Gain of An Auto-regulatory Site Led to Divergence of the ...

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Gain of An Auto-regulatory Site Led to Divergence of the Arabidopsis APETALA1 and 2

CAULIFLOWER Duplicate Genes in the Time, Space and Level of Expression and 3

Regulation of One Paralog by the Other 4

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Lingling Ye2, Bin Wang2, Wengen Zhang, Hongyan Shan*, and Hongzhi Kong* 6

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese 7

Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); and University of 8

Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.) 9

ORCID IDs: 0000-0001-6662-2935 (H.S.); 0000-0002-0034-0510 (H.K.). 10

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One sentence summary: 12

Gain of an auto-regulatory site in one paralog has led to divergence of two duplicate genes in the 13

time, space and level of expression and regulation of one paralog by the other. 14

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1 This work was supported by National Natural Science Foundation of China (Grants 31125005 and 30800065), 16

CAS Interdisciplinary Innovation Team, and CAS Youth Innovation Promotion Association. 17

2 These authors contributed equally to the article. 18

*Address correspondence to [email protected] or [email protected]. 19

The author responsible for distribution of materials integral to the findings presented in this article in 20

accordance with the policy described in the Instructions for Authors (www.plantphysiol.org ) are: Hongyan 21

Shan ([email protected]) and Hongzhi Kong ([email protected]). 22

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H.K. and H.S. conceived and designed the project. L.Y., B.W., and W.Z. performed experiments. L.Y. and 24

B.W. analyzed data. H.K., H.S., and L.Y. wrote the paper.25

Plant Physiology Preview. Published on April 5, 2016, as DOI:10.1104/pp.16.00320

Copyright 2016 by the American Society of Plant Biologists

www.plantphysiol.orgon January 31, 2018 - Published by Downloaded from Copyright © 2016 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

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ABSTRACT 26

How genes change their expression patterns over time is still poorly understood. Here, by 27

conducting expression, functional, bioinformatic and evolutionary analyses, we demonstrate that 28

the differences between the Arabidopsis thaliana APETALA1 (AP1) and CAULIFLOWER (CAL) 29

duplicate genes in the time, space and level of expression were determined by presence or 30

absence of functionally important transcription factor-binding sites (TFBSs) in regulatory regions. 31

In particular, a CArG box, which is the auto-regulatory site of AP1 that can also be bound by the 32

CAL protein, is a key determinant of the expression differences. Because of the CArG box, AP1 33

is both auto- and cross-regulated (by AP1 and CAL, respectively), and its relatively high-level 34

expression is maintained till to near-mature sepals and petals. The observation that the CArG box 35

was gained recently further suggests that the auto- and cross-regulation of AP1, as well as its 36

function in sepal and petal development, is a derived feature. By comparing the evolutionary 37

histories of this and other TFBSs, we further indicate that the divergence of AP1 and CAL in 38

regulatory regions has been markedly asymmetric and can be divided into several stages. 39

Specifically, shortly after duplication, when AP1 happened to be the paralog that maintained the 40

function of the ancestral gene, CAL experienced certain degrees of degenerate evolution, in which 41

several functionally important TFBSs were lost. Later, when functional divergence allowed 42

survival of both paralogs, CAL remained largely unchanged in expression whereas the functions 43

of AP1 were gradually reinforced by gains of the CArG-box and other TFBSs. 44

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INTRODUCTION 46

Expression pattern is one of the most important attributes of a gene. Understanding how the 47

expression pattern of a gene is precisely determined and changes over time are keys to 48

understanding the nature of organismal development and evolution. In the past few decades, 49

based on the studies of model organisms, much has been learned about the molecular basis of 50

gene regulation (Davidson, 2006; Arthur, 2011). Yet, it remains largely unclear how, why, to 51

which extent and under which condition genes change their expression patterns. One reason for 52

this is that expression itself is a complex process, or state, that requires measurements and 53

descriptions from different angles, such as time, space, amount, and type (Arthur, 2011). Another 54

reason is the difficulty of conducting appropriate experiments and analyses to determine the exact 55

contribution of each evolutionary change to the differences in expression pattern (Hardison and 56

Taylor, 2012; Wittkopp and Kalay, 2012). Nevertheless, based on theoretical and empirical 57

investigations, several principles have emerged regarding the molecular basis of expression 58

divergence (Prud'homme et al., 2007; Gordon and Ruvinsky, 2012; Romero et al., 2012). For 59

example, it has been suggested that evolutionary changes in the expression pattern of a gene may 60

be caused by alterations in cis-regulatory elements (CREs) or transcription environment, or both, 61

although the relative contributions of the two mechanisms are usually difficult to determine 62

(Wray et al., 2003). It has also been reported that while transcription environment itself is 63

evolving all the time, changes of CREs have played important roles in shaping the expression 64

patterns of genes (Wittkopp et al., 2004; Wray, 2007; Wittkopp and Kalay, 2012). Many studies 65

also tried to determine the tempo, mode and mechanisms of CRE evolution (Gordon and 66

Ruvinsky, 2012; Wittkopp and Kalay, 2012; Villar et al., 2014), yet the available data are still 67

insufficient for a general picture. 68



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69

Interestingly, compared with orthologs from different species, paralogs from the same species are 70

better systems for studying the tempo, mode and mechanisms of CRE evolution, for three reasons. 71

First, paralogs have evolved under the same transcription environment so that most, if not all, of 72

the differences in expression pattern may be attributed to changes in CREs (Li et al., 2005). 73

Second, paralogs from the same model species can be compared, analyzed or even manipulated 74

with ease, thereby avoiding the difficulties in conducting inter-species comparisons (Kleinjan et 75

al., 2008; Schauer et al., 2009). Third, and most importantly, the evolutionary fates of duplicate 76

genes have been investigated extensively in the past few decades, based on which a few models 77

have been proposed (Ohno, 1970; Force et al., 1999; He and Zhang, 2005; Moore and 78

Purugganan, 2005; Innan and Kondrashov, 2010). In general, these models are both elegant and 79

powerful, being able to explain the evolutionary fates of almost all duplicate genes. The problem, 80

however, is that they mainly consider the consequences rather than process of duplicate gene 81

evolution (Innan and Kondrashov, 2010). In addition, none of these models take into 82

consideration the cross-regulation between duplicate genes, and paralogs were generally assumed 83

to evolve more or less independently (Innan and Kondrashov, 2010; Baker et al., 2013; Dhar et 84

al., 2014; Rogozin, 2014). In reality, yet, many duplicate genes are parts of the same regulatory 85

network, in which the expression and function of one copy is dependent on that of the other, or 86

vice versa (Kafri et al., 2006; Sémon and Wolfe, 2007; Conant et al., 2014). Therefore, in many 87

cases, a careful study of the molecular basis of duplicate gene evolution in expression pattern will 88

not only uncover the tempo, mode and mechanisms of CRE evolution, but also shed new light on 89

the evolution of the corresponding regulatory network. 90

91

Arabidopsis thaliana APETALA1 (AP1) and CAULIFLOWER (CAL) are a pair of duplicate genes 92



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generated through a whole genome duplication (WGD) event within the flowering plant family 93

