wheat taspl8 modulates leaf angle through auxin and ...jun 17, 2019 · 147 that the flag leaf...

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Wheat TaSPL8 Modulates Leaf Angle Through Auxin and 1

Brassinosteroid Signaling 2

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Kaiye Liuabc,1, Jie Caoabc,1, Kuohai Yuabc, Xinye Liuabc, Yujiao Gaoabc, Qian Chenabc, 4 Wenjia Zhangabc, Huiru Pengabc, Jinkun Duabc, Mingming Xinabc, Zhaorong Huabc, 5 Weilong Guoabc, Vincenzo Rossid, Zhongfu Niabc, Qixin Sunabc, and Yingyin Yaoabc* 6

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aState Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing, 100193, China 8

bKey Laboratory of Crop Heterosis and Utilization (MOE), China Agricultural University, Beijing, 100193, China 9

cBeijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, 100193, China 10

dCouncil for Agricultural Research and Economics, Research Centre for Cereal and Industrial Crops, I-24126 11

Bergamo, Italy 12

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1These authors contributed equally to this work. 14

*Corresponding author: Yingyin Yao 15

China Agricultural University, Beijing, 100193, China 16

Tel: 86 +10 62732304 17

Email: [email protected] 18

Running Title: Wheat TaSPL8 affects leaf angle. 19

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One-sentence summary: 21

Wheat TaSPL8 regulates lamina joint development and leaf angle through auxin 22

signaling and the brassinosteroid biosynthesis pathway. 23

Author contributions 24

Z.N., Q.S., and Y.Y. conceived this project and designed all experiments. K.L., J.C, 25

K.Y., X.L., Y.G., M.X., W.Z. and W.G. performed the experiments and data analysis. 26

Q.C., H.P., and Z.H. contributed to the wheat transformation. Y.Y., V.R., and J.D. 27

contributed to manuscript writing and revision, and R.X. analyzed data. 28

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Plant Physiology Preview. Published on June 17, 2019, as DOI:10.1104/pp.19.00248

Copyright 2019 by the American Society of Plant Biologists

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Abstract 30

In grass crops, leaf angle is determined by development of the lamina joint, the tissue 31

connecting the leaf blade and sheath, and is closely related to crop architecture and 32

yield. In this study, we identified a mutant generated by fast neutron radiation that 33

exhibited an erect leaf phenotype caused by defects in lamina joint development. 34

Map-based cloning revealed that the gene TaSPL8, encoding a SQUAMOSA 35

PROMOTER BINDING-LIKE (SPL) protein, is deleted in this mutant. TaSPL8 36

knock-out mutants exhibit erect leaves due to loss of the lamina joint, compact 37

architecture, and increased spike number especially in high planting density, suggesting 38

similarity with its LIGULESS1 (LG1) homologs in maize (Zea mays) and rice (Oryza 39

sativa). Hence, LG1 could be a robust target for plant architecture improvement in grass 40

species. Common wheat (Triticum aestivum, 2n=6×=42; BBAADD) is an 41

allohexaploid containing A/B/D subgenomes and the homoeologous gene of TaSPL8 42

from the D subgenome contributes to the length of the lamina joint to a greater extent 43

than that from the A and B subgenomes. Comparison of the transcriptome between the 44

Taspl8 mutant and the wild type revealed that TaSPL8 is involved in the activation of 45

genes related to auxin and brassinosteroid pathways and cell elongation. TaSPL8 binds 46

to the promoters of the AUXIN RESPONSE FACTOR (TaARF6) gene and of the 47

brassinosteroid biogenesis gene CYP90D2 (TaD2) and activates their expression. 48

These results indicate that TaSPL8 might regulate lamina joint development through 49

auxin signaling and the brassinosteroid biosynthesis pathway. 50

Introduction 51

Leaf angle, defined as the inclination between the leaf blade midrib and the stem, 52

directly influences canopy structure and consequentially affects yield (Mantilla-Perez 53

and Salas Fernandez, 2017). Plants with erect leaves have an increased capacity to 54

intercept light and higher photosynthetic efficiency, which results in improved grain 55 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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filling (Sinclair et al., 1999). More efficient grain filling enables planting of larger 56

populations with a greater leaf area index (LAI). Hence, using plants with more erect 57

leaves generally improves the yield per unit of cultivated area (Pendleton et al., 1968; 58

Duvick, 2005; Lee and Tollenaar, 2007; Lauer et al., 2012). For example, the maize 59

(Zea mays) liguleless2 (lg2) mutant has erect leaves and produces 40% more grain than 60

its counterpart with horizontal-type leaves due to the relative efficiency of CO2 fixation 61

per unit of incoming sunlight, which increases as the leaf angle decreases (Pendleton et 62

al., 1968). In rice (Oryza sativa), the Osdwarf4-1 mutant exhibits an erect leaf 63

phenotype that is associated with brassinosteroid (BR) deficiency and has enhanced 64

grain yields under dense planting populations (Sakamoto et al., 2006). In wheat 65

(Triticum sp.), the important characteristics of the ideal plant architecture (ideotype) 66

include short and strong stems with few, small, and erect leaves (Donald, 1968). Wheat 67

genotypes with erect leaves also have a superior net carbon fixation capacity during 68

grain filling (Austin et al., 1976). Therefore, breeding grass crops for more erect leaves 69

is a reasonable strategy for improving crop productivity. 70

71

Leaf angle depends on cell division, expansion, and cell wall composition in the lamina 72

joint (including the auricle and ligule), which connects the leaf blade and sheath (Kong 73

et al., 2017; Zhou et al., 2017). Genetic and functional studies indicated that various 74

factors are involved in regulating lamina joint development, and consequentially affect 75

leaf angle. Phytohormones, such as BR and auxin, play crucial roles in regulating the 76

lamina inclination (Luo et al., 2016). In rice, loss of function of BR biosynthetic genes, 77

such as dwarf4-1 (Sakamoto et al., 2006), ebisu dwarf (d2) (Hong et al., 2003), 78

brassinosteroid-deficient dwarf1 (brd1) (Hong et al., 2002), and chromosome segment 79

deleted dwarf 1(csdd1) (Li et al., 2013) results in reduced leaf inclination. Lamina joint 80

development is also associated with BR signaling, as reported by studies of mutants 81

less sensitive to BR, such as the BR-defective mutant d61 (Yamamuro et al., 2000) and 82

transgenic rice plants with suppressed expression of BRI1-Associated receptor Kinase 83 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by

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1 (OsBAK1) (Li et al., 2009) and BRASSINAZOLE-RESISTANT1 (OsBZR1) (Bai et al., 84

2007). Similarly, auxin biosynthesis and signaling pathways influence lamina joint 85

development. Both the gain-of-function rice LEAF INCLINATION1 (OsLC1) (Zhao et 86

al., 2013) mutant and plants overexpressing Gretchen Hagen 3 acyl acid amido 87

synthetases (GH3) family members, including OsGH3-1, -2, -5, and -13 (Du et al., 88

2012; Zhao et al., 2013; Zhang et al., 2015), have reduced auxin levels and show an 89

enlarged leaf angle due to stimulated cell elongation at the lamina joint region. Rice 90

transgenic lines overexpressing the auxin response factor OsARF19 exhibit an enlarged 91

lamina inclination related to the increase of adaxial cell division (Zhang et al., 2015). 92

Furthermore, high concentrations of the auxin indole-3-acetic acid (IAA) influence leaf 93

inclination by interacting with BR (Wada et al., 1981; Cao and Chen, 1995) and 94

ethylene, which also participates in BR-induced leaf inclination (Jang et al., 2017). 95

Therefore, crosstalk occurs between different phytohormones in regulating lamina joint 96

development and leaf inclination. 97

98

Genetic approaches have identified several genes that affect lamina joint development 99

in rice and maize (Mantilla-Perez and Salas Fernandez, 2017). For instance, rice 100

BRASSINOSTEROID UPREGULATED 1-LIKE1 (OsBUL1), encoding a typical bHLH 101

transcription factor, is preferentially expressed in the lamina joint and affects leaf angle 102

by controlling cell elongation (Jang et al., 2017). Similarly, overexpression or ectopic 103

expression of other bHLH transcription factor genes, such as LAX PANICLE (LAX), 104

OsbHLH153, OsbHLH173, OsbHLH174, BRASSINOSTEROID UPREGULATED1 105

(BU1), INCREASED LAMINA INCLINATION1 (ILI1), and POSITIVE REGULATOR 106

OF GRAIN LENGTH1 (PGL1), results in a larger lamina inclination (Komatsu et al., 107

2003; Tanaka et al., 2009; Zhang et al., 2009; Dong et al., 2018). LEAF 108

INCLINATION2 (LC2), a VIN3-like protein, regulates lamina inclination by 109

repressing adaxial cell division in the collar region (Zhao et al., 2010). An increased 110

leaf angle 1 (ila1) mutant shows increased leaf angle due to abnormal vascular bundle 111 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



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formation and cell wall composition in the lamina joint (Ning et al., 2011). It was 112

suggested that rice SPX1 (SYG1/Pho81/XPR1) could interact with Regulator of Leaf 113

Inclination 1 (RLI1) and negatively regulate leaf inclination by affecting lamina joint 114

cell elongation (Ruan et al., 2018). Mutations in LIGULELESS1 (LG1), which encodes 115

a conserved SPL transcription factor in maize and rice, result in an erect leaf phenotype 116

with a complete loss of the auricle and ligule (Moreno et al., 1997; Lee et al., 2007). A 117

single-nucleotide polymorphism in the upstream region of OsLG1 may be responsible 118

for its expression and affects panicle closure or spreading by controlling cell 119

proliferation at the panicle pulvinus (Ishii et al., 2013; Zhu et al., 2013). However, the 120

contribution of LG1 to potential yield and its mechanism in affecting lamina joint 121

development are still unknown. 122

123

In wheat, genetic approaches have identified several quantitative trait loci (QTL) that 124

control leaf inclination. For example, QTL analysis of the markers for flag leaf angle 125

from durum wheat (Triticum durum) populations indicated the presence of large-effect 126

