1 Short Title: Virus-induced Flowering (VIF) Assay 3 …...2017/04/11 · 87 molecular pharming...

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Short Title: Virus-induced Flowering (VIF) Assay 1

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Corresponding Author: Yiguo Hong 3

Research Centre for Plant RNA Signaling, College of Life and Environmental Sciences, 4

Hangzhou Normal University, Hangzhou 310036, China and Warwick-Hangzhou RNA 5

Signaling Joint Laboratory, School of Life Sciences, University of Warwick, Coventry 6

CV4 7AL, UK. 7

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Telephone: +86-571-28866065 9

Fax: +86-571-28866065 10

E-mails: [email protected]; [email protected] 11

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Primary Research Area: Flowering and Reproduction/Breakthrough Technologies 13

2nd Research Area: Genes and Development 14

Plant Physiology Preview. Published on April 11, 2017, as DOI:10.1104/pp.17.00392

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon June 10, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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Article Title: A Virus-induced Assay for Functional Dissection and Analysis of Monocot 15

and Dicot Flowering Time Genes1 16

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Cheng Qin2, Weiwei Chen2, Jiajia Shen, Linming Cheng, Femi Akande, Ke Zhang, 18

Chen Yuan, Chunyang Li, Pengcheng Zhang, Nongnong Shi, Qi Cheng, Yule Liu, 19

Stephen Jackson, Yiguo Hong* 20

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Research Centre for Plant RNA Signaling, College of Life and Environmental Sciences, 22

Hangzhou Normal University, Hangzhou 310036, China (C.Q., W.C., J-J.S., L.C., K.Z., 23

C.Y., P.Z., N.S., Y.H.); Biotechnology Research Institute, Chinese Academy of 24

Agricultural Sciences, Beijing 100081, China (Q.C.); Centre for Plant Biology and 25

MOE Key Laboratory of Bioinformatics, School of Life Sciences, Tsinghua University, 26

Beijing 100084, China (Y.L.); Warwick-Hangzhou RNA Signaling Joint Laboratory, 27

School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK (F.A, C.L., 28

S.J., Y.H.) 29

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1Funding: This work was supported by grants from the Ministry of Agriculture of 31

China (National Transgenic Program 2016ZX08009-001-004 to Y.H.); the National 32

Natural Science Foundation of China (NSFC 31370180 to Y.H., 31500251 to C.Q., 33

31601765 to W.C.); Hangzhou Normal University (Pandeng Program 201108 to Y.H.); 34

the Hangzhou City Education Bureau (Innovative Program for Science Excellence 35

20131028 to Y.H.); the UK Biotechnology & Biological Sciences Research Council 36

(UK BBSRC–China Partnering Award BB/K021079/1 to S.J. and Y.H.); and the 37

Zhejiang Provincial Natural Science Foundation (LY14C010005 to N.S.). 38

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2These authors contributed equally to this work. 40

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Author Contributions: C.Q. and W.C. designed and performed experiments; J-J.S., 42

L.C., F.A., K.Z., C.Y., C.L. and P.Z. performed research; C.Q., N.S., Q.C., Y.L. and S.J. 43

were involved in the analysis of data and helped writing the paper. S.J. was also 44



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involved in designing experiments. Y.H. conceived and initiated the project, designed 45

experiments, analysed data and wrote the paper. 46

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One-sentence Summary: A PVX-based VIF assay was designed in order to identify 48

amino acids in the FT protein that are essential for flowering, and to examine floral 49

induction by mono- and dicotyledonous FT genes. 50

51 *Address correspondence to [email protected]; [email protected] 52

The author responsible for distribution of materials integral to the findings presented in 53

this article in accordance with the policy described in the instructions for Authors 54

(www.plantphysioll.org) is: Yiguo Hong ([email protected], 55

[email protected]). 56



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ABSTRACT 57

Virus-induced flowering (VIF) uses virus vectors to express Flowering Locus T (FT) to 58

induce flowering in plants. This approach has recently attracted wide interest for its 59

practical applications in accelerating breeding in crops and woody fruit-trees. However, 60

the insight into VIF and its potential as a powerful tool for dissecting florigenic proteins 61

remained to be elucidated. Here, we describe the mechanism and further applications of 62

Potato virus X (PVX)-based VIF in the short-day Nicotinana tabacum cultivar 63

Maryland Mammoth. Ectopic delivery of Arabidopsis AtFT by PVX/AtFT did not 64

induce the expression of the endogenous FT orthologue NtFT4, however it was 65

sufficient to trigger flowering in Maryland Mammoth plants grown under non-inductive 66

long-day conditions. Infected tobacco plants developed no systemic symptoms and the 67

PVX-based VIF did not cause transgenerational flowering. We showed that the 68

PVX-based VIF is a much more rapid method to examine the impacts of single 69

amino-acid mutations on AtFT for floral induction than making individual transgenic 70

Arabidopsis lines for each mutation. We also used the PVX-based VIF to demonstrate 71

that adding a histidine- or FLAG-tag to the N- or C-terminal of AtFT could affect its 72

florigenic activity, and that this system can be applied to assay the function of FT genes 73

from heterologous species including tomato SFT and rice Hd3a. Thus the PVX-based 74

VIF represents a simple and efficient system to identify individual amino acids that are 75

essential for FT-mediated floral induction, and to test the ability of mono- and 76

dicotyledonous FT genes and FT fusion proteins to induce flowering. 77

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Keywords: PVX; Virus-induced flowering; Arabidopsis FT; Nicotiana tabacum 79

