1 short title: flavanoid pathway regulation by mir858...2016/04/27 · 10 deepika sharma1, 2,...

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Short title: Flavanoid pathway regulation by miR858 1

Corresponding author: 2

Prabodh Kumar Trivedi, 3 CSIR-National Botanical Research Institute, Rana Pratap Marg, Lucknow-226001, INDIA 4 [email protected]; [email protected] 5 6

Research area: Biochemistry and metabolism 7

MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant 8 development in Arabidopsis 9

Deepika Sharma1, 2, Manish Tiwari1, $, Ashutosh Pandey1, #, Chitra Bhatia1, 2, Ashish Sharma1, 10 Prabodh Kumar Trivedi1, 2,* 11 1CSIR-National Botanical Research Institute, Council of Scientific and Industrial Research 12

(CSIR-NBRI), Rana Pratap Marg, Lucknow-226001, INDIA 13

2Academy of Scientific and Innovative Research (AcSIR), Anusandhan Bhawan, 2 Rafi 14

Marg, New Delhi-110 001, India 15

Summary: miR858a targets MYB transcriptions factors involved in flavonoid biosynthesis 16

and plant growth and development 17

DS, AP and CB thankfully acknowledge the Council of Scientific and Industrial Research 18

(CSIR), New Delhi for Senior Research Fellowship. MT acknowledges Indian Council of 19

Medical Research for Research Fellowship. Research was supported by Council of Scientific 20

and Industrial Research, New Delhi in the form of Network projects PlaGen (BSC-0107). 21

22 $Present address (MT): Department of Biology, Western Kentucky University Bowling 23

Green, KY, USA. 24

$Present address (AP): National Agri-Food Biotechnology Institute (NABI), Mohali-160071, 25

Punjab, INDIA 26

The authors responsible for distribution of materials integral to the findings presented in this 27

article in accordance with the policy described in the Instructions for Authors 28

(www.plantcell.org) are: Prabodh Kumar Trivedi ([email protected]). 29

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Corresponding author’s e-mail: [email protected]; [email protected] 31

Plant Physiology Preview. Published on April 27, 2016, as DOI:10.1104/pp.15.01831

Copyright 2016 by the American Society of Plant Biologists

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ABSTRACT 32

MicroRNAs (miRNAs) are endogenous, non-coding small RNAs which function as critical 33

regulators of gene expression. In plants, miRNAs have highlighted their potential as 34

regulators of growth, development, signal transduction and stress tolerance. Though miRNA-35

mediated regulation of several processes is known, the involvement of miRNAs in regulating 36

secondary plant product biosynthesis is poorly understood. In this study, we functionally 37

characterized Arabidopsis miR858a which putatively targets R2R3-MYB transcription 38

factors involved in flavonoid biosynthesis. Over-expression of miR858a in Arabidopsis led to 39

down-regulation of several MYB transcription factors regulating flavonoid biosynthesis. In 40

contrast to the robust growth and early flowering of miR858OX plants, reduction of plant 41

growth and delayed flowering was observed in Arabidopsis transgenic lines expressing 42

artificial miRNA target mimic (MIM858). Genome-wide expression analysis using transgenic 43

lines suggested that miR858a targets a number of regulatory factors which modulate 44

expression of down-stream genes involved in plant development, hormonal and stress 45

responses. Further, higher expression of MYBs in MIM858 lines leads to the redirection of 46

the metabolic flux towards the synthesis of flavonoids at the cost of lignin synthesis. 47

Altogether, our study established the potential role of light-regulated miR858a in flavonoids 48

biosynthesis and plant growth and development. 49

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Keywords: miR858, Arabidopsis, gene regulation, transcription factors, development, 51

secondary metabolites 52

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INTRODUCTION 61

MicroRNAs (miRNAs) are small mostly non-coding (22-24 nt) RNAs which modulate gene 62

expression by pairing to corresponding target mRNA and promote mRNA degradation and/or 63

translation inhibition (Llave et al., 2002; Brodersen et al., 2008; Filipowicz et al., 2008). 64

miRNAs are important regulators of many physiological and developmental processes 65

(Voinnet, 2009), and their misexpression leads to a variety of defects in plants (Wu, 2013). 66

Various studies have demonstrated that miRNAs regulate flowering, leaf, seed, root 67

morphology as well as stress and hormonal responses in plants (Leung and Sharp, 2010; Liu 68

and Chen, 2010; Stauffer and Maizel, 2014; Hong and Jackson, 2015; Zhang, 2015). Recent 69

developments in genome-wide experimental approaches involving miRNA over-expression 70

(Wu, 2013), use of miRNA target mimics (Franco-Zorrilla et al., 2007; Eamens and Wang, 71

2011; Meng et al., 2012) and detailed analysis of miRNA promoters (Baek et al., 2013; 72

Sharma et al., 2015) were helpful to understand the physical interactions between miRNAs 73

and their target mRNAs as well as biological significances in plant growth and development 74

(de Lima et al., 2012; Wu, 2013). The majority of miRNAs are known to target transcription 75

factors which regulate development, hormonal regulation and stress responses in plants 76

(Sunkar et al., 2012; Wu, 2013; Zhang, 2015; Zhang and Wang, 2015). 77

Flavonoids are low molecular weight polyphenolic compounds and encompass a 78

diverse class of phenolic compounds including flavonols, flavones, isoflavones, 79

anthocyanins, proanthocyanidins (PAs) and phlobaphene pigments (Taylor and Grotewold, 80

2005; Lepiniec et al., 2006; Buer et al., 2010). The biological functions of flavonoids are as 81

pigments, signalling molecules, UV-protectants, phytoalexins, and regulators of auxin 82

transport in plants (Winkel-Shirley, 2001; Buer and Muday, 2004; Santelia et al., 2008). The 83

phenylpropanoid pathway is the main route for flavonoid biosynthesis, and transcriptional 84

regulation of this pathway is one of the most studied pathways in plants (Quattrocchio et al., 85

2006; Stracke et al., 2007). The synthesis of the most flavonoid compounds shares common 86

enzymes, and sometimes the enzymes of the specific branch are controlled by distinct 87

regulators. MYB11, MYB12 and MYB111 have been demonstrated to regulate biosynthesis 88

of flavonols by targeting genes encoding early pathway enzymes such as CHS, CHI, F3’H 89

and FLS recruited in phenylpropanoid pathway (Mehrtens et al., 2005; Stracke et al., 2007; 90

Stracke et al., 2010). The MYB123 (TT2) controls the biosynthesis of PAs in the seed coat of 91

Arabidopsis (Xu et al., 2014). Similarly, members of the R2R3MYB protein family for 92

instance, MYB58, MYB63 and MYB85, regulate lignin biosynthesis in fibres and vessels 93



4

whereas MYB46 and MYB83 act as switch regulators during secondary wall biosynthesis 94

(Zhong et al., 2008; McCarthy et al., 2009; Zhou et al., 2009; Zhong and Ye, 2012). Flavonol 95

biosynthesis is a highly complex, tissue and developmentally regulated process in 96

Arabidopsis which is orchestrated by the group of R2R3-MYB transcription factors, 97

including MYB11, MYB12 and MYB111. These MYBs differentially affect the spatial 98

accumulation of specific flavonols in Arabidopsis (Stracke et al., 2007). 99

In past few years, studies demonstrated that miRNAs may act as master regulators of 100

flavonoid biosynthesis in Arabidopsis. It has been shown that the miR156-SPL9 network 101

directly influence anthocyanin production through targeting genes encoding PAP1 and DFR 102

(Gou et al., 2011; Cui et al., 2014). The miR163 targets S-adenosylmethionine-dependent 103

methyltransferases which methylate secondary metabolites and signalling molecules (Ng et 104

al., 2011). Studies have also revealed that miR397 regulate lignin biosynthesis by altering 105

lacasse expression in Arabidopsis and Populus (Lu et al., 2013; Wang et al., 2014). It has 106

been reported that miR159, miR319 and miR828 families deregulate MYB transcription 107

factors in Malus, Solanum lycopersicum, Vitis and Salvia miltiorrhiza (Xia et al., 2012; Rock, 108

2013; Li et al., 2014; Jia et al., 2015). Similarly, a study demonstrated that miR828 regulate 109

MYB2, which is involved in trichome and cotton fibre development (Guan et al., 2014). 110

In this study, we investigated the role of miR858a in the regulation of the 111

phenylpropanoid pathway and development in Arabidopsis. The genetic, molecular, cellular 112

and biochemical experiments using transgenic lines expressing miR858a (miR858OX) and 113

artificial miR858 target mimic (MIM858) show that miR858a targets flavonol-specific MYBs 114

involved in regulating early steps of the flavonoid biosynthetic pathway. Genome-wide 115

expression and detailed metabolite analyses of transgenic lines suggest that miR858a plays an 116

important role in plant growth and development. We conclude that the miR858a-MYB 117

network is an additional regulatory sector of the module that coordinates flavonoid and lignin 118

biosynthesis in plants. 119

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RESULTS 122

Identification of miRNAs Regulating Flavonoid Biosynthesis 123

As a first step to identify the potential miRNAs regulating MYB11, MYB12 and MYB111 124

transcription factors, nucleotide sequences of the mRNAs were used for BLAST searches 125

against the Sanger miRNA database (http://microrna.sanger.ac.uk). Ath-miR858 showed 126

significant sequence homology with these MYB transcription factors. Besides, analysis using 127

the WMD3 miRNA target identification tool (Schwab et al., 2006) identified a number of 128

putative targets of miR858. The result suggested that MYB11, MYB12 and MYB111 could be 129

the best potential targets of miR858 with hybridization energy of the duplex structure ≤ −35 130

kcal/mol and average homology ≥ 80% (Figure 1A). The detailed bioinformatic analysis 131

revealed that miR858 sequences are evolutionarily conserved in dicot species such as 132