Brassicaceae (Lawton-Rauh et al., 1999; Shan et al., 2007; Wang et al., 2012). As members of the 94

MADS-box gene family, both AP1 and CAL code for MIKC-type MADS domain-containing 95

transcription factors and participate in plant development (Mandel et al., 1992; Bowman et al., 96

1993; Kempin et al., 1995; Ferrandiz et al., 2000; Han et al., 2014). Like many other duplicate 97

gene pairs of the MADS-box gene family, AP1 and CAL have diverged considerably in 98

expression pattern (Supplemental Fig. S1). Specifically, AP1 is mainly expressed in floral 99

primordia and developing sepals and petals, and the expression levels are generally high. 100

Inactivation of AP1 caused conversion of sepals into bracts and concomitant formation of 101

additional flowers in the axis of the bracts (Irish and Sussex, 1990; Mandel et al., 1992; Bowman 102

et al., 1993), suggesting that AP1 not only determines the identity of floral meristem, but also 103

specifies the identities of sepals and petals (Coen and Meyerowitz, 1991; Theissen, 2001). Unlike 104

AP1, whose expression cannot be detected until floral meristems are formed, CAL expression can 105

be detected even in seedlings (William et al., 2004), suggestive of early functioning. CAL is also 106

expressed in floral meristems and developing sepals and petals, but the expression levels are 107

relatively low (Kempin et al., 1995). Inactivation of CAL alone did not cause obvious phenotypic 108

change, while silencing of CAL in the ap1 background enhanced the phenotype of the plant, 109

suggesting that CAL may have redundant function with AP1 (Bowman et al., 1993). The 110

observation that expression of AP1 decreased significantly in the young inflorescences of the ap1 111

cal double mutant but not in stages 1 and 2 flowers of the ap1 single mutant further led to the 112

proposal that AP1 is positively regulated by CAL at the very early stage of flower development 113

(Bowman et al., 1993). Clearly, as a pair of duplicate genes, AP1 and CAL have diverged 114

considerably in the time, space and level of expression, and can be an excellent system for 115

studying the molecular basis of expression evolution. 116



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117

Considerable progress has been made in understanding the mechanisms underlying the 118

differences between AP1 and CAL. Up to now, it has been shown that: 1) the protein products of 119

the two genes, AP1 and CAL, have redundant but slightly differentiated functions, being able to 120

interact with different numbers and sets of partners (Riechmann et al., 1996a; Riechmann et al., 121

1996b; Pelaz et al., 2001; de Folter et al., 2005; Kaufmann et al., 2005; Smaczniak et al., 2012); 2) 122

the amino acid differences in the K and C regions of the AP1 and CAL proteins are responsible 123

for their differences in function, whereas the M or I regions, which play key roles in binding to 124

CREs of downstream genes, are functionally indistinguishable (Alvarez-Buylla et al., 2006); and 125

3) the expression of the AP1 and CAL genes is precisely controlled by many regulators, of which 126

the vast majority are transcription factors (i.e., trans-regulatory elements, TREs) (Wagner et al., 127

1999; Wigge et al., 2005; Saddic et al., 2006; Sundström et al., 2006; Kaufmann et al., 2009; 128

Mathieu et al., 2009; Wang et al., 2009; Yamaguchi et al., 2009; Xu et al., 2010; Yant et al., 2010; 129

Pastore et al., 2011). Several TFBSs have also been identified in the regulatory regions of AP1 130

and CAL, and functional studies indicate that their relative contributions to expression vary 131

considerably (William et al., 2004; Wigge et al., 2005; Saddic et al., 2006; Sundström et al., 2006; 132

Kaufmann et al., 2009; Mathieu et al., 2009; Wang et al., 2009; Yamaguchi et al., 2009; 133

Kaufmann et al., 2010; Yant et al., 2010; Benlloch et al., 2011; Pastore et al., 2011; Wuest et al., 134

2012). Despite the rapid progress, it remains unclear how AP1 and CAL have diverged in the time, 135

space and level of expression, how AP1 has acquired its function in sepal and petal identities, and 136

how CAL has become a regulator of AP1. 137

138

In this study, by conducting a series of expression, functional, bioinformatic and evolutionary 139

analyses, we determine the molecular basis and evolutionary dynamics of the expression 140



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divergence between AP1 and CAL. We demonstrate that the differences between AP1 and CAL in 141

the time, space and level of expression were caused by gains and losses of functionally important 142

TFBSs. We also show that the gains and losses of TFBSs along the lineages leading to the two 143

paralogs have been quite dynamic and asymmetric, which, in turn, suggests that divergence of 144

duplicate genes in expression pattern is usually a complex process that cannot be easily depicted 145

by simple empirical models. Our results provide new insights into the tempo, mode and 146

mechanisms of CRE evolution, and highlight the necessity of conducting systematic experiments 147

in understanding the underlying mechanisms of duplicate gene evolution. 148

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RESULTS 151

Differences in the Time, Space and Level of Expression 152

Expression patterns of AP1 and CAL have been investigated in several studies (Mandel et al., 153

1992; Bowman et al., 1993; Gustafson-Brown et al., 1994; Kempin et al., 1995), yet the results 154

are not completely consistent or comparable because different authors focused on different stages 155

of flower development and because the resolution of the images was not always high. To get a 156

clear portrait of the expression patterns of the two genes, we performed detailed in situ 157

hybridization and qRT-PCR analyses. We found that AP1 is strongly expressed in floral 158

meristems (i.e., stage 2 flowers) and moderately expressed in developing sepals and petals in 159

stages 3–12 flowers (Fig. 1A–1D). The expression pattern of CAL is very similar to that of AP1 160

but has three interesting differences (Fig. 1E–1K). First, its expression levels in floral meristems 161

and developing sepals and petals are obviously lower than those of AP1, no matter which stage of 162

flower development is considered and which method is used to measure. Second, roughly from 163

stage 4 on, the expression of CAL decreases dramatically and vanishes eventually, while that of 164

AP1 persists to late stages of flower development, with strong signals being detectable even in 165

near-mature (stage 12) flowers. Third, CAL is also expressed in the cells underneath the floral 166

buttress, whereas AP1 is not, suggesting that expression of CAL is slightly earlier than that of 167

AP1. Taken together, these results confirm that AP1 and CAL have diverged considerably in the 168

time, space and level of expression. 169

170

Differences in the Number and Type of TFBSs 171

To understand the mechanisms by which AP1 and CAL have diverged in expression pattern, we 172

first compared the genomic sequences of the two genes. For AP1, a 6946-bp region was 173



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investigated, which covers all the eight exons and seven introns, plus 2900 base pairs (bps) 174

upstream of the translation start site and 519 bps downstream of the stop codon. Using the public 175

resources for TFBS prediction and referring to published results (for details, see Methods), we 176



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identified 19 relatively reliable TFBSs: 16 in the promoter region and 3 in the first intron (Fig. 2A 177

and Supplemental Figs. S2–S4). Twelve of these TFBSs have already been identified and 178

functionally characterized in previous studies, suggestive of reliability (Supplemental Table S1); 179



