MYB20, MYB42, MYB43 and MYB85 Regulate Phenylalanine …chorismate phenylalanine biosynthesis...

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Short title: MYBs regulate secondary metabolism 1

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Author for Contact details: Qiao Zhao ([email protected]) 3

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MYB20, MYB42, MYB43 and MYB85 Regulate Phenylalanine and 5

Lignin Biosynthesis during Secondary Cell Wall Formation 6

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Pan Geng,a Su Zhang,

a,b Jinyue Liu,

a Cuihuan Zhao,

a Jie Wu,

a,b Yingping Cao,

c 8

Chunxiang Fu,c Xue Han,

d Hang He,

d and Qiao Zhao

a,1 9

aCenter for Plant Biology, School of Life Sciences, Tsinghua University, Beijing 10

100084, China 11

bTsinghua University-Peking University, Joint Center for Life Sciences, Beijing 12

100084, China 13

cShandong Technology Innovation Center of Synthetic Biology, Key Laboratory of 14

Biofuels, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese 15

Academy of Sciences, Qingdao, Shandong, 266101, China 16

dState Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center 17

for Life Sciences, School of Advanced Agriculture Sciences and School of Life 18

Sciences, Peking University, Beijing, China 19

1Author for contact: [email protected] 20

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One-sentence Summary: MYB proteins regulate carbon flow into the 22

phenylpropanoid pathway for lignin biosynthesis. 23

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Author contributions: P.G. and Q.Z. designed the research. P.G., S.Z., J.L., C.Z., 25

J.W., Y.C. X.H., H.H., and C.F. performed the experiments. P.G. and Q.Z. wrote the 26

manuscript. 27

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Plant Physiology Preview. Published on December 23, 2019, as DOI:10.1104/pp.19.01070

Copyright 2019 by the American Society of Plant Biologists

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ABSTRACT 30

Lignin is a phenylpropanoid-derived polymer that functions as a major 31

component of cell walls in plant vascular tissues. Biosynthesis of the aromatic amino 32

acid phenylalanine provides precursors for many secondary metabolites including 33

lignins and flavonoids. Here, we discovered that MYB transcription factors MYB20, 34

MYB42, MYB43, and MYB85 are transcriptional regulators that directly activate 35

lignin biosynthesis genes and phenylalanine biosynthesis genes during secondary wall 36

formation in Arabidopsis (Arabidopsis thaliana). Disruption of MYB20, MYB42, 37

MYB43, and MYB85 resulted in growth development defects and substantial 38

reductions in lignin biosynthesis. In addition, our data showed that these MYB 39

proteins directly activated transcriptional repressors that specifically inhibit flavonoid 40

biosynthesis, which competes with lignin biosynthesis for phenylalanine precursors. 41

Together, our results provide important insights into the molecular framework for the 42

lignin biosynthesis pathway. 43

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Key words: Lignin biosynthesis, phenylalanine biosynthesis, primary metabolism, 45

secondary metabolism 46

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INTRODUCTION 48

Plant cell walls are commonly classified into primary and secondary based on 49

their composition and cellular location. In general, all plant cells form primary cell 50

walls during cell division, while secondary cell walls are produced after cessation of 51

cell division and expansion only in specific types of cells, such as vessel elements and 52

fibers (Cosgrove and Jarvis, 2012). Secondary cell walls play important roles in 53

providing long-distance water transport, mechanical support, and plant defense (Zhao 54

and Dixon, 2014; Hoson and Wakabayashi, 2015). 55

The main components of typical secondary cell walls are cellulose, 56

hemicellulose, and lignin. Lignins are phenylpropanoid-derived polymers resulting 57



4

from oxidative polymerization of three major hydroxycinnamyl alcohols (Bonawitz 58

and Chapple, 2010; Zhao, 2016). Natural lignin polymers are only composed of 59

p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) as basic units, however 60

occasionally some unconventional units such as coniferaldehyde, sinapaldehyde, 61

catechyl (C), and 5-hydroxyl guaiacyl (5-OH-G) units are also incorporated into 62

lignin monomers (Weng et al., 2010; Chen et al., 2012; Chen et al., 2013; Zhao et al., 63

2013). 64

It is widely accepted that lignin biosynthesis is controlled by regulatory 65

hierarchy involving NAC (no apical meristem (NAM), Arabidopsis transcription 66

activation factor (ATAF1/2), and cup-shaped cotyledon (CUC2)) and MYB 67

(myeloblastosis) transcription factors (Zhao, 2016; Ohtani and Demura, 2018). In this 68

network, NAC proteins including VASCULAR-RELATED NAC-DOMAIN 1-7 69

(VND1-7) and NAC SECONDARY WALL THICKNING PROMOTING FACTOR 70

1-3 (NST1-3) were identified in Arabidopsis (Arabidopsis thaliana) to serve as a first 71

layer of transcription factors (Kubo et al., 2005; Mitsuda et al., 2007). These NACs 72

are master regulators in various cell types. NST3, also called SND1, together with 73

NST1 redundantly regulates secondary cell wall formation in fibers (Mitsuda et al., 74

2007) and NST1 and NST2 activate the same process in the endothecium of anthers 75

(Mitsuda et al., 2005). MYB46 and MYB83 in Arabidopsis, the downstream targets of 76

the NAC proteins, are a second layer of the network, redundantly regulating 77

secondary cell wall formation (McCarthy et al., 2009; Ko et al., 2014). Recently two 78

types of cis-element sequences were reported by two different groups, Secondary wall 79

MYB-Responsive Element (SMRE) ACC(A/T)A(A/C)(T/C) and MYB46-Responsive 80

cis-Regulatory Element (M46RE) (T/C)ACC (A/T)A(A/C)(T/C) (Kim et al., 2012; 81

Zhong and Ye, 2012). Comprehensive survey of these cis-elements and DNA-protein 82

binding assays identified the direct targets of MYB46/83 including MYB genes 83

implicated in the regulation of lignin biosynthesis (for instance, MYB58, MYB63, 84

MYB103, and KNAT7), secondary cell wall biosynthesis genes such as cellulose 85



5

synthase genes (CesA4, CesA7, and CesA8), xylan biosynthesis genes (IRX7, IRX8, 86

and IRX9), and lignin biosynthesis genes (PAL1, C4H, 4CL1, CCoAOMT, HCT, 87

CCR1, and F5H1) (Kim et al., 2012; Kim et al., 2013; Kim et al., 2013; Kim et al., 88

2014; Wang et al., 2019). 89

It was previously revealed that the majority of promoters of lignin biosynthesis 90

genes contain so-called AC elements, including AC-I (ACCTACC), AC-II 91

(ACCAACC), and AC-III (ACCTAAC), that are recognized by transcription factors 92

(Raes et al., 2003). MYB58 and MYB63 were shown to activate lignin biosynthesis 93

genes by directly targeting the AC elements in Arabidopsis (Zhou et al., 2009). 94

Members from subfamily 4 of the R2R3-MYB family can also target the AC elements 95

to function as transriptional repressors of the lignin biosynthesis pathway. 96

AmMYB308 and AmMYB330 in Antirrhinum majus, EgMYB1 and EgMYB2 in 97

Eucalyptus gunnii, PtMYB1, PtMYB4, PtMYB8, and PtMYB14 in Pinus teada, 98

PgMYB1, PgMYB8, PgMYB14, and PgMYB15 in Picea glauca, ZmMYB31 and 99

ZmMYB42 in maize (Zea mays), and Arabidopsis MYB4, MYB32, and MYB75 were 100

all reported to directly regulate lignin biosynthesis genes (Tamagnone et al., 1998; Jin 101

et al., 2000; Patzlaff et al., 2003; Preston et al., 2004; Goicoechea et al., 2005; 102