QTL on chromosomes 2A, 2B, 3A, 3B, 4B, 5B, and 7A (Isidro et al., 2012). Several 127

environmentally-stable QTL for flag leaf angle were mapped on chromosomes 1B, 3D, 128

5A, 6B, 7B, and 7D using two recombinant inbred line (RIL) populations (Wu et al., 129

2015; Liu et al., 2018b). However, to date, no genes have been shown to be directly 130

involved in the control of leaf angle in wheat. In this study, we characterized a wheat 131

(Triticum aestivum) mutant with a multi-gene deleted region, which exhibits erect 132

leaves and compact plant architecture. We demonstrate that the TaSPL8 gene, which 133

encodes the SBP domain-containing transcription factor and is homologous to LG1 in 134

maize and rice, is responsible for this mutant phenotype. Our results indicate that 135

TaSPL8 regulates lamina joint development through affecting auxin response and BR 136

biogenesis pathways, thus providing information about the mechanisms linking the 137

activity of SPL family members and hormone-mediated regulation of leaf angle. 138

Results 139 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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The cpa mutant exhibits defects in lamina joint development 140

To study the molecular mechanism that controls leaf angle in wheat, we screened for 141

mutants with erect leaves from a wheat population mutagenized by fast neutron 142

radiation. We identified a mutant, named cpa for compact plant architecture, with a 143

smaller leaf angle and a more compact plant architecture compared to wheat cultivar 144

Liaochun10 (LC10) (Figure 1A). We measured the flag leaf angle between the midrib 145

of the flag leaf and the internode below the spike in the cpa mutant and LC10 and found 146

that the flag leaf angle was 11.50˚ and 28.23˚ in the cpa mutant and LC10, respectively 147

(Figure 1B and 1C). The smaller flag leaf angle of the cpa mutant is mainly caused by 148

abnormal development of the lamina joint (Figure 1D). In particular, the length of the 149

lamina joint of the flag leaf in the cpa mutant is 1.33 mm, while in LC10 it is 2.64 mm 150

(Figure 1E). Further morphological observation through scanning electron microscopy 151

showed that the lamina joint is much smaller in the cpa mutant than in LC10 due to a 152

decrease in cell number, while no changes in cell size were detected (Figure 1F and 153

1G). These results indicate that the cpa mutant exhibits defects in lamina joint 154

development. 155

156

Map-based cloning of mutated gene 157

A genetic linkage analysis of 450 F2 individuals derived from a cross between LC10 158

and the cpa mutant was performed. A total of 335 individual plants showed a large 159

lamina joint like LC10, while 115 plants showed a small lamina joint like the cpa 160

mutant. This result indicated that the lamina joint defect of the cpa mutant is caused by 161

a single recessive gene with a segregation ratio of ~3:1 (χ2 = 0.074 < χ2(0.05,1) = 3.84) of 162

the normal phenotype versus the mutant phenotype. We designated the dominant 163

wild-type gene as Compact plant architecture (TaCPA). 164

165

Following a map-based cloning approach using 450 F2 individuals, TaCPA was found 166

to co-segregate with markers 2D-235, 2D1377, LMC-3, and 2D-173 on chromosome 167 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



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2D (Figure 2A). By a larger segregation population consisting of 8352 individuals we 168

narrowed down the candidate region of TaCPA to ~19 Mb between LMC-3 and 2D-173 169

(Figure 2B and 2C). Generation of additional markers in this region allowed the 170

mapping of TaCPA as being completely linked to LMC-15, -18, -19, -23, -60, -71, and 171

-98 (Figure 2B and 2C). Near-isogenic lines (NILs) in the cpa genetic background 172

containing the LC10 allele (NILLC10) and NILs in the LC10 genetic background 173

containing the cpa allele (NILcpa) were generated through backcrossing of 174

heterozygous F1 plants to LC10 and the cpa mutant for three generations (BC3), 175

respectively (Supplemental Figure S1). The backcrossed line containing a 176

heterozygous fragment from markers LMC-3 and 2D-173 was selected. We found that 177

in NILLC10 plants, the flag leaf angle and lamina joint length is significantly increased 178

compared to the cpa mutant (Figure 2D), while these parameters are decreased in the 179

NILcpa plants compared to LC10 (Figure 2E). This confirmed that TaCPA is located in 180

the interval we have identified. 181

182

The region between markers LMC-3 and 2D-173 contains a total of 257 predicted genes 183

in the wheat Chinese Spring inbred line genome IWGSCv1(Appels et al., 2018). To 184

map TaCPA at a higher resolution, we performed bulked segregant RNA sequencing 185

(BSR-Seq), which makes use of the quantitative reads of RNA-Seq to efficiently map 186

genes (Liu et al., 2012). RNA samples were extracted from 30 homozygous F2-derived 187

F3 lines with normal or mutant phenotypes and from cpa and LC10 plants and were 188

combined into four separate pools used for RNA-Seq. Reads located in the region 189

between markers LMC-3 and 2D-173 were analyzed and the results indicated that 83 190

genes, distributed within this region, were expressed in both LC10 and homozygous 191

normal phenotype pools, but were absent in the cpa mutant and mutant phenotype 192

pools. These 83 genes could have been deleted in the cpa mutant by fast neutron 193

radiation. To test this hypothesis, 10 genes located within and 2 genes located outside 194

of the region (LMC-3 to 2D-173) were randomly selected and subjected to PCR 195 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



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amplification using genomic DNA of cpa and LC10 plants (Supplemental Figure S2A). 196

We found that all 10 genes within the LMC-3-2D-173 region are absent in the cpa 197

genome, while the 2 external genes are present (Supplemental Figure S2B). The 198

specificity of the primers used for the experiments was further assessed using Chinese 199

Spring null-tetrasomic lines. PCR products were not obtained in the lines with a 200

chromosome 2D deletion, but were present in the other null-tetrasomic lines 201

(Supplemental Figure S2B). These results indicate that the chromosome fragment 202

containing TaCPA is deleted in the cpa mutant. 203

204

TaSPL8, the homolog of LG1 in maize and rice, affects lamina joint development 205

and plant architecture in wheat. 206

Among the 83 genes deleted in the cpa mutant, one gene (TraesCS2D01G502900), 207

containing three exons and two introns, encodes a plant-specific SBP 208

domain-containing transcription factor, SPL, with a total protein length of 407 amino 209

acids. TraesCS2D01G502900 shows high amino acid similarity to OsLG1(SPL8) in 210

rice, ZmLG1 in maize, and SbLG1 in sorghum (Sorghum bicolor) (Figure 3A), which 211

are involved in controlling auricle, ligule, and lamina joint development (Moreno et al., 212

1997; Lee et al., 2007). Therefore, we renamed TaCPA as TaSPL8, a candidate gene for 213

lamina joint development in wheat. The expression of TaSPL8 in various wheat tissues 214

were detected by RT-qPCR, and we found that the TaSPL8 transcript is highly 215

expressed in the lamina joint and young spikes (Figure 3B). 216

217

Wheat is a hexaploid species that possesses three subgenomes originating from the 218

fusion of genomes from three diploid ancestral species (Triticum urartu, Aegilops 219

speltoides, and Aegilops tauschii) (El Baidouri et al., 2017). Accordingly, three 220

TaSPL8 homoeologs were identified from the wheat genome sequences database 221

(IWGSCv1, (Appels et al., 2018)) and designated TaSPL8-2A, TaSPL8-2B, and 222

TaSPL8-2D, respectively. To determine whether the loss of TaSPL8-2D is responsible 223 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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for the cpa mutant phenotype, we knocked out this gene using the clustered regularly 224

interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) 225

system. Due to the nucleotide similarity among TaSPL8-2A/2B/2D, single-guide RNA 226

(sgRNA) specifically targeting to TaSPL8-2D cannot be designed. Thus, a sgRNA 227

targeting a conserved region within the first exon of the TaSPL8-2A, TaSPL8-2B, and 228

TaSPL8-2D was designed and the CRISPR/Cas9 vector pBUE411::sgRNA was 229

introduced into LC10 (Figure 3C). A total of 10 independent transgenic T0 plants (KO 230

lines) were obtained and 3 lines with all three homoeologous genes mutated 231

simultaneously were selected for further analysis. Frameshift mutations in all three 232

subgenomes were also detected in the T1 offspring (Figure 3D). The KO-2-1 line was 233

backcrossed to LC10 to generate the TaSPL8-2A/2B/2d single mutant, which showed a 234

smaller lamina joint and flag leaf angle similar to the cpa mutant, compared with LC10 235

(Figure 3E and 3F). These results indicated that the loss of TaSPL8-2D is responsible 236

for the cpa mutant phenotype. 237

238

Three homoeologous genes of TaSPL8 differentially contribute to lamina joint 239

growth 240

One extraordinary feature of polyploid evolution is genomic asymmetry, which is the 241

predominant control of a variety of morphological, physiological, and molecular traits 242

by one subgenome over the others, which prompted us to determine the functional 243

divergence of TaSPL8 from 2A, 2B and 2D subgenomes (Wang et al., 2016). We firstly 244

compared the sequence similarity of open reading frames (ORFs) and protein 245

sequences of the three TaSPL8 homoeologous genes, and they showed 97.2% and 246

97.5% similarities for nucleotide and amino acid sequences, respectively. Primer 247

combinations located in the CDS region specific for each homoeolog were designed 248

and verified using the Chinese Spring null-tetrasomic lines of chromosome group 2. 249