Arabidopsis, Gossypium, Solanum and Cucumis (Supplementary Table S1). Similar to our 133

observation, Xia et al., (2012) reported that miR858 and its targets are well conserved in 134

diverse dicot species. There are two members of the miR858 family (ath-miR858a/b) present 135

in Arabidopsis genome as listed in miRBase, release 21. The mature sequence of miR858a 136

differs from miR858b by the single nucleotide (Supplementary Table S1). However, 137

miR858a and miR858b are transcribed from different loci, but target similar sets of MYB 138

transcription factors. Therefore, we focused on studying the role of miR858a as a putative 139

regulator of MYB transcription factors in this study. 140

Widespread Expression of miR858a in Arabidopsis 141

To investigate the spatio-temporal expression of endogenous miR858a, quantitative RT-PCR 142

analysis of mature miR858a was carried out at different stages of Arabidopsis development. 143

The analysis suggested that miR858a is expressed in rosette, root, stem, flower, silique and 144

seedling (Figure 1B). Comparative expression analysis revealed that miR858a is 145

predominantly found in the silique, at least, an order of magnitude higher compared to 146

seedling, root, stem, rosette leaves and flower of the mature plant. These results revealed that 147

miR858a is expressed extensively in all the studied tissues and indicated that it may have an 148

important role in the plant growth and development. 149

To study the tissue-specific expression of miR858a, a promoter-reporter 150

(ProMIR858a:GUS) expressing transgenic lines of Arabidopsis were developed. 151

Histochemical GUS analysis in tissues of various developmental stages revealed that 152

ProMIR858a is active in seedling, rosette leaf, stem, flower buds and mature silique (Figure 153

1C). It is important to mention that an intense GUS staining was observed in the vascular 154



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tissues of hypocotyl, root and leaf veins of the seedling (Figure 1C, b and c) as well as in 155

rosette leaf, stem, flower and silique of mature plants (Figure 1C, d to h). Though GUS 156

staining patterns (Figure 1C) are in general consistent with the miR858a transcript abundance 157

(Figure 1B), differences in relative GUS staining between rosette, flower and silique tissues 158



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were observed. These differences might be due to the limitation of the promoter:GUS 159

approach in studying the spatial expression of genes. Altogether, these results suggested that 160

miR858a is expressed in all the developmental stages and might be one of the key regulators 161

of the plant growth and development. 162

The search for cis-regulatory motifs in the promoter region of pre-miR858a using the 163

Plant-CARE database revealed the assortment of putative light responsive elements (LREs) 164

(Supplementary Table S2). Light is one the most important factors affecting MYB 165

transcription factor and thereby flavonoid biosynthesis in Arabidopsis (Stracke et al., 2010). 166

Based on the abundance of LREs in the miR858a promoter, we assumed that light may be an 167

important factor for transcriptional activation of miR858a. To verify this, we measured the 168

expression of miR858a and the ProMIR858a:GUS reporter gene under light and dark cycles. 169

In the light-to-dark transition assay, miR858a precursor transcript level was considerably 170

reduced in the WT (Col-0) background (Figure 1D). We further confirmed the transcriptional 171

activation of miR858a precursor gene in response to light (Figure 1E). A marked decrease in 172

GUS staining and GUS gene expression was observed when seedlings were grown under 173

continuous dark for 5 days as compared to standard growth conditions (Supplementary Figure 174

S1A, a, b, S1B). Interestingly, GUS staining and GUS gene expression increased after 175

transfer of dark-grown seedlings to light for different time periods (Supplementary Figure 176

S1A, c to e, S1C). The pattern of GUS staining was comparable to GUS gene expression 177

under light-dark cycle (Supplementary Figure S1). Together, our results demonstrate that 178

miR858a is extensively expressed in Arabidopsis, and its transcript levels are highly 179

dependent on light. 180

181

miR858a Targets R2R3-MYB Transcription Factors 182

To predict possible targets of miR858a in Arabidopsis, we used the online prediction 183

algorithm WMD3 and psRNAtarget. The analysis identified more than 40 putative targets of 184

miR858a including MYB11, MYB12 and MYB111 (Supplementary Table S3). Most of the 185

identified targets were members of Arabidopsis R2R3 domain containing MYB family 186

including MYB3, MYB4, MYB6, MYB11, MYB12, MYB32, MYB63, MYB85, MYB111, 187

MYB123, MYB305 and MYBL2. Our analysis suggests that miR858a may target these 188

transcription factors as it has a sequence complementary to the mRNA sequences encoding a 189

conserved part of the R2R3MYB DNA binding domain. To correlate expression of miR858a 190

and their putative targets, the abundance of the MYB11, MYB12 and MYB111 genes in 191

different tissues of Arabidopsis was analysed through qRT-PCR. Results demonstrated 192



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differential expression of miR858a as well as MYB11, MYB12 and MYB111 in rosette, stem, 193

flower, silique and seedling. The maximum expression of miR858a was observed in siliques 194

and the least in rosettes (Figure 1B). Interestingly, the expression of MYB11, MYB12 and 195

MYB111 overlapped with the abundance of miR858a in the stem and flower (Figure 1B). 196

These results correlate with previous reports where both miRNA and target mRNAs are 197

predominantly detected in the same tissues in Arabidopsis (Llave et al., 2002; Zhang and Li, 198

2013). The highest expression of miR858a was observed in the seedling with least expression 199

of MYB11 and MYB12. The observations clearly suggest that miR858a may target flavonol-200

specific MYBs in Arabidopsis. 201

Moreover, to experimentally confirm the target of miR858a, we analysed cleavage 202

products of RISCmiR858a action through RNA ligase-mediated 5' amplification of cDNA ends 203

(RLM-RACE). MYB11 and MYB111 were confirmed as targets of miR858a (Figure 1F). 204

Although, during RLM-RACE analysis, we were unable to get cleavage product of MYB12, 205

however, an earlier study has shown MYB12 to be a direct target of miR858 (Fahlgren et al., 206

2007). In addition, cleavage products for MYB6, MYB13, MYB20, MYB42, MYB48, MYB83, 207

TT2 and MYBL2 were also identified through RLM-RACE (Supplementary Figure S2). The 208

analysis confirmed MYB13 as a direct target of miR858a (Supplementary Figure S2B). A 209

majority of the cleavage products for MYB6, MYB20, MYB42, MYB48, MYB83, TT2 and 210

MYBL2 were detected outside of the canonical miRNA cleavage sites (Supplementary Figure 211

S2). It is likely that such cleavage might be mediated by variants of the mature miRNA, 212

abundant miRNA* sequences or miRNA/miRNA* duplexes from the same hairpin as 213

suggested by Addo-Quaye et al., (2008). Overall, the results showed that flavonol-specific 214

MYBs namely MYB11, MYB12 and MYB111 are direct targets of miR858a. 215

miR858a Modulates Phenylpropanoid Pathway in Arabidopsis 216

To investigate the function of miR858a, we developed miR858a over-expressing transgenic 217

lines (miR858OX) under the control of CaMV35S promoter in Arabidopsis. To further 218

strengthen the study, we generated the artificial target mimic (MIM858) expressing transgenic 219

lines that supposed to nullify the effect of the endogenous miR858a activity. Homozygous 220

transgenic lines for both, miR858OX and MIM858, were selected for further analysis. 221

Significant modulation in the expression of the miR858a was observed in miR858OX and 222

MIM858 transgenic lines (Figure 2A, 2B). As expected, expression of miR858a was 223

significantly higher in miR858OX lines (Figure 2A). Surprisingly, expression of miR858a 224

was significantly compromised in transgenic lines expressing MIM858 compared to WT 225



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plants (Figure 2B). Previous studies on Arabidopsis and bacteria have also described 226

decreased levels of the targeted miRNA after MIM expression. These studies suggested that 227

unproductive interaction of RISCmiRNA with MIM affects miRNA stability (Overgaard et al., 228

2009; Todesco et al., 2010). We suggest that a similar mechanism might be the reason for the 229



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decreased levels of miR858a in MIM858 transgenic lines. Mature miR858a accumulated in 230

miR858OX lines at significantly higher levels in all the tissues as compared to the WT 231

(Supplementary Figure S3) indicating the successful biogenesis of ectopic miR858a 232

precursors. 233

To study whether over-expression and sequestration of miR858a affected the 234

expression of MYB11, MYB12 and MYB111 genes, the transcript levels of these MYBs were 235

analyzed in the rosette tissue. Expression of MYB11, MYB12 and MYB111 was significantly 236

reduced in miR858OX lines (Figure 2C) which suggests a negative correlation between 237

miR858a and target gene expression. On the other hand, as a result of the sequestration of the 238

endogenous miR858a by the expression of MIM858, elevated levels of the MYB11, MYB12 239

and MYB111 transcripts were observed (Figure 2D). Detailed study of the expression patterns 240

of miR858a targets revealed that most of these genes were down-regulated in different tissues 241

in miR858OX lines (Supplementary Figure S4). 242

To study whether modulation of miR858a levels affects flavonoid pathway genes, 243

expression of CHS, CHI, F3’H and FLS1 was studied in transgenic lines. Analysis revealed 244

that expression of these genes was reduced in miR858OX lines in comparison to WT (Figure 245

2E). Contrasting results were obtained in MIM858 transgenic plants with a significant 246

enhanced expression of CHS, CHI, F3’H and FLS1 as compared to WT (Figure 2F). This 247

suggests that miR858a expression negatively affects the flavonoid biosynthetic pathway by 248

repressing activities of the MYB11, MYB12 and MYB111 transcription factors. Moreover, 249

we also performed comparative expression analysis between WT and miR858OX lines using 250

Affymetrix microarray platform. Analysis revealed that expression of the putative targets 251

(MYB40, MYB65, MYB83, MYB86 and MYB111) and flavonoid biosynthesis genes (CHS, 252

CHI and FLS1) are negatively correlated with the miR858a expression levels (Supplementary 253

Table S4, Supplementary Figure S5A, S5B). Altogether, the data implies that miR858a 254

controls the phenylpropanoid pathway by regulating expression of the flavonol-specific MYB 255

transcription factors in Arabidopsis. 256

miR858a is Required for Plant Growth and Development 257

Our genome-wide expression analysis and in silico prediction along with the RLM-RACE 258

analysis confirmed MYB20, MYB42, MYB83 as targets of miR858a (Supplementary Data Set 259

S1, Supplementary Figure S2). These MYBs are known to be associated with plant growth 260

and development (Zhong et al., 2008; McCarthy et al., 2009; Dubos et al., 2010; Zhong and 261

Ye, 2012). Therefore, we studied growth parameters of the transgenic and WT plants 262