Bhargava et al., 2010; Fornale et al., 2010; Legay et al., 2010; Bomal et al., 2013). 103

The synthesis of lignin monomers involves the phenylpropanoid pathway, which 104

is also shared by many other metabolites such as suberin, flavonoids, tannins, and 105

lignans (Fraser and Chapple, 2011). The aromatic amino acid phenylalanine, the 106

end-product of the shikimate pathway, serves as the precursor of downstream 107

phenylpropanoids (Maeda and Dudareva, 2012; Tohge et al., 2013). Lignin 108

biosynthesis is a high energy consuming and irreversible process; therefore, it is 109

critical that lignin deposition is tightly controlled to avoid overconsumption of 110

phenylalanine. Transcription factors have been identified that coordinately regulate 111

the expression of phenylalanine biosynthesis and downstream metabolism of 112

phenylalanine. Ectopic expression of Petunia hybrida transcription factor 113



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ODORANT1 in tomato can induce shikimate biosynthesis genes and 114

phenylpropanoid-associated genes (Dal Cin et al., 2011). Green tea MYB4 negatively 115

regulates the phenylpropanoid and shikimate biosynthesis by directly targeting the AC 116

elements of promoters of the genes involved in the two pathways (Li et al., 2017). 117

L-phenylalanine is an aromatic amino acid required not only for protein 118

biosynthesis, but also for many secondary metabolites such as flavonoids, condensed 119

tannins, lignans, and lignins (Maeda and Dudareva, 2012). In plants, phenylalanine is 120

produced by two alternative pathways. Most phenylalanine is produced via the 121

chloroplast-localized arogenate pathway (Maeda et al., 2010). In addition, a cytosolic 122

post-chorismate phenylalanine biosynthesis pathway has also been functionally 123

characterized (Yoo et al., 2013; Qian et al., 2019). It was proposed that the alternative 124

cytosolic pathway may contribute to produce specialized phenylalanine-derived 125

metabolites in response to biotic and abiotic stress in plants (Qian et al., 2019). 126

MYB20, MYB42, MYB43, and MYB85 were previously identified as secondary 127

cell wall related transcription factors based on a genome-wide transcriptome analysis 128

of NST1 downregulated mutants in Arabidopsis (Zhong et al., 2008). Dominant 129

repression of MYB85, which is a transcriptional activator, substantially reduced 130

secondary wall thickening in fiber cells, and overexpression of MYB85 caused 131

ectopic deposition of lignin in epidermal and cortical cells in stems. However, how 132

these MYBs are involved in secondary cell wall formation remains elusive. In this 133

study, we report that MYB20, MYB42, MYB43, and MYB85 redundantly activate 134

both phenylalanine and lignin biosynthesis. In addition, MYB20, MYB42, MYB43, 135

and MYB85 activate the transcription factor MYB4, which represses flavonoid 136

biosynthesis to optimize phenylalanine flux to the lignin biosynthesis pathway. This 137

discovery uncovers another level of complexity in the regulatory network of plant 138

lignin biosynthesis. 139

140

RESULTS 141



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MYB20, MYB42, MYB43, and MYB85 Genes are Regulated by NST3 and MYB46 142

It was previously revealed that several unknown transcription factors are under 143

the control of SND1 and NST1, including two NACs (SND2 and SND3) and eight 144

MYB genes (MYB20, MYB42, MYB43, MYB52, MYB54, MYB69, MYB85, and 145

MYB103) (Zhong et al., 2008). Phylogenetic analysis demonstrated that MYB42 and 146

MYB85 are closely related to each other, while MYB20 and MYB43 are likely more 147

closely related to one another (Supplemental Fig. S1). Furthermore, the two 148

subgroups are also closely related, but are remotely related to the previously reported 149

lignin transcriptional activators MYB58 and MYB63 (Supplemental Fig. S1). 150

Therefore, we selected MYB20, MYB42, MYB43, and MYB85 to functionally 151

characterize their roles in secondary cell wall biosynthesis. Consistent with the fact 152

that MYB20, MYB42, MYB43, and MYB85 are regulated by NST3, the transcript levels 153

of all four MYB genes were reduced in the double mutant of nst1/3 (Fig. 1A). 154

MYB46, which is a direct target of NST3, is also a master regulator of secondary cell 155

wall biosynthesis, potentially controlling the expression of MYB20, MYB42, MYB43, 156

and MYB85. To determine whether MYB46 and NST3 can activate MYB20, MYB42, 157

MYB43, and MYB85 transcription, we performed transient expression assays in 158

Nicotiana benthamiana leaves. The promoters of MYB20, MYB42, MYB43, and 159

MYB85 were respectively fused with Luciferase (LUC) to generate PMYB20-LUC, 160

PMYB42-LUC, PMYB43-LUC, and PMYB85-LUC. MYB46 and NST3 were driven by 35S 161

promoter to act as effectors. Coexpression of MYB46 or NST3 can activate 162

PMYB20-LUC, PMYB42-LUC, PMYB43-LUC, and PMYB85-LUC activity (Fig. 1, B and C). 163

However, neither NST1-3 nor MYB46 and MYB83 were able to bind these promoters 164

in yeast one-hybrid assays (Supplemental Fig. S2). 165

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Simultaneous Disruption of MYB20, MYB42, MYB43, and MYB85 causes Plant 167

Growth Defects 168

To further investigate the function of these genes, the T-DNA insertion lines of 169



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myb20-1 (GK-109C11-012312), myb42-1 (SALKseq_78190.1), myb43-1 170

(SALK_085312), and myb85-1 (SALK_052089) were characterized and the insertion 171

positions were verified by genomic sequencing (Fig. 1D). Reverse transcription PCR 172

(RT-PCR) showed that these T-DNA insertion lines were null mutants (Fig. 1E). . The 173

double mutants myb20/43 and myb42/85 exhibited a normal growth phenotype, 174

similar to the wild type (Fig. 2A). However, the quadruple mutant myb20/42/43/85 175

showed a semi-dwarfism phenotype compared to myb20/43 and myb42/85, indicating 176

genetic redundancy among these genes (Fig. 2A). In addition, the quadruple mutant 177

also showed shorter siliques with compromised fertility (Fig. 2, B-D). 178

179

MYB20, MYB42, MYB43, and MYB85 Coordinately Regulate Phenylalanine 180

and Lignin Biosynthesis 181

To determine the possible effects on gene expression of disrupting MYB20, 182

MYB42, MYB43, and MYB85, we used high-throughput mRNA sequencing to identify 183

differentially expressed genes in the quadruple mutant myb20/42/43/85, compared 184

with wild-type plants. In the quadruple mutant myb20/42/43/85, a total of 2,596 genes 185

were expressed at levels significantly different from wild type (Supplemental Datasets 186

S1 and S2). KEGG pathway analysis showed that biosynthesis of secondary 187

metabolites was changed greatly (Supplemental Fig. S3) and genes involved in lignin 188

and phenylalanine biosynthesis showed reduced expression in the quadruple mutant. 189

To further verify the RNA sequencing data, we performed Reverse transcription 190

quantitative PCR (RT-qPCR) to compare gene expression among the double mutants 191

myb20/43 and myb42/85, the quadruple mutant myb20/42/43/85, and wild type. 192

myb20/42/43/85 plants exhibited reduced transcript levels of lignin biosynthesis genes 193

such as PAL1, 4CL1, C4H, CSE, HCT, and CAD4, while the reduction was lesser 194

severe in both double mutants (Fig. 3B). The transcript levels of ADT4, ADT5, and 195