We found that the PCR fragments could not be amplified when the corresponding 250

chromosome was deleted (Figure 4A). Using these primers, the transcript level of 251 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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TaSPL8-2D was observed to be higher than that of TaSPL8-2A and TaSPL8-2B in the 252

lamina joint (Figure 4B). 253

Possible divergence among these homoeologs in their contribution to the observed 254

phenotype was investigated by generating single, double, and triple mutants for each 255

homoeolog. As mentioned above, we firstly obtained the triple mutant 256

TaSPL8-2a/2b/2d by gene editing. The KO-2-1, KO-3-1, and KO-7-1 mutants with 257

three TaSPL8 homoeologs knocked out simultaneously showed erect leaves at both 258

vegetative and reproductive stages (Figure 4C and 4D), with a notable decrease in flag 259

leaf angle compared to the wild-type LC10 (Figure 4D). Additionally, the lamina joint 260

was severely affected and the boundary between the blade and sheath was absent in 261

these KO lines (Figure 4E and 4F). Similar phenotypes were also observed for the KO 262

lines in CB037 and Bobwhite recipients (Supplemental Figure S3). The triple mutant 263

KO-2-1 was crossed to wild-type LC10 to generate single and double mutants. 264

Compared to LC10, the TaSPL8-2a/2B/2D single mutant did not show differences in 265

lamina joint length, while the TaSPL8-2A/2b/2D and TaSPL8-2A/2B/2d single mutants 266

had a shorter lamina joint, with the major effect detected in TaSPL8-2A/2B/2d (Figure 267

4G and 4H). Accordingly, the double mutant TaSPL8-2a/2B/2d had a smaller lamina 268

joint length compared with the TaSPL8-2a/2b/2D double mutant, indicating that the 269

TaSPL8-2D homeolog provides the major contribution for the lamina joint length 270

phenotype (Figure 4G and 4H). Observations from double mutants also corroborated 271

the information from single mutants that TaSPL8-2B affects lamina joint length to a 272

greater extent than TaSPL8-2A (Figure 4G and 4H). These results indicated that the 273

homoeologous gene from the D subgenome contributed to lamina joint length to a 274

greater extent than those from the A and B subgenomes. 275

276

To evaluate the potential of manipulating TaSPL8 for optimizing wheat leaf 277

architecture and improving grain yield, we compared the yield-related traits of the 278

TaSPL8 mutant KO-2-1 and the wild-type LC10 in different planting populations of 279 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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300, 450, 600, and 750 seeds/m2 in two different locations (Beijing and Yangling). 280

Spike numbers per plant for the KO-2-1 line were higher compared to LC10, especially 281

at dense planting populations (450, 600, and 750 seeds/m2) (Figure 4I), which could 282

contribute to higher grain yield. Other traits, including plant height, spike length, grain 283

number per spike, grain weight, heading date (flowering time), and the grain-filling 284

period (time to maturity) did not differ between the KO-2-1 line and LC10 285

(Supplemental Table S1). 286

287

Natural variation of TaSPL8-2D 288

To determine the variation of TaSPL8-2D in a natural wheat population, 192 wheat 289

cultivars were screened for nucleotide polymorphisms. No single nucleotide 290

polymorphism was identified in the coding and promoter region, suggesting that the 291

TaSPL8-2D sequence is conserved because of its pivotal role in controlling lamina joint 292

development. The TaSPL8 expression level and lamina joint length was also assessed 293

in 78 wheat cultivars, including 29 cultivars with larger lamina joints (1.5-2.6 cm) and 294

49 cultivars with smaller lamina joints (0.8-1.5 cm) (Supplemental Table S2). The 295

results indicated that the TaSPL8 mRNA level in the lamina joint is higher in cultivars 296

with larger lamina joints compared to those with smaller lamina joints (Figure 4J). 297

These results further corroborated the role of TaSPL8 in lamina joint development. 298

299

TaSPL8 regulates lamina joint development through the auxin and 300

brassinosteroid pathways 301

To understand the mechanisms behind TaSPL8-mediated lamina joint regulation, we 302

performed a transcriptome analysis using RNA-seq in the lamina joint of main tiller 303

from TaSPL8-2a/2b/2d (two independent KO lines: KO-2-1 and KO-7-1) and 304

TaSPL8-2A/2B/2d (single KO line) mutants, as well as of LC10 wild-type plants at the 305

heading stage. For each sample, three biological replicates were employed. The 306

TaSPL8-2A/2B/2d mutant was included in the experiments because the triple 307 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by


https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5376651/#S1


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TaSPL8-2a/2b/2d mutant lacks the lamina joint and the cell type between the sheath 308

and blade are completely different with respect to LC10, while the single mutant 309

exhibits a phenotype more similar to the wild type, but with a noticeable decrease in 310

lamina joint length. The results indicated that 5980 genes are down-regulated and 2986 311

genes are up-regulated in the TaSPL8-2a/2b/2d mutants compared to LC10 (Figure 5A) 312

(Supplemental Table S3, Supplemental Table S4). Furthermore, a comparison between 313

the TaSPL8-2A/2B/2d single mutant and the wild type indicated that 1841 genes are 314

down-regulated and 1509 are up-regulated (p-values<0.05, |Fold Change|>2). Among 315

the differentially expressed genes (DEGs), 408 and 1310 genes are up-regulated and 316

down-regulated, respectively, in both the triple and single TaSPL8-2D mutant (Figure 317

5A). 318

319

Gene ontology (GO) functional annotation of the DEGs shared between the triple and 320

single TaSPL8 mutants revealed statistically significant enrichment in down-regulated 321

genes for pathways related to ‘response to auxin’, ‘metabolic process for carbohydrate’, 322

‘cellular glucan’, ‘xyloglucan’, ‘biosynthetic process for fatty acid’, ‘cellulose’ and 323

‘cell wall’ (Figure 5B). Among the up-regulated genes, we found an enrichment in 324

pathways associated with protein phosphorylation and photosynthesis (Figure 5B). For 325

cell component ontology, down-regulated genes were enriched in the extracellular 326

region and apoplast and cell wall, while up-regulated genes were enriched in 327

photosystems I and II (Figure 5C). These observations suggest TaSPL8 involvement in 328

cell wall development through the auxin pathway. 329

330

Among the DEGs in the single and triple TaSPL8 mutants, we found 188 331

down-regulated genes related to auxin signaling, including the auxin-responsive 332

Aux/IAA gene family (IAAs), auxin responsive factors (ARFs), auxin efflux carrier 333

components (PINs), small auxin-upregulated RNA (SAUR), and GH3 family 334

(Supplemental Table S3, Supplemental Table S4, Supplemental Figure S4). 335 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



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Measurement of the IAA content in the lamina joint region (tissue between the blade 336

and sheath) of LC10 and the TaSPL8-2a/2b/2d mutant indicated that the IAA content 337

was similar between the mutant and the wild type (Figure 5D), indicating that TaSPL8 338

does not affect IAA biogenesis but may act through auxin response signaling. 339

340

Another interesting category of DEGs that were down-regulated in the single and triple 341

TaSPL8 mutants include genes involved in cell division, cell elongation, and the 342

cytoskeleton (Supplemental Table S3, Supplemental Table S4, Supplemental Figure 343

S4). Downregulation of these genes may lead to failure of cell elongation and result in 344

the lamina joint defects observed in the mutants. These effect can be envisaged 345

especially for the 128 genes encoding glycosyl hydrolase (which function in primary 346

cell wall structure (Lópezbucio et al., 2002)), the 48 genes for expansins (which 347

regulate cell wall extension (Cosgrove, 2015)) and 7 genes for pectinacetylesterase 348

(which function in cell wall extensibility by enhancing aggregation processes between 349

galacturonan chains inside the apoplasm (Sénéchal et al., 2014)). 350

351

Finally, among the down-regulated DEGs, we found three genes with high similarity to 352

rice BRD1/OsDWARF/OsBR6ox, BRD2, and Cytochrome P450 90D2 (D2/CYP90D2), 353

which are implicated in BR biosynthesis processes (Supplemental Table S3, 354

Supplemental Table S4, Supplemental Figure S4). Moreover, 14 genes encoding 355

BRASSINOSTEROID INSENSITIVE 1 (BRI1)-associated proteins and 356

BRASSINAZOLE-RESISTANT 1 (BZR1) homolog proteins, which are responsive to the 357

BR signaling pathway, were also among the down-regulated DEGs (Supplemental 358

Table S3, Supplemental Table S4, Supplemental Figure S4). In agreement with these 359

observations, we found that the brassinolide and castasterone content in the 360

TaSPL8-2a/2b/2d mutant is reduced in comparison with LC10 (Figure 5E), indicating 361

that TaSPL8 affects BR biosynthesis and signaling pathways. All together, our findings 362



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indicate that TaSPL8 might regulate lamina joint development through BR and auxin 363

pathways, which are essential for both cell elongation and cell proliferation. 364

365

TaSPL8 acts as a transcriptional activator of TaARF6 and TaD2 366

Since maize LG1 is expressed in ligule and activates PIN1a expression as a 367

transcription activator (Johnston et al., 2014), we screened the down-regulated DEGs 368

identified in our transcriptome analysis for the presence of the 16-nt sequence 369

containing a GTAC core motif (Motif ID: MA0578.1) in their putative promoters, 370

which was previously identified as the cis-element of AtSPL8 targets in Arabidopsis 371

(Kropat et al., 2005). Among the 5980 down-regulated genes in the TaSPL8-2a/2b/2d 372

mutant, 1687 have this motif in their putative promoter sequence, as tested using FIMO 373

(http://meme-suite.org/tools/fimo). The ability of TaSPL8 to bind to the sequence 374

containing the GTAC core motif was assessed using electrophoretic mobility shift 375

assays (EMSAs). To this end, nine probes were synthesized from the promoters of three 376

auxin-responsive genes and four cell expansin genes. The results indicated that TaSPL8 377

can bind to these probes (Supplemental Figure S5). 378

379

Among the DEGs down-regulated in the TaSPL8 mutant, one gene 380

TraesCS5B01G039800 (TaARF6) is the putative ortholog of Arabidopsis thaliana 381

AtARF6 (Supplemental Figure S6). ARFs are key players in mediating auxin-induced 382

gene activation (Lau et al., 2008). In addition, we found that TraesCS5B01G039800 is 383

up-regulated in wild-type LC10 plants after exogenous auxin treatment, while it does 384

not respond to auxin in the KO-2-1 (TaSPL8-2a/2b/2d) mutant (Figure 6A). Therefore, 385

we investigated whether TaSPL8 acts in auxin signaling by directly activating the 386

expression of ARF genes. Similarly, we also tested whether TaSPL8 activates the 387

expression of genes involved in BR biosynthesis because TraesCS3A01G103800 388

(TaD2), the putative ortholog of rice D2, is strongly down-regulated in TaSPL8 389

mutants. Rice D2 encodes a cytochrome P450, which catalyzes the steps from 390 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



