Short title: Alternative splicing in wheatOct 13, 2020 · 106 observed in polyploidization...

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Short title: Alternative splicing in wheat 1

Title: Changes in Alternative Splicing in Response to Domestication and 2

Polyploidization in Wheat 3

Author names and affiliations: Kuohai Yu1,3, Man Feng1,3, Guanghui Yang1,3, Lv Sun1, 4

Zhen Qin1, Jie Cao1, Jingjing Wen1, Haoran Li1, Yan Zhou1, Xiangping Chen1, Huiru 5

Peng1, Yingyin Yao1, Zhaorong Hu1, Weilong Guo1, Qixin Sun1, Zhongfu Ni1, Keith 6

Adams3 and Mingming Xin1* 7

1 State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis 8

Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China 9

Agricultural University, Beijing, 100193, China. 10

2 Botany Department, University of British Columbia, Vancouver, Canada. 11

3 These authors contributed equally to this work. 12

*Corresponding author: Mingming Xin, [email protected], Tel: 010-62731452 13

One-sentence summary: Transcriptomic analyses of several wheat species with different 14

ploidies reveal alternative splicing changes in response to wheat domestication or 15

polyploidization. 16

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Author contributions 19

M.X designed the project, K.Y., M.F. Z.Q., and G.Y. performed data analysis, M.F. and 20

G.Y. performed validation, L.S., J.C., J.W., H.L., Y.Z., X.C. collected tissue, H.P., Y.Y., 21

Z.H., and W.G., Q.S., Z.N., K.A. and M.X. wrote and edited the manuscript. 22

Funding 23

This work was supported by the Major Program of the National Natural Science 24

Foundation of China (31991210 and 91935304). 25

Plant Physiology Preview. Published on October 13, 2020, as DOI:10.1104/pp.20.00773

Copyright 2020 by the American Society of Plant Biologists

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Abstract 27

Alternative splicing (AS) occurs extensively in eukaryotes as an important mechanism for 28

regulating transcriptome complexity and proteome diversity, but variation in the AS 29

landscape in response to domestication and polyploidization in crops is unclear. 30

Hexaploid wheat (AABBDD, Triticum aestivum L.) has undergone two separate 31

allopolyploidization events, providing an ideal model for studying AS changes during 32

domestication and polyploidization events. In this study, we performed high-throughput 33

transcriptome sequencing of roots and leaves from wheat species with varied ploidies, 34

including wild diploids (AbAb, Triticum boeoticum) and tetraploids (AABB, Triticum 35

dicoccoides), domesticated diploids (AmAm, Triticum monococcum) and tetraploids 36

(AABB, Triticum dicoccum), hexaploid wheat (AABBDD, Triticum aestivum L.), as well 37

as newly synthesized hexaploids together with their parents. Approximately 22.1% of 38

genes exhibited AS, with the major AS type being intron retention. The number of AS 39

events decreased after domestication in both diploids and tetraploids. Moreover, the 40

frequency of AS occurrence tended to decrease after polyploidization, consistent with the 41

functional sharing model that proposes AS and duplicated genes are complementary in 42

regulating transcriptome plasticity in polyploid crops. In addition, the subgenomes 43

exhibited biased AS responses to polyploidization, and ~87.1% of homeologs showed AS 44

partitioning in hexaploid wheat. Interestingly, substitution of the D subgenome modified 45

42.8% of AS patterns of the A and B subgenomes, indicating subgenome interplay 46

reprograms AS profiles at a genome-wide level, although the causal–consequence 47

relationship requires further study. Conclusively, our study shows that AS variation 48

occurs extensively following polyploidization and domestication in wheat species. 49

Keywords: Wheat; Alternative splicing; Domestication; Polyploidization; Subgenome50



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Introduction 52

Polyploids experience whole-genome duplication (WGD) and often exhibit exceptional 53

hybrid vigor and enhanced stress tolerance compared to their progenitors (Chen, 2010; 54