Maryland Mammoth; rice Hd3a; tomato SFT80



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INTRODUCTION 81

Modified plant viruses have emerged as powerful tools for dissecting gene function in 82

plants. Such plant virus-based technology can be applied to facilitate or impede gene 83

expression, resulting in gain- or loss-of-function phenotypes. Although virus-based 84

technology was initially exploited for the purpose of high-level production of foreign 85

proteins such as recombinant subunit vaccines and pharmaceutical proteins for 86

molecular pharming (Scholthof et al., 1996; Porta and Lomonossoff, 2002), plant RNA 87

and DNA virus-based techniques such as small interfering RNA-mediated virus-induced 88

posttranscriptional gene silencing (VIGS) has been extensively utilized to silence genes 89

for functional genomic studies in dicots and monocots, including plants and crops 90

recalcitrant to classical forward or reverse genetic manipulation (Lindbo et al., 1993; 91

Kumagai et al., 1995; Ruiz et al., 1998; Liu et al., 2002; Becker and Lange, 2009; 92

Senthil-Kumar and Mysore, 2011; Qin et al., 2015; Liu et al., 2016). Various 93

virus-based technologies have been developed such as VIGS, microRNA-based VIGS 94

(Tang et al., 2010; Chen et al., 2014; Chen et al., 2015), virus-based microRNA 95

silencing (Sha et al., 2014), and virus-induced transcriptional gene silencing (Kanazawa 96

et al., 2011; Chen et al., 2015). More recently, virus-induced genome editing has been 97

employed to introduce mutations to specific genes and produce null mutants in plants 98

(Baltes et al., 2014; Ali et al., 2015; Yin et al., 2015). Apart from these gene 99

knock-down or knock-out techniques, virus expression vectors have become a valuable 100

tool to examine the mobility of cellular RNAs and the role of mobile RNA signals in 101

flowering (Li et al., 2009; 2011), potato tuberization (Cho et al., 2015) and RNA 102

silencing (Ryabov et al., 2004; Zhou et al., 2008; Qin et al., 2012). 103

Virus-based technology is also a useful means to transiently express endogenous 104

or exogenous genes for functional analysis in plant development and growth, plant 105

response to biotic stresses and viral DNA replication (Hong et al., 1997; Van Wezel et 106

al., 2002; Hong et al., 2003). For instance, expression of the tomato homeobox protein 107

LeHB1 from a Potato virus X (PVX) vector converts floral organs into fruit-like 108

structures, revealing a new function of LeHB1 in floral organogenesis in addition to its 109



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role in fruit ripening (Lin et al., 2008). Moreover in tomato rin and Cnr mutants, viral 110

expression of the MADS- or SBP-box transcription factor LeMADS-RIN or 111

LeSPL-CNR leads to virus-induced gene complementation and causes non-ripening 112

mutant fruits to ripen (Zhou et al., 2012; Kong et al., 2013). Another example is the use 113

of virus technology to study the roles of proteins and RNAs in the flowering process (Li 114

et al., 2011; McGarry et al., 2017). 115

Flowering is induced by florigen, an endogenous signal whose production 116

responds to environmental cues such as day length (Garner and Allard, 1922; 117

Chailakhyan, 1936; Srikanth and Schmid, 2011). In Arabidopsis thaliana, the major 118

component of florigen is a protein encoded by Flowering Locus T (AtFT; Koornneef et 119

al., 1991; Kardailsky et al., 1999; Kobayashi et al., 1999; Turck et al., 2008; Pin and 120

Nilsson, 2012). Many AtFT orthologues have been isolated from other species, for 121

instance, rice Hd3a, tomato SFT, tobacco NtFT4 and sugar beet BvFT2, and transgenic 122

over-expression of these genes results in early flowering (Kojima et al., 2002; Lifschitz 123

et al., 2006; Pin et al., 2010; Harig et al., 2012). Instead of generating transgenic plants, 124

virus-based technique has also been used as a more rapid method to demonstrate the 125

florigenic activity of FT proteins and RNA. Ectopic expression of FT proteins by 126

Zucchini yellow mosaic virus (ZYMV) induces early flowering in cucurbits (Lin et al., 127

2007; Yoo et al., 2013). FT protein or mRNA introduced by PVX promotes flowering in 128

short-day (SD) Nicotiana tabacum Maryland Mammoth (MM) under non-inductive (i.e. 129

non-flowering) long-day (LD) conditions (Li et al., 2009; 2011). These findings open up 130

possibilities for further development and application of the virus-induced flowering 131

(VIF) assay in plants (McGarry et al., 2017). Since then, several RNA and DNA viruses 132

including Apple latent spherical virus (ALSV), Cotton leaf crumple virus (CLCrV), and 133

Citrus leaf blotch virus (CLBV) have been engineered to express FT for floral induction 134

in soybean, apple, pear, gentian and lisianthus plants (Yamagishi and Yoshikawa, 2011; 135

Yamagishi et al., 2011; 2014; 2016; Fekih et al., 2016), cotton (McGarry and Ayre, 2012; 136

McGarry et al., 2016) and citrus (Velazquez et al., 2016). These latest developments 137

have generated broad interest in the application of VIF for the benefit of crop breeding 138

(McGarry et al., 2017). 139



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Whilst AtFT is involved in floral induction in Arabidopsis, a closely related gene 140

TERMINAL FLOWER1 (AtTFL1) encodes a flowering inhibitor. Exchange of a single 141

amino acid leads to functional conversion of AtFT (Y85H) to AtTFL1 (H88Y) and vice 142

versa (Hanzawa et al., 2005). This raises an intriguing question about how and to what 143

extent each individual amino acid residue contributes to AtFT functionality. A recent 144

elegant study through PCR-based random mutagenesis coupled with large-scale 145

Arabidopsis transformation identified 33 unique mutations that influence AtFT activity 146

among approximately 36,000 mutated AtFT alleles. Specific point mutations of E109, 147

Y138, Q140, or N152 can convert AtFT into a TFL1-like floral repressor (Ho and 148

Weigel, 2014). Nonetheless, this is a very time-consuming approach, whereas VIF 149

offers the potential of an alternate rapid, efficient and less labor-intensive flowering 150

assay to evaluate the influence of each amino acid residue, as well as the effect of 151

epitope tags on florigenic activity. 152

In this article, we describe further characterization and development of the 153

PVX-based VIF approach to assess FT protein function. Expression of Arabidopsis 154