15

6-deoxoteasterone to 3-dehydro-6-deoxoteasterone and from teasterone to 391

3-dehydroteasterone in the late BR biosynthesis pathway. The results of our EMSAs 392

revealed that binding of a TaSPL8 recombinant protein to the putative promoters of 393

TaARF6 and TaD2 occurs in vitro (Figure 6B and 6C). 394

395

In order to determine if the direct binding also takes place in vivo, we first generated a 396

transgenic wheat line (ProUbi::TaSPL8-9MYC) overexpressing a TaSPL8 chimeric 397

protein fused to a Myc tag and then performed chromatin immunoprecipitation (ChIP) 398

assays with a Myc-specific antibody. We achieved three independent transgenic lines 399

(OE-5, OE-10, and OE-12) with high levels of TaSPL8 mRNA and TaSPL8-9Myc 400

protein (Figure 6D). Compared to the wild type of reference (CB037), the OE lines 401

were smaller and displayed fewer tiller numbers at the seedling stage, and decreased 402

spike length and grain size (Supplemental Figure S7). ChIP followed by quantitative 403

PCR (qPCR) was performed from the lamina joint tissue of the OE lines and wild-type 404

CB037. The results indicated that TaSPL8-MYC enrichment of the GTAC core motif 405

of TaARF6 and TaD2 in OE lines is significantly higher than that in wild-type CB037 406

and its enrichment in another region (outside GTAC core motif) is very low, suggesting 407

that TaSPL8 specifically binds to the promoter region of TaARF6 and TaD2 with the 408

GTAC core motif (Figure 6E). The effect of TaSPL8 binding to the TaARF6 and TaD2 409

promoter was investigated using a transient expression assay. Specifically, a plasmid 410

containing the promoter of TaARF6 (pTaARF6::LUC) or the TaD2 promoter 411

(pTaD2::LUC) driving the expression of the luciferase (LUC) reporter gene was 412

co-transformed in tobacco (Nicotiana tabacum) leaves with the effector plasmid 413

(35S::TaSPL8) expressing TaSPL8. The results indicated that TaSPL8 can activate the 414

expression of the reporter for both promoters (Figure 6F). Overall, these findings 415

indicate that TaSPL8 directly binds to the promoter of TaARF6 and TaD2 in the region 416

containing the GTAC motif, which is also associated with their transcriptional 417

activation. Therefore, we can envisage that one of the mechanisms underlying 418 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



16

TaSPL8-mediated regulation of lamina joint development involves the direct activation 419

of key genes of auxin signaling and BR biogenesis. 420

Discussion 421

TaSPL8 and its homolog LG1 in maize and rice could be a robust target for plant 422

architecture improvement in grass 423

Erect leaves improve light interception and biomass production under field conditions, 424

resulting in increased grain yield in grass crops (Sakamoto et al., 2006). The erect-leaf 425

phenotype of a rice BR-deficient mutant, osdwarf4-1, is associated with enhanced grain 426

yields under dense planting populations, even without extra fertilizer (Sakamoto et al., 427

2006). Therefore, it can be assumed that a compact plant architecture mediated by erect 428

leaves is also an important goal for wheat breeding, but no potential target genes for 429

breeding programs have been identified to date in wheat. This study provides 430

information about the role and mechanisms of TaSPL8, which encodes an SPL-like 431

transcription factor, in controlling leaf angle by regulating lamina joint development. 432

Lamina joint formation is impaired in TaSPL8 knock-out mutants, resulting in erect 433

leaves and a more compact architecture. Our findings suggest that TaSPL8 is an 434

important regulator of compact architecture in wheat, and therefore, could be used as a 435

target to achieve elite wheat cultivars with erect leaves through genetic engineering and 436

molecular breeding. 437

438

TaSPL8 plays a similar function in lamina joint development as LG1 in maize and rice. 439

The mutation of LG1 in maize and rice also resulted in an erect leaf phenotype with a 440

complete loss of the auricle and ligule (Moreno et al., 1997; Lee et al., 2007). Although 441

the contribution of maize and rice LG1 to potential yield in high density planting is still 442

unknown, we speculated that this gene might be a robust target for compact plant 443

architecture in grass, considering the highly conserved function in lamina joint 444

development. However, we have to consider the functional variation among LG1 genes 445 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


17

of maize, rice, and wheat. Beside affecting ligule development, OsLG1 regulates 446

panicle closure or spreading by controlling cell proliferation at the panicle pulvinus 447

(Ishii et al., 2013; Zhu et al., 2013). ZmLG1 also controls the branch angle of the tassel 448

and its knockout mutants result in a more compact tassel than their wild-type 449

counterparts (Bai et al., 2012). Different from OsLG1 and ZmLG1, TaSPL8 does not 450

affect the spike structure, while directly or indirectly leading to the alteration of spike 451

numbers. TaSPL8 mutants show increased spike numbers especially under dense 452

planting condition. This phenotype may be due to erect leaves that allow greater 453

penetration of light to the lower leaves, thereby improving canopy photosynthesis, 454

which in turn, improves the formation of tillers or the ability to generate a spike. A 455

similar phenotype was observed in the osdwarf4-1 rice mutant with erect leaves due to 456

BR deficiency (Sakamoto et al., 2006). Alternatively, TaSPL8 may directly regulate 457

tiller and spike formation. TaSPL8 is highly expressed both in the lamina joint and 458

young spikes and overexpressing plants show a clear reduction in tiller number and 459

spike size. However, an overexpression transgenic line driven by the Ubi promoter 460

actually shows an ectopic effect from the early growth stage. Ubiquitous 461

overexpression may affect the natural function of a gene/protein, for example by 462

altering transcription factor binding specificity when binding is sensitive to doses, or by 463

altering the stoichiometric composition of a multiprotein complex, thus affecting its 464

possible activity and specificity. Therefore, ubiquitous overexpression mutants are not 465

the best for judging a gene’s function, because pleiotropic and “artificial” effects are 466

more likely to be observed. The specific upregulation of TaSPL8 in spikes or tillers will 467

help us to understand its biological function. 468

469

A wild species can be changed to a new form to meet human needs through crop 470

domestication. OsLG1 has experienced substantial artificial selection during rice 471

domestication (Ishii et al., 2013; Zhu et al., 2013). The selection of an SNP residing in 472

the cis-regulatory region of the OsLG1 gene was responsible for the transition from a 473 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



18

spread panicle typical of ancestral wild rice to the compact panicle of present cultivars 474

during rice domestication (Zhu et al., 2013). This selection led to the reduced 475

expression of OsLG1 specifically at the panicle pulvinus while maintaining normal 476

levels during ligule formation (Zhu et al., 2013). In wheat, we found that the level of 477

TaSPL8 mRNA in the lamina joint is higher in modern cultivars with larger lamina 478

joints (n=49) compared to those with smaller lamina joints (n=29) (Figure 4J), 479

indicating that TaSPL8 is also selected for leaf angle during wheat breeding. However, 480

we did not find sequence variation in the cis-regulatory region of TaSPL8 among these 481

cultivars. Hence, genetic variation in possible distal regulatory elements or epigenetic 482

variation in the TaSPL8 promoter may account for the observed difference in the 483

transcript level. 484

485

TaSPL8-2D is a major contributor to erect leaf in wheat 486

Common wheat is an allohexaploid (BBAADD) derived from a hybridization between 487

a cultivated form of allotetraploid wheat Triticum turgidum (BBAA) and diploid goat 488

grass Aegilops tauschii (DD). Triticum turgidum originates from the hybridization and 489

polyploidization of the diploid species Triticum urartu (AA) and Aegilops speltoides 490

(SS genomes, most probably the donor of the B genome). The combination and 491

interaction of subgenomes in the allohexaploid give rise to phenotypic variation during 492

wheat evolutionary history. The evolution of duplicated gene loci in allopolyploid 493

plants contribute either to a favorable effect of extra gene dosage or to build-up 494

asymmetric expression divergence: only one genome is active, while the homoeoalleles 495

on the other genome(s) are either eliminated or partially or completely suppressed by 496

genetic or epigenetic means (Feldman et al., 2012). However, there is no evidence 497

showing how asymmetric expression divergence affects the trait. We found that the 498

expression level of homoeoallele TaSPL8-2D was higher in the lamina joint compared 499

to the expression level of TaSPL8-2A and TaSPL8-2B. Observations from single, 500

double, and triple mutants also corroborated the information that the TaSPL8-2D 501 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



19

homeolog provides the major contribution for the lamina joint length phenotype and 502

TaSPL8-2B affects lamina joint length to a greater extent than TaSPL8-2A. These data 503

expand our knowledge about genome asymmetry during allopolyploid wheat evolution 504

and suggest a possible mechanism and evolutionary advantage of this divergence, but 505

addressing this requires further work. 506

507

The utilization of TaSPL8 for compact plant architecture in wheat breeding 508

Simultaneous mutations of all three TaSPL8 homeologs leads to the absence of the 509

lamina joint, sometimes resulting in flag leaves wrapping around the spikes, which 510

blocks spike extension. Thus, potential routes for TaSPL8 utilization in wheat breeding 511

include: 1) using a single mutation of TaCAP-2D or TaCAP-2B to obtain a shorter 512

lamina joint without affecting spike extension, and 2) using alleles associated with 513

lower expression of TaSPL8 and shorter lamina joints, which could be used in 514

marker-assisted selection to fine-tune lamina joint length and leaf angle. 515

516

TaSPL8 modulates leaf angle through auxin and brassinosteroid signaling 517

LG1 orthologs in maize, rice, and wheat function as key regulators of lamina joint 518

development. ZmLG1 was found to function downstream of maize WAB, a TCP 519

transcription factor (Lewis et al., 2014) and to regulate a series of downstream genes 520

including PIN1a, BEL14, and BEL12, which were identified by comparing transcript 521

accumulation between an lg1 mutant and wild type in the preligule region (Johnston et 522

al., 2014). Our study provides evidence that TaSPL8 affects lamina joint development 523

by directly activating the expression of genes involved in auxin and BR pathways. 524