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throughout the life cycle. The results suggested that ectopic expression of miR858a and 263

MIM858 changes the various morphological characters with contrasting phenotypes between 264

miR858OX and MIM858 transgenic lines. Transgenic plants over-expressing miR858a 265

showed an elevated vegetative growth phenotype while MIM858 exhibited reduced 266



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vegetative growth as compared to WT plants just after germination. Significantly longer root 267

length, cotyledonary growth and seedling fresh weight were observed in miR858OX lines as 268

compared to the WT. In addition, shorter primary roots with smaller cotyledonary growth and 269

lower seedling fresh weight were observed in MIM858 lines as compared to miR858OX lines 270

and WT (Figure 3A-3C, Supplementary Table S5, Supplementary Figure S6A). 271

Rapid growth and more serrate margins of rosette leaves were observed in mature 272

miR858OX transgenic lines as compared to WT (Figure 3D, 3E). However, no significant 273

difference was seen in the leaf number, rosette diameter, rosette fresh weight and plant height 274

in mature miR858OX transgenic plants (Figure 3E-3G, Supplementary Table S5, S6, 275

Supplementary Figure S6B). Concomitantly, MIM858 lines displayed smaller rosette 276

phenotype during the early developmental stage. Even at the time of bolting, the rosette 277

diameter is significantly reduced as compared to WT (Figure 3D, Supplementary Table S5). 278

The rosette leaves of mature MIM858 plants displayed elongated with sinuate margins 279

compared to WT and miR858OX (Supplementary Figure S6B). Marked differences in the 280

rosette fresh weight and plant height were also observed (Supplementary Table S6, 281

Supplementary Figure S6). These results suggest that miR858a is one of the crucial regulators 282

of plant growth and development. 283

Altered Reproductive Phase Parameters in Transgenic Lines 284

The variation in the flowering time and flower size of miR858OX and MIM858 transgenic 285

lines was observed as compared to WT plants (Figure 3, 4). Under standard growth 286

conditions, early bolt formation and flowering were observed in the miR858OX plants in 287

comparison to WT whereas bolt formation and flowering time was significantly delayed in 288

the MIM858 plants relative to the WT (Figure 3D, 3F). More rosette leaves as compared to 289

WT were observed in the MIM858 transgenic lines though no significant change was 290

observed in the miR858OX lines. Unlike miR858OX lines, a significantly reduced rosette 291

diameter was observed in the MIM858 transgenic lines as compared to the WT (Figure 3D, 292

3G). Aside from flowering time, a significant reduction in the length and width of flowers 293

was observed in MIM858 transgenic lines compared to the WT (Figure 4A, 4B, 294

Supplementary Table S7). However, no such difference was observed in the miR858OX 295

lines. These results suggested that modulation in the expression of miR858a affected 296

flowering time and flower size which might be controlled co-ordinately by miR858 in 297

flowering plants. 298



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Furthermore, observations also suggest that miR858OX lines have an increased 299

number and length of siliques per plant (Figure 4C-4E, Supplementary Table S8, 300

Supplementary Figure S6C) as well as enlarged seed size (Figure 4F-4G) as compared to 301

WT. In contrast, MIM858 lines produced a lower number but longer siliques per plant with 302



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seeds significantly smaller in size (Figure 4C-4F, Supplementary Table S8, Supplementary 303

Figure S6C). Additionally, miR858OX lines had a smaller number of seeds per silique while 304

MIM858 produced more seeds per silique as compared to WT (Figure 4H, Supplementary 305

Table S8). We have also counted the number of seeds per unit (5 mg) weight and observed a 306

significant increase in seed count in MIM858 as compared to miR858OX and WT plants 307

(Figure 4I, Supplementary Table S8) indicating larger seed size in miR858OX and smaller 308

seed size in MIM858 transgenic lines. Enhanced vegetative growth with increased seed size 309

and weight in miR858OX suggested an important role of miR858a during seed development 310

and plant yield. 311

To identify differentially expressed genes in miR858OX lines as compared to WT, 312

microarray analysis was carried out. Analysis revealed differential expression of genes 313

involved in jasmonate, ethylene and gibberellin signalling pathways and regulatory 314

mechanisms. In addition, expression of many developmental- and stress-responsive genes 315

was modulated in the transgenic lines (Supplementary Data Set S1). The expression of 316

significantly up-regulated genes identified through microarray analysis was validated using 317

qRT-PCR (Supplementary Figure S7) and showed a similar expression trend. Altogether, 318

significant changes in the phenotypes and microarray expression analysis suggested that 319

miR858a plays a versatile role in plant growth and development of Arabidopsis. 320

Metabolite profiling in miR858OX and MIM858 Transgenic Plants 321



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To investigate the impact of miR858a on synthesis of metabolites via phenylpropanoid 322

pathway, Q-Trap mass spectrometric analysis of methanolic extracts of rosette and stem of 5-323

week-old WT, miR858OX and MIM858 plants was carried out (Table 1). The modulation in 324

contents of molecules of various steps of the phenylpropanoid pathway in miR858OX and 325



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MIM858 transgenic plants as compared to the WT is summarized in Figure 5. The analysis 326

revealed higher accumulation of the major flavonoids such as kaempferol, quercetin and rutin 327

hydrate in MIM858 as compared to the WT plants. In contrast, a significant decrease in these 328

flavonoids was observed in the miR858OX rosette tissue (Table 1, Figure 5). Interestingly, 329



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these compounds are amongst the most abundant flavonol derivatives in WT plants (Stracke 330

et al., 2007). Kaempferol was significantly higher (10199.6 ± 161.0 µg/100 g DW) in rosette 331

tissues of MIM858 as compared to WT (4808.3 ± 93.3 µg/100 g DW) and miR858OX 332

(2320.4 ± 36.6 µg/100 g DW). In addition, other flavonols like quercetin-3-o-galactoside (Q-333



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3-O-G) and metabolites belonging to different classes of flavonoids such as flavanones 334

(naringenin and naringin) and flavan-3-ols (gallocatechin) showed similar accumulation 335

patterns (Table 1, Figure 5). 336



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Other phenylpropanoids such as p-coumaric acid, caffeic acid, ferulic acid, sinapic 337

acid and syringic acid were significantly increased in MIM858 while their accumulation 338

decreased in miR858OX line in comparison to the WT (Table 1, Figure 5). The accumulation 339

of metabolites in stem significantly varied as compared to rosette samples in the transgenic 340

lines. Surprisingly, higher metabolite accumulation was detected in stem tissue of miR858OX 341

as well as in MIM858 in contrast to the WT (Supplementary Table S9). These differences 342

were indicative of the existence of a differential regulation of metabolic pathways by 343

miR858a in different tissues. Collectively, higher accumulation of flavonoids in MIM858 and 344

their reduced levels in the miR858OX in rosette tissue of transgenic lines indicates that 345

miR858a regulates the biosynthesis of flavonoids through transcriptional regulation of 346

upstream transcription factors which controls the expression of genes involved in the 347

flavonoid biosynthesis pathway. 348

miR858a Affects Lignin Biosynthesis in Transgenic Plants 349

Lignin accumulation analysis suggested modulated lignin content in the vascular and inter-350

fascicular tissues of transgenic lines as compared to the WT. Lignin staining and 351

quantification of stem cross-section of the WT, miR858OX and MIM858 lines revealed an 352

enhanced lignification in the vascular and interfascicular tissues of the miR858OX lines 353

(Figure 6A, Supplementary Figure S8). Although, miR858a over-expression caused ectopic 354

deposition of lignin no prominent secondary wall thickening was observed in the epidermal 355

cells. These results are distinct from the observations of the MIM858 lines that showed less 356

lignification of cells (Supplementary Figure S8). The examination of vascular bundles and 357

epidermal cells showed that secondary wall thickness of both vessels and fibres were reduced 358

in the MIM858 line as compared to WT. Surprisingly, these results are inconsistent with 359

phenotypic observations with weaker inflorescence stems of MIM858 lines than the WT 360

plants (Figure 6B). Consistent with the histological data, the enhanced expression of several 361

secondary wall promoting and lignin biosynthetic genes including CESA4, SND1, MYB58, 362

HCT, CCoAOMT1, CCR1 and CAD6 was observed in the miR858OX stem tissue of 363

transgenic lines (Figure 6C). At the same time, reduced expression of these genes was 364

observed in the MIM858 lines. These observations explicitly suggest that miR858a-MYBs 365

interaction maintains the metabolic flux balance between the flavonoid and lignin 366

biosynthesis via activating a subset of the secondary wall and lignin biosynthetic genes. 367

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DISCUSSION 370

The regulation of gene expression in specific cells and tissues is essential for normal growth 371

of the plant. Over the past few years, large number of experiments have shown that a sub-372

group of R2R3-MYBs such as MYB11, MYB12 and MYB111 apparently influence the 373

spatial accumulation of flavonols via activating a branch of the phenylpropanoid pathway 374

(Mehrtens et al., 2005; Czemmel et al., 2009; Misra et al., 2010; Stracke et al., 2010; Liu et 375

al., 2015). These MYBs participate in fine-tuning of transcriptional activation of a set of 376

genes engaged in flavonol biosynthesis, and maintain a subtle balance with other branches of 377

the phenylpropanoid pathway (Xu et al., 2015). Studies suggest that the organ and temporal 378

distribution of flavonols are the consequence of differential expression of these MYBs and 379

environmental factors in Arabidopsis (Stracke et al., 2007). The fundamental question arises 380

about whether only cis-acting elements present in promoters of these MYBs are responsible 381

for differential expressions or any other trans-factors also determine their regulatory 382

mechanisms. Numerous past studies have suggested that miR858 can target R2R3-MYBs in 383

apple, grape and Salvia miltiorrhiza (Xia et al., 2012; Rock, 2013; Li et al., 2014). In a quest 384

for such factor, we have shown that miR858a controls the expression of flavonol-specific 385

MYBs for instance, MYB11, MYB12 and MYB111, in addition to other members of MYB 386

family, and studied its detailed role further, in Arabidopsis. 387

miR858 is transcribed from two genomic loci in Arabidopsis and targets similar 388

genes. The additional targets of miR858a identified in this study might be involved in 389

regulating diverse developmental aspects in the plant which confirmed the significance of 390

miR858a at specific developmental programs in Arabidopsis. The earlier function of miR858 391

has been recognised in trichome fibre development via regulating MYB2 in Arabidopsis 392