ADT6, which are specifically involved in phenylalanine biosynthesis, were greatly 196

reduced in myb20/42/43/85 plants, but were not significantly changed in the myb20/43 197



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and myb42/85 mutants, indicating genetic redundancy among the MYB genes (Fig. 198

3A). On the other hand, expression of ADH2, TSA1, and TSB1, involved in tyrosine 199

and tryptophan biosynthesis was not significantly changed in myb20/42/43/85 mutants 200

even though these genes are also related to the shikimate biosynthesis pathway (Fig. 201

3A). 202

The thioacidolysis method was used to determine the lignin composition of 203

double mutants myb20/43 and myb42/85, and the quadruple mutant myb20/42/43/85. 204

As shown in Fig. 3D, the G and S subunits were significantly reduced in 205

myb20/42/43/85 plants, while the reduction was less severe in the two double mutants, 206

which is consistent with the growth phenotypes and gene expression analysis (Fig. 2A 207

and Fig. 3B). To further confirm the impact on lignin biosynthesis of disrupting 208

MYB20, MYB42, MYB43, and MYB85, the total lignin content of mutants and 209

control plants was quantified by Klason analysis. As shown in Supplemental Fig. S4, 210

myb20/42/43/85 plants produced significantly reduced lignin, while double mutants 211

myb20/43 and myb42/85 contained similar lignin content as wild-type plants. 212

Phenylalanine content was also quantified using the same mature stem tissues 213

used for lignin measurements. Interestingly, both myb20/43 and myb42/85 214

accumulated greatly elevated levels of phenylalanine, and myb20/42/43/85 plants 215

contained even more phenylalanine than the double mutants (Fig. 3C). These results 216

were not consistent with the fact that ADT genes were downregulated in the mutants. 217

However, the increase of the free form of phenylalanine may be due to the reduction 218

of downstream phenylalanine-derived lignin biosynthesis. 219

220

MYB20, MYB42, MYB43, and MYB85 Activate Phenylalanine and Lignin 221

Biosynthesis Gene Expression 222

To investigate the molecular mechanism underlying the roles of the MYB 223

transcription factors in lignin and phenylalanine biosynthesis pathways, yeast 224

one-hybrid assay was performed. We found that full-length MYB proteins had very 225



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low expression levels in the EGY48 yeast strain, but truncated MYB proteins could be 226

easily expressed (Supplemental Fig. S5). Therefore, we used truncated proteins in the 227

yeast one-hybrid assay. ADT6 and HCT were selected as representative phenylalanine 228

and lignin biosynthesis genes, respectively. MYB20, MYB42, and MYB85 were able 229

to activate the LacZ reporter genes driven by the ADT6 and HCT promoters, while 230

MYB43 could only activate the LacZ reporter gene driven by the HCT promoter (Fig. 231

4A and Fig. 5A). We utilized the electrophoretic mobility shift assay (EMSA) to 232

further verify the direct binding to the ADT6 and HCT promoters. All four 233

recombinant MBP-MYB fusion proteins caused an up-shift of the labeled ADT6 234

promoter or HCT promoter. By contrast, MBP alone did not generate the same 235

mobility shift (Fig. 4, C-F and Fig. 5, C-F). The schematic diagrams of the promoters 236

in yeast one-hybrid assays and EMSA assays are shown in Fig. 4B and Fig. 5B. 237

To further confirm that MYB20, MYB42, MYB43, and MYB85 were able to 238

activate the expression of ADT6 and HCT, we performed a transient expression assay 239

in Arabidopsis protoplasts. Coexpression of MYB20, MYB42, MYB43, or MYB85 240

dramatically activated PADT6-LUC and PHCT-LUC activity in Arabidopsis Col-0 241

protoplasts (Fig. 4G and Fig. 5G). To further examine whether each MYB is able to 242

activate the genes independently, a similar transient expression assay was carried out 243

in Arabidopsis myb20/42/43/85 mutant protoplasts. It turned out that each MYB was 244

able to activate downstream targets alone (Fig. 4H and Fig. 5H), suggesting that these 245

four MYBs are not interdependent. 246

247

MYB20, MYB42, MYB43, and MYB85 Optimize Phenylalanine Distribution in 248

the Phenylpropanoid Biosynthesis Pathway 249

Our RNA sequencing data indicated that the previously identified 250

phenylpropanoid pathway transcription factor MYB7 was downregulated in 251

myb20/42/43/85 compared with the wild type (Supplemental Datasets S2). Through 252

RT-qPCR analysis, we showed that not only MYB7 but also two homologous genes, 253



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MYB4 and MYB32, showed lower transcript levels in the myb20/42/43/85 mutant 254

compared with the wild type (Fig. 6A). Transient expression assays in N. 255

benthamiana leaves indicated that MYB20, MYB42, MYB43, and MYB85 activate 256

the promoters of MYB4 (Fig. 6B). EMSA was performed to investigate whether MYB4 257

was directly targeted, as described previously (Zhao et al., 2007). EMSA showed that 258

all four MBP-MYB proteins could bind the MYB4 promoter, but not the MBP tag (Fig. 259

6, C-F). 260

It has been reported that MYB4 can repress the expression of Chalcone Synthase 261

(CHS), encoding the enzyme that catalyzes the first step of flavonoid biosynthesis, 262

which competes with lignin biosynthesis for phenylalanine as a precursor (Jin et al., 263

2000). Consistent with this finding, the transcript level of CHS was significantly 264

enhanced in myb20/42/43/85 compared with the wild type, and increased even more 265

in the myb4/7/32 mutant (Fig. 7A). The results suggest that MYB20, MYB42, 266

MYB43, and MYB85 activate MYB4, MYB7, and MYB32, resulting in downregulation 267

of CHS expression. To investigate the possible effects on the phenylpropanoid 268

biosynthesis pathway of disrupting MYB20, MYB42, MYB43, and MYB85, we 269

compared flavonoid accumulation among myb20/42/43/85, myb4/7/32, and wild-type 270

plants. As shown in Fig. 7B, kaempferol 3-O-[6"-O-(rhamnosyl) glucoside] 271

7-O-rhamnoside (K1), kaempferol 3-O-glucoside 7-O-rhamnoside (K2), and 272

kaempferol 3-O-rhamnoside 7-O-rhamnoside (K3) accumulated at significantly 273

higher amounts in myb20/42/43/85 and myb4/7/32. In addition, myb20/43, myb42/85, 274

and myb20/42/43/85 also accumulated enhanced levels of anthocyanin (Supplemental 275

Fig. S6). These data suggest that downregulation of the transcription repressors MYB4, 276

MYB7, and MYB32 in myb20/42/43/85 leads to enhanced flavonoid biosynthesis due 277

to elevated expression of CHS. 278

279

DISCUSSION 280

During the last decade, the transcriptional regulation of secondary cell wall 281



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formation has been extensively studied. Lignin biosynthesis has been shown to be 282

under the control of the NAC-MYB-based transcriptional regulatory network (Ohtani 283

and Demura, 2018). NAC proteins as master switches coordinately regulate the 284

entirety of secondary cell wall formation including cellulose, hemicellulose, and 285

lignin (Zhong et al., 2010). Lignin biosynthesis is derived from the aromatic amino 286

acid phenylalanine and the deposition process is believed to be irreversible. Therefore, 287

lignin biosynthesis is not only coordinately regulated along with other secondary cell 288

wall components, but also interacts with primary metabolic pathways related to 289

phenylalanine biosynthesis and other branches of the phenylpropanoid pathway (Li et 290

al., 2016; Ohtani et al., 2016). 291

MYB58 and MYB63 were first reported in Arabidopsis as lignin-specific 292

transcriptional activators (Zhou et al., 2009). These MYBs are able to directly activate 293

lignin biosynthesis genes, including early genes such as PAL, C4H, and 4CL that are 294

shared by other branches of the phenylpropanoid pathway such as flavonoid 295

biosynthesis. MYB4 was shown to directly target lignin biosynthesis genes as 296

repressors (Shen et al., 2012; Li et al., 2017). Currently, there is no evidence that 297