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the remaining seven have not been confirmed by experiments, but the available data suggest that 180

they are reliable because their sequences are identical, or nearly so, to those identified before and 181

because corresponding TREs have been reported to function in relevant pathways (Supplemental 182



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Table S1). Using the same strategy, we identified 12 TFBSs in the 5756-bp genomic region of 183

CAL: 7 in the promoter region and 5 in the first intron (Fig. 3A and Supplemental Figs. S2–S4). 184

Of these TFBSs, only three have been functionally characterized, suggestive of the scarcity of 185

studies on CAL relative to AP1 (Supplemental Table S1). Notably, only six TFBSs are shared by 186

CAL and AP1 (Figs. 1 and 2 and Supplemental Figs. S3 and S4), suggesting that the two genes 187

have diverged considerably in CRE constitution. Since independent gains of exactly the same 188

TFBS in different evolutionary lineages rarely occur (Wittkopp and Kalay, 2012), it is very likely 189

that the shared TFBSs have existed in the most recent common ancestor of AP1 and CAL; then, 190

after gene duplication, they were retained in both genes. For understanding the mechanisms 191

underlying the divergence of AP1 and CAL in expression pattern, however, these shared TFBSs 192

are not very useful. 193

194

Contributions of Different Regulatory Regions to Expression Pattern 195

To gain some insights into the roles of the identified TFBSs in gene expression, we performed a 196

series of transgenic experiments. Transformable constructs containing different lengths of 197

genomic regions (Fig. 2A) were first fused with the β-glucuronidase (GUS, a reporter) gene and 198

then introduced into plants of A. thaliana. When a construct (i.e., AP1pro2887+intr1) including the 199

promoter and the first intron of AP1 was used, an expression pattern of GUS that completely 200

matches that of AP1 was observed (Fig. 2B). This suggests that the GUS system worked well 201

here, and that the promoter and the first intron contain most, if not all, of the information needed 202

for the normal expression of AP1. The fact that the same results were obtained when the 203

AP1pro1163 and AP1pro855 constructs were used (Fig. 2C and 2D), however, suggests that the 204

contributions of the first half of the promoter (from -2887 to -855) and the first intron are 205

negligible. Interestingly, when a construct (i.e., AP1pro755) containing a shorter region was used, a 206



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slight but obvious decrease in expression level was observed (Fig. 2E), suggesting that the region 207

spanning from -855 to -755 contains the CREs that enhance the expression of AP1. The 208

observations that AP1pro577 gave the same results as AP1pro755 (Fig. 2F), whereas no GUS signal 209

could be detected for AP1pro276 (Fig. 2G), suggest that the region spanning from -577 to -276 210

contains the basic information for the spatiotemporal expression of AP1. 211

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We also applied the same strategy to CAL (Fig. 3A). In plants expressing the longest construct, 213

CALpro1210+intr1, the expression pattern of GUS is completely congruent with that of CAL (Fig. 3B), 214

suggesting that the region covering the promoter and the first intron contains almost all the CREs 215

needed for the normal expression of CAL. In plants expressing CALpro1109, no GUS signal could 216

be detected in floral meristem, whereas the signals in developing sepals and petals become 217

stronger (Fig. 3C). This suggests that the region spanning from -1210 to -1109 or the first intron, 218

or both, are critical for the repression of CAL expression in pedicel/stem and the promotion of 219

CAL expression in floral meristem. The observations that GUS signals in plants expressing 220

CALpro850, CALpro521 or CALpro340 are not very different from that of CALpro1109 (Fig. 3D, 3E and 221

3F), however, imply that the region spanning from -1109 to -340 is not very important for CAL 222

expression, in spite of the existence of several TFBSs. Alternatively, this region may have been 223

involved in CAL expression by coordinating with the TFBSs located within the region spanning 224

from -1210 to -1109 and/or the first intron. Like in AP1, the promoter region spanning from -340 225

to -240 may provide the basic information for the spatiotemporal expression of CAL, because no 226

GUS signal could be detected in the CALpro240 plants (Fig. 3G). 227

228

Functions of an Auto-regulatory Site 229

It is interesting that the region spanning from -855 to -755 is critical for the expression level of 230



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AP1 (Fig. 2D and 2E). To understand the function of this region, we measured the expression 231

levels of the GUS gene in plants expressing four different constructs (i.e., AP1pro1163, AP1pro855, 232

AP1pro755 and AP1pro685). We found that the expression level reduced to about a half when the 233



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region spanning from -855 to -755 was excluded (Fig. 4A), suggesting that this region is indeed 234

important in expression level maintenance. To figure out the mechanism behind this, we 235

inspected this region carefully and encountered a CArG box which, according to the recent 236

ChIP-seq studies of MADS-box proteins (Kaufmann et al., 2009; Zheng et al., 2009; Kaufmann 237

et al., 2010; Deng et al., 2011; Immink et al., 2012; Wuest et al., 2012; Gregis et al., 2013; 238

Ó'Maoiléidigh et al., 2013; Posé et al., 2013), is a putative binding site of the AP1 protein and its 239

interacting partner, SEPALLATA3 (SEP3). We therefore hypothesized that this CArG box may 240

have led to the formation of an auto-regulatory loop, through which the expression of AP1 is 241

maintained at high levels to later stages of sepal and petal development; CAL does not have this 242

CArG box, and thus is expressed at very low levels in near-mature sepals and petals. 243

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To test this hypothesis, we first re-analyzed the published ChIP-Seq data (Kaufmann et al., 2010), 245

and observed two obvious AP1-binding peaks in the promoter region of AP1; the corresponding 246

region of CAL, however, does not show such binding signals (Fig. 4B). We then performed 247

EMSA analyses, and found that the binding affinities of the AP1 and CAL proteins to the CArG 248

box-containing AP1 probe are clearly stronger than to the CArG box-lacking CAL probe (Fig. 249

4C). We also made two constructs in which the CArG box of AP1 was swapped with a stretch of 250

non-CArG box sequence in the corresponding region of CAL (Fig. 4D). As expected, the 251

expression level of GUS in AP1pro2887(mut805-796)+intr1 is significantly lower than that in 252

AP1pro2887+intr1 (two-tailed t-test, P = 0.004; Fig. 4E), while that in CALpro1210(mut703-693)+intr1 is 253

significantly higher than that in CALpro1210+intr1 (two-tailed t-test, P = 0.006; Fig. 4E). Notably, 254

when the CArG box was removed from AP1pro2887+intr1, the expression pattern became more 255

similar to CAL than to AP1: signals were initially detected in floral primordia and developing 256

sepals and petals but eventually vanished in near-mature flowers (Fig. 4F). Conversely, when the 257



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CArG box was added to CALpro1210+intr1, the expression pattern became more similar to AP1 than 258

to CAL: signals were detectable throughout flower development, even in near-mature sepals and 259

petals (Fig. 4G). Taken together, these results suggest that the CArG box is an auto-regulatory 260

site of AP1 that can also be bound by CAL, thereby functioning to maintain the relatively high 261

levels of AP1 expression in near-mature sepals and petals. 262

263

Origin of the Auto-regulatory Site 264

To understand the evolutionary history of the CArG box, we obtained orthologs of AP1 and CAL 265

in A. lyrata, Capsella rubella, Thellungiella parvula, and Aethionema arabicum (i.e., AlyAP1, 266