Previous findings indicated that these hormones and various transcription factors 525

contribute to cell division and elongation at the lamina joint region (Sakamoto et al., 526

2006; Bian et al., 2012; Zhao et al., 2013). Here, we have identified the mechanistic link 527

between one transcription factor and the auxin and BR pathways, which are involved in 528

lamina joint development and leaf architecture. Specifically, we found that TaSPL8 529 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



20

directly binds and activates TaARF6, which is involved in the auxin signaling pathway, 530

and TaD2, which regulates BR biosynthesis (Figure 7). Auxin is essential for cell 531

elongation in nearly all developmental processes. The two Arabidopsis TaARF6 532

orthologs, ARF6 and ARF8, are required for cell elongation in the inflorescence stem, 533

stamen filament, stigmatic papillae, and hypocotyls, and in anther dehiscence (Nagpal 534

et al., 2005; Oh et al., 2014; Liu et al., 2018a). TaARF6 may similarly act as a regulator 535

of cell elongation in the lamina joint. This scenario is supported by findings that other 536

members of the ARF gene family regulate leaf angle. OsARF19-overexpressing rice 537

lines show multiple phenotypes, including increased leaf angles (Zhang et al., 2015), 538

and an OsARF11 loss-of-function line exhibits a reduced angle of the flag leaves 539

(Sakamoto et al., 2013). Similarly, rice mutants with impaired expression of d2, the 540

ortholog of wheat TaD2, are deficient in BR biogenesis and have erect leaves (Hong et 541

al., 2003). This strongly supports our findings that another form of TaSPL8-mediated 542

regulation of lamina joint development occurs through transcriptional activation of 543

TaD2 and the subsequent increase in BR biosynthesis. Although rice BR-deficient 544

mutants are usually dwarfed with short internodes, TaSPL8 mutants do not exhibit 545

other phenotypic alterations except for lamina joint development. We speculate that 546

high expression of TaSPL8 in lamina joint tissue specifically regulates BR biogenesis 547

in this region. Our results indicate that TaSPL8 also affects the expression of genes 548

involved in cell elongation and expansion. For example, we found that 48 genes for 549

expansins are down-regulated in the TaSPL8-2a/2b/2d mutant, and TaSPL8 can bind to 550

the GTAC motif of the promoters of four cell expansin genes in vitro (Supplemental 551

Figure S5). This suggests that TaSPL8 regulates lamina joint development by directly 552

targeting expansin genes. An alternative and not mutually exclusive possibility is that 553

TaSPL8 regulates expansin genes through auxin signaling, since cell elongation genes 554

are also responsive to auxin (Pacheco-Villalobos et al., 2016). 555

556



21

In conclusion, this study reveals the mechanisms that link one member of the SPL 557

transcription factor family with hormones in regulating lamina joint development, in 558

that TaSPL8 acts upstream of genes involved in the regulation of lamina joint cell 559

elongation, such as TaARF6 and TaD2, which mediate the auxin signaling pathway and 560

BR biosynthesis, respectively. In addition, our results identify additional genes that 561

may function in lamina joint development (e.g., expansin). These findings will be 562

useful for programs aimed at manipulating wheat architecture for improved grain yield. 563

Methods 564

Plant materials 565

Names and geographical origins of all wheat (Triticum aestivum) cultivars used in this 566

study are listed in Supplemental Table S2. Plant materials used for visible phenotypic, 567

microscopic, and molecular analyses were grown in a greenhouse at a relative humidity 568

of 75% and 26/20°C day/night temperatures, with a light intensity of 3000 lux (Master 569

GreenPower CG T 400W E40, PHILIPS). Wheat cultivars used for seed reproduction 570

and phenotypic analysis were grown in the experimental field of China Agricultural 571

University in Beijing (39°57ʹN, 116°17ʹE), Yangling in the Shannxi province (34°16'N, 572

108°04'E). Lamina joints for gene expression analysis were harvested at the heading 573

stage. For each sample, the lamina joint from three different planting pots was 574

harvested, representing three biological replicates. All samples were immediately 575

frozen in liquid nitrogen and stored at -80°C. The natural wheat population consisted of 576

192 wheat cultivars including Chinese landraces (111), Chinese modern cultivars (42), 577

and foreign cultivars from other countries in Europe, Asia, America, and Australia (39). 578

579

Phenotypic analysis 580

The length of the lamina joint and auricle were measured as the widest section between 581

the leaf blade and the sheath with a Vernier caliper. Flag leaf angle was measured using 582

a protractor between the stem under the spike and the flag leaf midrib. Plant height and 583 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


22

the length of the main spike were measured before harvesting, and ten main spikes were 584

bagged at the same time to measure fertile grain number per spike and grain weight per 585

1000 grains. Spike number per plant was calculated as the average value of ten plants. 586

A randomized complete block design with three replicates was employed for 587

phenotyping in open field experiments. 588

589

Mapping of TaSPL8 590

Fine mapping was performed with an F2 and F2-derived F3 population from a cross 591

between cpa and LC10. Primers used for fine mapping were designed based on the 592

sequence of Chinese Spring (IWGSCv1, http://www.wheatgenome.org/) and Aegilops 593

tauschii (Luo et al., 2017) and listed in Supplemental Table S5. Near-isogenic lines 594

(NILs) in the cpa genetic background containing the LC10 allele (NILLC10) and NILs in 595

the LC10 genetic background containing the cpa allele (NILcpa) were generated through 596

backcrossing LC10×cpa F1 plants to LC10 and the cpa mutant for three generations 597

(BC3), respectively. The introgression fragment between markers 2D-173 and LMC-3 598

was screened at each generation. The BC3F1 plant was self-crossed to generate NILLC10 599

and NILcpa, respectively. 600

601

Plasmid construction and transformation 602

For genome editing via CRISPR/Cas9, a small guide RNA (sgRNA) was designed in 603

the first exon sequence of TaSPL8 using the E-CRISP Design website 604

(http://www.e-crisp.org/E-CRISP/designcrispr.html). Two reverse complementary 605

sgRNA sequences with the BsaI cohesive ends were synthesized. Double-stranded 606

oligonucleotides were annealed by cooling from 100°C to room temperature, followed 607

by insertion into the expression cassette of the pBUE411 vector (Xing et al., 2014). 608

Plasmids were transformed into three wheat cultivars (CB037, LC10, and Bobwhite) 609

using Agrobacterium-mediated (strain EHA105) transformation (Ishida et al., 2015). 610

For TaSPL8 overexpression, the ORF of TaSPL8-2D from CB037 and the 9 Myc 611 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by


http://www.e-crisp.org/E-CRISP/designcrispr.html


23

domain sequence were amplified and linked by PCR, then the TaSPL8-9Myc fragment 612

was inserted into the pMWB122 vector (Wang et al., 2017) using SmaI and SpeI 613

cloning sites to achieve the ProUbi::TaSPL8-9Myc construct. Plasmids were 614

transformed into the wheat cultivar CB037 using Agrobacterium-mediated (strain 615

EHA105) transformation (Ishida et al., 2015). 616

617

RT-qPCR analysis 618

Total RNA was extracted from different tissues using TRIzol reagent (Takara) 619

according to the manufacturer's instructions and cDNA was synthesized by a reverse 620

transcription kit (Vazyme Biotech, China). Wheat TaACTIN (TraesCS5B01G124100) 621

was used as an internal control. For reverse transcription quantitative PCR (RT-qPCR), 622

the reaction mixture was composed of the cDNA first-strand template, primers, and 623

SYBR Green Mix (Takara) to a final volume of 10 μl. Reactions were performed using 624

the CFX96 real-time system (Bio-Rad). For technical replicates, the RT-qPCR for each 625

sample was replicated three times. Three biological replicates were performed (one 626

replication is shown). The average values of 2-ΔCT were used to determine the 627

differences in gene expression (Applied Biosystems Research Bulletin No. 2 P/N 628

4303859). 629

630

ChIP-qPCR assay 631

Wheat leaves were cross-linked in fixative buffer (1% volume/volume(v/v) 632

formaldehyde) by vacuum infiltration. Cross-linking reactions were stopped by adding 633

glycine at a final concentration of 0.17 M. Chromatin extracts were sonicated and 634

pre-cleared with Dynabeads protein A agarose (Merck Milipore, Germany) for 1 h. For 635

immunoprecipitation, anti-Myc antibody (Abcam, ab9132) was added and samples 636

were incubated at 4°C overnight. The chromatin-antibody complex was recovered with 637

Dynabeads protein A+G and beads were washed sequentially with low salt wash buffer, 638

high salt wash buffer, LiCl wash buffer, and TE buffer for 5 min each (Yang et al., 639 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



24

2016). The protein/DNA complex was eluted with elution buffer (1% weight/volume 640

(w/v) SDS and 0.1 M NaHCO3). Cross-linking was reversed by adding NaCl at a final 641

concentration of 200 mM, followed by incubation for 5 h at 65°C. Proteins in the 642

resulting complex were removed by proteinase K at 45°C for 1 h. DNA was 643

precipitated in the presence of three volumes of ethanol and one-tenth volume of 3 M 644

sodium acetate at pH 5.2. Precipitated DNA was dissolved in 30 μL 10 mM Tris-HCl, 645

pH 7.5, and treated with RNase (DNase-free). Two independent ChIP assays were 646

performed for each sample. Quantitative PCR (qPCR) was carried out using the CFX96 647

real-time system (Bio-Rad). ChIP values were normalized to their respective DNA 648

input values, and the fold changes in concentration were calculated based on the 649

relative enrichment in the overexpression lines compared with wild-type 650

immunoprecipitates. Primer sequences used in the qPCR analysis are listed in 651

Supplemental Table S5. 652

653

Transient expression in tobacco leaves 654

Dual luciferase reporter assays were performed as previously described (Guan and Zhu, 655