Yang et al., 2014; Han et al., 2016). This mechanism has been recognized as a major 55

force driving and shaping the evolution and speciation of vascular plants (Otto, 2007; 56

Madlung, 2013; Van de Peer et al., 2017), since it supplies a vast reservoir of raw genetic 57

materials for mutation, selection, and evolution. In addition to gene duplication, 58

alternative splicing (AS) is also widely accepted as a major mechanism for transcriptome 59

plasticity and proteomic complexity during plant polyploidization (Filichkin et al., 2010). 60

AS refers to a mechanism of post-transcriptional RNA processing whereby multiple 61

distinct transcripts can derive from a single gene, mainly including intron retention (IR), 62

exon skipping (ES), alternative 5' splicing site (A5), and alternative 3' splicing site (A3) 63

(Syed et al., 2012). AS can result in alterations of protein structures, functions or 64

subcellular locations (Gracheva et al., 2011; Kriechbaumer et al., 2012), and thus 65

contributes to diverse regulation of biological process. Up to ~92.0% - 94.0% of human 66

genes and ~21.2% - 63.0% of plant genes undergo AS (Wang et al., 2008; Zhang et al., 67

2015). ES accounts for the largest proportion of AS in humans, whereas IR is the primary 68

form in plants (Reddy et al., 2013). 69

AS and gene duplication are two main processes responsible for protein functional 70

diversity expansion. What is the evolutionary relationship between them, and do they 71

evolve independently or can they be regarded as interchangeable repositories of protein 72

diversity? Genome-wide analyses report a negative correlation between the number of AS 73

events and the size of protein families in human (Homo sapiens), mouse (Mus musculus), 74

Drosophila melanogaster and Caenorhabditis elegans (Kopelman et al., 2005; Su et al., 75

2006; Talavera et al., 2007; Iniguez and Hernandez, 2017) and that larger gene families 76

tend to have fewer genes subjected to AS. In addition, duplicates may undergo fewer AS 77

events than single copy genes (singletons). Furthermore, AS is likely to gain an 78

acceleration in divergence after polyploidization in that AS events are lost in recent gene 79

duplicates, plus novel AS events are gained in ancient homologs (Zhang et al., 2010; Xu 80

et al., 2012). These findings are generalized as the functional sharing model for AS after 81

gene duplication, which illustrates the asymmetric AS evolution and subfunctionalization 82

of homologous genes, where one homolog would retain a certain number of ancestral AS 83

events and the other one adopt the rest of the isoforms. However, this AS-duplication 84

equivalence interpretation is debated by the accelerated AS model, which argues that an 85

age-dependent progressive acquisition of new AS occurs following gene duplication 86

probably due to the relaxation of selection (Jin et al., 2008; Chen et al., 2011; Roux and 87

Robinson-Rechavi, 2011). To reconcile the observation of negative correlation between 88

gene family size and AS event number, the model proposes that genes with fewer AS 89

events prefer to duplicate more frequently during evolutionary history, which accounts for 90



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why ancient homologs persist with increased AS events compared to recent duplicated 91

ones (Roux and Robinson-Rechavi, 2011). 92

It is particularly interesting to investigate the interplay of AS and gene duplication in 93

plants, because a majority of plant species have undergone polyploidization during their 94

evolutionary history. However, most of the above conclusions were drawn from 95

vertebrates, and the relationship between AS and gene duplication is still ambiguous in 96

plants. Lin et al. reported that duplicated genes tend to have more AS forms than those of 97

singletons in both rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana) by 98

analyzing families of paralogous genes (Lin et al., 2008). But another study demonstrates 99

that ~63% of multiexonic genes are subjected to AS in paleopolyploid soybean and shows 100

a decrease of AS events in polyploidization-derived duplicates compared with singletons, 101

causing a negative correlation between the amount of AS events and the size of the gene 102

family (Shen et al., 2014). Furthermore, extensive changes of AS patterns occur to 103

duplicated genes in both Arabidopsis and Brassica napus (Zhang et al., 2010; Zhou et al., 104