MYB58/63 and MYB4 dynamically regulate lignin biosynthesis. MYB103, a 298

NST1-regulated transcription factor, was recently suggested to be involved in syringyl 299

lignin biosynthesis (Ohman et al., 2013). However, MYB103 did not directly target 300

FERULATE-5-HYDROXYLASE (F5H), which is required for syringyl lignin 301

formation (Ohman et al., 2013). 302

Phenylalanine derived from the shikimate pathway, which also gives rise to the 303

other two aromatic amino acids tyrosine and tryptophan, serves as a precursor for 304

many secondary metabolites such as lignins, flavonoids, coumarins, and lignans 305

(Maeda and Dudareva, 2012). Since lignin deposition is a very energy-consuming and 306

non-reversible process, it is critical that phenylalanine distribution among the 307

phenylpropanoid pathway and protein synthesis is tightly controlled. AtMYB12 was 308

previously shown to not only increase flavonoid biosynthesis, but also to enhance the 309



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supply of precursors and carbon from primary metabolism (Zhang et al., 2015). It was 310

also reported that a MYB transcription factor ODO1 from petunia was able to activate 311

genes involved in the shikimate pathway and the biosynthesis of 312

phenylalanine-derived volatile compounds in tomato (Dal Cin et al., 2011). However, 313

it remained unclear how plants coordinately regulate phenylalanine formation in 314

response to lignin biosynthesis. 315

It was previously shown that MYB85 was able to activate the expression of a 316

lignin biosynthesis gene, 4CL1, in a transient assay in Arabidopsis protoplasts (Zhong 317

et al., 2008). In this study, we provided evidence that MYB85, MYB42, along with 318

MYB20 and MYB43, function as regulators of lignin and shikimate biosynthesis 319

pathways. MYB20, MYB42, MYB43, MYB85, MYB58, and MYB63 belong to a 320

monophyletic group in the tree of MYB transcription factors, indicating they have 321

high similar protein sequences (Supplemental Fig. S1). Among them, AtMYB20 and 322

AtMYB43 have the highest similarity with AtMYB42 and AtMYB85 in Arabidopsis, 323

forming a monophyletic clade with their putative orthologs in Amborella trichopoda 324

and Oryza sativa (Supplemental Fig. S1). 325

Disruption of MYB20, MYB42, MYB43, and MYB85 significantly reduced the 326

expression of genes involved in lignin biosynthesis (Fig. 3B). Consistent with gene 327

reduction, lignin content was significantly reduced in myb20/42/43/85 plants, 328

indicating that MYB20, MYB42, MYB43, and MYB85 are regulators of lignin 329

biosynthesis (Fig. 3D and Supplemental Fig. S4). Interestingly, ADT genes that are 330

specifically involved in phenylalanine biosynthesis were also downregulated in 331

myb20/42/43/85 plants (Fig. 3A). However, free phenylalanine content was increased 332

despite of the fact that ADT genes were downregulated (Fig. 3C). This may be a 333

consequence of downregulated flux toward lignin biosynthesis. Even though 334

phenylalanine must be shunted toward enhanced flavonoid biosynthesis, it seems that 335

lignin biosynthesis is downregulated to a higher extent. Our data suggested that 336

MYB20, MYB42, and MYB85 could directly target both lignin biosynthesis genes 337



14

and ADT genes (Fig. 4A and 5A). However, MYB43 was only able to bind to the 338

promoter of lignin biosynthesis genes, and not ADT6, in our yeast one-hybrid assay. 339

EMSA data indicated that all four recombinant MBP-MYB fusion proteins caused an 340

up-shift of the labeled ADT6 or HCT promoters. Interestingly, each MYB protein 341

could activate ADT or lignin biosynthesis genes independently (Fig. 4G and 5G). 342

Like lignin, flavonoids are derived from phenylalanine. Studies in Arabidopsis, 343

as well as in maize, have pointed out that R2R3-MYBs have dual 344

activation/repression effects on genes from flavonoid and lignin pathways that 345

compete for carbon. For example, MYB32 and MYB4 in Arabidopsis were shown to 346

influence the composition of the pollen wall by changing the flux through 347

phenylpropanoid pathways (Preston et al., 2004). Similarly, Arabidopsis MYB75, a 348

positive regulator of anthocyanin biosynthesis, was shown to regulate lignin 349

accumulation negatively in secondary cell walls, which reflects carbon flux 350

redistribution within the branches of phenylpropanoid metabolism (Bhargava et al., 351

2010). Overexpression of ZmMYB31 from Z. mays downregulated several genes 352

involved in monolignol biosynthesis and upregulated flavonoid biosynthesis in 353

Arabidopsis (Fornalé et al., 2010). However, it remains unclear how these MYBs 354

fine-tune the biosynthesis of lignins and flavonoids. The channeling of carbon toward 355

lignin and flavonoid pathways is thought to be highly coordinated by crosstalk 356

between these pathways. It was reported that AtMYB75 can interact with AtKNAT7, 357

which functions as a negative regulator of secondary cell wall formation in 358

interfascicular fibers (Bhargava et al., 2010; Wang et al., 2019). A recent study further 359

demonstrated that AtMYB4, a transcriptional repressor of lignin biosynthesis, along 360

with its homologs MYB7 and MYB32, can attenuate the transcriptional function of 361

MYB75-TT8-TTG1 complexes in flavonoid metabolism by interacting with the TT8 362

transcription factor (Wang et al., 2019). The coordinated action of MYB repressors 363

and activators has been proposed as a fine-tuning mechanism for the regulation of 364

plant secondary metabolism (Bomal et al., 2013). In this study, we found that MYB20, 365



15

MYB42, MYB43, and MYB85 redundantly activate MYB4, which was reported to 366

repress the expression of CHS, which encodes the enzyme that catalyzes the first step 367

of flavonoid biosynthesis. Consistent with the finding that the transcript level of CHS 368

is enhanced in myb20/42/43/85, flavonoid biosynthesis is upregulated in the mutant. 369

In addition, MYB20 was shown to positively regulate the CHS promoter (Ohman et 370

al., 2013), indicating that multiple levels of transcriptional control by MYB regulators 371

can allow fine-tuned regulation of carbon flux along the phenylpropanoid pathway. In 372

conclusion, our results showed that MYB20, MYB42, MYB43, and MYB85, in 373

addition to positively regulating lignin biosynthesis by directly activating lignin and 374

phenylalanine biosynthesis genes, repress flavonoid accumulation through 375

MYB4-mediated regulation of flavonoid biosynthesis. This suggests that the 376

transcription factors MYB20, MYB42, MYB43, and MYB85 control carbon flow into 377

the phenylpropanoid pathway by activating phenylalanine biosynthesis to ensure 378

precursor supply, while at the same time repressing other competing metabolic 379

pathways to optimize lignin biosynthesis. This discovery uncovers another level of 380

complexity in the regulatory network of plant lignin biosynthesis pathway. 381

382

MATERIALS AND METHODS 383

Plant Materials and Growth Conditions 384

The Arabidopsis (Arabidopsis thaliana) mutants myb20-1 (GK-109C11-012312), 385

myb42-1 (SALKseq_78190.1), myb43-1 (SALK_085312), myb85-1 (SALK_052089), 386

nst1 (SALK_120377), and nst3 (SALK_149909) were obtained from the Arabidopsis 387