(Guan et al., 2014) and anthocyanin biosynthesis in tomato (Jia et al., 2015). These reports 393

are in agreement with the idea that miR858 might target a number of R2R3-MYB genes and 394

may be involved in the regulatory responses leading to the secondary metabolite production 395

and specific developmental programs. The expression of miR858a was found to be 396

widespread in Arabidopsis as evident from qRT-PCR results and promoter activity (Figure 397

1). The GUS staining observed in the different developmental stages throughout the life cycle 398

of Arabidopsis suggests an active participation of miR858a mediated regulation in plant 399

growth and development. Despite the in planta expression, miR858a was specifically active 400

in vascular tissues of the seedling. 401



22

Light serves as a critical factor of the transcriptional activation of miR858a precursor 402

which indicates that similar to that of MYBs, this sector of flavonol biosynthesis regulation is 403

also under the tight control of light. In silico analysis of the promoter of miR858a revealed 404

the presence of many LREs, specifically HY5 binding sites indicating the putative light-405

mediated regulation of miR858a expression (Supplementary Table S2). HY5 is a member of 406

the bZIP/bHLH transcription factor family which plays a pivotal role in light signalling and 407

photomorphogenesis processes by interacting with various pathways (Lee et al., 2007; Delker 408

et al., 2014). It has been shown that HY5-mediated transcriptional activation of MYB12 and 409

MYB111 genes are the under control of UV-B and visible light (Stracke et al., 2010). Our 410

light-dark transition experiment revealed that miR858a is substantially reduced under dark 411

condition in Col-0 (Figure 1D). The expression of miR858a is induced so rapidly that it 412

reached to the maximum within 0.5 hr exposure of light showing the relevance of light in its 413

regulation (Figure 1E). Therefore, it would be concluded that light is the major factor that 414

controls the expression of miR858a and various genes of the phenylpropanoid pathway. 415

miR858a cleaves the flavonol-specific MYBs such as MYB11, MYB12 and MYB111 416

which are predicted as the potential target using online target prediction tools (Supplementary 417

Table S3). The MYB11 and MYB111 have been verified as targets through 5’- RLM-RACE 418

analysis; however, we were unable to detect the cleavage product of MYB12 in our 419

experimental conditions, although MYB12 was confirmed to be an actual target of miR858 in 420

an earlier study (Fahlgren et al., 2007). MYB transcription factors are considered as potential 421

targets of miR858 in several plant species (Addo-Quaye et al., 2008; Xia et al., 2012; Jeong 422

et al., 2013; Guan et al., 2014; Jia et al., 2015). In addition, our in silico prediction and 423

cleavage products analysis for a set of other MYBs (Supplementary Figure S2) suggest that 424

miR858a offers complex regulation in Arabidopsis and is not only confined to flavonol-425

specific MYBs. 426

miR858a Expression is Important for Arabidopsis Growth and Development 427

miR858a caused a decrease in the expression of target MYBs and affected growth and 428

morphology in Arabidopsis in miR858OX and MIM858 lines. To nullify the effect of 429

endogenous miR858a, we employed the sponge decoy strategy and developed MIM858 in 430

such a way that it contains two repeats of the exact complementary sequence of miR858a, 431

and three repeats have 3 nt bulge between 9-11 position (Ebert et al., 2007). As expected, 432

MIM858 lines successfully delivered the knockdown phenotype in Arabidopsis. A significant 433

reduction in miR858a and increase in target gene expression was observed in MIM858 lines 434



23

(Figure 2A-2D). Phenotypic examination of both types of transgenic lines revealed that 435

miR858OX and MIM858 lines produced contrasting features of various growth parameters 436

(Figure 3, 4, Supplementary Figure S6, Supplementary Table S5, S6). Though expression of 437

miR858a was least in rosette tissue (Figure 1B), transgenic lines overexpressing miR858a 438

significantly changed rosette size, flowering time and metabolite content. This indicates that 439

even a slight variation of miR858a expression in rosette tissue could lead to the much bigger 440

impact on morphology of the plant where this miRNA is lowly abundant. It is well known 441

that MYB transcription factors play an important role in many developmental processes 442

(Ishida et al., 2007; Reyes and Chua, 2007; McCarthy et al., 2009; Dubos et al., 2010; Cui et 443

al., 2013; Chaonan et al., 2014). Previous studies have found that AtMYB11 modulates overall 444

growth in the plants by reducing the proliferation activity of the meristematic cells and 445

delaying plant development whereas mutant showed a faster development of the 446

inflorescence and initiate more lateral inflorescences and fruits (Petroni et al., 2008). 447

Similarly, contrasting phenotypes were obtained in miR858OX and MIM858 transgenic lines 448

in which expression of the MYB11 is significantly altered (Figure 3, 4, Supplementary Figure 449

S6, Supplementary Table S5, S6). 450

The miRNAs such as miR156, miR172 and miR159 regulate key genes involved in 451

flowering related processes (Hong and Jackson, 2015; Teotia and Tang, 2015). The 452

contrasting observations of bolt formation, flowering and flower size between miR858OX 453

and MIM858 lines might be due to perturbation of flowering related MYBs. MYBs and 454

flavonoids play a very crucial role in the Arabidopsis seed development (Routaboul et al., 455

2006; Doughty et al., 2014; Xu et al., 2014), therefore, a significant change in seed size in 456

transgenic lines may be an outcome of varied flavonoids content brought by miR858a. On 457

other hand, validation of several other MYBs, participating in various developmental 458

processes, as targets of miR858a (Supplementary Table S3) could be another probable reason 459

for such developmental alteration in the transgenic lines. The relation of these transcription 460

factors with miR858a and the downstream cascade could be a subject of future study. 461

miR858a-mediated Regulation Affects the Phenylpropanoid Pathway 462

The regulation of the flavonol biosynthesis mainly takes place at transcriptional level and 463

feedback inhibition by the end products. The flavonol-specific MYBs induced expression of 464

the structural genes such as CHS, CHI, F3H and FLS1 of the phenylpropanoid pathway 465

(Stracke et al., 2007; Dubos et al., 2010; Xu et al., 2015). Previously, a plethora of reports 466

suggested that expression of such MYBs in tobacco and tomato enhances the expression of 467



24

structural genes of the pathway leading to the enhanced flavonoid content, nutritional quality 468

and insect resistance (Luo et al., 2008; Misra et al., 2010; Pandey et al., 2012; Pandey et al., 469

2014; Pandey et al., 2014; Pandey et al., 2015; Pandey et al., 2015; Zhang et al., 2015; 470

Choudhary et al., 2016). Here, we describe the participation of miR858a in transcription 471

factor regulon responsible for biosynthesis of flavonoids and development in Arabidopsis. 472

Our analysis suggested that the expression of CHS, CHI, F3H and FLS1 was down-regulated 473

in miR858OX whereas induced in MIM858 lines (Figure 2E, 2F). These results indicate that 474

MIM858 titrates the endogenous miR858a activity in vivo and enhances expression of genes 475

encoding enzymes of flavonoid biosynthesis. 476

Metabolic profiling demonstrated a significant rise in major flavonoids such as 477

kaempferol and rutin (Table 1) and other phenylpropanoids in the MIM858 transgenic lines. 478

Previous studies suggested that flavonoids influence plant architecture (Taylor and Grotewold 479

2005; Buer and Djordjevic 2009; Buer, 2010) mainly through their effects on auxin transport. 480

Flavonoid-defective mutants display a wide range of alterations in a myriad of developmental 481

processes such as root and shoot development flower organ number, overall architecture and 482

stature, and seed organ density (Buer and Djordjevic 2009). Modulation in major flavonoids, 483

namely, kaempferol and quercetin in our metabolic profiles (Table 1, Supplementary Table 484

S9) clearly provide the justification for diverse alteration in phenotype in the transgenic lines. 485

The notion was also supported by the microarray and RT-PCR analyses which revealed 486

down-regulation of flavonoid-specific MYBs and early pathway genes (Supplementary Data 487

Set S1, Supplementary Table S4 and Supplementary Figure S5). 488

CHS and HCT share a common substrate (p-coumaroyl CoA) leading to the 489

biosynthesis of flavonoids and lignin in the phenylpropanoid pathway (Besseau et al., 2007). 490

The repression of the lignin biosynthesis via HCT-silencing impacts flavonoid accumulation 491

significantly in Arabidopsis (Hoffmann et al., 2004; Besseau et al., 2007; Li et al., 2010). We 492

quantified lignin in the stem of the WT and transgenic lines and measured expression of 493

genes such as CESA4, SND1, MYB58, HCT, CoOAMT, CCR1 and CAD6. The results clearly 494

showed a high lignin content in the stem of miR858OX in contrast to lower lignin content in 495

MIM858 transgenic lines (Figure 6). This might be due to the atypical lignification of the 496

mechanical tissues in the stem of MIM858 lines. These results indicate that miR858a 497

mediated perturbation of flavonoid branch of the phenylpropanoid pathway can affect the 498

lignin biosynthesis branch of the pathway. The same interpretation could be applied to 499

explain the rosette diameter and fresh weight phenotype of MIM858 transgenic plants 500

(Supplementary Table S6). Together, flavonoid profiling and transcriptome data from 501



25

combinatorial analysis of miR858OX and MIM858 plants suggest that miR858a responses 502

affect the flavonoid biosynthetic pathway. Our results provide new insights into the 503

regulation of the phenylpropanoid pathway by miR858a besides various transcription factors. 504

505

MATERIALS AND METHODS 506

Bioinformatic Analyses 507

To identify miRNAs targeting A. thaliana MYB11, MYB12 and MYB111 genes, BLASTn 508

searches were performed on the Sanger database for miRNAs (http://microrna. sanger.ac.uk; 509

release 15) and for available genomic sequences on the National Centre for Biotechnology 510

Information (http://www.ncbi.nlm.nih.gov/BLAST). Sequences of the miR858a precursor 511

and mature isoforms in Arabidopsis and other plant species were retrieved from the miRBase 512

database. To evaluate the hybridization energies and percentage homology between miR858a 513

and their putative targets, alignments of 21 bp between the mature miRNA and the target 514

mRNAs were carriedout using psRNAtarget server (http://plantgrn.noble.org/psRNATarget) 515

