cells. 217

CLE9/CLE10 perception in xylem formation 218

CLE9 and CLE10, which encode the same CLE peptide, are preferentially expressed in 219

vascular cells of roots (Fig. 1B; Kondo et al. 2011). cle9 mutants and cle9 cle10 double 220

mutants exhibit a phenotype of increased metaxylem cell file numbers, which results 221

from enhanced periclinal cell division of xylem precursor cells in the RAM (Qian et al., 222

2018). The receptor kinase HAESA-LIKE1 (HSL1) is a CLE9/10 receptor that regulates 223

stomatal lineage cell division, while BARELY ANY MERISTEM (BAM) class 224

receptor kinases are CLE9/10 receptors that regulate periclinal cell division of xylem 225

precursor cells (Fig. 1B; Qian et al., 2018). Both HSL1 and BAM1 bind to CLE9/10, 226

but only HSL1 recruits SERKs as co-receptors in the presence of CLE9/10, suggesting 227

different signaling modes for these receptor systems (Hazak et al., 2017; Qian et al., 228

2018). Genetic analysis indicated that BAM1, BAM2, and BAM3 are involved in the 229

action of CLE9/10, but BAM1 is most important among them. Their genes are 230

expressed in vascular cells, with BAM1 being expressed in xylem and phloem precursor 231

cells in roots, consistent with the function of CLE9/10 in xylem precursor cells. 232

Application of CLE9/10 peptide suppressed protoxylem vessel formation in 233

Arabidopsis roots (Kondo et al., 2011). An early event caused by exogenous CLE9/10 234

peptide was the reduced expression of type-A ARR genes such as ARR5 and ARR6, 235

which are negative regulators of cytokinin signaling (Fig. 1B). Consistently, an arr10 236

arr12 double mutant, which is a combination of mutations of B-type ARRs, showed 237

CLE9/10-resistance in terms of protoxylem vessel suppression, and displayed ectopic 238

protoxylem vessel formation (Kondo et al., 2011). Therefore, CLE9/10 signaling may 239

control xylem differentiation through a cytokinin signaling pathway. However, because 240

cle9 cle10 double mutants did not enhance protoxylem vessel differentiation, other CLE 241

peptide(s) may also be involved redundantly in this process. 242

Phytosulfokine peptide perception in procambial cell fate 243



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Phytosulfokines (PSKs) are sulfated pentapeptides that are perceived by 244

PHYTOSULFOKINE RECEPTOR-1 and -2 (PSKR1/PSKR2) (Matsubayashi et al., 245

2002). PSK stabilizes the PSKR island domain for recruitment of a SERK (Wang et al., 246

2015). A recent study revealed a small RECEPTOR-LIKE PROTEIN 44 247

(RLP44)-mediated interaction between PSKRs and BRI1 that regulates procambial cell 248

fate in roots (Fig. 1B; Holzwart et al. 2018). In the rlp44 loss-of-function mutant, 249

supernumerary metaxylem-like cells are formed frequently outside the primary xylem 250

axis in the position of the procambium. This rlp44 phenotype can be rescued by 251

application of PSK peptide. Moreover, pskr1 pskr2 double mutants displayed an 252

rlp44-like xylem phenotype. Likewise, bri1 mutants show ectopic xylem in the 253

procambial position, while brassinosteroid-deficient mutants do not exhibit an 254

rlp44-like xylem phenotype. Therefore, PSK-PSKR signaling acts to maintain 255

procambial cell identity and RLP44 mediates the interaction between PSKR1 and BRI1. 256

These results may provide a model for the integration of multiple signaling pathways at 257

the plasma membrane by shifting associations of receptors in multiprotein complexes in 258

response to different ligands (Holzwart et al. 2018). Because RLP44 and most PSK 259

genes are expressed preferentially in xylem/phloem and procambium of roots, 260

respectively, this signaling may occur in a non-cell autonomous fashion. 261

ERECTA and related receptors cooperate with TDR/PXY family receptors 262

The LRR-RLK encoded by the ERECTA (ER) gene is part of a small gene family 263

together with ER-LIKE1 (ERL1) and ERL2. In er erl1 stems, intervening cambial cells 264

are decreased and phloem cells are frequently located adjacent to xylem cells (Uchida 265

and Tasaka, 2013). This also occurs in tdr (Fisher and Turner, 2007; Hirakawa et al., 266

2008), suggesting that ER and ERL1, like TDR, act by suppressing xylem 267

differentiation and promoting cambial cell activity. By contrast, er erl1 hypocotyls 268

display a remarkable expansion of the xylem and an increase in xylem fiber cells (Ragni 269

et al., 2011; Ikematsu et al., 2017). 270

On the one hand, this result supports the idea that ER and ERL1 suppress 271

xylem differentiation but appear to suppress cambial activity. On the other hand, the 272

relative xylem expansion in the Landsberg er (Ler) genotype was found to be due to 273

early cessation of phloem formation and reduced cambial activity (Sankar et al., 2014). 274

The difference between stems and hypocotyls in er erl1 may be explained by the 275



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tissue-specific gene regulation of ERL1 and ERL2: In the er pxy pxl1 pxyl2 genetic 276

background, ERL1 and ERL2 gene expression is reduced greatly in stems, while their 277

expression is strikingly enhanced in hypocotyls (Wang, et al., 2019). These findings 278

clearly indicate a tight interaction between PXY family genes and ER family genes (Fig. 279

1A). Indeed, the sextuple mutant, er erl1 erl2 pxy pxl1 pxyl2 shows a complete 280

suppression of secondary growth of hypocotyls, supporting the view that both TDR and 281

ER family genes are crucial factors of secondary growth (Wang, et al., 2019). 282

Both ER and ERL1 are expressed widely in the epidermis, phloem, and xylem 283

(Uchida and Tasaka, 2013), but the vascular defect in er erl1 stems is rescued by 284

phloem-specific activity of ER (Uchida and Tasaka, 2013), consistent with a proposed 285

role of ER in phloem proliferation (Sankar et al., 2014). Therefore, ER ERL1-dependent 286

suppression of xylem precursor cell division should occur in a non-cell autonomous 287

manner (Fig. 1A; Tamashige et al., 2017). ER and ERL1 also function in preventing 288

xylem fiber differentiation, which is mediated by the NAC SECONDARY WALL 289

THICKENING PROMOTING FACTORs (NSTs) in hypocotyls (Ikematsu et al., 2017). 290

Although BREVIPEDICELLUS is required for the hypocotyl to gain competency to 291

respond to gibberellin and trigger fiber differentiation in both the wild-type and er erl1, 292

it is still unknown whether the ER/ERL1 pathway is associated with the gibberellin 293

pathway. 294

Ligands for ER and EFR1 that function in xylem development have not been 295

identified. However, it is known that EPIDERMAL PATTERNING FACTOR 1 (EPF1), 296

EPF2, and EPF-LIKE9 (EPFL9) peptides function as ligands for ER and ERL1 in 297

stomata development (Han and Torii, 2016). In stem elongation, EPFL4 and EPFL6, 298

which are produced in epidermal cells, act as ligands for phloem-located ER (Abrash et 299

al., 2011; Uchida et al., 2012). In hypocotyls, EPFL4 and EPFL6 are expressed in 300

xylem parenchyma cells and differentiating xylem cells (Wang, et al., 2019). However, 301

there is presently no evidence that EPFL4 and EPFL6 function as ligands for regulating 302

hypocotyl secondary growth. In the Arabidopsis genome, there are 11 EPF/EPFL family 303

members (Hara et al., 2009). It is plausible that some EPF/EPFL family members may 304

function as ligands for ER and ERL1 to suppress xylem development in stems and 305

hypocotyls. TOO MANY MOUTHS (TMM) and SERK family proteins function as 306

co-receptors in ER signaling (Hang and Torii, 2016). Therefore, a specific combination 307

of ER/ERL1, EPF/EPFL peptides, and co-receptors, such as TMM and SERK family 308



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proteins, may function in vascular development in stems and hypocotyls. 309

Phloem-related CLE peptide signals 310

An interesting aspect emerging from the analysis of pxy/tdr and related mutants is that 311

they do not lose their capacity to produce proper xylem and phloem tissues, as judged 312

from morphological and molecular-genetic criteria (Fisher and Turner, 2007; Hirakawa 313

et al., 2008). This even holds true for higher order (sextuple) mutants that largely 314

remove redundancy (Wang et al., 2019). Thus, the main role of the 315

PXY/TDR-CLE41/44/TDIF system is likely the organization of vascular patterning, 316

which is, for instance, evident in the regular spacing of phloem strands during hypocotyl 317

expansion (Sankar et al., 2014). 318

An easier, more accessible system to study a possibly autonomous role of 319

CLE peptide signaling in vascular development is the root tip with its simple diarch 320

vascular organization. Here, two protophloem poles flank a central xylem axis and 321

allow continuous observation of development along a spatio-temporal gradient. 322

Moreover, protophloem expresses key players or markers, such as ALTERED PHLOEM 323

DEVELOPMENT (APL) (Bonke et al., 2003) or COTYLEDON VASCULAR PATTERN 2 324

(CVP2) (Carland and Nelson, 2004; Rodriguez-Villalon et al., 2015), that are also 325

expressed in secondary phloem development (Lehmann and Hardtke, 2016), indicating 326

that the principal findings in one context likely apply to the other. 327

Root-active CLE peptides are perceived in the phloem 328

The root protophloem is also a system where a key question can be answered: Is CLE 329

peptide signaling required to form functional phloem? Early hints that CLE peptides 330

could play a role in root development came from the observation that several CLE genes 331

are expressed in the root (Jun et al., 2010), and that treatments with many chemically 332

synthesized CLE peptides suppress root growth (Fiers et al., 2005; Ito et al., 2006; 333