AtFT by PVX/AtFT led to no increase in the levels of endogenous NtFT4 mRNA, but it 155

was sufficient to cause floral induction in MM tobacco in LD. Using the PVX-based 156

VIF, we were able to demonstrate in various approaches to (1) study the impact of 157

single amino-acid mutations on the floral inducing function of the AtFT protein; (2) 158

investigate the influence of histidine or FLAG tags on the AtFT activity; and (3) assess 159

the function of tomato SFT and rice Hd3a to induce flowering in MM tobacco under 160

non-inductive conditions within a matter of weeks. Thus, this PVX-based VIF 161

represents an efficient system for the functional analysis of proteins such as mono- and 162

dicotyledonous FT and FT-like genes that are involved in flowering. 163

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RESULTS 166

PVX-based VIF 167

We have previously described the development of the PVX-based VIF assay in SD MM 168

tobacco plants (Li et al., 2009), it involves three main steps. Firstly, the FT (or any 169

flowering gene) expression cassette needs to be cloned into the modified PVX-based 170

gene expression vector (van Wezel et al., 2002), and verified by sequencing. Secondly, 171

recombinant infectious PVX transcripts containing the FT or flowering gene mRNA are 172

produced by in vitro transcription from the vector’s T7 promoter using a commercially 173

available kit, or self-assembled reaction mixtures, as described (van Wezel et al., 2002). 174

Thirdly, SD MM tobacco plants at the 4-6 leaf stage were mechanically inoculated with 175

the in vitro transcribed infectious PVX RNA. Plants are grown under non-inducing 16h 176

LD (or inducing 8h SD) conditions and monitored for floral induction (Li et al., 2009). 177

In this paper we further characterized the PVX-based VIF by looking at the 178

effect of virally-expressed AtFT on the level of endogenous NtFT4 gene expression, and 179

also at whether the PVX or virally expressed AtFT RNA is seed transmissible. We then 180

used this VIF in three different approaches to evaluate the influence of individual amino 181

acids on AtFT activity, the impact of polypeptide tags on AtFT function, and the roles of 182

monocot and dicot FT genes in flowering. 183

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Viral delivery of AtFT induces flowering but no increase in endogenous NtFT4 185

expression in MM tobacco under non-inductive conditions 186

To investigate the mechanism through which VIF works, we analysed the temporal 187

expression profiles of the four known day-neutral tobacco FT-like genes NtFT1, NtFT2, 188

NtFT3 and NtFT4 (Harig et al., 2012) in MM plants grown in SD (Fig. 1). Under SD of 189

8 h light/16 h dark (i.e. florally inductive conditions for MM tobacco), the plants bolted 190

after 8 weeks and started to flower at 12 weeks after seed sowing (WASS), however, no 191

bolting or flowering occurred when plants grown under non-inductive LD conditions 192

(16 h light/8 h dark; Fig. 1A). The relative expression levels of NtFT1 and NtFT2 were 193

low until 16 WASS when flowers were already formed (Fig. 1A). The levels of NtFT3 194



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expression were consistently too low to be reliably quantified by qRT-PCR. 195

In contrast, NtFT4 was induced and its expression was high at 8 WASS, i.e. 196

around the time bolting was initiated. From 10 WASS onwards the expression of NtFT4 197

fell and was maintained at a constant level that was relatively higher than the other 198

NbFTs until they increased at 16 WASS (Fig. 1A). Consistent with the fact that NtFT4 is 199

known to be the true AtFT orthologue in day-neutral tobacco (Harig et al., 2012), viral 200

expression of NtFT4 from PVX/NtFT4 in MM plants was able to induce flowering 201



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under non-inductive LD (Fig. 1B; Fig. S1, Table S1). Control mock-inoculated tobacco 202

and those plants infected with PVX/mNtFT4 containing a mutated non-translatable 203

NtFT4 mRNA did not flower (Fig. 1B and C; Fig. S1). Viral expression of wild-type or 204

non-sense mutated NtFT4 in systemic tobacco leaf tissues was detected by RT-PCR and 205

verified by direct sequencing (Fig. 1C; Table S1). These data confirm that as in 206

day-neutral N. tabacum, NtFT4 also promotes flowering in short-day MM tobacco. 207

We previously showed that PVX-based expression of AtFT induces flowering in 208

tobacco (Li et al., 2009; 2011). However, as the expression of the plant’s own 209

endogenous FT gene(s) is still possible, the induction of flowering could either be a 210

direct effect of the virally expressed FT gene or caused by an indirect induction of the 211

expression of the endogenous FT gene. Such lack of understanding of the virus-induced 212

flowering mechanism is also true for other published VIF systems (McGarry et al., 213

2017). To address this, we performed time-course experiments in PVX/AtFT infected 214

tobacco plants and examined the expression levels of AtFT and of the endogenous 215

NbFT4 gene to investigate how they correlated with the flowering response (Fig. 2). 216

Plants at 4 WASS (4–6 leaves) were mock-inoculated or inoculated with PVX/AtFT or 217

PVX/mAtFT (Fig. S1A). As shown in Fig 2A, under LD conditions, endogenous NtFT4 218

was not induced in MM plants either before inoculation (WASS 1-4), or after mock 219

inoculation, or inoculation with PVX/AtFT (WASS 5-9). However, wild-type or mutant 220

AtFT mRNA was readily detected by qRT-PCR in viral infected plants at 5 WASS, i.e. 1 221

week post-inoculation (WPI; Fig. 2B), and verified by direct sequencing (Fig. 1C). The 222

level of AtFT transcripts reached a peak at 3 WPI (7 WASS) and then declined over the 223

next two weeks (Fig. 1B). On the other hand, no AtFT was detectable in the control 224

mock-inoculated plants (Fig. 1B). Consistent with the expression levels of AtFT mRNA, 225

tobacco plants infected with PVX/AtFT started bolting at 2 WPI (6 WASS) onwards and 226

flowered at 4-5 WPI (8-9 WASS; Fig. 2D). Control plants that had been 227

mock-inoculated or inoculated with PVX/mAtFT carrying a non-sense mutation in the 228