2011), and both loss of ancestral splicing forms and gain of new splicing forms are 105

observed in polyploidization duplicates and tandem duplicates (Tack et al., 2014). In 106

addition, AS patterns of homeologs in resynthesized polyploid B. napus are greatly 107

distinct from that of natural lines, presenting more AS pattern changes than does natural B. 108

napus compared with the progenitors (Zhou et al., 2011). 109

Hexaploid wheat (AABBDD, Triticum aestivum L.) is a typical allopolyploid with 110

three distinct subgenomes, involving two separate polyploidization events. The 111

progenitors and polyploids are extant, and the phylogenetic relationships between each 112

other have been well established. In addition, synthetic polyploid wheat can be readily 113

obtained, which enables us to mimic the polyploidization process and investigate the 114

transcriptomic and genomic variation at the onset of polyploidy. Furthermore, there are 115

plenty of Triticum boeoticum and Triticum dicoccoides as well as Triticum momococcum 116

and Triticum dicoccum in natural environments which can be used to interpret wheat 117

domestication events. Thus, the Aegilops-Triticum system provides an ideal model for 118

studying the genetic and epigenetic events that occur early during the evolutionary history 119

of polyploids. Our previous study demonstrates that AS occurs extensively in wheat, and 120

homeologs exhibit partitioned AS patterns in response to abiotic stresses (Liu et al., 2018). 121

Here, we studied AS divergence during wheat domestication and polyploidization events 122

and investigated the potential effects of subgenome interplay on AS profile using 123

Triticum boeoticum, Triticum momococcum, Triticum dicoccoides, Triticum dicoccum, 124

Triticum asestivum, and synthetic polyploid wheat. Our results also provide evidence of 125

an interesting relationship between AS and gene duplication in response to 126




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Results 129

RNA sequencing, transcriptome assembly and AS identification 130

Our interest here was to identify potential AS events in wheat and to investigate their 131

changes in response to domestication and polyploidization events at a genome-wide 132

level. To this end, we performed high-throughput RNA-seq for 40 libraries using the 133

Illumina platform, including leaf and root tissues at the seedling stage for wild diploid 134

and tetraploid wheat, domesticated diploid and tetraploid wheat, hexaploid wheat, as 135

well as resynthesized hexaploid wheat (See Materials). After adaptor sequence 136

trimming and data processing, 2.4 billion high-quality clean reads were obtained, with 137

an average of 28.3 million reads per subgenome (Supplemental Data set S1). By 138

comparison of unique mapping rate, we selected WEWv1 as the reference genome for 139

Triticum boeoticum, Triticum monococcum and Triticum dicoccum (Supplemental 140

Figure S1), whereas the AETv4 genome sequence was used for reference-guided 141

transcript assembly for Aegilops tauschii and IWGSCv1 for Triticum aestivum 142

ssp.yunnanense King, Triticum aestivum, extracted tetraploid wheat (ETW), and 143

synthesized allohexaploid wheat (Dobin et al., 2013; Avni et al., 2017; Appels et al., 144

2018; Ling et al., 2018). 145

After read mapping and transcript assembly, we excluded low-abundance 146

transcripts (less than 5 normalized supporting junction reads per splicing site per 147

sample) and obtained 46,837, 20,902 and 81,942 unique assembled transcripts 148

involving 35,836, 16,654 and 60,079 annotated genes based on WEWv1, AETv4 and 149

IWGSCv1 genomes, respectively (Figure 1A). Subsequently, we used custom scripts 150

to perform alternative splicing analysis of those filtered transcripts and only those 151

genes exhibiting AS in both biological replicates were considered (Supplemental 152

Figure S2). In total, we identified 7782 AS events in WEWv1 (A subgenome: 4,880; 153