AlyCAL, CruAP1, CruCAL, TpaAP1, TpaCAL, AarAP1 and AarCAL, respectively), as well as the 267

AP1/CAL-like genes in Tarenaya hassleriana and Carica papaya, and compared their regulatory 268

regions (Supplemental Fig. S5 and Table S2). We found that the aforementioned CArG box is 269

also present in AlyAP1, and the sequence is completely identical to that of AP1 (Fig. 5A); in other 270

genes, however, no such CArG box is recognizable, although similar sequences with very few 271

mismatches do exist in the corresponding regions (Fig. 5A). In CruAP1, for example, there is a 272

similar sequence that has an alignment gap in the third position and a cytosine (C) rather than 273

thymine (T) in the eighth position. Similarly, in TpaAP1 and AarAP1, there are similar sequences 274

that possess two nucleotide differences in this otherwise highly conserved region (Fig. 5A). 275

Previous studies have shown that when nucleotides at these positions were removed or mutated, 276

the resultant sequences would no longer be functional, unable to interact with relevant 277

MADS-box proteins (Huang et al., 1996). Therefore, it is very likely that the corresponding 278

sequences in CruAP1, TpaAP1 and AarAP1 are not CArG box. 279

280

To test this hypothesis, we first conducted EMSA experiments. We found that proteins of both 281



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CruAP1 and CruCAL can strongly bind to the CArG box-containing AP1 probe, whereas their 282

binding to the CArG box-like sequence of CruAP1 is rather weak (Fig. 5B). This confirms that 283

the CArG box-like sequences of CruAP1 is unlikely functional. We then compared the expression 284



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level of CruAP1 with that of AP1. Theoretically, because CruAP1 does not have the CArG box, it 285

would not be auto-regulated and thus its expression level should be lower than that of AP1. 286

Indeed, when flowers at the same developmental stages were compared, the expression level of 287

CruAP1 is markedly lower than that of AP1 (Fig. 5C); the expression levels of CruCAL and CAL, 288

however, do not show significant difference (Fig. 5C). This suggests that the CArG box-like 289

sequence of CruAP1 is also not functionally equivalent to the real CArG box. Taken together, 290

these results not only confirm the importance of the CArG box in AP1 expression, but also 291

indicate that this particular CArG box has been gained through modification of a pre-existing 292

non-CArG box sequence in the ancestor of AP1 and AlyAP1 and, as a result, contributed to the 293

differences between AP1 and CAL in the time, space and level of expression (Fig. 5D and 5E). 294

295

Gains and Losses of Other TFBSs 296

To understand the evolutionary context of the CArG box origination, we also tried to trace the 297

evolutionary histories of other TFBSs. However, because exact functions of the predicted TFBSs 298

in other species remain to be determined, we only considered the evolutionary changes of the 299

sequences per se, with special attention being paid to functionally important nucleotide sites. 300

Meanwhile, because the evolutionary histories of the TFBSs within the first intron turned out to 301

be extremely difficult to elucidate, we focused instead on the ones located in the promoter region. 302

We found that at least nine TFBSs existed in the most recent common ancestor of AP1 and CAL 303

(Fig. 6, Supplemental Fig. S5 and Table S2), among which five have been retained by both genes. 304

After gene duplication, seven and two new TFBSs were gained along the lineage leading to AP1 305

and CAL, respectively. Three TFBSs were also lost in the lineage leading to CAL, whereas no 306

TFBS loss events could be deduced for the lineage leading to AP1. Interestingly, while gains of 307

TFBSs along the AP1 lineage occurred more or less gradually, losses of three TFBSs along the 308



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CAL lineage all occurred at the very early stages of post-duplication evolution, immediately 309

followed by the gains of two new TFBSs (Fig. 6). This suggests that AP1 and CAL not only 310

gained/lost different sets of TFBSs but also experienced different modes of evolution. 311

312



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Notably, most of TFBSs gained or lost along the lineages leading to AP1 and CAL have resulted 313

from modifications of local sequences rather than from translocation of preexisting ones because 314

similar sequences can still be found in the corresponding regions of the orthologous and/or 315

paralogous genes (Supplemental Fig. S6). The LEAFY (LFY)-binding site located between -255 316

and -250 bps of the AP1 promoter, for example, have likely resulted from substitution of an 317

adenine (A) with a guanine (G) at the sixth position after the divergence between AP1 and 318

AlyAP1. This, together with the observation that the TFBSs gained or lost at nearly the same 319

evolutionary stage are usually located at different parts of the promoters (Fig. 6), further suggests 320

that gains and losses of TFBSs have occurred separately rather than collectively or massively. 321

322

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DISCUSSION 324

A Versatile CArG Box 325

In this study, by conducting extensive expression analyses, we first confirmed that AP1 and CAL 326

have diverged in the time, space and level of expression. Then, by comparing and functionally 327

dissecting the regulatory regions of the two genes, we identified the portions that are responsible 328

for the differences in expression pattern. We found that most of the differences in expression 329

pattern can be explained by the presence or absence of certain portions of the regulatory regions, 330

each of which contains functionally important TFBSs. In particular, a CArG box in the promoter 331

region of AP1 seems to be a key to understanding the mechanisms that underlie the expression 332

differences between AP1 and CAL. Replacement of the CArG box with a non-CArG box 333

sequence in the AP1-based GUS construct led to decreased GUS expression in developing sepals 334

and petals, whereas substitution of this non-CArG box sequence with the CArG box in the 335

CAL-based GUS construct led to increased GUS expression in those organs. This, together with 336

the fact that the CArG box can interact with proteins coded by AP1 and CAL, suggests that it is 337

the auto-regulatory site of AP1 that can also be bound by CAL. CAL and AP1, therefore, form a 338

regulatory cascade in which AP1 is both auto-regulated by itself and cross-regulated by CAL; it is 339

for this reason that the relatively high levels of AP1 expression can be maintained till to the late 340

stages of sepal and petal development. CAL does not have this CArG box (or any other TFBSs of 341

this kind) and thus cannot be directly regulated by either AP1 or CAL, so that its expression is 342

transient and low-leveled. In addition, because of the formation of a regulatory cascade, as well 343

as the slightly earlier expression of CAL than AP1, CAL promotes the expression of AP1 at the 344

very early stage of flower development (Bowman et al., 1993; Gustafson-Brown et al., 1994; 345

William et al., 2004). Up to now, although this last point still needs to be proved in vivo, it has 346



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already been clear that, as a particular CRE, the CArG box is versatile, being able to cause 347

considerable differences in the time, space and level of expression. 348

349

It is interesting that this particular CArG box has been gained recently, very likely before the 350

divergence of A. thaliana and A. lyrata but after the Arabidopsis–Capsella split (Fig. 5). This 351

implies that the regulation of AP1 by AP1 itself and CAL, as well as the relatively high level of 352

expression in developing sepals and petals, is a derived feature shared by AP1 and AlyAP1 but 353

not by CruAP1, TpaAP1, AarAP1 or the CAL orthologs. This is very interestingly, because unlike 354

its counterparts in many other species, which are generally not involved in floral organ identity 355

determination (Huijser et al., 1992; Taylor et al., 2002; Vrebalov et al., 2002; Litt, 2007), AP1 not 356

only regulates the formation of floral primordia but also is involved in sepal and petal 357

development. Presumably, it was the gain of this CArG box that has enabled AP1 to extend its 358

roles in sepal and petal development. 359

360

Auto-regulation and Duplicate Gene Evolution 361

Our results also highlighted the importance of auto-regulation in duplicate gene evolution. As a 362

special type of regulation, auto-regulation exists in all kinds of life form, and plays particularly 363

important roles in maintaining the expression level of genes (Crews and Pearson, 2009). 364