2014). A fragment corresponding to 1800 bp upstream of the transcription start site of 656

TaARF6 was PCR amplified from LC10 genomic DNA and cloned into the pGreenII 657

0800-LUC vector (Hellens et al., 2005), generating the reporter pGreenII 658

pTaARF::LUC and pTaD2::LUC plasmids. The ORF of TaSPL8 was cloned into the 659

pUC18-35S vector generating the effector 35S::TaSPL8 plasmid. Young leaves of 660

4-week-old tobacco (Nicotiana tabacum) plants were co-infiltrated with 661

Agrobacterium (strain GV3101) harboring the desired plasmids in the following 662

combination: pTaARF6::LUC + pUC18-35S (empty vector), pTaARF6::LUC + 663

35S::TaSPL8, pTaD2::LUC + pUC18-35S (empty vector), and pTaD2::LUC + 664

35S::TaSPL8. The activities of firefly luciferase under the control of the TaARF6 665

(pTaARF6::LUC) or TaD2 (pTaD2::LUC) promoter and Renilla luciferase under the 666

control of the 35S promoter (35S::REN) were quantified using the Dual-Luciferase 667 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



25

Reporter Assay system (Promega) with the Synergy 2 Multi-Detection Microplate 668

Reader (BioTek Instruments). Normalized data are presented as the ratio of 669

luminescent signal intensity for the pTaARF6::LUC or pTaD2::LUC reporter and 670

luminescent signal intensity for the internal control reporter 35S::REN from three 671

independent biological samples. 672

673

Western blot 674

Harvested leaves were ground in liquid nitrogen and proteins were extracted with 4× 675

loading buffer (200 mM Tris-HCl, pH 6.8, 40% v/v glycerol, 8% w/v SDS, and 20% 676

v/v β-mercaptoethanol) at 100°C for 5 min. The solution was placed on ice for 5 min 677

and centrifuged for 10 min at 12,000 x g at room temperature. Protein extracts were 678

separated on 10% sodium dodecyl sulfate–polyacrylamide gel electrophoresis 679

(SDS-PAGE) and transferred to a PVDF membrane (Bio-Rad 162-0177) for 60 min at 680

300 mA in temperature-controlled conditions. The membrane was blocked using 5% 681

(w/v) defatted milk for 1 h. The membrane and primary antibody (1:1000), dissolved in 682

5% (w/v) defatted milk and 1×TBST (1×TBS with 0.1% v/v Tween 20), were 683

incubated at 4°C overnight. After washing three times for 10 min with 1×TBST, the 684

secondary antibody (1:3000) was added in 5% (w/v) defatted milk-1×TBST solution 685

and incubated for 1 h at room temperature, followed by three washing steps of 10 min 686

with 1×TBST. Two-component reagent Clarity Western ECL Substrate (Bio-Rad 687

170-5060) was used for detection. The signal was detected with x-ray film. 688

689

RNA-seq 690

Total RNA was isolated as reported above. Lamina joint from TaSPL8-2A/2B/2d 691

mutant and LC10, and the corresponding part between the leaf blade and sheath from 692

the TaSPL8-2a/2b/2d mutant at the heading stage were collected. Three replicates of 10 693

plants each were used for each tissue type. Barcoded cDNA libraries were constructed 694

using Illumina Poly-A Purification TruSeq library reagents and sequenced on Illumina 695 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



26

HiSeq 2500 or NovaSeq platforms. About 10 Gb of high-quality 125-bp or 150-bp 696

paired-end reads were generated from each library. The overall sequencing quality of 697

the reads in each sample was evaluated by FastQC (v0.11.5) software 698

(http://www.bioinformatics.babraham.ac.uk). Poor-quality bases were removed using 699

Trimmomatic (v0.36) (Bolger et al., 2014) in its paired end model with parameters: 700

LEADING:3 TRAILING:3 HEADCROP:6 SLIDINGWINDOW:4:15 MINLEN:40. 701

The remaining reads were aligned to the wheat reference genome sequence IWGSCv1 702

(http://www.wheatgenome.org/) using Tohat2 v2.11 with the parameters “--b2-D 20 703

--b2-R 3 -N 3 --read-edit-dist 3”(Kim et al., 2013), and only the uniquely mapped reads 704

were retained for the following analysis. FeatureCounts (v1.5.2) with the parameters 705

“--readExtension5 70 --readExtension3 70 –p –C –s 0” was used to estimate the number 706

of reads mapped to respective high-confidence genes annotated from IWGSCv1 in each 707

sample. Bioconductor package "DESeq2" (Love et al., 2014) was used to perform 708

differential expression analysis between TaSPL8 mutant lines and the wild type, and 709

only the genes with an absolute value of log2 (fold change) ≥ 1 and p-value < 0.05 were 710

considered as DEGs. 711

712

For GO analysis, cDNAs of high-confidence genes were aligned to the protein 713

sequences of Oryza sativa and Arabidopsis using BLASTX with an e-value cut-off of 714

1e-05. Only the best alignment with identity ≥ 50% and aligned length ≥ 30 aa were 715

considered. GO annotations were obtained based on the orthologs with the priority: O. 716

sativa > A. thaliana. GO enrichment analysis of DEGs was implemented using the 717

GOseq R package, which is based on the Wallenius non-central hypergeometric 718

distribution and can adjust for gene length bias (Young et al., 2010). GO terms with 719

FDR < 0.01 were considered as statistically significantly enriched. 720

721

Electrophoretic mobility shift assay (EMSA) 722



27

The full-length ORF sequence of TaSPL8 was cloned into the BamHI site of the 723

pGEX6P-1 vector to produce the chimeric GST-TaSPL8 protein (primer sequences are 724

listed in Supplemental Table S5). Expression of recombinant protein in Transetta 725

(DE3) E. coli (TransGen, Beijing) was induced with 0.1 mM 726

isopropyl-b-D-thiogalactopyranoside (IPTG) in Luria Bertani (LB) buffer overnight at 727

16°C. Cells were subsequently harvested, washed, and suspended in 30 mL of 728

phosphate-buffered saline (PBS: 137 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, and 2 729

mM KH2PO4) containing 1 mM PMSF and 1/2 a tablet of protease inhibitor cocktail 730

(Roche, Germany). Then, cells were sonicated for 30 min and centrifuged at 13,000 x g 731

for 45 min at 4°C. The supernatant was filtered through a 0.22-μm membrane into a 732

50-mL tube. The supernatant was mixed with 1 mL of GST MAG Agarose Beads 733

(Novagen, USA) and shaken overnight at 4°C. GST beads were washed four times with 734

5 mL PBS and the recombinant proteins were eluted by incubation at 4°C for more than 735

4 hours with 50 mM Tris-HCl (pH 8.0) supplemented with 10 mM reduced glutathione. 736

Protein concentration was determined using a Nano Drop 2000 spectrophotometer 737

(ThermoScientific, USA). 738

The biotin-probe was 5' end labeled with biotin. Double-stranded oligonucleotides used 739

in the assays were annealed by cooling from 100°C to room temperature in annealing 740

buffer (Guo et al., 2018). DNA-binding reactions were performed in 20 μL with 741

1×binding buffer (100 mM Tris, 500 mM KCl, and 10 mM DTT; pH 7.5), 10% (v/v) 742

glycerol, 0.5 mM EDTA, 10 mM ZnCl2, and 50 ng μL-1 poly (dI-dC). Competition 743

analysis was done by adding 5- and 10- fold molar excess of the unlabeled DNA 744

fragment (same sequence used for the labeled probe) to the binding reaction, 5 min 745

prior to the labeled probe. After incubation at room temperature for 30 min, samples 746

were loaded onto a 6% native polyacrylamide gel. Electrophoretic transfer to a nylon 747

membrane and detection of the biotin-labeled DNA was performed with the Light Shift 748

Chemiluminescent EMSA Kit (ThermoScientific, USA) according to the 749

manufacturer’s instructions. 750 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



28

751

Quantification of Endogenous IAA and BR 752

The lamina joint of the wild type and the TaSPL8-2a/2b/2d line were harvested at the 753

heading stage. Quantification of endogenous IAA and BR were performed as 754

previously described (Chen et al., 2012; Ding et al., 2013). Each experiment was 755

performed using three replicates. 756

757

Statistical Analysis 758

The statistical analyses, including Student’s t-test and correlation, were performed by 759

SPSS software version 21 (SPSS Inc./IBM Corp., Chicago, IL, United States). All 760

barcharts and boxplot results were graphically presented using Graph Pad Prism 761

software (version 6.0, San Diego, CA, United States). 762

763

Phylogenetic Analysis 764

For phylogenetic analysis, related protein sequences to TaARF6 and TaD2 in 765

Arabidopsis and rice were selected by employing NCBI BLASTp search using nr (non- 766

redundant protein sequences) database. Their corresponding accession numbers were 767

shown in Supplemental Figure S6. The phylogenetic tree was generated by neighbor 768

joining tree method in MEGA5 software. 769

770

Primers for RT-qPCR and vector construction 771

All primers used in this research are listed in Supplemental Table S5. 772

773

Accession Numbers 774

Accession code: the genomic DNA sequence of TaSPL8 in LC10 has been deposited in 775

GenBank with the accession number MH765574. AUXIN RESPONSE FACTOR 776

TaARF6 gene: TraesCS5B01G039800.1; CYP90D2 TaD2 gene: 777

TraesCS3A01G103800. 778 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



29

779

RNA sequencing data are available at the National Center for Biotechnology 780

Information Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under the 781

accession number SRP157960. 782

783

Supplemental Data 784

Supplemental Figure S1. Schematic of genotype of LC10, cpa, NILLC10, and NILcpa. 785