B subgenome: 2,902), 3,064 AS events in AETv4 (D genome) and 18,358 AS events 154

in IWGSCv1 (A subgenome: 6,553; B subgenome: 7,622; D subgenome: 4,183) 155

(Figure 1B, Supplemental Data set S2) with 2,691 to 10,831 AS events identified for 156

different wheat species (Supplemental Figure S3, Supplemental Data set S3). Seven 157

major types of AS events were identified, including IR, ES, A5, A3, alternative first 158

exon (FE), alternative last exon (LE), and mutually exclusive exons (ME). Of these, 159

IR was the most abundant type, representing 64.0% of the total, followed by A3, A5, 160

ES, FE, LE, and ME (Figure 1B, Supplemental Figure S3), which was consistent with 161

the observation in Arabidopsis and rice (Syed et al., 2012). 162

Cumulative distribution analysis showed that 55.3% of annotated genes possessed 163

only one major transcript although with multiple AS isoforms (PSI>0.75 or PSI <0.25, 164

percent spliced index [PSI] measures the efficiency of splicing a sequence into the 165

transcript population of a gene, see Methods), whereas 44.7% of the genes 166

simultaneously exhibited two or more predominant transcripts (0.25<=PSI<=0.75, 167

Figure 2A). Pfam enrichment analysis showed that these genes were significantly 168



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enriched in an RNA recognition motif gene family, consistent with the fact that 169

splicing requires a large number of RNA-binding proteins that have one or 170

more RNA-recognition motifs (RRMs), indicating AS genes (ASGs) are involved in 171

the regulation of AS occurrence in wheat, such as serine/arginine-rich genes in 172

Arabidopsis (Rauch et al., 2013) (Figure 2B, Supplemental Data set S4). Further 173

investigation indicated GC content might be correlated with occurrence of ES and IR, 174

that is, skipped exons exhibited a significantly lower GC content than that of other 175

exons (46.9% vs 50.5%, Student's t-test, P-value < 0.001), whereas retained introns 176

had a significantly higher GC content (42.1% vs 39.1%, Student's t-test, P-value < 177

0.001, Figure 2C). In addition, the length of skipped exons or retained introns was 178

shorter than that of the counterpart (195.3 nt vs 402.8 nt for ES and 377.3 nt vs 511.5 179

nt for IR, Student's t-test, P-value < 0.001 respectively, Figure 2D). 180

To obtain an overview of the landscape of AS events in the wheat genome, we 181

investigated their distributions along the chromosomes and observed a significant 182

enrichment of ASGs in the arm regions that was positively associated with gene 183

distribution (P-value was 8.825e-09 and 2.2e-16 from Pearson correlation test, 184



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respectively. Figure 3A, 3B), which was consistent with a previous report in soybean 185

(Shen et al., 2014). Interestingly, we observed a significant difference in the number 186

of ASGs among subgenomes in hexaploid wheat (Kurskal-Wallis test, P-value = 187

0.01639), but not in tetraploid (Wilcoxon signed-rank test P-value = 0.875). In 188

addition, a large proportion of homeologous genes exhibited alternative splicing 189

partitioning in polyploid wheat (see details below); only 303 (3.6%) and 286 (4.0%) 190



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groups of homeologs exhibited similar alternative splicing patterns in tetraploid 191

(IW136 and DM4) and hexaploid wheat (TAA10, TKM and CS). 192

AS alteration in response to wheat domestication 193

To explore AS changes responsive to domestication, we compared the AS patterns of 194