Kinoshita et al., 2007). Such so-called “root-active” CLE peptides were also employed 334

to identify components that are necessary for CLE peptide perception in the root, and 335

notably identified the receptor-like protein CLV2 and its interacting partner, the 336

pseudokinase SUPPRESSOR OF OVEREXPRESSION OF LLP1-2/CORYNE 337

(SOL2/CRN) (Jeong et al., 1999; Miwa et al., 2008; Muller et al., 2008; Meng and 338

Feldman, 2010). 339



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Both clv2 and crn mutants display substantial resistance to root growth 340

inhibition by a range of root-active CLE peptides, and both the CLV2 and CRN genes 341

are essentially expressed at low levels throughout the root (Hazak et al., 2017). 342

However, recently it was shown that restricted expression of CRN in the developing 343

protophloem is sufficient to fully recover CLE perception in a crn null mutant 344

background (Hazak et al., 2017). This matched the observation that root-active CLE 345

peptides a priori suppress protophloem sieve element differentiation 346

(Rodriguez-Villalon et al., 2014; Hazak et al., 2017), which is essential for root growth 347

(Furuta et al., 2014; Rodriguez-Villalon et al., 2014). Given that interactions between 348

CLE peptides and their cognate receptors are rather specific (Hohmann et al., 2017), the 349

requirement of the CLV2|CRN heteromer for perception of root-active CLE peptides 350

likely reflects a more general rate-limiting role in receptor complex activity. For 351

example, it has been suggested that CLV2|CRN stabilizes the expression of BAM3, the 352

cognate CLE45 receptor in the root (Kang and Hardtke, 2016; Hazak et al., 2017). 353

Suppression of CLE peptide signaling permits root protophloem sieve element 354

differentiation 355

CLE45 is one of the few CLE peptides that is expressed in the developing protophloem 356

sieve elements, the others being the related CLE25 and CLE26 peptides 357

(Rodriguez-Villalon et al., 2014; Anne et al., 2018; Ren et al., 2019). Recently, it was 358

suggested that CLE25 is required for protophloem sieve element formation, although a 359

cle25 mutant did not display a root growth phenotype and only showed a marginal delay 360

in sieve element elongation (Ren et al., 2019). While this might reflect redundancy with 361

other CLE peptides, expression of a supposedly dominant negative mutant version of 362

CLE25 (a G6T exchange in the peptide) abolished protophloem sieve element 363

differentiation as well as one of the formative divisions in the phloem lineage (Ren et al., 364

2019). 365

Interestingly, such divisions can also be suppressed by mild auxin antagonist 366

treatment (Rodriguez-Villalon et al., 2014) and appear to be non-essential. However, it 367

often remains unclear which of the two successive periclinal formative divisions in the 368

phloem lineage is affected, and it might very well turn out that one of them is essential 369

for sieve element formation. Nonetheless, the CLE25G6T

phenotype strongly resembles 370

the so-called Disturbed Protophloem Syndrome observed in backgrounds with elevated 371



13

CLE45 signaling (Rodriguez-Villalon et al., 2014; Anne and Hardtke, 2017) and is 372

consistent with simple dominant (rather than dominant negative) action of the 373

CLE25G6T

version, as observed for other CLE peptides in other contexts (Czyzewicz et 374

al., 2015), including CLE45G6T

in protophloem formation (Rodriguez-Villalon et al., 375

2014; Czyzewicz et al., 2015). This interpretation is also consistent with observations in 376

pertinent receptor mutants. For example, neither crn loss-of-function mutants, nor 377

CLE-RESISTANT RECEPTOR KINASE (clerk) loss-of-function mutants, which are both 378

strongly resistant to CLE25, CLE26, and CLE45 application, display any root growth or 379

protophloem sieve element differentiation phenotypes (Hazak et al., 2017; Anne et al., 380

2018). The same applies to the crn clerk double mutant (Anne et al., 2018). 381

In summary, current data suggest that CLE peptide signaling is not required 382

per se for sieve element formation in the Arabidopsis root. On the contrary, it seems that 383

suppression of autocrine CLE peptide signaling is a pre-requisite for proper 384

protophloem sieve element differentiation (Breda et al., 2019). This does not, however, 385

preclude a role in other aspects of root development, for example formative divisions or 386

radial organization. For instance, CLE9 and CLE10 redundantly appear to affect 387

formative xylem divisions in the root, through their interaction with the BAM1 and 388

BAM2 receptors (Qian et al., 2018). Such mechanisms may also exist for phloem 389

formation. 390

CLE peptide signaling as rapid mediators of stress-induced sink shutdown 391

Beyond purely developmental aspects, CLE peptides may also transmit environmental 392

inputs, and these two roles might not be mutually exclusive in the case of individual 393

peptides. Indeed, CLE25 is a prime example in this context. In addition to its expression 394

in the protophloem, CLE25 expression is induced by drought stress and acts as a 395

long-distance signal that is transported through the vasculature to convey this 396

physiological state to the shoot system (Takahashi et al., 2018). Coincidentally, such 397

induction should also suppress protophloem differentiation and thereby root growth 398

(Anne and Hardtke, 2017; Hazak et al., 2017), which could be advantageous in drought 399

conditions. Yet another example is the root-active CLE peptide, CLE14, which is 400

induced upon phosphate starvation and triggers a breakdown of root meristem 401

maintenance and root growth (Gutierrez-Alanis et al., 2017). Since this response 402

requires the CLV2|CRN module, it appears that it is achieved through a shutdown of 403



14

protophloem formation (Meng and Feldman, 2010; Gutierrez-Alanis et al., 2017; Hazak 404

et al., 2017). 405

In summary, beyond any positive developmental roles in phloem development 406

that largely remain to be discovered, root-active CLE peptides might be mainly 407

involved in the sensing of adverse environmental conditions. From the current data, it 408

seems that their upregulation in response to such adverse conditions suppresses 409

protophloem differentiation and thereby halts root growth. From a physiological 410

perspective, such a mechanism would be a very efficient and rapid way to stop growth 411

and eliminate a metabolic sink that finds itself in sub-optimal conditions. Because 412

phloem transport is essentially auto-regulated, this would “automatically” redirect 413

phloem sap to actively growing roots. Thus, CLE peptide regulation may primarily 414

serve to fine-tune and optimize root system exploration of the wildly heterogenous soil 415

matrix, which could represent a substantial adaptive advantage. 416

Concluding remarks 417

In summary, peptide signaling pathways have been increasingly implicated in vascular 418

development over recent years (Figure 1 summarizes peptide and hormone signaling 419

pathways discussed in this update). From the current data, it appears clear that various 420

peptides and plant hormones not only function as ligands in vascular cell proliferation, 421

but also in both xylem and phloem cell type fate regulation, and both in a 422

cell-autonomous or non-cell autonomous manner. In addition, the emerging picture is 423

becoming considerably complex since the exact impact of a given signaling pathway 424

seems to depend on the developmental stage or the organ. For example, the TDIF-TDR 425

signaling pathway apparently acts in the cambium and actively proliferating 426

procambium of hypocotyls and stems, but not in the root apical meristem. Moreover, 427

the picture is complicated by the observation that at least in the RAM context, 428

CLE45-BAM3 signaling has to be suppressed to permit phloem differentiation, 429

although CLE peptide signaling might be required to initiate proper phloem formation. 430

From the genetic analyses, it is also apparent that the complex network composed of 431

multi-signaling pathways makes the regulation of procambial/cambial cell identity and 432

proliferation robust. Similar redundancy might exist at the level of differentiation of 433

vascular tissues, and future efforts could focus on uncovering such redundancy through 434

genetic as well as biochemical/cell biological investigations. 435



15

436

FIGURE LEGENDS 437

Figure 1. Peptide-related signaling pathways that regulate proliferation of 438

procambial/cambial cells and their differentiation into xylem and phloem cells. A: 439

Signaling pathways in hypocotyls and stems. B: Signaling pathways in the root apical 440

meristem. BR: brassinosteroid; CK: cytokinin; AHKs: cytokinin receptors. 441

442



16

REFERENCES 443

Anne P, Amiguet-Vercher A, Brandt B, Kalmbach L, Geldner N, Hothorn M, 444

Hardtke CS (2018) CLERK is a novel receptor kinase required for sensing of 445

root-active CLE peptides in Arabidopsis. Development 145: dev162354 446

Anne P, Azzopardi M, Gissot L, Beaubiat S, Hematy K, Palauqui JC (2015) 447

OCTOPUS negatively regulates BIN2 to control phloem differentiation in 448

Arabidopsis thaliana. Curr Biol 25: 2584-2590 449

Anne P, Hardtke CS (2017) Phloem function and development-biophysics meets 450

genetics. Curr Opin Plant Biol 43: 22-28 451

Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y (2003) APL 452

regulates vascular tissue identity in Arabidopsis. Nature 426: 181-186 453

Brackmann K, Qi J, Gebert M, Jouannet V, Schlamp T, Grunwald K, Wallner ES, 454

Novikova DD, Levitsky VG, Agusti J, Sanchez P, Lohmann JU, Greb T 455

(2018) Spatial specificity of auxin responses coordinates wood formation. Nat 456

Commun 9: 875 457

Breda AS, Hazak O, Schultz P, Anne P, Graeff M, Simon R, Hardtke CS (2019) A 458

cellular insulator against CLE45 peptide signaling. Curr Biol 29: 2501-2508 459

e2503 460

Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, 461

Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that 462

function in vascular differentiation in Arabidopsis. Development 131: 463

5341-5351 464

Carland FM, Nelson T (2004) Cotyledon vascular pattern2-mediated inositol (1,4,5) 465

triphosphate signal transduction is essential for closed venation patterns of 466