Biological Resource Center at Ohio State University. Seeds were sterilized with 3% 388

(v/v) sodium hypochlorite (NaClO), sown on half-strength Murashige and Skoog (1/2 389

MS) plates, stored at 4℃, and then transferred into a chamber under long-day 390

conditions at 22℃ (day/night cycle 16/8 h). The primers used for genotyping are 391

listed in Supplemental Table S1. 392

393



16

Phylogenetic Tree Analysis 394

Arabidopsis MYB20 was used as query to perform a BLASTP search against all 395

genes annotated on 19 published genomes, covering all main Archaeplastida clades 396

(Supplemental Table S2). Then, similar sequences with E-values less than 1e-3 and 397

an annotation term “MYB transcription factors” assigned by InterProScan (v5.24) 398

were selected (Jones et al., 2014). Multiple protein sequence alignments of MYB 399

transcription factors were performed using MAFFT (v7), positions with more than 50% 400

gaps were removed using Phyutility program (v2.2.6) (Smith and Dunn, 2008; 401

Katoh and Standley, 2013). Phylogenetic analyses were performed with a maximum 402

likelihood method by FastTree (v2.1) with optimal model of amino acid substitution 403

(LG+G) chosen based on the result of ProtTest (v3.4.2), and the bootstrap analysis 404

with 500 replicates were performed (Price et al., 2010; Darriba et al., 2011). 405

Sequences belonging to the monophyletic group of Arabidopsis MYB20, MYB43, 406

MYB42, MYB85, MYB58, and MYB63 were identified and selected for another 407

round of phylogenetic analyses as described above. Only sequences annotated from 408

Arabidopsis thaliana, Oryza sativa, Amborella trichopoda, Salvinia cucullata, Azolla 409

filiculoides, Sphagnum fallax, and Physcomitrella patens genomes were displayed on 410

the final tree. Sequences with very atypical sizes and extremely long braches were 411

manually removed. 412

Anthocyanin Measurement 413

Seedlings were grown on 1/2 MS medium containing 100 μM norflurazon. The 414

seedlings were then grown for 4 days in a growth chamber. Photographs of the 415

seedlings were taken by a microscope. To analyze anthocyanin content, the seeds 416

were grown on plates with 1/2 MS medium containing 1% (w/v) sucrose for 14 days 417

and then transferred to 1/2 MS medium containing 12% (w/v) sucrose for 3 days 418

(Yonekura-Sakakibara et al., 2012). Plants were harvested and frozen with liquid 419

nitrogen immediately. Anthocyanins were extracted with methanol containing 0.2% 420

(v/v) formic acid and 30% (v/v) water, and then placed at -20℃ overnight to remove 421



17

chlorophyll. The determination of anthocyanin content was carried out by 422

spectrophotometry at 530 nm. The anthocyanin level of wild type Col-0 (1.13 mg 423

cyanidin 3-O-glucoside equivalence g–1

) was set to 100. 424

425

RNA Analyses 426

Total RNA was extracted from the inflorescence stems of 33-day-old Arabidopsis 427

wild type Col-0 and myb20/42/43/85 mutants using the RNeasy Plant Mini Kit 428

(QIAGEN). Three biological replicates of each sample were sent to BGI Genomics 429

Co., Ltd (The Beijing Genomics Institute) for construction of libraries and RNA-seq. 430

Data was analyzed on the Dr. Tom system from BGI. 431

The double mutants, myb20/43 and myb42/85, were planted and harvested at the 432

same time as wild type Col-0 and the myb20/42/43/85 mutant. Total RNA was 433

reverse-transcribed by Superscript Reverse Transcriptase III (Invitrogen). Reverse 434

transcription quantitative PCR (RT-qPCR) was performed with SYBR Premix Ex Taq 435

(Takara). The average levels of transcripts were from three biological replicates, and 436

each biological replicate was from triplicate cDNA. The Arabidopsis Tubulin gene 437

was used as a reference. The primers are listed in Supplemental Table S1. 438

439

KEGG (Kyoto Encyclopedia of Genes and Genomes) Pathway Analysis. 440

KEGG pathway enrichment analysis was performed using the Dr. Tom system from 441

BGI. According to KEGG pathway annotation, phyper function in the R project was 442

used to calculate P value and false discovery rates (FDRs). Q value was the correction 443

of P value. Terms with Q values ≤ 0.05 were considered as enriched. 444

445

Dual-luciferase Assay 446

To test transcriptional activation, the dual-luciferase assay was performed in 447

Nicotiana benthamiana leaves. About 1kb of the promoters of MYB20, MYB42, 448

MYB43, MYB85, and MYB4 were cloned into the pGreenII 0800-LUC vector to 449

generate P-LUC reporter constructs (Hellens et al., 2005). Each promoter in pGreenII 450



18

0800-LUC was transformed into Agrobacterium tumefaciens strain GV3101 451

containing the helper plasmid pSoup-P19 (Hellens et al., 2005). The full-length 452

coding sequences (without stop codons) of NST3, MYB46, MYB20, MYB42, MYB43, 453

MYB85, and GUS were cloned into the pEarleyGate 101 vector (pEG101). These six 454

constructs were transformed into Agrobacterium tumefaciens strain GV3101. 455

Overnight cultures of Agrobacterium strains were re-suspended in infiltration buffer 456

(10mM MgCl2, 10mM MES and 0.1 mM acetosyringone) to OD600 ~ 0.6 and 457

incubated at room temperature for 2 hours. The reporter:effector ratio was 2:8. 458

Different combinations of Agrobacterium suspension were infiltrated onto N. 459

benthamiana leaves. After 48 hours, leaf samples were collected and ground in liquid 460

nitrogen for the dual-luciferase assay. Luciferase activities were detected using the 461

Dual-luciferase Reporter Assay System (Promega). Each sample contained three 462

biological repeats. 463

To examine whether each MYB was able to activate the genes independently, a 464

transcriptional activation assay was conducted in Arabidopsis Col-0 and 465

myb20/42/43/85 protoplasts. About 1kb promoters of ADT6 and HTC were cloned 466

into the pGreenII 0800-LUC. The coding sequences of MYB20, MYB42, MYB43, and 467

MYB85 were inserted into p2GW7 under the control of the 35S promoter. After the 468

protoplast preparation and subsequent transfection were completed (Yoo et al., 2007), 469

samples were collected. The test of luciferase activities was described above. The raw 470

data was in the Supplemental Table S3. 471

472

Yeast One-hybrid Assays 473

GAD fusion constructs were co-transformed with the LexAop::LacZ (Clontech) 474

reporter gene plasmid into the EGY48 yeast strain. Transformants were grown on 475

appropriate drop-out plates containing X-gal 476

(5-bromo-4-chloro-3-indolyl-b-D-galactopyranoside) for blue color test. 477

478



19

EMSA 479

The DNA fragments of MYBs were cloned into pMAL-c2x vector, and 480

expressed in the Escherichia coli BL21 (DE3) cell line, which were cultured in LB 481

culture at 37°C to an OD600 between 0.6–0.8 was reached. To induce protein 482

expression, a final concentration of 0.5 mM isopropyl β-D-1-thiogalactopyranoside 483

was added to the cultures, after which the cells were incubated for 8 h at 28°C. Cells 484

were harvested and resuspended in buffer containing 20 mM Tris-HCl pH 7.4, 200 485

mM NaCl, and 1 mM EDTA pH 8.0. After sonication and centrifugation, the MBP-TF 486

proteins were purified using amylose resin from the supernatant. 487

The oligonucleotide probes were labeled with TAMRA or FAM and synthesized 488

from Sangon Biotech. Then, the oligonucleotides were diluted to 10 μM, and heated 489

to 95℃ for 5 min, and slowly cooled to room temperature. Briefly, 1 pmol of labeled 490

probe was incubated with 0.1 μg of the indicated protein in 20-μL reaction buffer (25 491

mM HEPES, pH 8.0, 40 mM KCl, 5 mM MgCl2, 1 mM DTT, 1 mM EDTA, 8% v/v 492

glycerol, 1 μg poly (dI-dC)) for 20 min at room temperature. Then, to the reaction 493

mixture was added 5 μL of 5X loading buffer (12.5% w/v Ficoll-400, 0.2% w/v 494

bromophenol blue, 0.2% w/v xylene cyanol FF) and loaded onto as 4.5% 495

polyacrylamide gel in 0.5X TBE. The labeled DNAs were detected using a Typhoon 496