(Dai and Zhao, 2011) and WMD3 (http://wmd3.weigelworld.org) (Schwab et al., 2006). 516

Plant Material and Growth Conditions 517

A. thaliana (ecotype Col-0) was used as WT plant in this study. For germination, seeds were 518

surface-sterilized and placed on half-strength Murashige and Skoog (MS) medium (Sigma, 519

India) containing 1% sucrose. After stratification for 2-3 days at 4°C in the dark, seeds were 520

transferred to the growth chamber (Conviron, USA) under controlled conditions of 16 hr 521

light-8 hr dark photoperiod cycle, 22ºC temperature, 150–180 µm E m-2 s-1 light intensity and 522

60% relative humidity for 10 days unless otherwise mentioned. Measurements of the root 523

length and fresh weight were performed on 10-day-old seedlings. Rosette fresh weight and 524

diameter were determined for 20-day-old and 1-month-old plants. Plant height and silique 525

data were taken from the mature plants. For light-to-dark transition assay, WT (Col-0) and 526

ProMIR858a:GUS transgenic seeds were transferred to standard light and complete dark 527

conditions for 5 days. After dark treatment, seedlings were exposed to light for different time 528

periods (0.5 hr, 2 hr and 6 hr) and used for further analysis. 529

Construct Preparation and Transformation 530

To over-express miR858a, the miR858a precursor (187 bp) (AT1G71002) was amplified 531

from the single stranded cDNA library prepared from Arabidopsis rosette leaves through 532



26

PCR using specific primers (Supplementary Table S10). Amplicon was cloned into pT/Z sub-533

cloning vector (Fermentas, USA), and then transferred into plant expression vector, pBI121, 534

containing CaMV35S promoter. To reduce miR858a activity, a target mimicry approach 535

(Franco-Zorrilla et al., 2007) was used in the study. To synthesise and clone the miR858a 536

target mimic, forward and reverse overlapping primers were designed (Supplementary Table 537

S10). The amplified PCR product was cloned into pT/Z sub-cloning vector (Fermentas, 538

USA), and then transferred into plant expression vector pBI121. All the constructs were 539

transformed into the Agrobacterium tumefaciens (strain GV3101) and used to transform A. 540

thaliana (Col-0) using floral dip method (Clough and Bent, 1998). Transformants were 541

screened on half-strength MS agar plates containing kanamycin (50 µg/mL). For promoter 542

analysis, 1847 bp upstream region from the transcription start site of miR858a precursor 543

(Figure 1C, a) was PCR amplified using High Fidelity enzyme mix (Fermentas, USA) from 544

genomic DNA. Amplicon was cloned into pCAMBIA1303 plant binary vector resulting in 545

the construct ProMIR858:GUS. For identification of the transcription start site of miR858a, 546

plant promoter analysis navigator (PlantPAN; http://PlantPAN2.itps.ncku.edu.tw) resource 547

was used. Transgenic plants were generated and screened on hygromycin (10 mg/mL). Out of 548

minimum six transgenic lines generated using different constructs, three independent lines for 549

each of miR858OX, MIM858 and ProMIR858:GUS were selected for further analysis. All the 550

studies were performed in T4 homozygous lines. 551

Expression Analysis 552

For expression analysis, microRNA858a TaqMan PCR assays were used following the 553

recommendations of the manufacturer (Applied Biosystems, USA). A TaqMan PCR assay for 554

the small nuclear RNA snoR41Y was used as normalization control. For qRT-PCR, total 555

RNA was treated with TURBO DNAfree (Ambion, USA), and 2 µg was reverse transcribed 556

using RevertAid H minus first strand cDNA synthesis Kit (Fermentas, USA) according to the 557

manufacturers’ instructions. The cDNA was diluted 20 times with nuclease free water and 1 558

µl was used as template into qPCR reactions performed using Fast Syber Green mix (Applied 559

Biosystems, UK) in Fast 7500 Thermal Cycler instrument (Applied Biosystems, UK). 560

Expression was normalized using Tubulin and analysed through comparative ∆∆CT method 561

(Livak and Schmittgen, 2001). Primer sequences used for expression analysis are listed in 562

Supplementary Table S10. 563

Microarray Analysis 564



27

Genome-wide expression analysis was performed using Affymetrix GeneChip Arabidopsis 565

Genome ATH1 microarrays (Affymetrix, USA) and as per MIAME guidelines (Brazma et 566

al., 2001). Total RNA was extracted from 3-week-old rosette leaves of Col-0 and miR858OX 567

plants using Spectrum Plant Total RNA Kit (Sigma, USA). Briefly, total RNA (250 ng) of 568

each sample was taken as starting material and strictly followed the Affymetrix protocol 569

during RNA amplification, hybridization, washing-staining and scanning of the arrays. After 570

hybridization, raw data from CEL files were initially analyzed using Affymetrix Expression 571

Console with library files supplied by Affymetrix. Analyses were performed using the RMA 572

for gene levels without normalization. The log2 transformed data were exported for analysis 573

using Affymetrix Transcriptome Analysis Console (TAC) 2.0 software. Quantitative Real-574

Time PCR (qRT-PCR) was carried out to validate microarray data. 575

RNA Ligase-mediated (RLM) 5’ RACE 576

To map cleavage sites in the candidate targets of miR858a in planta, modified RLM 5’ 577

RACE was performed using First Choice RLM-RACE kit (Ambion, USA). Total RNA was 578

extracted from WT and miR858OX rosette leaves and directly ligated to RNA oligo adapter 579

without CIP and TAP treatments. cDNA synthesis was performed using oligo(dT) primer 580

using RevertAid H minus first strand cDNA synthesis Kit (Fermentas, USA) according to the 581

manufacturers’ instructions. RACE and nested-RACE PCR were subsequently carried out 582

with adaptor-specific forward primers and gene-specific reverse primers for the detection of 583

cleavage products of the target mRNAs. PCR products were cloned into the pT/Z sub-cloning 584

vector (Fermentas, USA) and sequenced to locate miRNA cleavage sites. 585

586

Histochemical Assays 587

GUS staining was performed using standard method (Jefferson, 1989). Different tissues of 588

ProMIR858:GUS transgenic lines were incubated in a solution containing 100 mM Na 589

phosphate buffer, pH 7.2; 10 mM EDTA; 0.1% Triton X-100; 2 mM potassium ferricyanide; 590

2 mM potassium ferrocyanide; and 1 mg/mL 5-bromo-4-chloro-3-indolyl-b-D-glucuronide at 591

37ºC overnight for 4 to 6 hr. The chlorophyll was removed by incubation and multiple 592

washes using 70% ethanol. 593

Flavonoid Accumulation Analysis 594



28

Dried tissues (100-500 mg rosette and stem from mature plants) were ground into the fine 595

powder in liquid N2 and were extracted in 80% methanol using an Ultra-Turrax T-25 Digital 596

Homogenizer (IKA, Germany) at 16000 RPM for 2 min. The homogenate was centrifuged at 597

20,000xg for 10 min at 4°C and the supernatant was filtered through a 0.22 µm PTFE syringe 598

filter (Millipore, USA). The Filtrate was collected in a clear glass HPLC vial (Agilent 599

Technologies, Singapore) and inject into HPLC-MS. All the samples were analysed on 1260 600

infinity series HPLC system (Agilent Technologies, Singapore) equipped with 1260 infinity 601

series pump, autosampler, column compartment and thermostat using Zorbax Eclipse Plus 602

column (4.6 x 100 mm, 3.5 µm) maintained at 40°C. The mobile phase consisted aqueous 603

solution of 0.1% formic acid LCMS grade (Solution A) and 0.1% formic acid in LCMS grade 604

acetonitrile (Solution B). The gradient was programmed as follows: 0-2 min, solution B 605

(2%); 2-22 min, Solution B (2-98%); 22.01-25 min, Solution B (98-2%). Other 606

chromatographic parameters included a constant flow of 600 µl/min (injection volume 5 µl), 607

autosampler temperature 10°C and a run time of 25 min including equilibration. Before 608

analysis, all of the samples were filtered through a 0.22 µm syringe membrane filters 609

(Millipore, USA). 610

The detection of different molecules was performed using HPLC system (Agilent 611

Technologies 1260 infinity series) coupled to a triple quadrupole system QTRAP5500 612

(ABSciex, Singapore) using ESI probe in both the mode of ionisation. The voltage was set at 613

5500V for positive ionisation and -4500V for negative ionisation. The values of Gas1 and 614

Gas2 (50), curtain gas (CUR; 30), collision assisted dissociation (CAD; medium), and 615

temperature of the source (TEM; 550°C) were used. The mass spectrometer was used in 616

Multiple Reaction Monitoring (MRM) mode for the identification and quantification analysis. 617

Analytical standards of phenolics were purchased from Sigma-Aldrich (India). The 618

identification and quantitative analysis was carried out using Analyst software (version 1.5.2) 619

and MultiQuant software (version 2.0.2). The Signal finder algorithm was used in Multiquant 620

software for quantitative analysis. 621

Lignin Analysis 622

To visualize lignified cell in stems, hand cut sections were stained for 2 min using Toluidine 623

blue O (Sigma-Aldrich, USA) and visualized on Leica DM2500 microscope (Leica 624

Microsystems, Germany). Lignin quantification was carried out using method described by 625

Bruce and West (1989). Briefly, samples (600 mg) were pulverized in liquid N2 and 626

suspended in 2 ml ethanol. Following centrifugation at 12,000xg (30 min, 4ºC), the pellet was 627



29

dried at 25ºC for 12 hr. Dried pellet was resuspended in 5 ml HCl (2N) and 0.5 ml 628

thioglycolic acid and incubated at 95ºC for 8 hr followed by cooled to room temperature. The 629

suspension was centrifuged at 12000xg for 30 min, and the pellet was washed with 2.5 ml 630

double distilled H2O. After recentrifuging at 12000xg (4ºC) for 5 min, the resulting pellet was 631

suspended in 5 ml of 1N NaOH and agitated gently at 25ºC for 18 hr. After centrifugation at 632