Arabidopsis foliar organs. Plant Cell 16: 1263-1275 467

Czyzewicz N, Wildhagen M, Cattaneo P, Stahl Y, Pinto KG, Aalen RB, Butenko 468

MA, Simon R, Hardtke CS, De Smet I (2015) Antagonistic peptide technology 469

for functional dissection of CLE peptides revisited. J Exp Bot 66: 5367-5374 470

De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME, Novak O, Yamaguchi N, 471

Yoshida S, Van Isterdael G, Palovaara J, Nijsse B, Boekschoten MV, 472

Hooiveld G, Beeckman T, Wagner D, Ljung K, Fleck C, Weijers D (2014) 473

Plant development. Integration of growth and patterning during vascular tissue 474

formation in Arabidopsis. Science 345: 1255215 475



17

De Rybel B, Audenaert D, Vert G, Rozhon W, Mayerhofer J, Peelman F, Coutuer 476

S, Denayer T, Jansen L, Nguyen L, Vanhoutte I, Beemster GT, Vleminckx 477

K, Jonak C, Chory J, Inze D, Russinova E, Beeckman T (2009) Chemical 478

inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates 479

brassinosteroid signaling. Chem Biol 16: 594-604 480

Denis E, Kbiri N, Mary V, Claisse G, Conde ESN, Kreis M, Deveaux Y (2017) 481

WOX14 promotes bioactive gibberellin synthesis and vascular cell 482

differentiation in Arabidopsis. Plant J 90: 560-572 483

Etchells JP, Mishra LS, Kumar M, Campbell L, Turner SR (2015) Wood formation 484

in trees is increased by manipulating PXY-regulated cell division. Curr Biol 25: 485

1050-1055 486

Etchells JP, Provost CM, Mishra L, Turner SR (2013) WOX4 and WOX14 act 487

downstream of the PXY receptor kinase to regulate plant vascular proliferation 488

independently of any role in vascular organisation. Development 140: 489

2224-2234 490

Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a 491

multifunctional pathway that controls the rate and orientation of vascular cell 492

division. Development 137: 767-774 493

Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM 494

(2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger 495

consumption of the root meristem in Arabidopsis through a 496

CLAVATA2-dependent pathway. Plant Cell 17: 2542-2553 497

Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining 498

polarity during plant vascular-tissue development. Curr Biol 17: 1061-1066 499

Fukuda H, Ohashi-Ito K (2019) Vascular tissue development in plants. Curr Top Dev 500

Biol 131: 141-160 501

Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vaten A, 502

Lindgren O, De Rybel B, Van Isterdael G, Somervuo P, Lichtenberger R, 503

Rocha R, Thitamadee S, Tahtiharju S, Auvinen P, Beeckman T, Jokitalo E, 504

Helariutta Y (2014) Plant development. Arabidopsis NAC45/86 direct sieve 505

element morphogenesis culminating in enucleation. Science 345: 933-937 506

Gutierrez-Alanis D, Yong-Villalobos L, Jimenez-Sandoval P, Alatorre-Cobos F, 507

Oropeza-Aburto A, Mora-Macias J, Sanchez-Rodriguez F, Cruz-Ramirez 508



18

A, Herrera-Estrella L (2017) Phosphate starvation-dependent iron mobilization 509

induces CLE14 expression to trigger root meristem differentiation through 510

CLV2/PEPR2 signaling. Dev Cell 41: 555-570 e553 511

Han S, Cho H, Noh J, Qi J, Jung HJ, Nam H, Lee S, Hwang D, Greb T, Hwang I 512

(2018) BIL1-mediated MP phosphorylation integrates PXY and cytokinin 513

signalling in secondary growth. Nat Plants 4: 605-614 514

Han SK, Torii KU (2016) Lineage-specific stem cells, signals and asymmetries during 515

stomatal development. Development 143: 1259-1270 516

Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, 517

Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory 518

peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant 519

Cell Physiol 50: 1019-1031 520

Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez-Villalon A, Hothorn M, 521

Hardtke CS (2017) Perception of root-active CLE peptides requires CORYNE 522

function in the phloem vasculature. EMBO Rep 18: 1367-1381 523

Hazak O, Hardtke CS (2016) CLAVATA 1-type receptors in plant development. J 524

Exp Bot 67: 4827-4833 525

Hirakawa Y, Bowman JL (2015) A role of TDIF peptide signaling in vascular cell 526

differentiation is conserved among euphyllophytes. Front Plant Sci 6: 1048 527

Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular 528

stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 529

22: 2618-2629 530

Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, 531

Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous 532

control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl 533

Acad Sci U S A 105: 15208-15213 534

Hohmann U, Lau K, Hothorn M (2017) The structural basis of ligand perception and 535

signal activation by receptor kinases. Annu Rev Plant Biol 68: 109-137 536

Holzwart E, Huerta AI, Glockner N, Garnelo Gomez B, Wanke F, Augustin S, 537

Askani JC, Schurholz AK, Harter K, Wolf S (2018) BRI1 controls vascular 538

cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling. 539

Proc Natl Acad Sci U S A 115: 11838-11843 540



19

Ikematsu S, Tasaka M, Torii KU, Uchida N (2017) ERECTA-family receptor kinase 541

genes redundantly prevent premature progression of secondary growth in the 542

Arabidopsis hypocotyl. New Phytol 213: 1697-1709 543

Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) 544

Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 545

313: 842-845 546

Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene 547

encodes a receptor-like protein required for the stability of the CLAVATA1 548

receptor-like kinase. Plant Cell 11: 1925-1934 549

Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, 550

Meyerowitz EM, Feldman LJ, Fletcher JC (2010) Comprehensive analysis of 551

CLE polypeptide signaling gene expression and overexpression activity in 552

Arabidopsis. Plant Physiol 154: 1721-1736 553

Kang YH, Hardtke CS (2016) Arabidopsis MAKR5 is a positive effector of 554

BAM3-dependent CLE45 signaling. EMBO Rep 17: 1145-1154 555

Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S (2007) 556

Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related 557

(CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48: 558

1821-1825 559

Kondo Y, Fujita T, Sugiyama M, Fukuda H (2015) A novel system for xylem cell 560

differentiation in Arabidopsis thaliana. Mol Plant 8: 612-621 561

Kondo Y, Hirakawa Y, Kieber JJ, Fukuda H (2011) CLE peptides can negatively 562

regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol 563

52: 37-48 564

Kondo Y, Ito T, Nakagami H, Hirakawa Y, Saito M, Tamaki T, Shirasu K, 565

Fukuda H (2014) Plant GSK3 proteins regulate xylem cell differentiation 566

downstream of TDIF-TDR signalling. Nat Commun 5: 3504 567

Kondo Y, Nurani AM, Saito C, Ichihashi Y, Saito M, Yamazaki K, Mitsuda N, 568

Ohme-Takagi M, Fukuda H (2016) Vascular cell induction culture system 569

using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of 570

sieve element-like cells. Plant Cell 28: 1250-1262 571



20

Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, 572

Fukuda H, Demura T (2005) Transcription switches for protoxylem and 573

metaxylem vessel formation. Genes Dev 19: 1855-1860 574

Kucukoglu M, Nilsson J, Zheng B, Chaabouni S, Nilsson O (2017) 575

WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulate cambial 576

cell division activity and secondary growth in Populus trees. New Phytol 215: 577

642-657 578

Lehmann F, Hardtke CS (2016) Secondary growth of the Arabidopsis 579

hypocotyl-vascular development in dimensions. Curr Opin Plant Biol 29: 9-15 580

Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He 581

XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, 582

Lopez-Millan AF, Grusak MA, Kachroo P (2013) The plant vascular system: 583

evolution, development and functions. J Integr Plant Biol 55: 294-388 584

Matsubayashi Y (2011) Small post-translationally modified peptide signals in 585

Arabidopsis. Arabidopsis Book 9: e0150 586

Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase 587

involved in perception of a peptide plant hormone, phytosulfokine. Science 296: 588

1470-1472 589

Meng L, Feldman LJ (2010) CLE14/CLE20 peptides may interact with 590

CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division 591

in the root meristem of Arabidopsis. Planta 232: 1061-1074 592

Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The 593

receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell 594

Physiol 49: 1752-1757 595

Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo JO, Mellor N, 596

Help-Rinta-Rahko H, Otero S, Smet W, Boekschoten M, Hooiveld G, 597

Hashimoto K, Smetana O, Siligato R, Wallner ES, Mahonen AP, Kondo Y, 598

Melnyk CW, Greb T, Nakajima K, Sozzani R, Bishopp A, De Rybel B, 599

Helariutta Y (2019) Mobile PEAR transcription factors integrate positional 600

cues to prime cambial growth. Nature 565: 490-494 601

Morita J, Kato K, Nakane T, Kondo Y, Fukuda H, Nishimasu H, Ishitani R, 602

Nureki O (2016) Crystal structure of the plant receptor-like kinase TDR in 603

complex with the TDIF peptide. Nat Commun 7: 12383 604



21

Mou S, Zhang X, Han Z, Wang J, Gong X, Chai J (2017) CLE42 binding induces 605

PXL2 interaction with SERK2. Protein Cell 8: 612-617 606

Muller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of 607

Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently 608

of CLAVATA1. Plant Cell 20: 934-946 609

Ohashi-Ito K, Saegusa M, Iwamoto K, Oda Y, Katayama H, Kojima M, 610

Sakakibara H, Fukuda H (2014) A bHLH complex activates vascular cell 611

division via cytokinin action in root apical meristem. Curr Biol 24: 2053-2058 612

Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A 613

glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chem 614

Biol 5: 578−580 615

Qian P, Song W, Yokoo T, Minobe A, Wang G, Ishida T, Sawa S, Chai J, 616

Kakimoto T (2018) The CLE9/10 secretory peptide regulates stomatal and 617

vascular development through distinct receptors. Nat Plants 4: 1071-1081 618

Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke 619

CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem 620

expansion. Plant Cell 23: 1322-1336 621

Ren SC, Song XF, Chen WQ, Lu R, Lucas WJ, Liu CM (2019) CLE25 peptide 622

regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor 623

complex. J Integr Plant Biol 61: 1043-1061 624

Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P, Depuydt S, 625

Hardtke CS (2014) Molecular genetic framework for protophloem formation. 626

Proc Natl Acad Sci U S A 111: 11551-11556 627

Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS (2015) 628

Primary root protophloem differentiation requires balanced 629

phosphatidylinositol-4,5-biphosphate levels and systemically affects root 630

branching. Development 142: 1437-1446 631

Saito M, Kondo Y, Fukuda H (2018) BES1 and BZR1 redundantly promote phloem 632

and xylem differentiation. Plant Cell Physiol 59: 590-600 633

Sankar M, Nieminen K, Ragni L, Xenarios I, Hardtke CS (2014) Automated 634

quantitative histology reveals vascular morphodynamics during Arabidopsis 635

hypocotyl secondary growth. Elife 3: e01567 636



22

Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, 637

Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root 638

initiation by regulating a mobile transcription factor. Nature 464: 913-916 639

Shi D, Lebovka I, Lopez-Salmeron V, Sanchez P, Greb T (2019) Bifacial cambium 640

stem cells generate xylem and phloem during radial plant growth. Development 641

146: dev171355 642

Shinohara H, Matsubayashi Y (2013) Chemical synthesis of Arabidopsis CLV3 643

glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide 644

conformation and activity. Plant Cell Physiol 54: 369-374 645

Smet W, Sevilem I, de Luis Balaguer MA, Wybouw B, Mor E, Miyashima S, Blob 646

B, Roszak P, Jacobs TB, Boekschoten M, Hooiveld G, Sozzani R, Helariutta 647

Y, De Rybel B (2019) DOF2.1 controls cytokinin-dependent vascular cell 648

proliferation downstream of TMO5/LHW. Curr Biol 29: 520-529.e526 649

Smetana O, Mäkilä R, Lyu M, Amiryousefi A, Rodríguez FS, Wu M-F, Solé-Gil A, 650

Gavarrón ML, Siligato R, Miyashima S, Roszak P, Blomster T, Reed JW, 651

Broholm S, Mähönen AP (2019) High levels of auxin signalling define the 652

stem-cell organizer of the vascular cambium Nature 565: 433-435 653

Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts auxin 654

responsiveness to cambium cells in Arabidopsis. Plant Cell 23: 3247-3259 655

Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, 656

Yamaguchi-Shinozaki K, Shinozaki K (2018) A small peptide modulates 657

stomatal control via abscisic acid in long-distance signalling. Nature 556: 658

235-238 659

Tameshige T, Ikematsu S, Torii KU, Uchida N (2017) Stem development through 660

vascular tissues: EPFL-ERECTA family signaling that bounces in and out of 661

phloem. J Exp Bot 68: 45-53 662

Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of 663

indole-3-acetic acid is related to secondary xylem development in hybrid aspen. 664

Plant Physiol 115: 577-585 665

Uchida N, Tasaka M (2013) Regulation of plant vascular stem cells by 666

endodermis-derived EPFL-family peptide hormones and phloem-expressed 667

ERECTA-family receptor kinases. J Exp Bot 64: 5335-5343 668



23

Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015) 669

Allosteric receptor activation by the plant peptide hormone phytosulfokine. 670

Nature 525: 265-268 671

Wang N, Bagdassarian KS, Doherty RE, Kroon JT, Connor KA, Wang XY, Wang 672

W, Jermyn IH, Turner SR, Etchells JP (2019) Organ-specific genetic 673

interactions between paralogues of the PXY and ER receptor kinases enforce 674

radial patterning in Arabidopsis vascular tissue. Development 146: dev177105 675

Yamaguchi YL, Ishida T, Sawa S (2016) CLE peptides and their signaling pathways 676

in plant development. J Exp Bot 67: 4813–4826 677

Yamamoto R, Fujioka S, Demura T, Takatsuto S, Yoshida S, Fukuda H (2001) 678

Brassinosteroid levels increase drastically prior to morphogenesis of tracheary 679

elements. Plant Physiol 125: 556-563 680

Yamamoto R, Fujioka S, Iwamoto K, Demura T, Takatsuto S, Yoshida S, Fukuda 681

H (2007) Co-regulation of brassinosteroid biosynthesis-related genes during 682

xylem cell differentiation. Plant Cell Physiol 48: 74-83 683

Zhang H, Lin X, Han Z, Qu LJ, Chai J (2016a) Crystal structure of PXY-TDIF 684

complex reveals a conserved recognition mechanism among CLE 685

peptide-receptor pairs. Cell Res 26: 543-555 686

Zhang H, Lin X, Han Z, Wang J, Qu LJ, Chai J (2016b) SERK family receptor-like 687

kinases function as co-receptors with PXY for plant vascular development. Mol 688

Plant 9: 1406-1414 689

Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, 690

Kay SA, Meyerowitz EM (2015) Control of plant stem cell function by 691

conserved interacting transcriptional regulators. Nature 517: 377-380 692

Zhu Y, Song D, Zhang, R, Luo, L, Cao, S, Huang, C, Sun J, Gui J, Li L (2019) A 693

xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in 694

Populus. Plant Biotechnol J: doi: 10.1111/pbi.13187 695

696



ADVANCES

• Various peptides and plant hormones function as ligands in vascular cell proliferation, as well as in xylem and phloem cell type fate regulation, in both a cell-autonomous or non-cell autonomous manner.

• The role of a given signaling pathway can be context-dependent and depend on the developmental stage or the organ.

• The complex network composed of multiple intersecting signaling pathways renders the regulation of procambial/cambial cell identity and proliferation robust.

• CLE peptide signals might convey environmental inputs as a rapid control of sink organ development.



OUTSTANDING QUESTIONS

• How does crosstalk between different peptide signaling pathways occur mechanistically during vascular development? Do different receptors form a complex on the plasma membrane, and/or are there signaling hubs that connect different signaling pathways?

• Are long-distance peptide signaling pathways controlling vascular development?

• Are the peptide processing and secretion processes regulated as a function of vascular development?

• What are the mechanisms that underlie developmental stage- and organ-specific peptide signaling?

• Where do the processed peptides act at high spatio-temporal resolution?



Parsed CitationsAnne P, Amiguet-Vercher A, Brandt B, Kalmbach L, Geldner N, Hothorn M, Hardtke CS (2018) CLERK is a novel receptor kinaserequired for sensing of root-active CLE peptides in Arabidopsis. Development 145: dev162354

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Anne P, Azzopardi M, Gissot L, Beaubiat S, Hematy K, Palauqui JC (2015) OCTOPUS negatively regulates BIN2 to control phloemdifferentiation in Arabidopsis thaliana. Curr Biol 25: 2584-2590


Anne P, Hardtke CS (2017) Phloem function and development-biophysics meets genetics. Curr Opin Plant Biol 43: 22-28Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature426: 181-186


Brackmann K, Qi J, Gebert M, Jouannet V, Schlamp T, Grunwald K, Wallner ES, Novikova DD, Levitsky VG, Agusti J, Sanchez P,Lohmann JU, Greb T (2018) Spatial specificity of auxin responses coordinates wood formation. Nat Commun 9: 875


Breda AS, Hazak O, Schultz P, Anne P, Graeff M, Simon R, Hardtke CS (2019) A cellular insulator against CLE45 peptide signaling. CurrBiol 29: 2501-2508 e2503


Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novelbrassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351


Carland FM, Nelson T (2004) Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential forclosed venation patterns of Arabidopsis foliar organs. Plant Cell 16: 1263-1275


Czyzewicz N, Wildhagen M, Cattaneo P, Stahl Y, Pinto KG, Aalen RB, Butenko MA, Simon R, Hardtke CS, De Smet I (2015) Antagonisticpeptide technology for functional dissection of CLE peptides revisited. J Exp Bot 66: 5367-5374


De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME, Novak O, Yamaguchi N, Yoshida S, Van Isterdael G, Palovaara J, Nijsse B,Boekschoten MV, Hooiveld G, Beeckman T, Wagner D, Ljung K, Fleck C, Weijers D (2014) Plant development. Integration of growthand patterning during vascular tissue formation in Arabidopsis. Science 345: 1255215


De Rybel B, Audenaert D, Vert G, Rozhon W, Mayerhofer J, Peelman F, Coutuer S, Denayer T, Jansen L, Nguyen L, Vanhoutte I,Beemster GT, Vleminckx K, Jonak C, Chory J, Inze D, Russinova E, Beeckman T (2009) Chemical inhibition of a subset of Arabidopsisthaliana GSK3-like kinases activates brassinosteroid signaling. Chem Biol 16: 594-604


Denis E, Kbiri N, Mary V, Claisse G, Conde ESN, Kreis M, Deveaux Y (2017) WOX14 promotes bioactive gibberellin synthesis andvascular cell differentiation in Arabidopsis. Plant J 90: 560-572


Etchells JP, Mishra LS, Kumar M, Campbell L, Turner SR (2015) Wood formation in trees is increased by manipulating PXY-regulatedcell division. Curr Biol 25: 1050-1055


Etchells JP, Provost CM, Mishra L, Turner SR (2013) WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plantvascular proliferation independently of any role in vascular organisation. Development 140: 2224-2234


Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and www.plantphysiol.orgon July 27, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Anne P%2C Amiguet%2DVercher A%2C Brandt B%2C Kalmbach L%2C Geldner N%2C Hothorn M%2C Hardtke CS %282018%29 CLERK is a novel receptor kinase required for sensing of root%2Dactive CLE peptides in Arabidopsis%2E Development 145%3A dev&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Anne&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Anne&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Anne P%2C Azzopardi M%2C Gissot L%2C Beaubiat S%2C Hematy K%2C Palauqui JC %282015%29 OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana%2E Curr Biol&dopt=abstract


https://scholar.google.com/scholar?as_q=OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Anne&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Anne P%2C Hardtke CS %282017%29 Phloem function and development%2Dbiophysics meets genetics%2E Curr Opin Plant Biol&dopt=abstract


https://scholar.google.com/scholar?as_q=Phloem function and development-biophysics meets genetics&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Phloem function and development-biophysics meets genetics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Anne&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Bonke M%2C Thitamadee S%2C Mahonen AP%2C Hauser MT%2C Helariutta Y %282003%29 APL regulates vascular tissue identity in Arabidopsis%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bonke&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=APL regulates vascular tissue identity in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=APL regulates vascular tissue identity in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bonke&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Brackmann K%2C Qi J%2C Gebert M%2C Jouannet V%2C Schlamp T%2C Grunwald K%2C Wallner ES%2C Novikova DD%2C Levitsky VG%2C Agusti J%2C Sanchez P%2C Lohmann JU%2C Greb T %282018%29 Spatial specificity of auxin responses coordinates wood formation%2E Nat Commun&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brackmann&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Spatial specificity of auxin responses coordinates wood formation.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Spatial specificity of auxin responses coordinates wood formation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brackmann&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Breda AS%2C Hazak O%2C Schultz P%2C Anne P%2C Graeff M%2C Simon R%2C Hardtke CS %282019%29 A cellular insulator against CLE45 peptide signaling%2E Curr Biol 29%3A 2501%2D2508 e&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Breda&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A cellular insulator against CLE45 peptide signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A cellular insulator against CLE45 peptide signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Breda&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Cano%2DDelgado A%2C Yin Y%2C Yu C%2C Vafeados D%2C Mora%2DGarcia S%2C Cheng JC%2C Nam KH%2C Li J%2C Chory J %282004%29 BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis%2E Development&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cano-Delgado&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cano-Delgado&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Carland FM%2C Nelson T %282004%29 Cotyledon vascular pattern2%2Dmediated inositol %281%2C4%2C5%29 triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Carland&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Carland&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Czyzewicz N%2C Wildhagen M%2C Cattaneo P%2C Stahl Y%2C Pinto KG%2C Aalen RB%2C Butenko MA%2C Simon R%2C Hardtke CS%2C De Smet I %282015%29 Antagonistic peptide technology for functional dissection of CLE peptides revisited%2E J Exp Bot&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Czyzewicz&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Antagonistic peptide technology for functional dissection of CLE peptides revisited&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Antagonistic peptide technology for functional dissection of CLE peptides revisited&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Czyzewicz&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=De Rybel B%2C Adibi M%2C Breda AS%2C Wendrich JR%2C Smit ME%2C Novak O%2C Yamaguchi N%2C Yoshida S%2C Van Isterdael G%2C Palovaara J%2C Nijsse B%2C Boekschoten MV%2C Hooiveld G%2C Beeckman T%2C Wagner D%2C Ljung K%2C Fleck C%2C Weijers D %282014%29 Plant development%2E Integration of growth and patterning during vascular tissue formation in Arabidopsis%2E Science&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=De&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Plant development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Plant development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=De Rybel B%2C Audenaert D%2C Vert G%2C Rozhon W%2C Mayerhofer J%2C Peelman F%2C Coutuer S%2C Denayer T%2C Jansen L%2C Nguyen L%2C Vanhoutte I%2C Beemster GT%2C Vleminckx K%2C Jonak C%2C Chory J%2C Inze D%2C Russinova E%2C Beeckman T %282009%29 Chemical inhibition of a subset of Arabidopsis thaliana GSK3%2Dlike kinases activates brassinosteroid signaling%2E Chem Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=De&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Denis E%2C Kbiri N%2C Mary V%2C Claisse G%2C Conde ESN%2C Kreis M%2C Deveaux Y %282017%29 WOX14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis%2E Plant J&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Denis&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=WOX14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=WOX14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Denis&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Etchells JP%2C Mishra LS%2C Kumar M%2C Campbell L%2C Turner SR %282015%29 Wood formation in trees is increased by manipulating PXY%2Dregulated cell division%2E Curr Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Etchells&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Wood formation in trees is increased by manipulating PXY-regulated cell division&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Wood formation in trees is increased by manipulating PXY-regulated cell division&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Etchells&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Etchells JP%2C Provost CM%2C Mishra L%2C Turner SR %282013%29 WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation%2E Development&dopt=abstract


https://scholar.google.com/scholar?as_q=WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Etchells&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


orientation of vascular cell division. Development 137: 767-774Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM (2005) The 14-amino acid CLV3, CLE19, and CLE40peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17: 2542-2553


Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. CurrBiol 17: 1061-1066


Fukuda H, Ohashi-Ito K (2019) Vascular tissue development in plants. Curr Top Dev Biol 131: 141-160Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vaten A, Lindgren O, De Rybel B, Van Isterdael G, Somervuo P,Lichtenberger R, Rocha R, Thitamadee S, Tahtiharju S, Auvinen P, Beeckman T, Jokitalo E, Helariutta Y (2014) Plant development.Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345: 933-937


Gutierrez-Alanis D, Yong-Villalobos L, Jimenez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, Mora-Macias J, Sanchez-RodriguezF, Cruz-Ramirez A, Herrera-Estrella L (2017) Phosphate starvation-dependent iron mobilization induces CLE14 expression to triggerroot meristem differentiation through CLV2/PEPR2 signaling. Dev Cell 41: 555-570 e553


Han S, Cho H, Noh J, Qi J, Jung HJ, Nam H, Lee S, Hwang D, Greb T, Hwang I (2018) BIL1-mediated MP phosphorylation integrates PXYand cytokinin signalling in secondary growth. Nat Plants 4: 605-614


Han SK, Torii KU (2016) Lineage-specific stem cells, signals and asymmetries during stomatal development. Development 143: 1259-1270


Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via asecretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50: 1019-1031


Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez-Villalon A, Hothorn M, Hardtke CS (2017) Perception of root-active CLE peptidesrequires CORYNE function in the phloem vasculature. EMBO Rep 18: 1367-1381


Hazak O, Hardtke CS (2016) CLAVATA 1-type receptors in plant development. J Exp Bot 67: 4827-4833Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Hirakawa Y, Bowman JL (2015) A role of TDIF peptide signaling in vascular cell differentiation is conserved among euphyllophytes.Front Plant Sci 6: 1048


Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox genein Arabidopsis. Plant Cell 22: 2618-2629


Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci U S A 105: 15208-15213


Hohmann U, Lau K, Hothorn M (2017) The structural basis of ligand perception and signal activation by receptor kinases. Annu RevPlant Biol 68: 109-137


Holzwart E, Huerta AI, Glockner N, Garnelo Gomez B, Wanke F, Augustin S, Askani JC, Schurholz AK, Harter K, Wolf S (2018) BRI1 www.plantphysiol.orgon July 27, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Etchells JP%2C Turner SR %282010%29 The PXY%2DCLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division%2E Development&dopt=abstract


https://scholar.google.com/scholar?as_q=The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Etchells&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Fiers M%2C Golemiec E%2C Xu J%2C van der Geest L%2C Heidstra R%2C Stiekema W%2C Liu CM %282005%29 The 14%2Damino acid CLV3%2C CLE19%2C and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2%2Ddependent pathway%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fiers&hl=en&c2coff=1


https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fiers&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Fisher K%2C Turner S %282007%29 PXY%2C a receptor%2Dlike kinase essential for maintaining polarity during plant vascular%2Dtissue development%2E Curr Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fisher&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fisher&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Fukuda H%2C Ohashi%2DIto K %282019%29 Vascular tissue development in plants%2E Curr Top Dev Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fukuda&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Vascular tissue development in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Vascular tissue development in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fukuda&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Furuta KM%2C Yadav SR%2C Lehesranta S%2C Belevich I%2C Miyashima S%2C Heo JO%2C Vaten A%2C Lindgren O%2C De Rybel B%2C Van Isterdael G%2C Somervuo P%2C Lichtenberger R%2C Rocha R%2C Thitamadee S%2C Tahtiharju S%2C Auvinen P%2C Beeckman T%2C Jokitalo E%2C Helariutta Y %282014%29 Plant development%2E Arabidopsis NAC45%2F86 direct sieve element morphogenesis culminating in enucleation%2E Science&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Furuta&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Plant development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Furuta&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Gutierrez%2DAlanis D%2C Yong%2DVillalobos L%2C Jimenez%2DSandoval P%2C Alatorre%2DCobos F%2C Oropeza%2DAburto A%2C Mora%2DMacias J%2C Sanchez%2DRodriguez F%2C Cruz%2DRamirez A%2C Herrera%2DEstrella L %282017%29 Phosphate starvation%2Ddependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2%2FPEPR2 signaling%2E Dev Cell 41%3A 555%2D570 e&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gutierrez-Alanis&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gutierrez-Alanis&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Han S%2C Cho H%2C Noh J%2C Qi J%2C Jung HJ%2C Nam H%2C Lee S%2C Hwang D%2C Greb T%2C Hwang I %282018%29 BIL1%2Dmediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth%2E Nat Plants&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Han&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Han&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Han SK%2C Torii KU %282016%29 Lineage%2Dspecific stem cells%2C signals and asymmetries during stomatal development%2E Development&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Han&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Lineage-specific stem cells, signals and asymmetries during stomatal development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Lineage-specific stem cells, signals and asymmetries during stomatal development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Han&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hara K%2C Yokoo T%2C Kajita R%2C Onishi T%2C Yahata S%2C Peterson KM%2C Torii KU%2C Kakimoto T %282009%29 Epidermal cell density is autoregulated via a secretory peptide%2C EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hara&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hara&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hazak O%2C Brandt B%2C Cattaneo P%2C Santiago J%2C Rodriguez%2DVillalon A%2C Hothorn M%2C Hardtke CS %282017%29 Perception of root%2Dactive CLE peptides requires CORYNE function in the phloem vasculature%2E EMBO Rep&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hazak&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Perception of root-active CLE peptides requires CORYNE function in the phloem vasculature&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Perception of root-active CLE peptides requires CORYNE function in the phloem vasculature&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hazak&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hazak O%2C Hardtke CS %282016%29 CLAVATA 1%2Dtype receptors in plant development%2E J Exp Bot&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hazak&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLAVATA 1-type receptors in plant development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLAVATA 1-type receptors in plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hazak&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hirakawa Y%2C Bowman JL %282015%29 A role of TDIF peptide signaling in vascular cell differentiation is conserved among euphyllophytes%2E Front Plant Sci&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hirakawa&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A role of TDIF peptide signaling in vascular cell differentiation is conserved among euphyllophytes.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A role of TDIF peptide signaling in vascular cell differentiation is conserved among euphyllophytes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hirakawa&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hirakawa Y%2C Kondo Y%2C Fukuda H %282010%29 TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis%2E Plant Cell&dopt=abstract