FLA 9500 Instrument (General Electric Company). 497

498

Amino Acid Extraction and Analysis 499

Amino acids were extracted from 50 mg (dry weight) of 5-week-old Arabidopsis 500

stem samples with 1 mL of 0.5 M HCl solution. The supernatants were subsequently 501

filtered using a 0.22 μm nylon membrane and 250 μL of the extraction supernatant 502

was transferred into autosamper vials. Finally, the mixture was diluted to 1 mL with 503

20% (v/v) water in ACN prior to further analysis. Ultra-performance liquid 504

chromatography-electrospray ionization tandem mass spectrometric 505

(UPLC-ESI-MS/MS) analysis was carried out on an Agilent 1290 LC system coupled 506



20

to an Ultivo Triple Quadrupole mass spectrometer by means of an electrospray 507

ionization (ESI) probe. Eluent A was 20 mM ammonium formate in water (pH 3), 508

while eluent B was 20 mM aqueous ammonium formate (pH 3) in 9:1 509

acetonitrile/water. The separation gradient was: 100% B at 0 min, 70% B at 5 min, 510

and 100% B at 8 min. The column temperature was maintained at 25°C. The injection 511

volume of each sample was 1 μL. The MRM-MS method was employed for the 512

quantitation of amino acids. Data for phenylalanine was acquired in positive-ion (PI) 513

mode under the following operating conditions: desolvation temperature: 330°C; 514

desolvation gas (N2) rate, 13 L/min; collision energy, 13 V for quantitative ion (m/z 515

120.1) and 29 V for qualitative ion (m/z 103), respectively. 516

517

Determination of Lignin Composition 518

Thioacidolysis analysis was performed to determine lignin composition. Briefly, 519

30 mg samples were reacted with 3 mL of 0.2 M BF3-etherate in an 8.75:1 520

dioxane/ethanethiol mixture at 100°C for 4 h. After adding 4 mL of water, the mixture 521

was extracted using 4 mL of dichloromethane (three times). The organic layer was 522

separated and dried under a stream of nitrogen. After derivatization with 523

N,O-bis-(trimethylsily)trifluoroacetamide (BSTFA) + 1% (w/v) trimethylchlorosilane 524

(TMCS) (Sigma-Aldrich), lignin-derived monomers were identified by GC-MS and 525

quantified by GC as their trimethylsilyl derivatives. GC-MS was performed on an 526

Agilent Intuvo 9000 GC system with a 5977B series mass-selective detector (column: 527

HP-5MS; 30 m × 0.25 mm; 0.25-μm film thickness), and mass spectra were recorded 528

in electron impact mode (70 eV) with a 50–650 m/z scanning range. 529

530

Quantification of Flavonoids 531

Samples of three replicates of Arabidopsis stems were collected and ground into 532

a fine powder with a mortar and pestle under liquid nitrogen. Twenty microgram dried 533

samples were extracted with 1 mL 80% (v/v) methanol (containing 100 μM 534



21

naringenin as an internal reference), and then ultrasonic processing was conducted for 535

30 min at room temperature. After that, the samples were centrifuged at 14000 g for 536

10 min, and the supernatant was transferred to a sterile 1.5 mL Eppendorf tube for 537

another centrifugation as above. 300 μL sterile milli-Q water was added to each 1 mL 538

supernatant solution and stored at -20℃ overnight to precipitate chlorophyll. The 539

following day, 5 μL of the supernatant solution after another centrifugation was 540

injected for UPLC analysis. The identification of soluble flavonoid compounds was 541

described previously (Yonekura-Sakakibara et al., 2008) and quantification of 542

detected compounds was based on the standard curves of a kaempferol standard 543

detected in the same UPLC runs. 544

545

Statistical Analyses 546

The SPSS 20.0 statistical package was used for the statistical data analysis. 547

Statistical analysis was done with univariate analysis and Scheffe post-hoc testing at 548

the 5% level. Samples included in the analysis were arranged based on at least three 549

biological replicates. 550

551

Data Availability 552

RNA-seq data have been uploaded to the SRA (http://www.ncbi.nlm.nih.gov/sra) 553

with the accession number PRJNA578015. 554

555

Accession Numbers 556

The Arabidopsis Information Resource accession numbers of genes mentioned 557

are as follows: AT2G46770 (NST1), AT3G61910 (NST2), AT1G32770 (NST3), 558

AT5G12870 (MYB46), AT1G66230 (MYB20), AT4G12350 (MYB42), AT5G16600 559

(MYB43), AT4G22680 (MYB85), AT4G38620 (MYB4), AT2G16720 (MYB7), 560

AT4G34990 (MYB32), AT2G37040 (PAL1), AT2G30490 (C4H), AT1G15710 561

(ADH2), AT3G44720 (ADT4), AT5G22630 (ADT5), AT1G08250 (ADT6), 562


http://www.ncbi.nlm.nih.gov/sra


22

AT1G51680 (4CL1), AT3G19450 (CAD4), AT1G52760 (CSE), AT5G48930 (HCT), 563

AT3G54640 (TSA1), AT5G54810 (TSB1), AT5G13930 (CHS). 564

565

SUPPLEMENTAL DATA 566

The following supplemental materials are available. 567

Supplemental Figure S1. Phylogenetic tree analysis of MYBs in 19 published 568

genomes in main archaeplastida clades. 569

Supplemental Figure S2. NST1/2/3 and MYB46/83 could not bind the promoters of 570

MYB20/42/43/85 directly. 571

Supplemental Figure S3. KEGG pathway enrichment analysis. 572

Supplemental Figure S4. Lignin content Klason analysis of wild type (Clo-0), 573

myb20/43, myb42/85, and myb20/42/43/85. 574

Supplemental Figure S5. Truncated MYB proteins have higher expression in yeast. 575

Supplemental Figure S6. Disruption of MYB20/42/43/85 promotes anthocyanin 576

accumulation. 577

Supplemental Table S1. Primers used for vector construction and gene expression 578

analysis. 579

Supplemental Table S2. Resources of 19 representative genomes used in 580

phylogenetic tree analysis. 581

Supplemental Table S3. Source data of the firefly and Renilla luciferase signal in the 582

dual-luciferase assay. 583

Supplemental Dataset S1. A full list of the genes that are upregulated in 584

myb20/42/43/85 (FDR < 0.05, log2FC > 1). 585

Supplemental Dataset S2. A full list of the genes that are downregulated in 586

myb20/42/43/85 (FDR < 0.05, log2FC < -1). 587

588

Acknowledgments: This work was supported by grants from the Youth Thousand 589

Scholar Program of China, National Natural Science Foundation of China (grant 590