AtFT mRNA start codon remained growing vegetatively in LD and did not flower (Fig. 229

2E and F). 230

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Latent PVX-based VIF induces no transgenerational epi-flowering 232

To assess whether the effects of virus infection on plant growth and development 233

would affect the usefulness of the PVX-based VIF, we examined the development of 234

systemic symptoms of PVX infection in MM tobacco grown in LD. Plants at 4 WASS 235



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(4–6 leaves) were inoculated with PVX/AtFT or PVX/mAtFT (Fig. 3). Local infection 236

occurred and chlorotic lesions appeared on inoculated-leaves at approximately 7–10 237

days post inoculation (Fig. 3A). In contrast, in newly developing young leaves no viral 238

mosaic or chlorosis was observed and systemic leaves were persistently symptomless 239



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(Fig. 3B and C). Recombinant viral RNA was, however, present and readily detected in 240

systemic leaf tissues (Fig. 1C; Fig. 2B, C), suggesting PVX was able to establish latent 241

infection in tobacco plants (Fig. 2D, E). In all cases, tobacco plants infected with PVX 242

virus vectors consistently appeared healthy (Fig. 1B; Fig. 2D-F; Fig. S1A; also see 243

below), likely due to RNA silencing-mediated recovery of virus infection (Baulcombe, 244

2004). 245

In order to investigate if the virally expressed AtFT and PVX RNA could be 246

transmitted through seed to progeny, RT-PCR was performed on seedlings that were 247

grown from seeds harvested from tobacco and tomato (Lycopersicon esculentum) plants 248

infected with PVX/AtFT (Fig. 4). Neither AtFT nor PVX coat protein RNA was 249

detected in descendant seedlings (Fig. 4A). Moreover, once mature these MM tobacco 250

plants were unable to flower in LD (Fig. 4B and C), in exactly the same as plants grown 251

from seeds collected from non-infected MM tobacco plants grown to flowering in SD. 252

253

Application of PVX-based VIF – Approach 1: VIF for assessing the role of 254

individual amino acid in AtFT activity 255

To test whether the PVX-based VIF could be used for assessing the influence of 256

individual amino acids on AtFT activity, we substituted T27, Y85, R119 and R173, 257

respectively, with Alanine (A) and produced PVX/AtFTT27A, PVX/AtFTY85A, 258

PVX/AtFTR119A and PVX/AtFTR173A (Fig. S1A). We selected Y85 and R119 because 259

their impacts on flowering have been shown in Arabidopsis (Bradley et al. 1997; 260

Wickland and Hanzawa, 2015); whilst T27 and R173 of previously unknown 261

contribution to FT activity were randomly selected for site-directed mutagenesis. 262

Tobacco plants were inoculated with each of the recombinant PVX vectors and grown 263

in LD (Fig. 5). Using PVX/AtFT as a positive control and PVX/mAtFT and mock 264

inoculation as negative controls, we found that viral expression of AtFTT27A, AtFTY85A, 265

AtFTR119A and AtFTR173A resulted in distinctive flowering phenotypes (Fig. 5A-G). 266

Similar to the mock inoculated controls and to plants infected with PVX/mAtFT, those 267

plants infected with PVX/AtFTY85A, PVX/AtFTR119A or PVX/AtFTR173A were unable to 268

flower (Fig. 5A, B and E-G). However, infection by PVX/AtFTT27A induced plants to 269



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flower at 5-WPI in a similar manner to the PVX/AtFT positive control (Fig. 5C and D). 270

Expression of AtFT, mAtFT, AtFTT27A, AtFTY85A, AtFTR119A and AtFTR173A mRNAs were 271

detected by RT-PCR and verified by direct sequencing (Fig. 5H-L). These findings 272

suggest that AtFTY85A, AtFTR119A and AtFTR173A are defective in their ability to induce 273

normal flowering compared to AtFT, whilst the T27A substitution did not affect the 274

ability of AtFT to induce flowering. 275

To make comparisons, we conducted transgenic complementation experiments 276

in which the T-DNA insertion mutant ft-10 was transformed with a binary vector 277



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containing a SUC2:AtFT, SUC2:mAtFT, SUC2:AtFTT27A, SUC2:AtFTY85A, 278

SUC2:AtFTR119A or SUC2:AtFTR173A expression cassette under the control of the 279

phloem-specific SUCROSE TRANSPORTER 2 (SUC2) promoter (Fig. S1B; Clough 280



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and Bent, 1998). 3-5 independent single-copy homozygous lines were generated for 281

each transgene and their flowering time in LD was analyzed. Similar to 282

non-transformed ft-10 and transgenic control ft-10/SUC2:mAtFT plants, transgenic lines 283

ft-10/SUC2:AtFTY85A, ft-10/SUC2:AtFTR119A or ft-10/SUC2:AtFTR173A were late 284

flowering when compared to wild-type Col plants. This is in agreement with our 285

previous observation that MM tobacco plants inoculated with PVX vectors expressing 286

AtFTY85A, FTR119A or AtFTR173A did not flower at all (Fig. 5E-G). However, transgenic 287

expression of AtFT or AtFTT27A led to early flowering in ft-10/SUC2:AtFT and 288

ft-10/SUC2:AtFTT27A plants (Fig. 5M; Table S2), again consistent with the results of the 289