https://scholar.google.com/scholar?as_q=TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hirakawa&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hirakawa Y%2C Shinohara H%2C Kondo Y%2C Inoue A%2C Nakanomyo I%2C Ogawa M%2C Sawa S%2C Ohashi%2DIto K%2C Matsubayashi Y%2C Fukuda H %282008%29 Non%2Dcell%2Dautonomous control of vascular stem cell fate by a CLE peptide%2Freceptor system%2E Proc Natl Acad Sci U S A&dopt=abstract


https://scholar.google.com/scholar?as_q=Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hirakawa&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Hohmann U%2C Lau K%2C Hothorn M %282017%29 The structural basis of ligand perception and signal activation by receptor kinases%2E Annu Rev Plant Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hohmann&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The structural basis of ligand perception and signal activation by receptor kinases&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The structural basis of ligand perception and signal activation by receptor kinases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hohmann&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling. Proc Natl Acad Sci U S A 115: 11838-11843


Ikematsu S, Tasaka M, Torii KU, Uchida N (2017) ERECTA-family receptor kinase genes redundantly prevent premature progression ofsecondary growth in the Arabidopsis hypocotyl. New Phytol 213: 1697-1709


Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem celldifferentiation. Science 313: 842-845


Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability ofthe CLAVATA1 receptor-like kinase. Plant Cell 11: 1925-1934


Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, Meyerowitz EM, Feldman LJ, Fletcher JC (2010)Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154:1721-1736


Kang YH, Hardtke CS (2016) Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling. EMBO Rep 17: 1145-1154Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S (2007) Gain-of-function phenotypes of chemically syntheticCLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48: 1821-1825


Kondo Y, Fujita T, Sugiyama M, Fukuda H (2015) A novel system for xylem cell differentiation in Arabidopsis thaliana. Mol Plant 8: 612-621


Kondo Y, Hirakawa Y, Kieber JJ, Fukuda H (2011) CLE peptides can negatively regulate protoxylem vessel formation via cytokininsignaling. Plant Cell Physiol 52: 37-48


Kondo Y, Ito T, Nakagami H, Hirakawa Y, Saito M, Tamaki T, Shirasu K, Fukuda H (2014) Plant GSK3 proteins regulate xylem celldifferentiation downstream of TDIF-TDR signalling. Nat Commun 5: 3504


Kondo Y, Nurani AM, Saito C, Ichihashi Y, Saito M, Yamazaki K, Mitsuda N, Ohme-Takagi M, Fukuda H (2016) Vascular cell inductionculture system using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element-like cells. Plant Cell 28: 1250-1262


Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches forprotoxylem and metaxylem vessel formation. Genes Dev 19: 1855-1860


Kucukoglu M, Nilsson J, Zheng B, Chaabouni S, Nilsson O (2017) WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulatecambial cell division activity and secondary growth in Populus trees. New Phytol 215: 642-657


Lehmann F, Hardtke CS (2016) Secondary growth of the Arabidopsis hypocotyl-vascular development in dimensions. Curr Opin PlantBiol 29: 9-15


Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J,Yoshida A, Lopez-Millan AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J IntegrPlant Biol 55: 294-388


https://www.ncbi.nlm.nih.gov/pubmed?term=Holzwart E%2C Huerta AI%2C Glockner N%2C Garnelo Gomez B%2C Wanke F%2C Augustin S%2C Askani JC%2C Schurholz AK%2C Harter K%2C Wolf S %282018%29 BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling%2E Proc Natl Acad Sci U S A&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Holzwart&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Holzwart&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ikematsu S%2C Tasaka M%2C Torii KU%2C Uchida N %282017%29 ERECTA%2Dfamily receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl%2E New Phytol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ikematsu&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=ERECTA-family receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=ERECTA-family receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ikematsu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ito Y%2C Nakanomyo I%2C Motose H%2C Iwamoto K%2C Sawa S%2C Dohmae N%2C Fukuda H %282006%29 Dodeca%2DCLE peptides as suppressors of plant stem cell differentiation%2E Science&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ito&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Dodeca-CLE peptides as suppressors of plant stem cell differentiation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Dodeca-CLE peptides as suppressors of plant stem cell differentiation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ito&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Jeong S%2C Trotochaud AE%2C Clark SE %281999%29 The Arabidopsis CLAVATA2 gene encodes a receptor%2Dlike protein required for the stability of the CLAVATA1 receptor%2Dlike kinase%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jeong&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jeong&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Jun J%2C Fiume E%2C Roeder AH%2C Meng L%2C Sharma VK%2C Osmont KS%2C Baker C%2C Ha CM%2C Meyerowitz EM%2C Feldman LJ%2C Fletcher JC %282010%29 Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis%2E Plant Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jun&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jun&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kang YH%2C Hardtke CS %282016%29 Arabidopsis MAKR5 is a positive effector of BAM3%2Ddependent CLE45 signaling%2E EMBO Rep&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kinoshita A%2C Nakamura Y%2C Sasaki E%2C Kyozuka J%2C Fukuda H%2C Sawa S %282007%29 Gain%2Dof%2Dfunction phenotypes of chemically synthetic CLAVATA3%2FESR%2Drelated %28CLE%29 peptides in Arabidopsis thaliana and Oryza sativa%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kinoshita&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kinoshita&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kondo Y%2C Fujita T%2C Sugiyama M%2C Fukuda H %282015%29 A novel system for xylem cell differentiation in Arabidopsis thaliana%2E Mol Plant&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kondo&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A novel system for xylem cell differentiation in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A novel system for xylem cell differentiation in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kondo&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kondo Y%2C Hirakawa Y%2C Kieber JJ%2C Fukuda H %282011%29 CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling%2E Plant Cell Physiol&dopt=abstract


https://scholar.google.com/scholar?as_q=CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kondo&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kondo Y%2C Ito T%2C Nakagami H%2C Hirakawa Y%2C Saito M%2C Tamaki T%2C Shirasu K%2C Fukuda H %282014%29 Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF%2DTDR signalling%2E Nat Commun&dopt=abstract


https://scholar.google.com/scholar?as_q=Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kondo&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kondo Y%2C Nurani AM%2C Saito C%2C Ichihashi Y%2C Saito M%2C Yamazaki K%2C Mitsuda N%2C Ohme%2DTakagi M%2C Fukuda H %282016%29 Vascular cell induction culture system using Arabidopsis leaves %28VISUAL%29 reveals the sequential differentiation of sieve element%2Dlike cells%2E Plant Cell&dopt=abstract


https://scholar.google.com/scholar?as_q=Vascular cell induction culture system using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element-like cells&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Vascular cell induction culture system using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element-like cells&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kondo&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kubo M%2C Udagawa M%2C Nishikubo N%2C Horiguchi G%2C Yamaguchi M%2C Ito J%2C Mimura T%2C Fukuda H%2C Demura T %282005%29 Transcription switches for protoxylem and metaxylem vessel formation%2E Genes Dev&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kubo&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Transcription switches for protoxylem and metaxylem vessel formation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Transcription switches for protoxylem and metaxylem vessel formation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kubo&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Kucukoglu M%2C Nilsson J%2C Zheng B%2C Chaabouni S%2C Nilsson O %282017%29 WUSCHEL%2DRELATED HOMEOBOX4 %28WOX4%29%2Dlike genes regulate cambial cell division activity and secondary growth in Populus trees%2E New Phytol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kucukoglu&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulate cambial cell division activity and secondary growth in Populus trees&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulate cambial cell division activity and secondary growth in Populus trees&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kucukoglu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Lehmann F%2C Hardtke CS %282016%29 Secondary growth of the Arabidopsis hypocotyl%2Dvascular development in dimensions%2E Curr Opin Plant Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lehmann&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Secondary growth of the Arabidopsis hypocotyl-vascular development in dimensions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Secondary growth of the Arabidopsis hypocotyl-vascular development in dimensions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lehmann&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1



Matsubayashi Y (2011) Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book 9: e0150Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone,phytosulfokine. Science 296: 1470-1472