23

number 31522008 and 31570296) and the School of Life Sciences, Tsinghua 591

University. 592

593

Figure Legends 594

595

Figure 1. Description of myb20, myb42, myb43, and myb85 mutants. A, Relative 596

transcript levels of MYB20, MYB42, MYB43, and MYB85 in the inflorescence stems of 597

33-day-old wild-type (Col-0) and nst1/3 mutant plants were determined by reverse 598

transcription quantitative PCR (RT-qPCR). The expression level in Col-0 was set to 1. 599

Tubulin was used as the internal control. B and C, Transient expression assays showed 600

that the promoters of MYB20, MYB42, MYB42, and MYB85 can be activated by NST3 601

(B) and MYB46 (C). The PMYB20-LUC, PMYB42-LUC, PMYB43-LUC, and 602

PMYB85-LUC reporters were respectively cotransformed with the indicated 603

constructs in Nicotiana benthamiana leaves. The LUC/REN ratio represents the LUC 604

activity relative to the REN activity. CK was the vector of GUS-pEarleyGate 101, 605

used as a control, and was set to 1. Data are means ± SD of three biological replicates. 606

D, Schematic diagrams of the structures of MYB20, MYB42, MYB43, MYB85, and 607

T-DNA insertions. Solid boxes represent exons, black lines represent introns, and 608

hollow boxes represent UTRs. E, RT-qPCR analysis of MYB20, MYB42, MYB42, and 609

MYB85 transcripts in the inflorescence stems of 33-day-old plants. Tubulin was used 610

as a positive control. Data are means ± SD of three biological replicates. Asterisks 611

indicate significant differences by the Student’s t test (*P <0.05, **P <0.01, ***P 612

<0.001, and ****P <0.0001). 613

614

Figure 2. Disruption of MYB20/42/43/85 causes growth and fertility defects. A, 615

Five-week-old plants of Col-0, the double mutants myb20/43 and myb42/85, and the 616

quadruple mutant myb20/42/43/85. B, The inflorescence stems of six-week-old plants 617

of Col-0 and myb20/42/43/85. C, The upper inflorescence stems as in (B). D, The 618

middle inflorescence stems as in (B). 619

620

Figure 3. MYB20, MYB42, MYB43, and MYB85 redundantly regulate 621

phenylalanine and lignin biosynthesis. A and B, Relative transcript levels of 622

aromatic amino acid (A) and lignin (B) biosynthesis genes in the inflorescence stems 623

of 33-day-old Arabidopsis wild type, myb20/43, myb42/85, and myb20/42/43/85 624

mutants as determined by RT-qPCR. C, Phenylalanine level (Phe) in the inflorescence 625

stems of plants with the same genotypes and period as in (A). DW, dry weight. D, 626

Lignin composition analysis of the inflorescence stems of plants with the same 627

genotypes and period as in (A). Gas chromatographic quantification of H, G, and S 628

lignin units by thioacidolysis. Data are means ± SD of three biological replicates. 629

Based on Tukey’s test, columns with the same letters are not significantly different 630

and columns with the different letters are significantly different (P < 0.05; one-way 631



24

ANOVA). 632

633

Figure 4. MYBs activate phenylalanine biosynthesis genes. A, GAD-MYBs 634

activate the expression of the LacZ reporter gene driven by the ADT6 promoter in 635

yeast. GFP was used as the negative control. B, The upper schematic diagram and the 636

lower one show the promoter regions of ADT6 in (A) and in (C-F) separately. C-F, 637

EMSA showed that MYB20 (C), MYB42 (D), MYB43 (E), and MYB85 (F) bind to 638

the promoter of ADT6. The cold probes used as competitors were with the same 639

sequence as the TAMRA-labeled probes. Truncated MYB20 (Δ166-282 a.a.), MYB42 640

(Δ138-286 a.a.), MYB43 (Δ201-327 a.a.), and MYB85 (Δ168-266 a.a.) were used for 641

yeast one-hybrid assay (A) and EMSA assay (C-F). G and H, Transient expression 642

assays showed that the ADT6 promoter can be activated by MYB20/42/43/85 in 643

Arabidopsis Col-0 protoplasts (G) and in Arabidopsis myb20/42/43/85 mutant 644

protoplasts (H). CK was empty vector as control and was set to 1. Data are means ± 645

SD of three biological replicates. Based on Tukey’s test, columns with the same letters 646

are not significantly different and columns with the different letters are significantly 647

different (P < 0.05; one-way ANOVA). 648

649

Figure 5. MYBs activate lignin biosynthesis genes. A, GAD-MYBs activate the 650

expression of the LacZ reporter gene driven by the HCT promoter in yeast. GFP was 651

used as the negative control. B, The upper schematic diagram and the lower one show 652

the promoter regions of HCT in (A) and in (C-F) separately. C-F, EMSA showed that 653

MYB20 (C), MYB42 (D), MYB43 (E), and MYB85 (F) bind to the promoter of HCT. 654

The cold probes used as competitors were with the same sequence as the 655

FAM-labeled probes. Truncated MYB20 (Δ166-282 a.a.), MYB42 (Δ138-286 a.a.), 656

MYB43 (Δ201-327 a.a.), and MYB85 (Δ168-266 a.a.) were used for yeast one-hybrid 657

assay (A) and EMSA assay (C-F). G and H, Transient expression assays showed that 658

the HCT promoter can be activated by MYB20/42/43/85 in Arabidopsis Col-0 659

protoplasts (G) and in Arabidopsis myb20/42/43/85 mutant protoplasts (H). CK was 660

empty vector as control and was set to 1. Data are means ± SD of three biological 661

replicates. Based on Tukey’s test, columns with the same letters are not significantly 662

different and columns with the different letters are significantly different (P < 0.05; 663

one-way ANOVA). 664

665

Figure 6. MYBs activate MYB4/7/32 genes directly. A, MYB4, MYB7, and MYB32 666

transcript levels in the inflorescence stems of 33-day-old wild type, myb20/43, 667

myb42/85, and myb20/42/43/85 mutants as determined by RT-qPCR. B, Transient 668

expression assays showed that the MYB4 promoter can be activated by MYB20, 669

MYB42, MYB43, and MYB85 in N. benthamiana leaves. CK was the vector of 670

GUS-pEarleyGate 101, used as a control, and was set to 1. C-F, EMSA showing that 671

MYB20 ©, MYB42 (D), MYB43 (E), and MYB85 (F) bind to the promoter of MYB4. 672

The cold probes used as competitors were with the same sequence as the 673



25

FAM-labeled probes. Truncated MYB20 (Δ166-282 a.a.), MYB42 (Δ138-286 a.a.), 674

MYB43 (Δ201-327 a.a.), and MYB85 (Δ168-266 a.a.) were used for EMSA assay 675

(C-F). Data are means ± SD of three biological replicates. Based on Tukey’s test, 676

columns with the same letters are not significantly different and columns with the 677

different letters are significantly different (P < 0.05; one-way ANOVA). 678

679

Figure 7. Disruption of MYB20/42/43/85 promotes soluble flavonoids 680

accumulation. A, RT-qPCR analysis of CHS in the inflorescence stems of 5-week-old 681

wild type, myb20/42/43/85, and myb4/7/32 mutants. B, Quantification of the three 682

major flavonols in the inflorescence stems of the same plants as (A). K1, kaempferol 683

3-O-[6"-O-(rhamnosyl)glucoside] 7-O-rhamnoside; K2, kaempferol 3-O-glucoside 684

7-O-rhamnoside; K3, kaempferol 3-O-rhamnoside 7-O-rhamnoside. Data are means ± 685

SD of three biological replicates. Based on Tukey’s test, columns with the same letters 686

are not significantly different and columns with the different letters are significantly 687

different (P < 0.05; one-way ANOVA). 688

689

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Figure 1. Description of myb20, myb42, myb43, and myb85 mutants. A, Relative transcript levels of MYB20,

MYB42, MYB43, and MYB85 in the inflorescence stems of 33-day-old wild type (Col-0) and nst1/3 mutant

plants were determined by reverse transcription quantitative PCR (RT-qPCR). The expression level in Col-0

was set to 1. Tubulin was used as the internal control. B and C, Transient expression assays showed that the

promoters of MYB20, MYB42, MYB42, and MYB85 can be activated by NST3 (B) and MYB46 (C). The

PMYB20-LUC, PMYB42-LUC, PMYB43-LUC, and PMYB85-LUC reporters were respectively cotransformed with the

indicated constructs in Nicotiana benthamiana leaves. The LUC/REN ratio represents the LUC activity

relative to the REN activity. CK was the vector of GUS-pEarleyGate 101, used as a control, and was set to 1.