19,590 and 35,836 pairs of genes between AA2 (Triticum boeoticum, AbAb) and 195

AA11 (Triticum monococcum, AmAm) as well as between IW136 (Triticum 196

dicoccoides, AABB) and DM4 (Triticum dicoccum, AABB), respectively. We 197

identified 1,531 and 1,350 ASGs with 2,691 and 2,318 AS events in wild diploid 198

wheat AA2 and cultivated diploid wheat AA11, respectively, and thus the proportion 199

of AS events decreased by 13.9% after domestication in diploid wheat. In addition, a 200

total of 2,996 (5,137 events) and 1,663 (2,546 events) ASGs were revealed from wild 201

emmer IW136 and domesticated tetraploid wheat DM4, respectively. Of these, 1,503 202

and 862 AS genes resided in subgenome A, whereas 1,493 and 801 were located in 203

subgenome B, and the number of AS events reduced by 50.4% in response to 204

domestication in tetraploid wheat (Figure 4A). Specifically, 1,481 and 3,481 AS 205

events were lost, whereas 1,108 and 890 were newly generated in diploid and 206

tetraploid wheat, respectively, during the domestication process (Figure 4B). 207

Due to insufficient read coverage, genome variation, and species-specific AS 208

occurrence, a proportion of eliminated AS events mentioned above were probably not 209

due to domestication. To minimize artifacts, we next focused on the quantitative 210



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differential alternative splicing events (QDASEs) and altering transcript isoform (ATI) 211

before and after domestication. QDASE refers to one splicing isoform exhibiting 212

differential transcript abundance, which was defined by these criteria: junction 213

supporting reads based FDR < 0.05 and > 20% variation of PSI (ΔPSI, see Methods) 214

after domestication. ATI indicates an ASG showing changes in splicing isoform in 215

response to domestication. In total, 293 AS events from 218 genes were exploited as 216

domestication responsive ASGs in diploid wheat, including 218 QDASEs and 75 217

ATIs. We also investigated the divergence of AS events in tetraploid wheat in 218

response to domestication. By pairwise comparison, 419 responsive AS events from 219



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322 genes were identified in tetraploid wheat, including 325 QDASEs and 94 ATIs. 220

(Figure 4B, Supplemental Data set S5). To confirm the altered AS patterns in 221

response to domestication identified by RNA-seq data, we performed RT-PCR using 222

conserved primer pairs amplifying different splicing variants in a single reaction 223

across five wild diploid species, five domesticated diploid species, five wild tetraploid 224

species, and five domesticated tetraploid species (Figure 4C, 4D). As expected, most 225

of the examined alternative ASGs showed consistent splicing patterns with the 226

prediction. For example, two transcript isoforms of WEWv1_A_gene.77369.0 227

(armadillo-type fold domain containing gene) were expressed in all examined 228

domesticated diploid wheat, whereas only one isoform was detected in 60% (3/5) wild 229

diploid wheat (Figure 4C). Similarly, WEWv1_A_gene.80316.0, encoding a 230

phosphoinositide phosphatase gene, transcribed one more isoform in response to 231

domestication in most domesticated tetraploid wheat. Whereas 232

WEWv1_B_gene.13387.3, encoding an ATPase, had two major transcript isoforms 233

before domestication, but only one major was detected after domestication (Figure 234

4D). To explore the underlying molecular mechanism of AS event reduction in 235

response to domestication, we analyzed the expression abundance of genes involved 236

in AS regulation in wild and domesticated wheat species, and 17 and 21 237

AS-regulation related genes were down-regulated after domestication in diploid and 238

tetraploid wheat, respectively, whereas only 7 and 11 genes were up-regulated 239

(Supplemental Data set S6). RT-qPCR results further confirmed our observation that 240

the three examined genes exhibited decreased expression abundance in domesticated 241

varieties compared with wild ones (Supplemental Figure S4). Therefore, we propose 242

that the reduced expression level of splicing regulators might contribute to decreased 243

splicing efficiency in domesticated species compared with wild species, which may 244

lead to a decrease of AS occurrence in response to domestication in wheat. 245

To analyze conservation of AS changes in response to domestication in both 246

diploid and tetraploid wheat, we compared 293 domestication responsive AS events 247