12000xg (4ºC) for 30 min, 1 ml HCl was added to the supernatant, and the solution was 633

allowed to precipitate at 4ºC overnight. Following centrifugation at 12000xg (4ºC) for 30 634

min, the pellet was dissolved in 3 ml of 1N NaOH, and the absorbance at 280 nm was 635

recorded as lignin content. 636

Statistical Analysis 637

The experiments were arranged in a completely randomized design. Each sample time point, 638

for each treatment, was comprised of three independent biological replicates. Data were 639

plotted as means ± standard errors (SE) in figures. Phenotypic observations were monitored 640

up to 2–3 generations for consistency. One-way ANOVA followed by post hoc Newman–641

Keuls was used for multiple comparison test of significance by using GraphPad Prism 6.05 642

software. 643

644

Acknowledgements 645

DS, AP and CB thankfully acknowledge the Council of Scientific and Industrial Research 646

(CSIR), New Delhi for Senior Research Fellowship. MT acknowledges Indian Council of 647

Medical Research for Research Fellowship. Research was supported by Council of Scientific 648

and Industrial Research, New Delhi in the form of Network projects PlaGen (BSC-0107). 649

650

651

Author contributions 652

P.K.T. designed and supervised this study. D.S., M.T., A.P., C.B., and A.S. performed the 653

experiments. D.S., M.T., and P.K.T. performed the data analysis. D.S. and P.K.T. prepared 654

the article. All authors read, contributed, and approved the article. 655

656

Competing financial interest statements 657

All the authors declare that they have no conflict of interest. 658



30

659

FIGURE LEGENDS 660 661 Figure 1. Identification and characterization of the miR858a in Arabidopsis. (A) Sequences 662

of MYB11, MYB12 and MYB111 mRNAs (5’ to 3’) aligned with the mature sequence of 663

miR858a (3’ to 5’). Dashed line and space represent perfect match and G:U wobble pairing, 664

respectively. The free energy of binding (ΔG) is indicated. (B) Expression of miR858a, 665

MYB11, MYB12 and MYB111 in rosette, root, stem, flower and silique from the 5-week-old 666

plant and 10-day-old seedling of Arabidopsis thaliana Col-0 ecotype. For miR858a, 667

SnoR41Y RNA and for MYB11, MYB12 and MYB111, tubulin was used as the endogenous 668

control to normalize the relative expression levels. Error bars represents ±SE (n = 3). (C) 669

Histochemical staining showing GUS activity in different developmental organs in the 670

ProMIR858:GUS transgenic lines. (a) Schematic representation of miR858a promoter 671

upstream of the precursor (b) 5-day-old seedling, (c) 12-day-old seedling, (d) rosette leaf, (e) 672

stem, (f) inflorescence, (g) silique and (h) seed. Bars indicate 1 cm for a, b, c, d, e, f and 500 673

µm for g image. (D) qRT-PCR analysis of the mRNA level of miR858a in WT (Col-0) 674

seedlings grown in the light and dark conditions for 5 days. Error bars indicate ±SE (n=3) 675

from three biological replicates. (E) qRT-PCR analysis of the mRNA level of miR858a in 676

WT (Col-0) upon exposure to light (150 µmol m-2 s-1) at the indicated times. Error bars 677

indicate ±SE (n=3) from three biological replicates. (F) Target validation for miR858a by 678

RLM-RACE. Cleavage products of MYB11 and MYB111 mRNA are shown. The fraction of 679

clones with the expected 5’ end among all sequenced products is indicated above the target 680

site. Arrows indicate the cleavage sites detected by RLM-RACE. 681

Figure 2. Characterization of miR858OX and MIM858 transgenic lines. (A) qRT-PCR 682

analysis showing expression of mature miR858a in rosette tissue of different miR858OX 683

transgenic lines. (B) qRT-PCR analysis showing expression of mature miR858a in rosette 684

tissue of different MIM858 transgenic lines. (C) Expression of MYB11, MYB12 and MYB111 685

in miR858OX transgenic lines. (D) Expression of MYB11, MYB12 and MYB111 in the 686

MIM858 transgenic lines. (E) Expression of CHS, CHI, F3’H and FLS1 in miR858OX 687

transgenic lines. (F) Expression of CHS, CHI, F3’H and FLS1 in the MIM858 transgenic 688

lines. For miR858a, SnoR41Y RNA and for MYBs and pathway genes, tubulin was used as 689

the endogenous control to normalize the relative expression levels. Error bars in each figure 690

represents ±SE (n=3). 691



31

Figure 3. Alteration of morphology in the miR858a transgenic lines. (A) The seedling 692

phenotype of WT, miR858OX (L1) and MIM858 (MIM1) transgenic lines grown on ½ MS 693

media for 10 days. (B) Root length of the seedlings of WT, miR858OX (L1) and MIM858 694

(MIM1) after growth of 10 days on ½ MS media. (C) Seedling fresh weight (mg) of the WT, 695

miR858OX (L1) and MIM858 (MIM1) after growth of 10 days on ½ MS media. Phenotype 696

(A) and other data included in B and C for other transgenic lines (L2, L3, MIM2 and MIM3) 697

are shown in Supplementary Figure S6. (D) Rosette phenotypes of WT, miR858OX and 698

MIM858 transgenic lines. (E) Leaf sizes and pattern of each rosette leaf beginning from the 699

oldest one of WT, miR858OX and MIM858 transgenic plants. (F) Number of rosette leaves 700

(black bars) and days at bolting (gray bars) of WT and transgenic lines of the miR858OX and 701

MIM858 grown under LD conditions (16 hr light-8 hr dark cycles). (G) Rosette diameter of 702

transgenic lines and WT. Plants were grown for 3 weeks under 16 hr light-8 hr dark 703

photoperiod before photograph. Error bars represent +SE of 8-10 individual plants. The level 704

of significance was evaluated by One-way ANOVA (Newman-Keuls used as post hoc test). 705

***Significantly different from WT (P < 0.0001). White line indicates the scale bar (1 cm). 706

L1, L2 and L3 are miR858OX transgenic lines whereas MIM1, MIM2 and MIM3 represent 707

MIM858 transgenic lines. 708

Figure 4. Variation of flower, silique and seed parameters in the transgenic lines. (A) Flower 709

size, both length and width, was reduced in MIM858 transgenic plants while no significant 710

change was observed in miR858OX flowers. Photograph of flowers were taken after 5 week 711

growth under standard conditions. White line indicates the scale bar (1 cm). (B) Bars are 712

mean of length and width of independent transgenic line and variation represent as +SE (n = 713

8-12). (C) The phenotype of transgenic lines producing longer silique than WT. Photographs 714

of 6-week-old grown plants were taken. (D) Bars represented transgenic line produced longer 715

silique per plant than WT. (E) Bars represented transgenic lines produced more silique per 716

plant than WT. (F) Representative photograph of seed size of transgenic and WT plants. Seed 717

size of miR858OX was bigger, and that of MIM858 was significantly smaller as compared to 718

WT. White line indicates the scale bar (500 µm). (G) Seed size of different transgenic lines 719

and WT plants. (H) Seed number per silique was higher in MIM858 transgenic line while no 720

difference was observed in miR858OX line. (I) Number of seeds per 5 mg was counted less 721

for miR858OX while more in MIM858 transgenic lines. Data of one transgenic line presented 722

as mean and +SE (n=8-12). Data was recorded from 15 siliques per plant and 8-12 plant for 723

each line and WT. L1, L2 and L3 are miR858OX transgenic lines whereas MIM1, MIM2 and 724



32

MIM3 represent MIM858 transgenic lines. Significance was determined by One-way 725

ANOVA (Newman-Keuls used as post hoc test). ***Significantly different from WT (P < 726

0.0001). 727

Figure 5. Metabolic profiling of miR858OX and MIM858 transgenic lines. Schematic 728

diagram of the phenylpropanoid pathway. Heat maps indicate log2 transformed values of the 729

concentrations of metabolites in rosette tissue of WT, miR858OX and MIM858 transgenic 730

lines (for values, refer Table 1). LC-MS-MS analysis was performed with the methanolic 731

extracts of dried rosette tissues. Arrows indicate the order of steps in the pathway; dashed 732

arrows represent multiple enzymatic steps. The main enzymes included PAL, phenylalanine 733

ammonia lyase; C4H cinnamate 4-hydroxylase; 4CL, 4-coumaroyl CoA ligase; CHS, 734

chalcone synthase; CHI, chalcone isomerase; F3H, flavanone 3-hydroxylase; F3’H, flavonoid 735

3’ hydroxylase; FLS, flavonol synthase; DFR, dihydro flavonol 4-reductase; LDOX, 736

Leucoanthocyanidin dioxygenase; LAR, leucoanthocyanidin reductase; UGT78D1, flavonol 737

3-O-rhamnosyltransferase; UGT78D2, flavonoid 3-O-glucosyltransferase; 3GRT, flavonol-3-738

O-glucoside L-rhamnosyltransferase; HCT, p-hydroxycinnamoyl-CoA:quinate shikimate p–739

hydroxycinnamoyltransferase; C3H, p-coumaroyl ester 3-hydroxylase; COMT I, caffeic acid 740

O-methyltransferase of class I; CAD, cinnamyl alcohol dehydrogenase; CCoAOMT, 741

caffeoyl-CoA O-methyltransferase; CCR, cinnamoyl-CoA reductase; F5H, ferulic acid 5-742

hydroxylase. MYB transcription factors are shown in green and red colours (Green for 743

activation and red for inhibition). Likewise green arrow is for activation and red arrow for 744

inhibition. 745

Figure 6. miR858a expressions affects lignin depositions in Arabidopsis. (A) Quantification 746

of total lignin content in WT and transgenic lines. Mature stems of WT, miR858OX and 747

MIM858 transgenic lines were equally weighed and used for quantification. Bars indicate 748

standard error of three biological replicates at each sampling time-point. Significance was 749

determined by One-way ANOVA (Newman-Keuls used as post hoc test). ***Significantly 750

different from WT (P < 0.0001). (B) Growth phenotypes of 5-week-old WT, miR858OX and 751

MIM858 transgenic plants. Rectangular boxes representing close-ups of stems of WT, 752

miR858OX and MIM858 transgenic stems (representative of 1 line of each transgenic). Bar = 753