PVX-based VIF (Fig. 5A-G). 290

291

Application of PVX-based VIF – Approach 2: VIF for assessing the impact of 292

polypeptide tags on AtFT floral induction 293

Polypeptide-tags have been widely used to study correlations between function and 294

spatial distribution of target proteins in tissues and cellular compartments. It has been 295

documented that AtFT-GFP and AtFT-myc expressed in leaf companion cells are 296

transported via the phloem over long-distance to the shoot apical meristem where these 297

fusion proteins can initiate flowering in transgenic Arabidopsis (Abe et al., 2005; Wigge 298

et al., 2005; Searle et al., 2006; Corbesier et al., 2007; Mathieu et al., 2007; Liu et al., 299

2012, Zhu et al., 2016). However, it remains to be clarified whether any free AtFT that 300

may co-exist with AtFT-GFP and AtFT-myc fusion proteins due to premature 301

translational termination was responsible for floral induction in those transgenic plants. 302

In contrast, viral expression of GFP-AtFT was functionally inactive in floral induction 303

in tobacco under LD conditions (Li et al., 2009). This suggests peptide tags at the N- or 304

C-terminus could affect AtFT florigenic activity. To test this, we generated 305

PVX/His6-AtFT, PVX/AtFT-His6 and PVX/AtFT-FLAG (Fig. S1A) and inoculated 306

these viruses onto tobacco plants grown in LD (Fig. 6). At 1 WPI chlorotic lesions were 307

visible on inoculated leaves of all virus-infected but not mock-inoculated plants. Similar 308

to plants infected with PVX/AtFT, plants infected with PVX/AtFT-His6 started to bolt at 309

2 WPI and subsequently flowered at 5–6 WPI. Plants infected with PVX/FT-FLAG 310



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started bolting at 3 WPI and flowered at 8–9 WPI (Fig. 6A). The average height of the 311

plants infected with PVX/AtFT, PVX/AtFT-His6 and PVX/AtFT-FLAG at 52 days post 312

inoculation were 55, 49, and 35 cm respectively (Fig. 6B). Plants infected with 313

PVX/His6-AtFT, however, remained in their vegetative phase and behaved similarly to 314

the mock controls with a mean height of 9 and 11 cm, respectively (Fig. 6A and B). 315

RT-PCR analysis showed that virally expressed free or tagged AtFT transcripts were 316

present in systemic leaf tissues of all virus-infected plants (Fig. 6C). These data 317

demonstrate that AtFT-His and free AtFT were equally efficient to induce flowering in 318

tobacco. AtFT-FLAG was slightly less active than AtFT, and His-AtFT was completely 319

inactive. These functional differences are likely to be due to the alternations in size, 320



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overall structure, solubility and/or stability of the fusion protein. 321

322

Application of PVX-based VIF – Approach 3: Functional analyses of mono- and 323

dicotyledonous FT genes 324

The FT gene belongs to a gene family that encodes closely related FT-like proteins, not 325

all of which induce flowering. To identify which of the FT-like genes that have been 326

identified in a plant species are the ones responsible for controlling floral induction a 327

rapid and efficient functional assay is necessary, previously this has been done through 328

the generation of transgenic plant lines. We tested whether PVX-based ectopic 329

expression of mono- and dicotyledonous FT genes was able to demonstrate their 330

functional ability to induce flowering (Fig. 7). We cloned wild-type and non-sense 331

mutated rice (Oryza sativa) Hd3a and tomato (Solanum lycopersicum) SFT genes into 332

the PVX vector to generate PVX/Hd3a, PVX/mHd3a, PVX/SFT and PVX/mSFT (Fig. 333

S1A, Table S1). Tobacco plants were then inoculated with these viruses and grown in 334

LD (Fig. 7A-F). All plants infected with either PVX/Hd3a or PVX/SFT developed no 335

systemic symptom, but nevertheless bolted at 2 WPI and flowered at 5–6 WPI (Fig. 7B 336

and E). Mock controls and plants infected with PVX/mHd3a or PVX/mSFT did not 337

flower (Fig. 7A, C, D and F). Expression of wild-type Hd3a or SFT mRNA from 338

PVX/Hd3a or PVX/SFT, as well as mutated non-translatable mHd3a or mSFT 339

transcripts from PVX/mHd3a or PVX/mSFT were readily detectable by RT-PCR and 340

were verified by direct sequencing (Fig. 7G and H). 341

342

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DISCUSSION 344

VIF has been developed in several plants and fruit trees (McGarry et al., 2017) since its 345

early establishment in cucurbit (Lin et al., 2007) and tobacco (Li et al., 2009), however, 346

the exact mechanism has not been fully investigated in each case. As the expression of 347

the plant’s own endogenous FT gene(s) is still possible, it remains to be elucidated 348

whether VIF was due to a direct or indirect effect of the virally expressed FT. Thus 349

further work is required to develop the full potential of VIF for the study of plant 350

reproductive biology. Here we demonstrate that viral expression of wild-type AtFT 351



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induces flowering of MM tobacco plants grown under non-inductive LD conditions, 352

without the involvement of the endogenous NtFT4 gene (Fig.1; Fig. 2). 353

There are two major concerns over pathogenic virus-induced flowering which 354

may restrict its usefulness in plant reproductive biology and crop breeding. Firstly, viral 355

infection often causes host plant developmental abnormalities and occasionally death. 356

Plants respond to such biotic stresses by speeding up their reproductive process to 357

flower earlier. This could complicate the interpretation of results of VIFs, such as those 358

based on ZYMV, CLCrV or CLBV, because all these viruses produced severe systemic 359

symptoms in viral infected plants (Lin et al., 2007; 2011; McGarry and Ayre, et al., 2011; 360