Auto-regulation can be positive or negative, direct or indirect, depending on the function of the 365

genes (Crews and Pearson, 2009). In any case, duplication of a gene capable of auto-regulation 366

may lead to complex consequences because the resultant duplicates would form a regulatory 367

network (Studer et al., 1998; Czerny et al., 1999; Sémon and Wolfe, 2007; Lenser et al., 2009). 368

Loss of the auto-regulatory site, therefore, will cause interruption of existing regulatory 369

relationship(s) between genes. In the past, possibly because of its complexity, auto-regulation has 370



23

not been explored extensively in terms of its effects on duplicate gene evolution. Even in the 371

limited published case studies, much attention has been paid to the effect of gene duplication on 372

the maintenance of the regulatory relationships between genes (Teichmann and Babu, 2004; 373

Sémon and Wolfe, 2007); the contribution of newly established auto-regulation to duplicate gene 374

evolution, however, remains largely unexplored. 375

376

In this study, it is clear that the gain of the CArG box not only enabled divergence of AP1 and 377

CAL in the time, space and level of expression, but also led to the formation of a regulatory 378

cascade, thereby further splitting the function domains of the two genes. Meanwhile, because 379

AP1 is both auto- and cross-regulated, its function is strengthened, with relatively high-level 380

expression being maintained till to the late stages of sepal and petal development. Without the 381

CArG box, the expression level of AP1 would not be that high, and the high-level expression 382

would not be maintained from floral meristem to developing and near-mature sepals and petals. 383

Consistent with this, AP1 has evolved under more stringent functional constraint than CAL, as is 384

reflected by its relatively low dN/dS value (Lawton-Rauh et al., 1999). Apparently, gain of the 385

auto-regulatory site has enabled AP1 and CAL to arrive at a state that cannot be easily reached 386

through many other mechanisms. Because independent origins of CREs through modifications of 387

pre-existing sequences are rather easy, it is quite possible that similar phenomena exist in other 388

genes and other organisms, and more studies are needed to clarify this issue. 389

390

Contribution of Other TFBSs 391

In spite of its importance, the CArG box is unlikely to be the only CRE that determines the 392

expression differences between AP1 and CAL. Direct evidence supporting this comes from the 393

sequence-swapping experiments: when the CArG box of AP1pro2887+intr1 was replaced by a piece 394



24

of non-CArG sequence, the expression of GUS decreased but not down to the level as low as that 395

in CALpro1210+intr1; when the non-CArG sequence of CALpro1210+intr1 was replaced by the CArG 396

box, the expression of GUS increased but not up to the level as high as that in AP1pro2887+intr1 (Fig. 397

4E). This suggests that the CArG box is only part of the story and that other TFBSs, especially 398

those gained or lost along the lineages leading to the two genes, must have also been essential, 399

although their exact contributions are still unclear. Indeed, of the recently gained TFBSs along 400

the lineage leading to AP1, several have been shown to be functionally important. The 401

LFY-binding site between positions -419 and -414, for example, has been shown to be critical for 402

the initial expression of AP1 because deletion of it can cause later response to photoperiodic 403

induction (Benlloch et al., 2011). Similarly, the PISTILLATA (PI)-binding site, which is also a 404

CArG box but spans from -603 to -595, is the CRE to which the APETALA3 (AP3)-PI 405

heterodimer binds and represses AP1 expression (Sundström et al., 2006; Wuest et al., 2012). The 406

fact that exclusion of a 100 bp-long promoter region and the first intron led to nearly complete 407

loss of CAL expression in floral primordia further suggests that the differences between AP1 and 408

CAL in the time, space and level of expression have been caused by multiple factors. Additional 409

analyses are needed to elucidate the functions and contributions of the TFBSs in this region. 410

411

Interestingly, in both AP1 and CAL, a relatively short region seems to be sufficient for the basic 412

expression: constructs lacking this region were generally not expressed anywhere. In CAL, this 413

region spans from -340 to -240 and contains at least four TFBSs, whereas in AP1, the region 414

spans from -450 to -310 and contains at least five TFBSs (Wigge et al., 2005; Kaufmann et al., 415

2009). Because the binding sites of FLOWERING LOCUS D (FD) and PERIANTHIA (PAN) are 416

shared by the two genes, these results highlighted the importance of the FD and PAN proteins in 417

AP1 and CAL expression. As members of the bZIP transcription factor family, both FD and PAN 418



25

are key regulators of flower development, able to bind to the regulatory regions of AP1 and CAL 419

and induce their expression (Wigge et al., 2005; Xu et al., 2010). FD can form a protein complex 420

with FLOWERING LOCUS T (FT), the florigen, to activate flower identity genes (Wigge et al., 421

2005), whereas PAN plays key roles in determining the number and position of floral organs, as 422

inactivation of it led to the generation of pentamerous rather than the normally tetramerous 423

flowers (Chuang et al., 1999). The fact that the binding sites of FD and PAN are largely 424

overlapping and highly conserved further implies that their functions may be interdependent. 425

Presumably, it is the FD/PAN binding site, together with other TBFSs (e.g., LFY) in this region, 426

that determines the on/off of the two genes, whereas the TFBSs in other regions adjust and 427

fine-tune the time, space and level of expression. 428

429

Dynamics of TFBS Evolution 430

It is interesting that the divergence of AP1 and CAL in expression has been markedly asymmetric. 431

In the lineage leading to AP1, at least seven TFBSs were gained while no loss event could be 432

deduced. In the lineage leading to CAL, however, at least three and two TFBSs were lost and 433

gained, respectively. Interestingly, while the gains of TFBSs along the AP1 lineage occurred more 434

or less gradually during evolution, the losses and gains of TFBSs along the lineage leading to 435

CAL all occurred at the early stages of post-duplication evolution (Fig. 6); after that, CAL did not 436

gain or lose any TFBS while AP1 gained seven more TFBSs in a step-by-step manner. This 437

suggests that, shortly after gene duplication, CAL has experienced a period of degenerate 438

evolution so that several functionally important TFBSs (i.e., Dof, TCP4 and SPL9) were lost. 439

Consistent with this, CAL has evolved under less stringent functional constraint than AP1 and has 440

even experienced an exonization event in the 5’ end of the third exon during roughly the same 441

period (Supplemental Figs. S7 and S8). Presumably, it was the degenerate evolution of CAL that 442



26

allowed survival and additional diversification of both CAL and AP1. 443

444

Notably, of the TFBSs that were gained along the lineage leading to AP1, most have been shown 445

to be functionally important, through which a regulatory network involving a handful of genes 446

was formed (Parcy et al., 1998; Sundström et al., 2006; Mathieu et al., 2009; Yamaguchi et al., 447