Supplemental Figure S2. A Fragment on Chromosome 2D was Deleted in the cpa 786

Mutant. 787

Supplemental Figure S3. CRISPR/Cas9 Knock-out TaSPL8 Mutants in CB037 and 788

Bobwhite Cultivars. 789

Supplemental Figure S4 Heat Map for the DEGs Involved in Auxin and BR Signaling 790

and Cell Elongation in the Wild Type and TaSPL8 Mutants. 791

Supplemental Figure S5 TaSPL8 in vitro Binding of Sequences Containing the 792

GTAC Motif. 793

Supplemental Figure S6 Phylogenetic Tree of TraesCS5B01G039800.1 (TaARF6) 794

and TraesCS3A01G103800.1 (TaD2) with Arabidopsis or Rice Proteins. 795

Supplemental Figure S7 The Phenotypes of TaSPL8-Myc Overexpression (OE) and 796

Wild-type CB037 Lines. 797

Supplemental Table S1 Morphological Characterization of Wild Type and KO-2-1 798

(TaSPL8-2a/2b/2d) Mutant Plants. 799

Supplemental Table S2. The names and geographical origins of all wheat cultivars 800

used in this research. 801

Supplemental Table S3. Differentially expressed transcripts in the Taspl8-2a/2b/2d 802

mutant and the wild type in lamina joint tissue. 803

804

Supplemental Table S4. Differentially expressed transcripts in the Taspl8-2A/2B/2d 805

mutant and the wild type in lamina joint tissue. 806 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by


http://www/






30

Supplemental Table S5. Primers and Gene IDs for sequences used in this study. 807

808

809

Data availability 810

The authors declare that all data supporting the findings of this study are available 811

within the manuscript and its Supplemental files or are available from the 812

corresponding authors upon request. 813

814

815

Acknowledgments 816

We thank Dr. Qijun Chen (China Agricultural University), Dr. Rentao Song (China 817

Agricultural University), and Dr. Xingguo Ye (Chinese Academy of Agricultural 818

Sciences) for providing the CRISPR-Cas9 vector (pBUE11), the transient expression 819

vectors (pUC18-35S and pGreenII 0800-LUC) and the overexpression vector 820

(pMWB122), respectively. We thank Prof. Mingcheng Luo (University of California, 821

Davis, USA) for providing the Aegilops tauschii genome sequence. We thank Prof. 822

Guihua Bai (Kansas State University, USA) for critical reading of the manuscript. We 823

thank Dr. Yuqi Feng (Wuhan University) for assistance in IAA and BR quantification 824

and Dr. Hongxia Li and Dr. Yu Wang (Northwest A&F University) for help in 825

phenotypic measurements of yield-related traits. We also thank the International Wheat 826

Genome Sequencing Consortium (IWGSC) for providing the wheat reference 827

sequence. This work was supported by the National Key Research and Development 828

Program of China (2016YFD0100801, 2016YFD0101004). 829

830

831

Figure Legends 832

Figure 1. Morphological Comparison of the Wheat Cultivar Liaochun10 (LC10) and 833

the cpa Mutant. 834 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



31

(A) Morphologies of LC10 and cpa plants at the heading stage. Bar = 2 cm. 835

(B) Morphologies of the flag leaf in LC10 and cpa plants at the flowering stage. Bar = 2 836

cm. 837

(C) Flag leaf angle of LC10 and cpa plants at the flowering stage. The double asterisk 838

represents significant differences determined by the two-tailed Student’s t-test at P < 839

0.01. Error bars indicate the Standard Deviation (n=10). 840

(D The lamina joint phenotype of LC10 and cpa plants. Bar = 2 cm. 841

(E) Lamina joint length of LC10 and cpa plants. The double asterisk represents 842

significant differences determined by two-tailed Student’s t-test at P < 0.01. Error bars 843

indicate the Standard Deviation (n=10). 844

(F) Morphology of the adaxial surface by a scanning electron microscope of the lamina 845

joint of the LC10 and cpa flag leaf. Image magnification of the red box in the left part 846

(Bar= 200 μm) is shown on the right (Bar = 60 μm). 847

(G) Quantitative cell number and cell size of lamina joint from LC10 and cpa flag leaf. 848

The cell number from the bottom to the top of the lamina joint was counted manually 849

(n=10) and cells size measured by IMAGEJ (n=15). The double asterisk represents 850

significant differences determined by two-tailed Student’s t-test at P < 0.01. Error bars 851

indicate the Standard Deviation. NS: Not Significant. 852

853

Figure 2. Fine Mapping of the TaCPA Locus and Complementation Test Using 854

Near-Isogenic Lines (NILs). 855

(A) Coarse linkage map of TaCPA on chromosome 2D. Numbers indicate the genetic 856

distance between the adjacent markers. Thick black line indicates partial region of 2D 857

chromosome. 858

(B) High-resolution linkage map of TaCPA. The number of recombinants (labeled as r) 859

between the molecular markers and TaCPA is indicated. Thick black line indicates 860

partial region of 2D chromosome. 861



32

(C) Fine mapping of TaCPA. Genotypes and phenotypes of recombinants of five F2 862

plants including (F2-820, F2-1990, F2-4153, F2-5088, and F2-7243) are reported. The 863

name and phenotype of F2 individual plants were labeled in the left and right parts, 864

respectively. Black and white blocks indicate genomic region from LC10 and cpa, 865

respectively. Gray block indicates the heterozygous region. 866

(D-E) Phenotype of the flag leaf angle and lamina joint in cpa and NILLC10 (D) and 867

NILcpa (E) plants. Bar = 1 cm. Single and double asterisks represent statistically 868

significant differences determined by the two-tailed Student’s t-test at P < 0.05 and P < 869

0.01, respectively. Error bars indicate the Standard Deviation (n=10). 870

871

Figure 3. Cloning and Characterization of TaSPL8 and the phenotype of its knockout 872

lines by the CRISPR/Cas9 System. 873

(A) Amino acid sequence alignment of TaSPL8 and its orthologs in rice 874

(Os04g0656500), maize (Zm00001d002005), and sorghum (SORBI_3006G247700). 875

The conserved SBP domain is indicated by a red line. 876

(B) Expression pattern of TaSPL8 in various tissues. The expression levels were 877

normalized to wheat TaACTIN. Each bar in the graph corresponds to the mean value of 878

three data points, which are shown by dots. 879

(C) Sequence of an sgRNA designed to target a conserved region of exon 1 among the 880

three TaSPL8 homoeologs. The protospacer-adjacent motif (PAM) sequence is 881

highlighted in red. 882

(D) The genotypes of three mutant lines were identified by sequencing. "+" and "−" 883

indicate the insertion or deletion caused by CRISPR/Cas9-induced mutations, 884

respectively. Numbers indicate the length of the insertion or deletion. 885

(E) Flag leaf phenotypes of mutant Taspl8-2A/2B/2d, cpa and LC10. Bar=1 cm. 886

(F) Flag leaf angle and lamina joint length of Taspl8-2A/2B/2d, cpa and LC10 plants. 887

The double asterisk represents significant differences determined by two-tailed 888

Student’s t-test at P < 0.01. Error bars indicate the Standard Deviation (n=10). 889 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



33

890

Figure 4. Three homoeologous genes of TaSPL8 differentially contribute to lamina 891

joint growth. 892

(A) The specificity of primers for three TaSPL8 homoeologous genes were verified by 893

amplifying the genomic DNA of the wheat cultivar Chinese Spring null-tetrasomic 894

lines of chromosome group 2, where N2DT2B represents nullisomic2D-tetrasomic2B, 895

for example. 896

(B) Relative abundance of three homoeologous genes, TaSPL8-2A, TaSPL8-2B, and 897

TaSPL8-2D, in the lamina joint. DNA of the Chinese Spring cultivar was used to 898

analyze the amplification efficiency of the three pairs of primers. The RT-qPCR data 899

were normalized to wheat TaACTIN and each bar in the graph corresponds to the mean 900

value of three data points, which are shown by dots. 901

(C-D) Leaf phenotype of LC10 and mutant lines at heading (C) and flowering stages 902

(D). Bar = 2 cm. 903

(E-F) Adaxial (E) and abaxial side (F) phenotypes of the lamina joint region of LC10 904

and mutant lines. Bar = 2 cm. 905

(G) Lamina joint phenotype of TaSPL8 single, double, and triple homoeologous mutant 906

plants. Bar = 1 cm. 907

(H) The lamina joint length of TaSPL8 single, double, and triple homoeologous 908

mutants. The values shown are averages from three plants and the Standard Deviation 909

is indicated. NS: non-significant. Single and double asterisks represent statistically 910


0.01, respectively. 912

(I) Spike number per plant in LC10 and mutant lines in different planting densities 913

(300, 450, 600, and 750 seeds/m2) in Beijing and Yangling. The values shown are 914

averages from three replicates and the Standard Deviation (SD) is reported. Single and 915

double asterisks represent statistically significant differences determined by the 916

two-tailed Student’s t-test at P < 0.05 and P < 0.01, respectively. 917 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



34

(J) Comparison of TaSPL8 expression levels between the wheat cultivars with larger 918

(1.5-2.6 cm) (n = 29) and smaller (0.8-1.5 cm) (n = 49) lamina joints. The level of 919

TaSPL8 mRNA was normalized to wheat ACTIN. Lines in the box plots indicate the 920

median. The 10th/90th percentiles of outliers are shown. The single asterisk represents 921

statistically significant differences as determined by Student’s t-test at P < 0.05. 922

923

Figure 5. Gene Ontology (GO) Term Enrichment Analysis and IAA/BR Level 924

Measurement in TaSPL8 Mutants and Wild Type Plants. 925

(A) Venn diagram analysis of DEGs in TaSPL8-2A/2B/2d and TaSPL8-2a/2b/2d 926

mutants compared to the wild type (LC10). 927

(B) GO terms for biological processes exhibiting statistically significant enrichment in 928