1 cm. (C) Expression profiles of CESA4, SND1, MYB58, HCT, CCoAOMT1, CCR1 and 754

CAD6 in the stem of WT, miR858X and MIM858 lines. Transcript abundance of each gene 755

was normalized by the level of tubulin gene. Bars indicate ±SE (n=3). 756

757



33

SUPPLEMENTARY INFORMATION 758

Supplementary Figure S1. Expression of the miR858a is regulated by light and requires 759

HY5. (A) GUS activity in ProMIR858:GUS transgenic driven by light. (a) GUS activity 760

driven by a 1.8 kbp upstream promoter sequence of pre-miR858a in the ProMIR858:GUS 761

expressing seedlings after 5 days of germination in light. Bar = 1 mm (b) GUS activity in 762

ProMIR858:GUS expressing seedlings grown in complete dark condition for 5 days. (c) GUS 763

activity in dark-grown seedlings exposed to light for 0.5 hr. (d) GUS activity in dark-grown 764

seedlings exposed to light for 2 hr. (e) GUS activity in dark-grown seedlings exposed to light 765

for 6 hr. For b to e, Bar = 0.5 mm. (B) Relative expression of GUS and Chlorophyll A/B 766

Binding (CAB) genes in ProMIR858:GUS expressing seedling grown under light and dark 767

conditions for 5 days. CAB is taken as positive control. Transcript abundance of each gene 768

was normalized by the level of tubulin gene. (C) Relative expression of GUS gene in 769

ProMIR858:GUS transgenic lines (Pro-1, Pro-2 and Pro-3) at different times of exposure to 770

light after 5 days of growth in dark. Error bars indicate ±SE (n=3) from three biological 771

replicates (each with three technical replicates). 772

773

Supplementary Figure S2. miR858a-mediated cleavage of the MYB genes. Cleavage 774

analysis was performed using RLM-RACE. Amplified products were sequenced for (A) 775

MYB6, (B) MYB13, (C) MYB20, (D) MYB42, (E) MYB48, (F) MYB83, (G) TT2 and (H) 776

MYBL2. miR858a mature sequence is written in 3’ to 5’ direction while target gene sequence 777

in 5’ to 3’. The identified cleavage sites are indicated by black arrows with the frequency of 778

cleavage showing on the bottom of the arrows and position of cleavage showing on the top of 779

the target sequence. 780

Supplementary Figure S3. Expression analysis of miR858a expression in Arabidopsis. 781

Expressions of mature miR858a gene in different tissues of WT and miR858OX transgenic 782

lines. Tubulin was taken as internal control for normalization. Error bars represents ±SE 783

(n=3). 784

Supplementary Figure S4. Relative expression of MYB transcription factors in miR858OX 785

transgenic lines. A to H, Expression of MYB6, MYB13, MYB20, MYB48, MYB63, MYB111, 786

TT2, MYBL2 in seedling, rosette, root, stem, flower and silique tissue of miR858OX lines. 787

For MYB111 (F) no expression was obtained in the root. Tubulin was taken as internal control 788

for normalization. Error bars represents ±SE (n=3). 789



34

Supplementary Figure S5. Modulation of gene expression in transgenic line expressing 790

miR858a. (A) Relative expression of MYB genes identified through microarray analysis. (B) 791

Relative expression of structural genes of flavonoid pathway. Tubulin was taken as 792

endogenous control. Data given are fold expression log2 (transgenic/WT). Error bars 793

represents ±SE (n=3). 794

Supplementary Figure S6. Phenotypic variations in miR858a transgenic lines. (A) The 795

seedling phenotype of WT, miR858OX (L2 and L3) and MIM858 (MIM2 and MIM3) 796

transgenic lines. Phenotypic changes in WT, miR858OX and MIM858 transgenic lines grown 797

on ½ MS media for 10 days are shown. Bars = 1 cm. (B) Growth phenotypes of 5-week-old 798

WT, miR858OX and MIM858 transgenic plants. Bar = 1 cm. (C) Phenotype of transgenic 799

lines producing longer silique than WT. Photograph of 6 week grown plants was taken. 800

Supplementary Figure S7. Expression analysis of significantly up-regulated genes in 801

transgenic line expressing miR858a. Relative expression of significantly up-regulated genes 802

in miR858OX line. Tubulin was taken as endogenous control. Data given are fold expression 803

log2 (transgenic/WT). Error bars represents ±SE (n=3). 804

Supplementary Figure S8. miR858a affects lignin depositions in Arabidopsis stem. 805

Histochemical staining of stem sections of mature Arabidopsis stem sections with toluidine 806

blue O (TBO) for detection of lignin. i, interfascicular fiber; x, xylem. Bars = 500 µm. (A) 807

TBO staining (blue colour) of a WT stem section showing the normal lignin deposition in the 808

walls of interfascicular fibers and xylem cells. (B) TBO stained miR858OX stem section 809

showing ectopic lignin deposition in the walls of interfascicular fibers and xylem cells. (C) 810

TBO stained MIM858 stem section showing reduced lignin deposition in the walls of 811

interfascicular fibers and xylem cells. 812

813

Supplementary Table S1. Alignment of miR858a mature sequence among different plant 814

species 815

Supplementary Table S2. Putative cis-acting elements in miR858a promoter 816

Supplementary Table S3. Putative targets of Arabidopsis miR858a 817

Supplementary Table S4. Differentially expressed MYB transcription factors and flavonoid 818

structural genes 819



35

Supplementary Table S5. Comparisons of seedling root length, fresh weight and rosette 820

diameter in WT and miR858a transgenic lines 821

Supplementary Table S6. Comparisons of plant height, rosette fresh weight and rosette 822

diameter in mature WT and miR858a transgenic lines 823

Supplementary Table S7. Comparisons silique, seed number and morphology in WT and 824

miR858a transgenic lines 825

Supplementary Table S8. Comparisons of flower size in WT and miR858a transgenic lines 826

Supplementary Table S9. Metabolite content in stem tissues of wild-type, miR858OX and 827

MIM858 transgenic lines 828

Supplementary Table S10. Information of primers used 829

Supplementary Data Set S1. List of differentially expressed genes in miR858OX identified 830

through microarray analysis. 831

832

833

834

835

836

Table 1. Metabolite content in rosette tissues of wild-type, miR858OX and MIM858 transgenic lines 837

MOLECULE WT miR858OX MIM858

Naringenin 108.6 ± 1.4 34.91 ± 0.4*** 276.89 ± 3.7***

Naringin 77.4 ± 1.2 19.5 ± 0.2** 104.73 ± 1.4**

Kaempferol 4861.65 ± 85.6 2331.8 ± 38.9** 10249.41 ± 171.2***

Quercetin 701.59 ± 13.6 285.84 ± 3.9*** 1995.2 ± 33.3***

Q-3-O-G 110.71 ± 2.7 92.8 ± 1.5* 430.84 ± 7.1***

Rutin hydrate 3898.99 ± 65.1 3540.58 ± 59.1* 6683.54 ± 111.6**

Gallocatechin 431.4 ± 7.2 306.93 ± 4.0** 763.9 ± 10.2***

p-Coumaric acid 14434.29 ± 194.1 7120.55 ± 118.9** 32506.44 ± 444.3***

Caffeic acid 1961 ± 34.2 1062.07 ± 17.7* 4516.59 ± 75.4***

Ferulic acid 3793.51 ± 66.8 679.3 ± 11.3*** 1333.91 ± 18.2**

Sinapic Acid 32940.7 ± 550.3 8701.96 ± 145.3** 66980.51 ± 915.5***



36

Syringic acid 15325.29 ± 269.9 3901.08 ± 36.7** 19290.53 ± 252.7*

Rosette tissue samples from plants were taken and metabolite contents analyzed by LC/MS/MS. Values presented are means ±SE (n=6) (µg 100 g-1 dry weight) of measurements from at least five biological replicates per genotype. Statistically significant values from the WT is based on One-way ANOVA (*P < 0.01, **P < 0.001 and ***P < 0.0001). 838

839



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Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed inlignin synthesis affects auxin transport and plant growth. Plant Cell 19: 148-162


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Bruce RJ, West CA (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension culturesof castor bean. Plant Physiol 91: 889-897


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Chaonan L, Ng. CKY, Liu-Min F (2014) MYB transcription factors, active players in abiotic stress signaling. Environmental andExperimental Botany 114 80-91


Choudhary D, Pandey A, Adhikary S, Ahmad N, Bhatia C, Bhambhani S, Trivedi PK, Trivedi R (2016). Genetically engineeredflavonol enriched tomato fruit modulates chondrogenesis to increase bone length in growing animals. Sci Rep 5: 12412


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Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605-1619


Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun YH, Yuan L, Yeh TF, Peszlen I, Ralph J, Sederoff RR,Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc NatlAcad Sci U S A 110: 10848-10853


Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid andflavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56: 316-326


McCarthy RL, Zhong R, Ye ZH (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation ofsecondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50: 1950-1964


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http://scholar.google.com/scholar?as_q=MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=McCarthy&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mehrtens&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

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

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http://scholar.google.com/scholar?as_q=Target mimics: an embedded layer of microRNA-involved gene regulatory networks in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Meng&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Modulation%5BTitle%5D%29 AND 12%5BVolume%5D AND leads to insect resistance%2E Plant Physiol 152%3A 2258%5BPagination%5D AND Misra P%2C Pandey A%2C Tiwari M%2C Chandrashekar K%2C Sidhu OP%2C Asif MH%2C Chakrabarty D%2C Singh PK%2C Trivedi PK%2C Nath P%2C Tuli R%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 23%5BVolume%5D AND 1729%5BPagination%5D AND Ng DW%2C Zhang C%2C Miller M%2C Palmer G%2C Whiteley M%2C Tholl D%2C Chen ZJ%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=cis- and trans-Regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ng&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Microbiol%5BTitle%5D%29 AND 73%5BVolume%5D AND 790%5BPagination%5D AND Overgaard M%2C Johansen J%2C M�ller%2DJensen J%2C Valentin%2DHansen P%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Switching off small RNA regulation with trap-mRNA&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Overgaard&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Expression of Arabidopsis MYB transcription factor%2C AtMYB111%2C in tobacco requires light to modulate flavonol content%2E%5BTitle%5D%29 AND Pandey A%2C Misra P%2C Bhambhani S%2C Bhatia C%2C Trivedi PK%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pandey&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Rep%5BTitle%5D%29 AND 31%5BVolume%5D AND 1867%5BPagination%5D AND Pandey A%2C Misra P%2C Chandrashekar K%2C Trivedi PK%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Development of AtMYB12-expressing transgenic tobacco callus culture for production of rutin with biopesticidal potential&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pandey&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