2009; Kaufmann et al., 2010; Yant et al., 2010; Pastore et al., 2011). Within this network, some 448

genes function as activators whereas others as repressors, so that the expression of AP1 is 449

precisely regulated. Without these TFBSs, the regulation of AP1 would be as simple as that of 450

CAL, and the regulatory network specifying floral primordia would not be so sophisticated. In 451

addition, because these TFBSs were gained gradually, it is very likely that after gene duplication, 452

when AP1 happened to be the one that maintained the function of the ancestral gene, its functions 453

were further reinforced by gaining additional TFBSs. Thereafter, because of the continuous 454

reinforcements, AP1 became one of the most important regulators of flower development. Clearly, 455

the processes through which AP1 and CAL become diverged in expression pattern have been both 456

dynamic and asymmetric, and can be regarded as an excellent model for duplicate gene evolution 457

in regulatory regions. 458

459

Mechanisms of CRE Evolution 460

Several studies have attempted to summarize the mechanisms through which CREs may evolve, 461

but no consensus has been reached (Wittkopp and Kalay, 2012; Villar et al., 2014). In this study, 462

it is clear that the vast majority of the gained or lost TFBSs along the lineages leading to AP1 and 463

CAL were results of modifications of pre-existing sequences (Fig. 5A and Supplemental Fig. S6). 464

For the TFBSs whose evolutionary histories remain unclear, the possibility of modification also 465

cannot be excluded. This suggests that modification (rather than translocation) of pre-existing 466



27

sequences may be a common way of CRE origination. Indeed, because the number of nucleotides 467

is very large whereas CREs are generally short DNA pieces, it may not be very difficult for CREs 468

to evolve through modification of pre-existing sequences, if the time of evolution is sufficiently 469

long and if the sequences with degenerate sites can also be recognized by corresponding 470

transcription factors. The fact that the binding sites of the same transcription factor (such as LFY) 471

can sometimes be found in the different, non-homologous regions of paralogous genes (Fig. 6) 472

further indicates the ease of TFBS origination and the fluidic nature of TFBS functioning. 473

However, without detailed comparisons between closely related species within a phylogenetic 474

framework, like what we have done in this study, it is very difficult to determine whether the 475

TFBSs of the same sequence features and/or functional properties are homologous and how 476

newly originated TFBSs were generated. 477

478

MATERIALS AND METHODS 479

Plant Materials and Growth Conditions 480

Seeds of A. thaliana (ecotype Col-0) and C. rubella (accession 86IT1) were surface-sterilized by 481

treating with 70% ethanol and 10% hypochlorite, and plated on 1/2 Murashige and Skoog (MS) 482

medium supplemented with 1% Suc and 0.8% agar. The plates were cold treated at 4°C for 3–4 d, 483

and then transferred to the standard growth room. After germination, seedlings were transferred 484

to soil and grown under 16-h-light (22°C)/8-h-dark (18°C) photoperiod and 60% relative 485

humidity. 486

487

Identification and Evolutionary Analyses of TFBSs 488

Genomic sequences of the A. thaliana AP1 and CAL genes were retrieved from TAIR10 489



28

(http://www.arabidopsis.org/). Putative TFBSs along the genomic sequences were first predicted 490

with the help of AGRIS (http://arabidopsis.med.ohio-state.edu) (Yilmaz et al., 2011) and 491

AthaMap (http://www.athamap.de/) (Bülow et al., 2009), and then refined by referring to 492

literatures reporting the sequence features and functional properties of CREs (Supplemental Table 493

S1). Because the promoter regions and first introns of the two genes contain most, if not all, of 494

the CREs required for normal expression, special attention was paid to them. 495

496

To trace the evolutionary history of the TFBSs, we first obtained the genomic sequences of the 497

AP1 and CAL homologs from four other Brassicaceous species (A. lyrata, C. rubella, T. parvula, 498

and A. arabicum) and two non-Brassicaceous species of the Brassicales (T. hassleriana of 499

Cleomaceae, and C. papaya of Caricaceae). The sequences of A. lyrata, C. rubella, and C. 500

papaya were all obtained from Phytozome 9.1 (http://www.phytozome.net/) by TBLASTN 501

searches. In the case of T. parvula, A. arabicum, and T. hassleriana, genome sequences were 502

downloaded from GenBank (http://www.ncbi.nlm.nih.gov/). Exon-intron structures of these 503

genes were annotated with Wise2 (http://www.ebi.ac.uk/Tools/psa/genewise/) (Birney and 504

Durbin, 2000), and TFBSs were determined based on sequence similarity and relative positions 505

(Supplemental Table S2). Alignments of comparable regions were first generated in CLUSTALX 506

1.83 (Thompson et al., 1997) and then refined manually in GeneDoc (Nicholas et al., 1997). 507

Phylogenetic relationships among the sampled species were determined based on the most recent 508

study of the Brassicaceae (Couvreur et al., 2010). Gains and losses of TFBSs were inferred 509

according to the maximum parsimony algorithm. 510

511

Expression Analysis 512

Total RNA was extracted from different tissues using the PureLink Plant RNA Reagent 513



29

(Invitrogen) according to the user manual. First-strand cDNA was synthesized from 1 μg of total 514

RNA using an oligo (dT) primer and SuperScript III first-strand cDNA synthesis kit (Invitrogen), 515

following manufacturer’s instructions. Quantitative real-time reverse transcription-polymerase 516

chain reaction (qRT-PCR) was performed using the PrimerScript RT Reagent Kit (Perfect Real 517

Time) (Takara) in an Applied Biosystems ViiA™ 7 Real-Time PCR System (Life Technologies). 518

For each gene, at least two pairs of primers were designed, and their amplification efficiencies 519

were determined by comparing the standard curves. Only primer pairs showing amplification 520

efficiencies between 90 to 105% were used (Supplemental Table S4). Relative expression values 521

were first normalized to a house-keeping gene, ACTIN, and then calculated by the comparative Ct 522

(2-ΔΔCt) method (Livak and Schmittgen, 2001). All reactions were run in three biological 523

replicates, each of which has three technical replicates. Statistical analyses of the qRT-PCR data 524

were performed with the two-tailed t-test. 525

526

For in situ hybridization, inflorescences with floral buds at various developmental stages were 527

first fixed in 4% (wt/vol) paraformaldehyde, and then embedded in Paraplast (Sigma). The 528

323-bp probe fragment specific to AP1 and the 313-bp probe fragment specific to CAL, both of 529

which cover the C-terminal ends of their coding sequences, were amplified from cDNA using 530

gene-specific primers, with the T7 adapter being introduced into the reverse primer 531

(Supplemental Table S4). PCR products were used as templates for synthesizing antisense 532

digoxigenin-labeled RNA probes with the DIG RNA Labeling Kit (Roche). Pretreatment, 533

hybridization, and washing of sections (10 μm) were performed as described (Zhang et al., 2013), 534

with minor modifications. The sections were exposed to 1μg/ml Proteinase K buffer for 30 min at 535