DEGs (only DEGs in common for both single and triple TaSPL8 mutants were 929

considered). 930

(C) GO terms for cell components exhibiting statistically significant enrichment in 931

DEGs. 932

(D-E) IAA (Indoleacetic acid), BL (Brassinolide), and CS (Castasterone) levels were 933

measured in the lamina joint tissue of LC10 and KO-2-1 (TaSPL8-2a/2b/2d) plants. NS 934

indicates a non-significant difference. Single and double asterisks represent statistically 935


0.01, respectively. Error bars indicate the Standard Deviation (n=3). NS: Not 937

Significant. 938

939

940

Figure 6. TaSPL8 Binds and Activates TaARF6 and TaD2. 941

(A) TaARF expression analysis after auxin treatment (10-4 mol/L) in the wild-type 942

LC10 plant and a TaSPL8 mutant (KO-2-1). Each bar in the graph corresponds to the 943

mean value of three data points, which are shown by dots. 944



35

(B-C) EMSAs to assess the TaSPL8 binding to the promoter region of TaARF6 (B) and 945

TaD2 (C) containing the GTAC motif. "+" and "−" indicate the presence and absence, 946

respectively, of corresponding probes, proteins, or competitors. "1×" and "2×" indicate 947

the amount of proteins in the reaction. "5×" and "10×" indicate 5- and 10-fold molar 948

excess, respectively, of competitor or mutated competitor (MT) probes relative to 949

biotin-labeled probes. 950

(D) Generation of wheat transgenic lines overexpressing TaSPL8-Myc chimeric 951

protein (OE lines) in the CB037 genetic background. The level of TaSPL8 transcripts 952

(left panel) and TaSPL8-Myc protein (right panel) were measured. RT-qPCR data were 953

normalized to wheat TaACTIN and each bar in the graph corresponds to the mean value 954

of three data points, which are shown by dots. Double asterisks represent statistically 955

significant differences determined by the two-tailed Student’s t-test at P < 0.01. 956

(E) ChIP assays to detect TaSPL8 binding of TaARF6 and TaD2 in vivo. Arrows 957

indicate the position (P1 and P2) of primer combinations used in qPCR after ChIP 958

assays. P1 indicates the region where GTAC is located and P2 indicates the region 959

without GTAC with more than 400bp distance from P1. Each bar in the graph 960

corresponds to the mean value of three data points, which are shown by dots. Double 961

asterisks represent statistically significant differences determined by the two-tailed 962

Student’s t-test at P < 0.01. 963

(F) Transactivation assays with tobacco leaves infiltrated with different combinations 964

of effector and reporter constructs. Individual values (black dots) and means (bars) of 965

three independent biological replicates are shown. The double asterisks represent 966

significant differences determined by the two-tailed Student’s t-test at P < 0.01. 967

968

Figure 7. Molecular Model for the Regulation of Wheat Lamina Joint Development by 969

TaSPL8. 970

TaSPL8 directly binds to the TaARF6 and TaD2 promoters to activate their expression. 971

TaARF6 mediates the auxin signaling pathway, while TaD2 is involved in BR 972 https://plantphysiol.orgDownloaded on March 22, 2021. - Published by



36

biogenesis. Both hormones are well known for regulating cell elongation, lamina joint 973

development, and leaf angle. 974

975

Supplemental Data 976

Supplemental Figure S1. Schematic of genotype of LC10, cpa, NILLC10, and NILcpa. 977

Black bar, genomic region from LC10; white bar, genomic region from cpa. 978

979

Supplemental Figure S2. A Fragment on Chromosome 2D was Deleted in the cpa 980

Mutant. 981

982

Supplemental Figure S3. CRISPR/Cas9 Knock-out TaSPL8 Mutants in CB037 and 983

Bobwhite Cultivars. 984

Supplemental Figure S4 Heat Map for the DEGs Involved in Auxin and BR 985

Signaling and Cell Elongation in the Wild Type and TaSPL8 Mutants. 986

987

Supplemental Figure S5 TaSPL8 in vitro Binding of Sequences Containing the 988

GTAC Motif. 989

990

Supplemental Figure S6 Phylogenetic Tree of TraesCS5B01G039800.1 (TaARF6) 991

and TraesCS3A01G103800.1 (TaD2) with Arabidopsis or Rice Proteins. 992

993

Supplemental Figure S7 The Phenotypes of TaSPL8-Myc Overexpression (OE) and 994

Wild-type CB037 Lines. 995

Supplemental Table S1 Morphological Characterization of Wild Type and KO-2-1 996

(TaSPL8-2a/2b/2d) Mutant Plants. 997

998




37

Supplemental Table S2. The names and geographical origins of all wheat cultivars 999

used in this research. TaSPL8 expression level and lamina joint length in 78 wheat 1000

cultivars are also included. 1001

1002

Supplemental Table S3. Differentially expressed transcripts in the Taspl8-2a/2b/2d 1003


1005

Supplemental Table S4. Differentially expressed transcripts in the Taspl8-2A/2B/2d 1006


1008

1009

Supplemental Table S5. Primers and Gene IDs for sequences used in this study. 1010

1011

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https://scholar.google.com/scholar?as_q=An SPX-RLI1 module regulates leaf inclination in response to phosphate availability in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ruan,&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=S�n�chal%2C F%2E%2C Wattier%2C C%2E%2C Rust�rucci%2C C%2E%2C and Pelloux%2C J%2E %282014%29%2E Homogalacturonan%2Dmodifying enzymes%3A structure%2C expression%2C and roles in plants%2E J%2E Exp%2E Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Wang%2C K%2E%2C Liu%2C H%2E%2C Du%2C L%2E%2C and Ye%2C X%2E %282017%29%2E Generation of marker%2Dfree transgenic hexaploid wheat via an agrobacterium%2Dmediated co%2Dtransformation strategy in commercial chinese wheat varieties%2E Plant Biotechnol%2E J&dopt=abstract

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https://scholar.google.com/scholar?as_q=OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Transcriptome asymmetry in synthetic and natural allotetraploid wheats, revealed by RNA-sequencing&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=QTL mapping of flag leaf traits in common wheat using an integrated high-density SSR and SNP genetic linkage map&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu,&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=A CRISPR/Cas9 toolkit for multiplex genome editing in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A CRISPR/Cas9 toolkit for multiplex genome editing in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xing,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yamamuro%2C C%2E%2C Ihara%2C Y%2E%2C Wu%2C X%2E%2C Noguchi%2C T%2E%2C Fujioka%2C S%2E%2C Takatsuto%2C S%2E%2C Ashikari%2C M%2E%2C Kitano%2C H%2E%2C and Matsuoka%2C M%2E %282000%29%2E Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint%2E Plant Cell&dopt=abstract

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https://scholar.google.com/scholar?as_q=Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamamuro,&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yang%2C H%2E%2C Liu%2C X%2E%2C Xin%2C M%2E%2C Du%2C J%2E%2C Hu%2C Z%2E%2C Peng%2C H%2E%2C Rossi%2C V%2E%2C Sun%2C Q%2E%2C Ni%2C Z%2E%2C and Yao%2C Y%2E %282016%29%2E Genome%2Dwide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development%2E Plant Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Young%2C M%2ED%2E%2C Wakefield%2C M%2EJ%2E%2C Smyth%2C G%2EK%2E%2C and Oshlack%2C A%2E %282010%29%2E Gene ontology analysis for RNA%2Dseq%3A accounting for selection bias%2E Genome Biol%2E 11%3AR14%2DR&dopt=abstract

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https://scholar.google.com/scholar?as_q=Gene ontology analysis for RNA-seq: accounting for selection bias&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Young,&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang%2C L%2E%2DY%2E%2C Bai%2C M%2E%2DY%2E%2C Wu%2C J%2E%2C Zhu%2C J%2E%2DY%2E%2C Wang%2C H%2E%2C Zhang%2C Z%2E%2C Wang%2C W%2E%2C Sun%2C Y%2E%2C Zhao%2C J%2E%2C and Sun%2C X%2E %282009%29%2E Antagonistic HLH%2FbHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis%2E Plant Cell&dopt=abstract

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https://scholar.google.com/scholar?as_q=Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang%2C S%2E%2C Wang%2C S%2E%2C Xu%2C Y%2E%2C Yu%2C C%2E%2C Shen%2C C%2E%2C Qian%2C Q%2E%2C Geisler%2C M%2E%2C Jiang%2C D%2EA%2E%2C and Qi%2C Y%2E %282015%29%2E The auxin response factor%2C OsARF19%2C controls rice leaf angles through positively regulating OsGH3%2D5 and OsBRI1%2E Plant Cell Environ&dopt=abstract

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


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

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhao%2C S%2E%2DQ%2E%2C Hu%2C J%2E%2C Guo%2C L%2E%2DB%2E%2C Qian%2C Q%2E%2C and Xue%2C H%2E%2DW%2E %282010%29%2E Rice leaf inclination2%2C a VIN3%2Dlike protein%2C regulates leaf angle through modulating cell division of the collar%2E Cell Res&dopt=abstract

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https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao,&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhao%2C S%2E%2DQ%2E%2C Xiang%2C J%2E%2DJ%2E%2C and Xue%2C H%2E%2DW%2E %282013%29%2E Studies on the rice LEAF INCLINATION1 %28LC1%29%2C an IAA%2Damido synthetase%2C reveal the effects of auxin in leaf inclination control%2E Mol%2E plant&dopt=abstract

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https://scholar.google.com/scholar?as_q=Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou%2C L%2EJ%2E%2C Xiao%2C L%2ET%2E%2C and Xue%2C H%2EW%2E %282017%29%2E Dynamic cytology and transcriptional regulation of rice lamina joint development%2E Plant Physiol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Dynamic cytology and transcriptional regulation of rice lamina joint development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Dynamic cytology and transcriptional regulation of rice lamina joint development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou,&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


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https://scholar.google.com/scholar?as_q=Genetic control of inflorescence architecture during rice domestication&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


wheat taspl8 modulates leaf angle through auxin and ...jun 17, 2019 · 147 that the flag leaf...

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