Velazquez et al., 2016). However, the PVX infected tobacco plants exhibited normal 361

vegetative and reproductive growth (Fig. 3), making PVX-VIF in MM tobacco a good 362

system for studying the control of flowering. Secondly, VIFs based on 363

seed-transmissible viruses are likely to hinder the technology from being used as a 364

viable tool in breeding programmes, whereas lack of seed transmission means progeny 365

plants would be virus-free. Thus, if VIF is to be used commercially the recombinant 366

virus should not be transmitted through seed to the progeny, thus making it easier to 367

contain and control. Indeed, we were unable to detect the presence of PVX RNA or 368

virally expressed AtFT mRNA in next generation seedlings of tobacco or tomato plants 369

infected with PVX/AtFT, and these seedlings subsequently grew and flowered as WT 370

plants (Fig. 4). This implies that neither PVX virus or virally expressed AtFT mRNA is 371

seed-transmissible despite the fact that AtFT RNA is able to facilitate the entry of PVX 372

to the apical shoot meristem (Li et al., 2011), and that PVX/AtFT infection cannot 373

induce transgenerational epi-flowering in progeny plants. 374

The transition from vegetative to reproductive growth is essential for most plants 375

to complete a successful life cycle, and the tight regulation of when this transition 376

occurs is important for their long-term evolutionary survival. In Arabidopsis the key 377

gene involved in this process is AtFT which encodes a small protein consisting of 175 378

amino acid residues. Moreover, both AtFT and AtTFL1 (AtTFL1 is the TERMINAL 379

FLOWER 1 protein, an inhibitor of flowering in Arabidopsis) belong to the PEBP 380

(phosphatidylethanolamine-binding protein) family and only 39 non-conserved residues 381



21

are found between the two functionally antagonizing proteins (Bradley et al., 1997; 382

Ohshima et al., 1997; Wickland and Hanzawa, 2015). Genetic analyses revealed that 383

late flowering in many Arabidopsis ft mutants often resulted from a dysfunctional AtFT 384

with single amino acid substitution such as G171E in ft-1, R119H in ft-3, E84K in ft-4 385

and P94L in ft-6. A number of AtFT alleles with specific point-mutations were further 386

characterized through an intensive mutagenesis programme (Ho and Weigel, 2014). 387

Whilst these studies were elegantly performed and extremely informative, a more rapid 388

and less labor-intensive flowering assay would make it easier to efficiently evaluate the 389

contribution of each of the 175 amino acids to the florigenic activity. 390

The efficacy of the PVX-VIF system was demonstrated in several approaches: (1) 391

To assess the influence of individual amino acids on protein function. Through this 392

analysis we were rapidly able to show that, in addition to the known contributions of 393

both Y85 and R119, residue R173 is essential for AtFT to induce flowering, whereas 394

T27 is not (Fig. 5). (2) To assess the impact of various tags at the N- or C-terminal on 395

protein function (Fig. 6). In the case of the AtFT protein we used this approach to show 396

that N- terminal fusions are likely to disrupt AtFT function, consistent with previous 397

findings (Li et al., 2009). (3) To analyze the floral inducing function of different mono- 398

and dicotyledonous FT genes (Fig. 7). The fact that virally expressed mono- and 399

dicotyledonous FT genes can induce flowering in MM tobacco under non-inductive 400

conditions also provides further evidence for high conservation of the FT-mediated 401

pathway in floral induction among many different plant species (Turck et al., 2008). 402

403

CONCLUSIONS 404

We have further developed our PVX-based VIF (Li et al., 2009) and demonstrated that 405

it is a powerful tool for assessing the functions of FT and its mono- and dicotyledonous 406

orthologues in flowering, as well as for evaluating the impact of specific amino acids or 407

polypeptide tags on florigenic activity. Floral induction in this system is exclusively 408

caused by the virally expressed FT genes independent of the endogenous tobacco FT. 409

Compared with other virus-based flowering induction systems, the PVX-based VIF is (1) 410



22

ideal for studying plant floral induction because symptomless PVX infection has no 411

perceptible influence on plant growth and flowering. (2) Non-seed transmissibility of 412

the virus also provides benefits in terms of biosafety and potential commercial 413

application of the PVX-based VIF. (3) Whilst our work has focused on the use of the 414

PVX-based VIF for assessing the ability of modified, or different, FT proteins to induce 415

flowering, the system can also be used more widely for the analysis of other proteins (or 416

RNAs) involved in flowering, both in the floral induction and flower development 417

processes. (4) The work described here can be easily translated to other viral expression 418

vectors that could be used in other plant species besides tobacco. On the other hand, the 419

current PVX-based VIF vector involves traditional cloning and production of infectious 420

recombinant viral RNA transcripts by in vitro transcription for plant infection. To 421

overcome these shortcomings, ongoing work in our laboratory aims to develop more 422

user-friendly version of the PVX-based VIF for systems biology and high throughput 423

analysis of FT and flowering-related genes, alleles and mutants. 424

425

MATERIALS AND METHODS 426

Plant Material and Growth Conditions 427

Tobacco plants (Nicotiana tabacum Maryland Mammoth) and Arabidopsis thaliana 428

Columbia-0 (Col) and mutant ft-10 (seeds were obtained from the Nottingham 429

Arabidopsis Stock Center) were grown under long-day (LD, 16 h light/8 h dark) or 430

short-day (SD, 8 h light/16 h dark) conditions at 23°C. Tomato (Lycopersicon 431

esculentum var Ailsa Craig) was grown in glasshouse or growth room in LD at 23°C. 432

433

Construction of VIF and Plant Transformation Vectors. 434

PVX/AtFT, PVX/mAtFT, PVX/Hd3a, PVX/mHd3a, PVX/SFT, PVX/mSFT, 435

PVX/NtFT4 and PVX/mNtFT4 were constructed as previously described (Li et al., 436

2009). Briefly wild-type and mutant Arabidopsis AtFT were RT-PCR amplified using 437

PrimeSTAR HS DNA polymerase and the primers RC0061/RC0062 or RC0066/ 438

RC0062 (Table S1), digested with BspEI and SalI, and cloned into the BspEI/SalI sites 439



23

of the PVX vector to produce PVX/AtFT and PVX/mAtFT, respectively (Fig. S1A). 440