37°C before hybridization, and final washing of the hybridized sections were carried out in 536

0.5×SSC at 50°C for 30 min. Images were captured with a Zeiss Axio imager microscope. 537



30

538

Transgenic Constructs and Genetic Transformation 539

To generate the AP1pro2887+intr1:GUS construct, a 2887-bp promoter fragment upstream of the 540

translation start site and intron 1 of AP1 were amplified by using the primer combinations 541

AP1pro2887-F/AP1pro2887-R and AP1intr1-F/AP1intr1-R (Supplemental Table S4), respectively. 542

Amplified fragments were cloned into the pEASY-Blunt Simple vector (TransGen 543

Biotechnology), and assembled into the pENTR4 vector (Invitrogen) by digestion with 544

appropriate restriction enzymes. The full-length fragment containing the promoter region and 545

intron 1 of AP1 was subsequently transferred into pHGWFS7 destination vectors by LR clonase 546

reaction (Invitrogen). For the CALpro1210+intr1:GUS construct, a 1210-bp promoter fragment and 547

intron 1 of CAL were amplified with the primer combinations CALpro1210-F/CALpro1210-R and 548

CALintr1-F/CALintr1-R, respectively (Supplemental Table S4). PCR-based mutagenesis was 549

performed to yield the AP1pro2887(mut805-796)+intr1:GUS and CALpro1210(mut703-693)+intr1:GUS constructs 550

(Supplemental Table S4). To generate constructs containing different lengths of AP1 or CAL 551

promoters, truncated fragments were amplified from Col-0 genomic DNA by PCR using 552

position-specific primers (Supplemental Table S4), and the amplified fragments were then 553

recombined into the pHGWFS7 destination vector. 554

555

All recombinant plasmids were transferred into the wild type A. thaliana (Col-0) plants by using 556

the Agrobacteriaum tumefaciens (GV3101)-mediated floral dip method (Clough and Bent, 1998). 557

Seeds of transgenic plants were selected on solid 1/2 MS medium containing hygromycin (25 558

µg/ml) and genotyped by PCR with GUS-specific primers (Supplemental Table S4). For each 559

construct, at least 30 independent positive transgenic plants were analyzed in terms of GUS 560

activity (Supplemental Table S5). 561



31

562

GUS Staining 563

Inflorescences under investigation were incubated in 90% ice-cold acetone for 15 to 20 min, 564

rinsed in the solution containing 100mM sodium-phosphate buffer (pH7.0), 1 mM K3Fe(CN)6, 565

and 1 mM K4Fe(CN)6, immersed into GUS staining solution containing 100mM 566

sodium-phosphate buffer (pH 7.0), 1 mM K3Fe(CN)6, 1 mM K4Fe(CN)6, 2 mM X-gluc, 10 mM 567

EDTA, and 0.1% TritonX-100, and then vacuum-infiltrated until tissues became translucent. The 568

materials were incubated overnight at 37℃ in the GUS staining solution. After staining, the 569

inflorescences were cleared with an ethanol series and maintained in 70% ethanol. For 570

anatomical observations, GUS-stained inflorescences were embedded and sectioned as above 571

described. Whole-mount staining samples and histological sections were visualized using Leica 572

S8 APO and Leica DM5000 B microscopes, respectively. 573

574

Electrophoretic Mobility Shift Assay (EMSA) 575

Coding sequences of AP1, CAL, CruAP1 and CruCAL were amplified with the AthAP1-F/R, 576

AthCAL-F/R, CruAP1-F/R and CruCAL-F/R primer combinations (Supplemental Table S4), 577

respectively. Amplified fragments were first digested and inserted into the pET28a expression 578

vector (Novagen), and then transformed into Escherichia coli BL21(DE3) competent cells. 579

Expression of corresponding proteins was induced by adding 0.1 mM isopropyl 580

β-D-thiogalactoside, and the concentration of proteins was measured with a BCA Protein Assay 581

Kit (Pierce). 582

583

EMSA assays were done using a Light Shift Chemiluminescent EMSA Kit (Thermo Scientific). 584



32

Briefly, 500 fmol 5’-biotin-labeled probe DNA was incubated with 1.5 μg poly(dI.dC) and 1 μg 585

proteins in 1× binding buffer at room temperature for 20 min. Reactions were then loaded onto a 586

6.5% polyacrylamide gel (0.25×TBE) and run at 180 Volts constant for 1 hour at 4℃. Blots were 587

cross-linked using Stratalinker-UV1800 device for 10min. 588

589

Probe AP1 (5’-GACAAAATACTATTTTTGGGTTTGAAA-3’) was derived from AP1 promoter. 590

Probe CAL (5’-ATATTTCCTTAATTAACCCAAACTTC-3’) and probe CruAP1 591

(5’-ACAGAACACTTTTTCGGGTTTGAATAC-3’) were derived from the corresponding 592

regions of probe AP1 in the CAL and CruAP1 promoters, respectively. The sequence of positive 593

control is 5’-AATACATTCCATATTTGGCAGGTGG-3’, which can be bound by AP1 in vitro 594

(Huang et al., 1993; Riechmann et al., 1996b). The CArG box in probe AP1 and positive probe is 595

underlined. 596

597

ChIP-seq Data Analysis 598

Short sequence read dataset from ChIP-Seq experiments for AP1 (Kaufmann et al., 2010) was 599

downloaded from the ArrayExpress database (http://www.ebi.ac.uk/arrayexpress/). Low-quality 600

reads in the raw data were filtered out using FastQC software 601

(http://www.bioinformatics.bbsrc.ac.uk/projects/fastqc/). The processed reads were then mapped 602

to the A. thaliana genome (TAIR10) using Bowtie2 (Langmead and Salzberg, 2012) with 603

allowing 0 mismatches and only uniquely mapped reads to be counted. Peak calling was done 604

using MACS2 (Zhang et al., 2008) with default parameters. ChIP-seq data visualized using IGV 605

(Thorvaldsdottir et al., 2013). 606

607



33

Supplemental Data 608

The following supplemental materials are available. 609

Supplemental Figure S1. Heatmap showing the prevalence of expression divergence between 610

duplicated MIKC-type MADS-box genes in Arabidopsis thaliana. 611

612

Supplemental Figure S2. The DotPlot result of AP1 (6946 bps, horizontal axis) and CAL (5756 613

bps, vertical axis). 614

615

Supplemental Figure S3. Comparison of the promoter regions of AP1 and CAL. 616

617

Supplemental Figure S4. The DotPlot result of genomic sequences of AP1 (4046 bps, horizontal 618

axis) and CAL (3756 bps, vertical axis). 619

620

Supplemental Figure S5. TFBS evolution. TFBSs gained or lost during different evolutionary 621

stages are indicated in the corresponding positions of the phylogenetic tree by filled and open 622

boxes, respectively. 623

624

Supplemental Figure S6. Alignments of representative TFBS-containing regions in a 625

phylogenetic framework. 626

627

Supplemental Figure S7. CAL evolved under the less stringent constraint than AP1. 628

629

Supplemental Figure S8. Sequence alignment of ancestral and present-day AP1- and CAL- like 630