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Pandey A, Misra P, Khan MP, Swarnkar G, Tewari MC, Bhambhani S, Trivedi R, Chattopadhyay N, Trivedi PK (2014) Co-expressionof Arabidopsis transcription factor, AtMYB12, and soybean isoflavone synthase, GmIFS1, genes in tobacco leads to enhancedbiosynthesis of isoflavones and flavonols resulting in osteoprotective activity. Plant Biotechnol J 12: 69-80


Pandey A, Misra P, Trivedi PK (2015) Constitutive expression of Arabidopsis MYB transcription factor, AtMYB11, in tobaccomodulates flavonoid biosynthesis in favor of flavonol accumulation. Sci Rep 5: 1-14


Petroni K, Falasca G, Calvenzani V, Allegra D, Stolfi C, Fabrizi L, Altamura MM, Tonelli C (2008) The AtMYB11 gene fromArabidopsis is expressed in meristematic cells and modulates growth in planta and organogenesis in vitro. J Exp Bot 59: 1201-1213


Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006) PH4 of Petunia is an R2R3 MYB protein that activates vacuolaracidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell 18: 1274-1291


Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seedgermination. Plant J 49: 592-606


Rock CD (2013) Trans-acting small interfering RNA4: key to nutraceutical synthesis in grape development? Trends Plant Sci 18:601-610


Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L (2006) Flavonoid diversity and biosynthesisin seed of Arabidopsis thaliana. Planta 224: 96-107


Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, Martinoia E (2008) Flavonoidsredirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283: 31218-31226


Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs inArabidopsis. Plant Cell 18: 1121-1133


Sharma D, Tiwari M, Lakhwani D, Tripathi RD, Trivedi PK (2015) Differential expression of microRNAs by arsenate and arsenitestress in natural accessions of rice. Metallomics 7: 174-187


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues%2E%5BTitle%5D%29 AND Pandey A%2C Misra P%2C Choudhary D%2C Yadav R%2C Goel R%2C Bhambhani S%2C Sanyal I%2C Trivedi R%2C Trivedi PK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pandey A, Misra P, Choudhary D, Yadav R, Goel R, Bhambhani S, Sanyal I, Trivedi R, Trivedi PK (2015) AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues. 5: 12412


http://scholar.google.com/scholar?as_q=AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pandey&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Co%5BTitle%5D%29 AND 12%5BVolume%5D AND and soybean isoflavone synthase%2C GmIFS1%2C genes in tobacco leads to enhanced biosynthesis of isoflavones and flavonols resulting in osteoprotective activity%2E Plant Biotechnol J 12%3A 69%5BPagination%5D AND Pandey A%2C Misra P%2C Khan MP%2C Swarnkar G%2C Tewari MC%2C Bhambhani S%2C Trivedi R%2C Chattopadhyay N%2C Trivedi PK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pandey A, Misra P, Khan MP, Swarnkar G, Tewari MC, Bhambhani S, Trivedi R, Chattopadhyay N, Trivedi PK (2014) Co-expression of Arabidopsis transcription factor, AtMYB12, and soybean isoflavone synthase, GmIFS1, genes in tobacco leads to enhanced biosynthesis of isoflavones and flavonols resulting in osteoprotective activity. Plant Biotechnol J 12: 69-80



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

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Constitutive%5BTitle%5D%29 AND 11%5BVolume%5D AND in tobacco modulates flavonoid biosynthesis in favor of flavonol accumulation%2E Sci Rep 5%3A 1%5BPagination%5D AND Pandey A%2C Misra P%2C Trivedi PK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pandey A, Misra P, Trivedi PK (2015) Constitutive expression of Arabidopsis MYB transcription factor, AtMYB11, in tobacco modulates flavonoid biosynthesis in favor of flavonol accumulation. Sci Rep 5: 1-14



http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pandey&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 59%5BVolume%5D AND 1201%5BPagination%5D AND Petroni K%2C Falasca G%2C Calvenzani V%2C Allegra D%2C Stolfi C%2C Fabrizi L%2C Altamura MM%2C Tonelli C%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Petroni K, Falasca G, Calvenzani V, Allegra D, Stolfi C, Fabrizi L, Altamura MM, Tonelli C (2008) The AtMYB11 gene from Arabidopsis is expressed in meristematic cells and modulates growth in planta and organogenesis in vitro. J Exp Bot 59: 1201-1213

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

http://scholar.google.com/scholar?as_q=The AtMYB11 gene from Arabidopsis is expressed in meristematic cells and modulates growth in planta and organogenesis in vitro&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The AtMYB11 gene from Arabidopsis is expressed in meristematic cells and modulates growth in planta and organogenesis in vitro&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Petroni&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 18%5BVolume%5D AND 1274%5BPagination%5D AND Quattrocchio F%2C Verweij W%2C Kroon A%2C Spelt C%2C Mol J%2C Koes R%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006) PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell 18: 1274-1291

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

http://scholar.google.com/scholar?as_q=PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Quattrocchio&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 49%5BVolume%5D AND 592%5BPagination%5D AND Reyes JL%2C Chua NH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49: 592-606

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

http://scholar.google.com/scholar?as_q=ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Trans%5BTitle%5D%29 AND 4%5BVolume%5D AND key to nutraceutical synthesis in grape development%3F Trends Plant Sci 18%3A 601%5BPagination%5D AND Rock CD%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rock CD (2013) Trans-acting small interfering RNA4: key to nutraceutical synthesis in grape development? Trends Plant Sci 18: 601-610

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rock&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Planta%5BTitle%5D%29 AND 224%5BVolume%5D AND 96%5BPagination%5D AND Routaboul JM%2C Kerhoas L%2C Debeaujon I%2C Pourcel L%2C Caboche M%2C Einhorn J%2C Lepiniec L%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L (2006) Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224: 96-107

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

http://scholar.google.com/scholar?as_q=Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 283%5BVolume%5D AND 31218%5BPagination%5D AND Santelia D%2C Henrichs S%2C Vincenzetti V%2C Sauer M%2C Bigler L%2C Klein M%2C Bailly A%2C Lee Y%2C Friml J%2C Geisler M%2C Martinoia E%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, Martinoia E (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283: 31218-31226

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

http://scholar.google.com/scholar?as_q=Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Santelia&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 18%5BVolume%5D AND 1121%5BPagination%5D AND Schwab R%2C Ossowski S%2C Riester M%2C Warthmann N%2C Weigel D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133

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http://scholar.google.com/scholar?as_q=Highly specific gene silencing by artificial microRNAs in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Highly specific gene silencing by artificial microRNAs in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schwab&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Metallomics%5BTitle%5D%29 AND 7%5BVolume%5D AND 174%5BPagination%5D AND Sharma D%2C Tiwari M%2C Lakhwani D%2C Tripathi RD%2C Trivedi PK%5BAuthor%5D&dopt=abstract

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R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660-677


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Xia R, Zhu H, An YQ, Beers EP, Liu Z (2012) Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol 13: R47Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends PlantSci 20: 176-185


Xu W, Lepiniec L, Dubos C (2014) New insights toward the transcriptional engineering of proanthocyanidin biosynthesis. PlantSignal Behav 9


Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66: 1749-1761Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhang B, Wang Q (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230: 1-15Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development inArabidopsis. Plant J 74: 98-109


Zhang Y, Butelli E, Alseekh S, Tohge T, Rallapalli G, Luo J, Kawar PG, Hill L, Santino A, Fernie AR, Martin C (2015) Multi-levelengineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun 6: 8635

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

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http://search.crossref.org/?page=1&rows=2&q=Teotia S, Tang G (2015) To bloom or not to bloom: role of microRNAs in plant flowering. Mol Plant 8: 359-377

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

http://scholar.google.com/scholar?as_q=To bloom or not to bloom: role of microRNAs in plant flowering&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://scholar.google.com/scholar?as_q=Origin, biogenesis, and activity of plant microRNAs&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Origin, biogenesis, and activity of plant microRNAs&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Voinnet&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28A colorful model for genetics%2C biochemistry%2C cell biology%2C and biotechnology%2E Plant Physiol%5BTitle%5D%29 AND 126%5BVolume%5D AND 485%5BPagination%5D AND Winkel%2DShirley B%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28New insights toward the transcriptional engineering of proanthocyanidin biosynthesis%2E%5BTitle%5D%29 AND Xu W%2C Lepiniec L%2C Dubos C%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 66%5BVolume%5D AND 1749%5BPagination%5D AND Zhang B%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Cell Physiol%5BTitle%5D%29 AND 230%5BVolume%5D AND 1%5BPagination%5D AND Zhang B%2C Wang Q%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Multi%2Dlevel engineering facilitates the production of phenylpropanoid compounds in tomato%2E%5BTitle%5D%29 AND Zhang Y%2C Butelli E%2C Alseekh S%2C Tohge T%2C Rallapalli G%2C Luo J%2C Kawar PG%2C Hill L%2C Santino A%2C Fernie AR%2C Martin C%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cellwall biosynthesis in Arabidopsis. Plant Cell 20: 2763-2782


Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors andsecondary wall biosynthetic genes. Plant Cell Physiol 53: 368-380


Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway duringsecondary cell wall formation in Arabidopsis. Plant Cell 21: 248-266



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 20%5BVolume%5D AND 2763%5BPagination%5D AND Zhong R%2C Lee C%2C Zhou J%2C McCarthy RL%2C Ye ZH%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Physiol%5BTitle%5D%29 AND 53%5BVolume%5D AND 368%5BPagination%5D AND Zhong R%2C Ye ZH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53: 368-380

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

http://scholar.google.com/scholar?as_q=MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhong&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 21%5BVolume%5D AND 248%5BPagination%5D AND Zhou J%2C Lee C%2C Zhong R%2C Ye ZH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21: 248-266

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

http://scholar.google.com/scholar?as_q=MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1


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