Using a similar strategy, we constructed PVX/Hd3a, PVX/mHd3a, PVX/SFT, 441

PVX/mSFT, PVX/NtFT4 and PVX/mNtFT4 but using different sets of primers 442

RC0536/RC0537 for PVX/Hd3a, RC0538/RC0537 for PVX/mHd3a, RC0541/RC0542 443

for PVX/SFT, RC0543/RC0542 for PVX/mSFT, RC0779/RC0780 for PVX/NtFT4 and 444

RC1639/RC0780 for PVX/mNtFT4, respectively (Fig. S1A; Table S1). These genes 445

were cloned into the EagI/SalI sites of the PVX vector. 446

Single amino acid mutated FT alleles were created by overlapping PCR and 447

cloned into the PVX vector. Primers used for the construction of PVX/AtFTY85A, 448

PVX/AtFTR119A, PVX/AtFTR173A and PVX/AtFTT27A are listed in Supplemental Table S1. 449

To generate binary plant transformation vectors SUC2:AtFT, SUC2:AtFTY85A, 450

SUC2:AtFTR119A, and SUC2:AtFTT27A, mutated AtFT genes were amplified using 451

primers RC0783/RC0784 along with plasmid DNA temples PVX/AtFT, PVX/AtFTY85A, 452

PVX/AtFTR119A or PVX/AtFTT27A, digested with SalI and SacI, and cloned into the 453

SalI/SacI sites of pBI101.3 (Fig. S1B; Table S1). To generate SUC2:mAtFT and 454

SUC2:AtFTR173A, mutated genes were amplified using PVX/AtFT as templates along 455

with primers RC0798/RC0784 or RC0783/RC0799, digested with SalI and SacI, and 456

cloned into the SalI/SacI sites of pBI101.3 (Fig. S1B; Table S1). All constructs were 457

verified by nucleotide sequencing. 458

459

VIF in Tobacco and Transgenic Complementation in Arabidopsis ft-10 460

VIF was carried out in repeated experiments as previously described (Li et al., 2009). In 461

each experiment, 3-6 young SD MM tobacco plants were mock-inoculated or inoculated 462

with recombinant PVX and maintained in insect-free containment growth room at 23 °C 463

under LD. Transformation of Arabidopsis ft-10 plants was carried out using the floral 464

dip method and transgenic plants were selected on 1/2 MS medium supplemented with 465

Kanamycin (Clough and Bent, 1998). Through selfing, 3-5 single-copy homozygous 466

lines were generated for each transgene and used for analysis. Flowering time was 467

calculated and represented by the average number of rosette and cauline leaves. 468

469



24

RT–PCR and Quantitative RT–PCR 470

Total RNA was extracted from Arabidopsis, MM and tomato young leaf tissues. 471

First-strand cDNA was synthesized from DNase I-treated total RNAs by M-MLV 472

Reverse Transcriptase according to the manufacturer’s instructions (Promega). RT-PCR 473

was performed to detect virally expressed FT RNAs and the resulting RT-PCR products 474

were isolated and directly sequenced using primer PP82 as previously described (Li et 475

al. 2009). Quantitative RT–PCR was performed in a CFX96 machine (Bio-Rad) using 476

the iQ™ SYBR Green Supermix and gene-specific primers listed in Supplemental Table 477

1 following the manufacturer's instructions. The amplification program for SYBR Green 478

I was performed at 95 °C for 10 s, 55 °C for 30 s and 72 °C for 20 s. Triplicate 479

quantitative assays were performed on each of triplicate cDNA samples. The relative 480

quantification of each sample was determined by normalization to the amount of 481

NtEF1α cDNA detected in the same sample. Relative expression level was calculated by 482

the formula 2–△△Ct as described (Qin et al., 2012). 483

484

Supplemental Data 485

The following materials are available in the online version of this article. 486

Supplemental Figure S1. VIF vectors and Arabidopsis transformation constructs 487

Supplemental Table S1. Primers used in this work. 488

Supplemental Table S2. Flowering time of Arabidopsis transgenic plants 489

490

ACKNOWLEDGMENTS 491

We are grateful to David Baulcombe for providing the original PVX vector and to Miss 492

Meiling He for her technical support. 493

494

FIGURE LEGENDS 495

Figure 1. Floral induction by NtFT4 in short-day (SD) Nicotiana tabacum Maryland 496

Mammoth. A, Expression of NtFTs in tobacco plants grown under inductive SD 497

conditions was analyzed by qRT-PCR. Young leaf samples were taken at 2–16 weeks 498

after seed sowing (WASS). Plants grown under SD had started to bolt after 8 WASS and 499



25

flower after 12-WASS. No plants bolted or flowered under non-inductive long-day (LD) 500

conditions. B, Viral expression of NtFT4 by PVX/NtFT4 induced SD tobacco to flower 501

at 9 WASS in LD, 5 weeks post inoculation. Mock inoculated controls and plants 502

infected with PVX/mNtFT4 remained vegetative in LD. C, RT-PCR detection and 503

sequencing confirmation of wild-type and mutant NtFT4 transcripts expressed in 504

tobacco. Plants were photographed as indicated WASS in panel A, or 9 WASS in panel 505

B. Bar = 4 cm. 506

507

Figure 2. Viral expression of AtFT induces flowering. A, Endogenous NtFT4 expression 508

was not induced in systemic leaves of tobacco plants prior to inoculation (H), mock 509

inoculated (Mo), or infected with PVX/AtFT (vFT) under non-inductive long-day (LD) 510

conditions. Levels of the NtFT4 transcripts were analyzed by qRT-PCR in 511

non-inoculated MM plants grown to flowering (12 WASS) under short-day (SD) are 512

shown for comparison. B, Ectopic expression of AtFT mRNA by PVX/AtFT. WASS: 513

weeks after seed sowing; WPI: week post inoculation (0 indicates the inoculation week). 514