34

proteins. 631

632

Supplemental Table S1. Functionally confirmed TFBSs in AP1 and CAL regulatory regions. 633

634

Supplemental Table S2. Sequences and positions of the TFBSs shown in Supplemental Figure 635

S5. 636

637

Supplemental Table S3. AP1- and CAL-like genes included in this study. 638

639

Supplemental Table S4. Primer sequences used in this study. 640

641

Supplemental Table S5. Independent transgenic lines examined by GUS-staining analyses. 642

643

ACKNOWLEDGEMENTS 644

We thank Yalong Guo for generously providing C. rubella seeds, Xianxian Yu, Rui Zhang and 645

Peipei Wang for technical assistances in qRT-PCR and microscopy, Chunce Guo and Guixia Xu 646

for help in bioinformatic and statistical analyses, and Hong Ma, Shin-Han Shiu, the Kong Lab 647

members and two anonymous reviewers for valuable comments. 648

649

Figure Legends 650

Figure 1. Expression patterns of AP1 and CAL. (A) to (H) Results of in situ hybridization for 651

AP1 (A–D) and CAL (E–H). Scale bar, 100 µm. fm, floral primordia; se, sepal; pe, petal; st, 652

stamen; ca, carpel. Stages of flower development were determined as described (Smyth et al., 653

1990). The black triangle points to the cells underneath the floral buttress.(I) to (K) Results of 654



35

qRT-PCR for AP1 (purple) and CAL (blue) in inflorescences bearing flowers of stages 1–12 (I), 655

1–9 (J), and 10–12 (K), respectively. For each gene, three biological replicates were conducted, 656

and error bars indicate the standard deviation (SD) of the three technical replicates of each 657

biological replicates. 658

659

Figure 2. Regulatory regions of AP1 and their contributions to expression pattern. (A) Predicted 660

TFBSs in the promoter (white box), the first exon (black box), and the first intron (gray box). 661

TFBSs in black are those shared by AP1 and CAL, whereas those in purple are AP1-specific. 662

Experimentally confirmed TFBSs are underlined. (B) to (G) Genomic regions used to drive the 663

expression of GUS and the resultant expression patterns. Scale bars, 1 mm in 1, 2, and 6; 100 µm 664

in 3–5. 665

666

Figure 3. Regulatory regions of CAL and their contributions to expression pattern. (A) Predicted 667

TFBSs in the promoter (white box), the first exon (black box), and the first intron (gray box). 668

TFBSs in black are those shared by AP1 and CAL, while those in blue are CAL-specific. 669

Experimentally confirmed TFBSs are underlined. (B) to (G) Genomic regions used to drive the 670

expression of GUS and the resultant expression patterns. Scale bars, 1 mm in 1, 2, and 6; 100 µm 671

in 3–5. 672

673

Figure 4. Function of the AP1-binding CArG box. (A) qRT-PCR results showing GUS signals in 674

plants expressing four different constructs. For each construct, three independent transgenic lines 675

were conducted. Error bars indicate the SD of three technical replicates. (B) ChIP-seq results, 676

reanalyzed from the data of Kaufmann et al. (2010), showing the AP1-binding regions around the 677

AP1 (up) and CAL (below) genes. Sequenced reads from two biological replicates were combined 678



36

and plotted as normalized read coverage on the vertical axis against the genomic location along 679

the horizontal axis. “Treat” and “control” represent 35S:AP1-GR ap1-1 cal-1 plants treated and 680

untreated with dexamethasone-containing solution, respectively. Arrows indicate gene 681

orientations. The scale division corresponds to 1,000 nt. (C) EMSA assays showing that the 682

binding affinities of the AP1 and CAL proteins to the CArG box-containing AP1 probe are much 683

stronger than the CArG box-lacking CAL probe. Positive probe contains a canonical AP1-binding 684

CArG box that has been verified in vitro (Riechmann et al., 1996b). pET28a represents a negative 685

control in which the in vitro translation assay was programmed with the empty pET28a vector. 686

Asterisks indicate the positions of the protein-DNA complexes. (D) GUS constructs used to 687

determine the functions of the CArG box. AP1pro2887(mut805-796)+intr1 and CALpro1210(mut703-693)+intr1 688

are two constructs in which the CArG box of AP1 was swapped with a piece of non-CArG box 689

sequence of CAL in the corresponding position. (E) qRT-PCR results showing GUS expression in 690

plants expressing the four constructs in (D). (F) and (G) GUS signals in the plants expressing the 691

AP1pro2887(mut805-796)+intr1 (F) and CALpro1210(mut703-693)+intr1 (G) constructs, respectively. Scale bars, 1 692

mm in 1, 2, and 6, and 100 µm in 3–5. 693

694

Figure 5. Origin of the AP1-binding CArG box and its consequences. (A) An alignment of the 695

corresponding regions in a phylogenetic framework, which suggests that the CArG box was 696

gained in the ancestor of AP1 and AlyAP1, likely through modification of a pre-existing 697

non-CArG box sequence. Dots represent the same nucleotides as those in AP1 whereas dashes 698

indicate alignment gaps. (B) EMSA assay showing the binding ability of CruAP1 and CruCAL in 699

vitro. Positive probe contains a canonical AP1-binding CArG box that has been verified in vitro 700

(Riechmann et al., 1996b). pET28a represents the negative control in which an in vitro translation 701

assay was programmed with the empty pET28a vector. Asterisks show the position of the 702



37

DNA-protein complexes. (C) qRT-PCR results showing the relative expression levels of AP1, 703

CruAP1 in inflorescences bearing flowers of stages 10–12. For each gene, three biological 704

replicates were conducted, and error bars indicate the SD of three technical replicates. (D) A 705

cartoon showing the divergence of AP1 and CAL in expression pattern. The gene duplication 706

giving rise to AP1 and CAL occurred before the origin of Brassicaceae, while the gain of the 707

CArG box happened after the divergence of Arabidopsis from Capsella. Because of the gain of 708

the CArG box, AP1 and CAL diverged in the time, space and level of expression. fm, floral 709

primordia; se, sepal; pe, petal; st, stamen; ca, carpel. (E) A model depicting the gain of the CArG 710

box and the formation of a regulatory cascade involving AP1 and CAL. AncAP1, the ancestor of 711

the AP1 orthologs; AncCAL, the ancestor of the CAL orthologs; ovals, proteins of the 712

corresponding genes. 713

714

Figure 6. TFBS evolution along the lineages leading to AP1 and CAL. In the ancestral gene, 715

TFBSs shared by AP1 and CAL are in black whereas those specific to AP1 are in purple. 716

Experimentally confirmed TFBSs are underlined. TFBSs gained and lost during different 717

evolutionary stages are indicated in the corresponding positions of the phylogenetic tree by filled 718

and open boxes, respectively. The loss of the binding site of SQUAMOSA 719

PROMOTER-BINDING PROTEIN-LIKE 3/9 (SPL3/9) along the CAL lineage is not shown, 720

however, because its exact position is still uncertain. Ages (mya: million years ago) of nodes 721

indicated by gray numbers are based on (Beilstein et al., 2010). For details, see Supplemental 722

Figure S5. 723

724

725



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Gain of An Auto-regulatory Site Led to Divergence of the ...

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