Data are means ± SD of three biological replicates. D, Schematic diagrams of the structures of MYB20,

MYB42, MYB43, MYB85, and T-DNA insertions. Solid boxes represent exons, black lines represent introns,

and hollow boxes represent UTRs. E, RT-qPCR analysis of MYB20, MYB42, MYB42, and MYB85 transcripts

in the inflorescence stems of 33-day-old plants. Tubulin was used as a positive control. Data are means ± SD

of three biological replicates. Asterisks indicate significant differences by the Student’s t test (*P <0.05, **P

<0.01, ***P <0.001, and ****P <0.0001).



Figure 2. Disruption of MYB20/42/43/85 causes growth and fertility defects. A, Five-week-old plants of

Col-0, the double mutants myb20/43 and myb42/85, and the quadruple mutant myb20/42/43/85. B, The

inflorescence stems of six-week-old plants of Col-0 and myb20/42/43/85. C, The upper inflorescence stems

as in (B). D, The middle inflorescence stems as in (B).



Figure 3. MYB20, MYB42, MYB43, and MYB85 redundantly regulate phenylalanine and lignin

biosynthesis. A and B, Relative transcript levels of aromatic amino acid (A) and lignin (B) biosynthesis

genes in the inflorescence stems of 33-day-old Arabidopsis wild type, myb20/43, myb42/85, and

myb20/42/43/85 mutants as determined by RT-qPCR. C, Phenylalanine level (Phe) in the inflorescence

stems of plants with the same genotypes and period as in (A). DW, dry weight. D, Lignin composition

analysis of the inflorescence stems of plants with the same genotypes and period as in (A). Gas

chromatographic quantification of H, G, and S lignin units by thioacidolysis. Data are means ± SD of three

biological replicates. Based on Tukey’s test, columns with the same letters are not significantly different and

columns with the different letters are significantly different (P < 0.05; one-way ANOVA).



Figure 4. MYBs activate phenylalanine biosynthesis genes. A, GAD-MYBs activate the expression of the

LacZ reporter gene driven by the ADT6 promoter in yeast. GFP was used as the negative control. B, The

upper schematic diagram and the lower one show the promoter regions of ADT6 in (A) and in (C-F)

separately. C-F, EMSA showed that MYB20 (C), MYB42 (D), MYB43 (E), and MYB85 (F) bind to the

promoter of ADT6. The cold probes used as competitors were with the same sequence as the

TAMRA-labeled probes. Truncated MYB20 (Δ166-282 a.a.), MYB42 (Δ138-286 a.a.), MYB43 (Δ201-327

a.a.), and MYB85 (Δ168-266 a.a.) were used for yeast one-hybrid assay (A) and EMSA assay (C-F). G and

H, Transient expression assays showed that the ADT6 promoter can be activated by MYB20/42/43/85 in

Arabidopsis Col-0 protoplasts (G) and in Arabidopsis myb20/42/43/85 mutant protoplasts (H). CK was

empty vector as control and was set to 1. Data are means ± SD of three biological replicates. Based on

Tukey’s test, columns with the same letters are not significantly different and columns with the different

letters are significantly different (P < 0.05; one-way ANOVA). www.plantphysiol.orgon February 29, 2020 - Published by Downloaded from

Copyright © 2019 American Society of Plant Biologists. All rights reserved.


Figure 5. MYBs activate lignin biosynthesis genes. A, GAD-MYBs activate the expression of the LacZ

reporter gene driven by the HCT promoter in yeast. GFP was used as the negative control. B, The upper

schematic diagram and the lower one show the promoter regions of HCT in (A) and in (C-F) separately. C-F,

EMSA showed that MYB20 (C), MYB42 (D), MYB43 (E), and MYB85 (F) bind to the promoter of HCT.

The cold probes used as competitors were with the same sequence as the FAM-labeled probes. Truncated

MYB20 (Δ166-282 a.a.), MYB42 (Δ138-286 a.a.), MYB43 (Δ201-327 a.a.), and MYB85 (Δ168-266 a.a.)

were used for yeast one-hybrid assay (A) and EMSA assay (C-F). G and H, Transient expression assays

showed that the HCT promoter can be activated by MYB20/42/43/85 in Arabidopsis Col-0 protoplasts (G)

and in Arabidopsis myb20/42/43/85 mutant protoplasts (H). CK was empty vector as control and was set to 1.

Data are means ± SD of three biological replicates. Based on Tukey’s test, columns with the same letters are

not significantly different and columns with the different letters are significantly different (P < 0.05;

one-way ANOVA). www.plantphysiol.orgon February 29, 2020 - Published by Downloaded from



Figure 6. MYBs activate MYB4/7/32 genes directly. A, MYB4, MYB7, and MYB32 transcript levels in the

inflorescence stems of 33-day-old wild type (Col-0), myb20/43, myb42/85, and myb20/42/43/85 mutants as

determined by RT-qPCR. B, Transient expression assays showed that the MYB4 promoter can be activated

by MYB20, MYB42, MYB43, and MYB85 in N. benthamiana leaves. CK was the vector of

GUS-pEarleyGate 101, used as a control, and was set to 1. C-F, EMSA showing that MYB20 (C), MYB42

(D), MYB43 (E), and MYB85 (F) bind to the promoter of MYB4. The cold probes used as competitors were

with the same sequence as the FAM-labeled probes. Truncated MYB20 (Δ166-282 a.a.), MYB42 (Δ138-286

a.a.), MYB43 (Δ201-327 a.a.), and MYB85 (Δ168-266 a.a.) were used for EMSA assay (C-F). Data are

means ± SD of three biological replicates. Based on Tukey’s test, columns with the same letters are not

significantly different and columns with the different letters are significantly different (P < 0.05; one-way

ANOVA).



Figure 7. Disruption of MYB20/42/43/85 promotes soluble flavonoids accumulation. A, RT-qPCR analysis

of CHS in the inflorescence stems of 5-week-old wild type (Col-0), myb20/42/43/85, and myb4/7/32 mutants.

B, Quantification of the three major flavonols in the inflorescence stems of the same plants as (A). K1,

kaempferol 3-O-[6"-O-(rhamnosyl)glucoside] 7-O-rhamnoside; K2, kaempferol 3-O-glucoside

7-O-rhamnoside; K3, kaempferol 3-O-rhamnoside 7-O-rhamnoside. Data are means ± SD of three biological

replicates. Based on Tukey’s test, columns with the same letters are not significantly different and columns

with the different letters are significantly different (P < 0.05; one-way ANOVA).



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MYB20, MYB42, MYB43 and MYB85 Regulate Phenylalanine …chorismate phenylalanine biosynthesis...

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Transcript of MYB20, MYB42, MYB43 and MYB85 Regulate Phenylalanine …chorismate phenylalanine biosynthesis...