C, RT-PCR detection and sequencing confirmation of virally expressed with-type and 515

mutant AtFT mRNA (vFT and mFT, respectively). The start codon and the mutated start 516

codon are underlined. D-F, Flowering phenotype of tobacco plants infected with 517

PVX/AtFT (vFT), PVX/mAtFT (mFT) or mock (Mo) inoculation. Plants were 518

photographed at 6, 7, 8 and 9 WASS. Bar = 4 cm. 519

520

Figure 3. PVX latent infection of Maryland Mammoth tobacco plants. A, A tobacco 521

plant inoculated with PVX/AtFT developed local chlorotic lesions on the inoculated 522

leaves. B, A tobacco plant infected with PVX/AtFT developed no systemic symptoms 523

but was induced to flower. C, A tobacco plants inoculated with PVX/mAtFT did not 524

show systemic symptoms and did not flower. Plants were photographed at 11 (A) or 34 525

(B and C) days post-inoculation. Right panels for A, B and C show an enlarged section 526

of the boxed region in the left panels. Bar = 5 cm. 527

528

Figure 4. PVX-based VIF induces no transgenerational flowering. A, RT-PCR detection 529



26

of virally expressed Arabidopsis AtFT (FT) and PVX coat protein (CP) RNAs in 530

seedlings grown from seeds collected from PVX/AtFT infected tobacco (Maryland 531

Mammoth, MM) and tomato plants. The positions and sizes of the 1kb plus ladder 532

marker are indicated. PVX specific forward primer PP82 and gene specific reverse 533

primer PP356 were used for detection of the virally expressed AtFT (750-bp), TCPF and 534

TCPR for PVX CP (714-bp) and EF1F and EF1R for the house-keeping gene NbEF1α 535

(380-bp). Primer sequences are listed in Supplemental Table S1. The positive control 536

was systemic leaf tissue materials harvested from PVX/AtFT infected MM tobacco. B, 537

Tobacco plants grown from seeds harvested from PVX/AtFT-infected tobacco plants did 538

not flower in LD. C, Tobacco grown from seeds collected from MM plants under SD 539

remained in the vegetative phase in LD. Plants were photographed at 75 days after 540

sowing seeds. 541

542

Figure 5. Impact of single amino acid on AtFT-mediated floral induction. A-F, 543

Functional assessment of novel FT alleles using the PVX-based VIF. Maryland 544

Mammoth tobacco plants mock-inoculated (A), or infected with PVX/mAtFT (B), 545

PVX/AtFT (C), PVX/AtFTT27A (D), PVX/AtFTY85A (E), PVX/AtFTR119A (F) and 546

PVX/AtFTR173A (G) resulted in distinctive flowering phenotypes. Plants were 547

photographed at 5 weeks post-inoculation. Bar = 4 cm. H-L, RT-PCR detection and 548

sequencing confirmation of virally expressed with-type and mutant AtFT mRNAs as 549

indicated in each panel. The start codons and the mutated start codons are underlined. M, 550

Flowering time of Arabidopsis Col, ft-10, and transgenic ft-10/SUC2:AtFT, 551

ft-10/SUC2:mAtFT, ft-10/SUC2:AtFTY85A, ft-10/SUC2:FTR119A, ft-10/SUC2:AtFTR173A 552

and ft-10/SUC2:FTT27A plants under LD conditions. Flowering times were determined as 553

the numbers of rosette (white bars) and cauline (gray bars) leaves in 3-5 independent 554

single-copy transgenic lines for each gene. A representative line for each transgene is 555

shown (also see Supplemental Table S2). 556

557

Figure 6. Influence of polypeptide tags on AtFT florigenic activity. A, Maryland 558

Mammoth plants infected with PVX expressing AtFT with and without different tags 559



27

flowered differently under non-inductive long-day (LD) conditions. Plants were 560

photographed at 52 days post inoculation. B, Effect of expression of AtFT with and 561

without different tags, on bolting of tobacco plants. The average stem length (cm) at 52 562

days post inoculation is shown. C, RT-PCR detection of virally expressed Arabidopsis 563

AtFT, AtFT-His, His-AtFT and AtFT-FLAG mRNAs in systemic leaf tissues of four 564

different tobacco plants (Lanes 1–4) infected with PVX/AtFT (AtFT), PVX/AtFT-His 565

(AtFT-His), PVX/His-FT (His-FT) or PVX/AtFT-FLAG (AtFT-FLAG). PVX-specific 566

forward primer PP82 and a gene-specific reverse primer (Supplemental Table S1) were 567

used for RT-PCR detection. Positive controls (+) was the respective recombinant 568

plasmids, while no DNA was used in the negative control PCR. The positions and sizes 569

of 1kb plus ladder are indicated. 570

571

Figure 7. Viral transient expression of mono- and dicot FT genes promotes short-day 572

tobacco flowering under non-inducing long-day conditions. A-C, Maryland Mammoth 573

tobacco plants were mock inoculated or inoculated with PVX/Hd3a or PVX/mHd3a. 574

D-F, Tobacco plants were mock inoculated or inoculated with PVX/SFT or PVX/mSFT. 575

In three separate experiments, ectopic expression of Hd3a or SFT caused tobacco plants 576

to bolt at 2-3 weeks post inoculation (WPI) and flower at 5 WPI. Plants mock 577

inoculated or infected with PVX/mHd3a or PVX/mSFT did not flower. Plants were 578

photographed at 5 WPI. Bar = 4 cm. G and H, RT-PCR detection and sequencing 579

confirmation of virally expressed wild-type and mutant rice Hd3a and SFT mRNA in 580

systemic leaves of infected tobacco plants. The wild-type and mutated start codons are 581

underlined. 582

583

584



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Google Scholar: Author Only Title Only Author and Title

Zhu Y, Liu L, Shen L, Yu H (2016) NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis. Nat Plants 2:16075.



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1 Short Title: Virus-induced Flowering (VIF) Assay 3 …...2017/04/11 · 87 molecular pharming...

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