Meng L, Feldman LJ (2010) CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibitcell division in the root meristem of Arabidopsis. Planta 232: 1061-1074


Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The receptor-like kinase SOL2 mediates CLE signaling inArabidopsis. Plant Cell Physiol 49: 1752-1757


Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo JO, Mellor N, Help-Rinta-Rahko H, Otero S, Smet W, Boekschoten M,Hooiveld G, Hashimoto K, Smetana O, Siligato R, Wallner ES, Mahonen AP, Kondo Y, Melnyk CW, Greb T, Nakajima K, Sozzani R,Bishopp A, De Rybel B, Helariutta Y (2019) Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature565: 490-494


Morita J, Kato K, Nakane T, Kondo Y, Fukuda H, Nishimasu H, Ishitani R, Nureki O (2016) Crystal structure of the plant receptor-likekinase TDR in complex with the TDIF peptide. Nat Commun 7: 12383


Mou S, Zhang X, Han Z, Wang J, Gong X, Chai J (2017) CLE42 binding induces PXL2 interaction with SERK2. Protein Cell 8: 612-617Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Muller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3independently of CLAVATA1. Plant Cell 20: 934-946


Ohashi-Ito K, Saegusa M, Iwamoto K, Oda Y, Katayama H, Kojima M, Sakakibara H, Fukuda H (2014) A bHLH complex activates vascularcell division via cytokinin action in root apical meristem. Curr Biol 24: 2053-2058


Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana.Nature Chem Biol 5: 578−580


Qian P, Song W, Yokoo T, Minobe A, Wang G, Ishida T, Sawa S, Chai J, Kakimoto T (2018) The CLE9/10 secretory peptide regulatesstomatal and vascular development through distinct receptors. Nat Plants 4: 1071-1081


Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulatesArabidopsis hypocotyl xylem expansion. Plant Cell 23: 1322-1336


Ren SC, Song XF, Chen WQ, Lu R, Lucas WJ, Liu CM (2019) CLE25 peptide regulates phloem initiation in Arabidopsis through aCLERK-CLV2 receptor complex. J Integr Plant Biol 61: 1043-1061


Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P, Depuydt S, Hardtke CS (2014) Molecular genetic framework forprotophloem formation. Proc Natl Acad Sci U S A 111: 11551-11556


Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS (2015) Primary root protophloem differentiation requires balancedphosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development 142: 1437-1446 www.plantphysiol.orgon July 27, 2020 - Published by Downloaded from

Copyright © 2019 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Lucas WJ%2C Groover A%2C Lichtenberger R%2C Furuta K%2C Yadav SR%2C Helariutta Y%2C He XQ%2C Fukuda H%2C Kang J%2C Brady SM%2C Patrick JW%2C Sperry J%2C Yoshida A%2C Lopez%2DMillan AF%2C Grusak MA%2C Kachroo P %282013%29 The plant vascular system%3A evolution%2C development and functions%2E J Integr Plant Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lucas&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The plant vascular system: evolution, development and functions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The plant vascular system: evolution, development and functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lucas&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Matsubayashi Y %282011%29 Small post%2Dtranslationally modified peptide signals in Arabidopsis%2E Arabidopsis Book 9%3A e&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Matsubayashi&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Small post-translationally modified peptide signals in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Small post-translationally modified peptide signals in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matsubayashi&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Matsubayashi Y%2C Ogawa M%2C Morita A%2C Sakagami Y %282002%29 An LRR receptor kinase involved in perception of a peptide plant hormone%2C phytosulfokine%2E Science&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Matsubayashi&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matsubayashi&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Meng L%2C Feldman LJ %282010%29 CLE14%2FCLE20 peptides may interact with CLAVATA2%2FCORYNE receptor%2Dlike kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis%2E Planta&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Meng&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Meng&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Miwa H%2C Betsuyaku S%2C Iwamoto K%2C Kinoshita A%2C Fukuda H%2C Sawa S %282008%29 The receptor%2Dlike kinase SOL2 mediates CLE signaling in Arabidopsis%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Miwa&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Miwa&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Miyashima S%2C Roszak P%2C Sevilem I%2C Toyokura K%2C Blob B%2C Heo JO%2C Mellor N%2C Help%2DRinta%2DRahko H%2C Otero S%2C Smet W%2C Boekschoten M%2C Hooiveld G%2C Hashimoto K%2C Smetana O%2C Siligato R%2C Wallner ES%2C Mahonen AP%2C Kondo Y%2C Melnyk CW%2C Greb T%2C Nakajima K%2C Sozzani R%2C Bishopp A%2C De Rybel B%2C Helariutta Y %282019%29 Mobile PEAR transcription factors integrate positional cues to prime cambial growth%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Miyashima&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Mobile PEAR transcription factors integrate positional cues to prime cambial growth&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Mobile PEAR transcription factors integrate positional cues to prime cambial growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Miyashima&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Morita J%2C Kato K%2C Nakane T%2C Kondo Y%2C Fukuda H%2C Nishimasu H%2C Ishitani R%2C Nureki O %282016%29 Crystal structure of the plant receptor%2Dlike kinase TDR in complex with the TDIF peptide%2E Nat Commun&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Morita&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Crystal structure of the plant receptor-like kinase TDR in complex with the TDIF peptide.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Crystal structure of the plant receptor-like kinase TDR in complex with the TDIF peptide.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morita&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Mou S%2C Zhang X%2C Han Z%2C Wang J%2C Gong X%2C Chai J %282017%29 CLE42 binding induces PXL2 interaction with SERK2%2E Protein Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mou&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLE42 binding induces PXL2 interaction with SERK2&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLE42 binding induces PXL2 interaction with SERK2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mou&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Muller R%2C Bleckmann A%2C Simon R %282008%29 The receptor kinase CORYNE of Arabidopsis transmits the stem cell%2Dlimiting signal CLAVATA3 independently of CLAVATA1%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Muller&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Muller&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ohashi%2DIto K%2C Saegusa M%2C Iwamoto K%2C Oda Y%2C Katayama H%2C Kojima M%2C Sakakibara H%2C Fukuda H %282014%29 A bHLH complex activates vascular cell division via cytokinin action in root apical meristem%2E Curr Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ohashi-Ito&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A bHLH complex activates vascular cell division via cytokinin action in root apical meristem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A bHLH complex activates vascular cell division via cytokinin action in root apical meristem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ohashi-Ito&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ohyama K%2C Shinohara H%2C Ogawa%2DOhnishi M%2C Matsubayashi Y %282009%29 A glycopeptide regulating stem cell fate in Arabidopsis thaliana%2E Nature Chem Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ohyama&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A glycopeptide regulating stem cell fate in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A glycopeptide regulating stem cell fate in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ohyama&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Qian P%2C Song W%2C Yokoo T%2C Minobe A%2C Wang G%2C Ishida T%2C Sawa S%2C Chai J%2C Kakimoto T %282018%29 The CLE9%2F10 secretory peptide regulates stomatal and vascular development through distinct receptors%2E Nat Plants&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Qian&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Qian&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ragni L%2C Nieminen K%2C Pacheco%2DVillalobos D%2C Sibout R%2C Schwechheimer C%2C Hardtke CS %282011%29 Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ragni&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ragni&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ren SC%2C Song XF%2C Chen WQ%2C Lu R%2C Lucas WJ%2C Liu CM %282019%29 CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK%2DCLV2 receptor complex%2E J Integr Plant Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ren&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ren&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Rodriguez%2DVillalon A%2C Gujas B%2C Kang YH%2C Breda AS%2C Cattaneo P%2C Depuydt S%2C Hardtke CS %282014%29 Molecular genetic framework for protophloem formation%2E Proc Natl Acad Sci U S A&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rodriguez-Villalon&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Molecular genetic framework for protophloem formation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Molecular genetic framework for protophloem formation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rodriguez-Villalon&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1



Saito M, Kondo Y, Fukuda H (2018) BES1 and BZR1 redundantly promote phloem and xylem differentiation. Plant Cell Physiol 59: 590-600


Sankar M, Nieminen K, Ragni L, Xenarios I, Hardtke CS (2014) Automated quantitative histology reveals vascular morphodynamicsduring Arabidopsis hypocotyl secondary growth. Elife 3: e01567


Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controlsembryonic root initiation by regulating a mobile transcription factor. Nature 464: 913-916


Shi D, Lebovka I, Lopez-Salmeron V, Sanchez P, Greb T (2019) Bifacial cambium stem cells generate xylem and phloem during radialplant growth. Development 146: dev171355


Shinohara H, Matsubayashi Y (2013) Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyprolinearabinosylation on peptide conformation and activity. Plant Cell Physiol 54: 369-374


Smet W, Sevilem I, de Luis Balaguer MA, Wybouw B, Mor E, Miyashima S, Blob B, Roszak P, Jacobs TB, Boekschoten M, Hooiveld G,Sozzani R, Helariutta Y, De Rybel B (2019) DOF2.1 controls cytokinin-dependent vascular cell proliferation downstream of TMO5/LHW.Curr Biol 29: 520-529.e526


Smetana O, Mäkilä R, Lyu M, Amiryousefi A, Rodríguez FS, Wu M-F, Solé-Gil A, Gavarrón ML, Siligato R, Miyashima S, Roszak P,Blomster T, Reed JW, Broholm S, Mähönen AP (2019) High levels of auxin signalling define the stem-cell organizer of the vascularcambium Nature 565: 433-435


Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell23: 3247-3259


Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K (2018) A smallpeptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556: 235-238


Tameshige T, Ikematsu S, Torii KU, Uchida N (2017) Stem development through vascular tissues: EPFL-ERECTA family signaling thatbounces in and out of phloem. J Exp Bot 68: 45-53


Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylemdevelopment in hybrid aspen. Plant Physiol 115: 577-585


Uchida N, Tasaka M (2013) Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases. J Exp Bot 64: 5335-5343


Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015) Allosteric receptor activation by the plant peptidehormone phytosulfokine. Nature 525: 265-268


Wang N, Bagdassarian KS, Doherty RE, Kroon JT, Connor KA, Wang XY, Wang W, Jermyn IH, Turner SR, Etchells JP (2019) Organ-specific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsisvascular tissue. Development 146: dev177105

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon July 27, 2020 - Published by Downloaded from

Copyright © 2019 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Rodriguez%2DVillalon A%2C Gujas B%2C van Wijk R%2C Munnik T%2C Hardtke CS %282015%29 Primary root protophloem differentiation requires balanced phosphatidylinositol%2D4%2C5%2Dbiphosphate levels and systemically affects root branching%2E Development&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rodriguez-Villalon&hl=en&c2coff=1


https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rodriguez-Villalon&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Saito M%2C Kondo Y%2C Fukuda H %282018%29 BES1 and BZR1 redundantly promote phloem and xylem differentiation%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Saito&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=BES1 and BZR1 redundantly promote phloem and xylem differentiation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=BES1 and BZR1 redundantly promote phloem and xylem differentiation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Saito&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Sankar M%2C Nieminen K%2C Ragni L%2C Xenarios I%2C Hardtke CS %282014%29 Automated quantitative histology reveals vascular morphodynamics during Arabidopsis hypocotyl secondary growth%2E Elife 3%3A e&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sankar&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Automated quantitative histology reveals vascular morphodynamics during Arabidopsis hypocotyl secondary growth.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Automated quantitative histology reveals vascular morphodynamics during Arabidopsis hypocotyl secondary growth.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sankar&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Schlereth A%2C Moller B%2C Liu W%2C Kientz M%2C Flipse J%2C Rademacher EH%2C Schmid M%2C Jurgens G%2C Weijers D %282010%29 MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schlereth&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schlereth&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Shi D%2C Lebovka I%2C Lopez%2DSalmeron V%2C Sanchez P%2C Greb T %282019%29 Bifacial cambium stem cells generate xylem and phloem during radial plant growth%2E Development 146%3A dev&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Shi&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Bifacial cambium stem cells generate xylem and phloem during radial plant growth.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Bifacial cambium stem cells generate xylem and phloem during radial plant growth.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shi&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Shinohara H%2C Matsubayashi Y %282013%29 Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Shinohara&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shinohara&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Smet W%2C Sevilem I%2C de Luis Balaguer MA%2C Wybouw B%2C Mor E%2C Miyashima S%2C Blob B%2C Roszak P%2C Jacobs TB%2C Boekschoten M%2C Hooiveld G%2C Sozzani R%2C Helariutta Y%2C De Rybel B %282019%29 DOF2%2E1 controls cytokinin%2Ddependent vascular cell proliferation downstream of TMO5%2FLHW%2E Curr Biol 29%3A 520%2D529%2Ee&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Smet&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=DOF2&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=DOF2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smet&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Smetana O%2C M�kil� R%2C Lyu M%2C Amiryousefi A%2C Rodr�guez FS%2C Wu M%2DF%2C Sol�%2DGil A%2C Gavarr�n ML%2C Siligato R%2C Miyashima S%2C Roszak P%2C Blomster T%2C Reed JW%2C Broholm S%2C M�h�nen AP %282019%29 High levels of auxin signalling define the stem%2Dcell organizer of the vascular cambium Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Smetana&hl=en&c2coff=1


https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smetana&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Suer S%2C Agusti J%2C Sanchez P%2C Schwarz M%2C Greb T %282011%29 WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis%2E Plant Cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Suer&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suer&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Takahashi F%2C Suzuki T%2C Osakabe Y%2C Betsuyaku S%2C Kondo Y%2C Dohmae N%2C Fukuda H%2C Yamaguchi%2DShinozaki K%2C Shinozaki K %282018%29 A small peptide modulates stomatal control via abscisic acid in long%2Ddistance signalling%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Takahashi&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A small peptide modulates stomatal control via abscisic acid in long-distance signalling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A small peptide modulates stomatal control via abscisic acid in long-distance signalling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Takahashi&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Tameshige T%2C Ikematsu S%2C Torii KU%2C Uchida N %282017%29 Stem development through vascular tissues%3A EPFL%2DERECTA family signaling that bounces in and out of phloem%2E J Exp Bot&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tameshige&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Stem development through vascular tissues: EPFL-ERECTA family signaling that bounces in and out of phloem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Stem development through vascular tissues: EPFL-ERECTA family signaling that bounces in and out of phloem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tameshige&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Tuominen H%2C Puech L%2C Fink S%2C Sundberg B %281997%29 A radial concentration gradient of indole%2D3%2Dacetic acid is related to secondary xylem development in hybrid aspen%2E Plant Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tuominen&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tuominen&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Uchida N%2C Tasaka M %282013%29 Regulation of plant vascular stem cells by endodermis%2Dderived EPFL%2Dfamily peptide hormones and phloem%2Dexpressed ERECTA%2Dfamily receptor kinases%2E J Exp Bot&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Uchida&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Uchida&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang J%2C Li H%2C Han Z%2C Zhang H%2C Wang T%2C Lin G%2C Chang J%2C Yang W%2C Chai J %282015%29 Allosteric receptor activation by the plant peptide hormone phytosulfokine%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Allosteric receptor activation by the plant peptide hormone phytosulfokine&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Allosteric receptor activation by the plant peptide hormone phytosulfokine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang N%2C Bagdassarian KS%2C Doherty RE%2C Kroon JT%2C Connor KA%2C Wang XY%2C Wang W%2C Jermyn IH%2C Turner SR%2C Etchells JP %282019%29 Organ%2Dspecific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsis vascular tissue%2E Development 146%3A dev&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Organ-specific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsis vascular tissue.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Organ-specific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsis vascular tissue.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1


Yamaguchi YL, Ishida T, Sawa S (2016) CLE peptides and their signaling pathways in plant development. J Exp Bot 67: 4813–4826Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Yamamoto R, Fujioka S, Demura T, Takatsuto S, Yoshida S, Fukuda H (2001) Brassinosteroid levels increase drastically prior tomorphogenesis of tracheary elements. Plant Physiol 125: 556-563


Yamamoto R, Fujioka S, Iwamoto K, Demura T, Takatsuto S, Yoshida S, Fukuda H (2007) Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation. Plant Cell Physiol 48: 74-83


Zhang H, Lin X, Han Z, Qu LJ, Chai J (2016a) Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanismamong CLE peptide-receptor pairs. Cell Res 26: 543-555


Zhang H, Lin X, Han Z, Wang J, Qu LJ, Chai J (2016b) SERK family receptor-like kinases function as co-receptors with PXY for plantvascular development. Mol Plant 9: 1406-1414


Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2015) Control of plant stem cellfunction by conserved interacting transcriptional regulators. Nature 517: 377-380


Zhu Y, Song D, Zhang, R, Luo, L, Cao, S, Huang, C, Sun J, Gui J, Li L (2019) A xylem-produced peptide PtrCLE20 inhibits vascularcambium activity in Populus. Plant Biotechnol J: doi: 10.1111/pbi.13187



https://www.ncbi.nlm.nih.gov/pubmed?term=Yamaguchi YL%2C Ishida T%2C Sawa S %282016%29 CLE peptides and their signaling pathways in plant development%2E J Exp Bot 67%3A 4813%26%23x&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yamaguchi&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=CLE peptides and their signaling pathways in plant development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=CLE peptides and their signaling pathways in plant development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamaguchi&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yamamoto R%2C Fujioka S%2C Demura T%2C Takatsuto S%2C Yoshida S%2C Fukuda H %282001%29 Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements%2E Plant Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yamamoto&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamamoto&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yamamoto R%2C Fujioka S%2C Iwamoto K%2C Demura T%2C Takatsuto S%2C Yoshida S%2C Fukuda H %282007%29 Co%2Dregulation of brassinosteroid biosynthesis%2Drelated genes during xylem cell differentiation%2E Plant Cell Physiol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yamamoto&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamamoto&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang H%2C Lin X%2C Han Z%2C Qu LJ%2C Chai J %282016a%29 Crystal structure of PXY%2DTDIF complex reveals a conserved recognition mechanism among CLE peptide%2Dreceptor pairs%2E Cell Res&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang H%2C Lin X%2C Han Z%2C Wang J%2C Qu LJ%2C Chai J %282016b%29 SERK family receptor%2Dlike kinases function as co%2Dreceptors with PXY for plant vascular development%2E Mol Plant&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=SERK family receptor-like kinases function as co-receptors with PXY for plant vascular development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=SERK family receptor-like kinases function as co-receptors with PXY for plant vascular development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou Y%2C Liu X%2C Engstrom EM%2C Nimchuk ZL%2C Pruneda%2DPaz JL%2C Tarr PT%2C Yan A%2C Kay SA%2C Meyerowitz EM %282015%29 Control of plant stem cell function by conserved interacting transcriptional regulators%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhou&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Control of plant stem cell function by conserved interacting transcriptional regulators&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Control of plant stem cell function by conserved interacting transcriptional regulators&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhu Y%2C Song D%2C Zhang%2C R%2C Luo%2C L%2C Cao%2C S%2C Huang%2C C%2C Sun J%2C Gui J%2C Li L %282019%29 A xylem%2Dproduced peptide PtrCLE20 inhibits vascular cambium activity in Populus%2E Plant Biotechnol J%3A doi%3A 10%2E1111%2Fpbi&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhu&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in Populus.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in Populus.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1


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