(both QDASEs and ATI) from diploid wheat (A genome) and 237 from the A 248

subgenome of tetraploid wheat. A total of 27 AS events (including 26 QDASEs and 249

one ATI) from 18 ASGs commonly occurred in both wheat species in response to 250

domestication which were significantly enriched in GO terms of “nucleic acid binding” 251

(GO:0003676) (Supplemental Figure S5, Supplemental Data set S4). Of these ASGs, 252

WEWv1_A_gene.112770.0 and WEWv1_A_gene.1336.0 encoded 253

serine/arginine-rich splicing factors highly similar to RSZ22 (AT4G31580) and 254

RS2Z32 (AT3G53500) in Arabidopsis, respectively, which are required for the 255

regulation of gene alternative splicing (Golovkin and Reddy, 1998; Lopato et al., 256

2002; Lorkovic et al., 2004). To confirm the observation, we verified the AS patterns 257

in multiple diploid and tetraploid wheat lines. The two transcript isoforms of the 258

RSZ22 homolog (WEWv1_A_gene.112770.0) showed similar expression level in wild 259

diploid and tetraploid lines (except IW47 and IW104), whereas isoform 1 transcript 260

exhibited higher expression abundance than that of isoform 2 in all examined 261



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domesticated wheat. In contrast, isoform 2 of the RS2Z32 homolog 262

(WEWv1_A_gene.1336.0) showed higher expression level than that of isoform 1 after 263

domestication (Supplemental Figure S6). Thus, we propose that the splicing variation 264

of AS regulators might also contribute to AS occurrence efficiency after 265

domestication in wheat, which needs further investigation. 266

To further investigate the biological significance of the domestication responsive 267

ASGs, we performed translation analysis and Pfam assignment of different transcript 268

isoforms of intron-retained genes. AS resulted in the change of coding sequence, thus 269

subsequently leading to 590 and 850 pairs of isoforms showing differences in Pfam 270

domain in diploid and tetraploid wheat, respectively (Supplemental Data Set S7). 271

Dormancy is a desired trait for wild species to prevent seed germination during 272

unsuitable external conditions, whereas domesticated crops have undergone artificial 273

selection against seed dormancy (Liu et al., 2018). Of these genes, we identified two 274

ABA responsive transcription factors (WEWv1_A_gene.9008.0 and 275

WEWv1_A_gene.75640.0 similar to DI19-3 and BZIP63 in Arabidopsis, respectively) 276

involved in regulating seed germination under stress conditions (Qin et al., 2014; 277

Veerabagu et al., 2014) and one dormancy/auxin-associated protein 278

(WEWv1_A_gene.66541.0 homolog to DRMH2 in Arabidopsis) subjected to AS in 279

response to domestication in both diploid and tetraploid wheat (Supplemental Data 280

Set S5). In addition, rachis brittleness and seed shattering are also typical 281

characteristics altered during the wheat domestication process, whereas the Q gene is 282

an important domestication gene involved in pleiotropical influences on phenotypic 283

variation, including rachis fragility and seed threshability (Simons and J., 2005). 284

Previous genetic and molecular evidence indicates that the phenotypic effect of the Q 285

gene on domestication related traits is associated with the presence of mutation at the 286

miRNA binding site (which affects transcript abundance) and the 161bp transposon 287

insertion (which results in a deletion of conserved domains) (Simons et al., 2006; 288

Debernardi et al., 2017; Jiang et al., 2019). Interestingly, the homolog of the Q gene 289

(WEWv1_A_gene.90708.0) in diploid and tetraploid wheat was also subjected to 290

differential AS, and the IR retention isoform abundance decreased in domesticated 291

species compared to wild species in both diploid and tetraploid wheat (Supplemental 292

Figure S7). 293

AS changes in response to wheat polyploidization 294

To determine whether AS patterns changed after wheat polyploidization, we 295

examined the AS landscape in extracted tetraploid wheat (ETW), TQ18, and XX329. 296

Allohexaploid XX329 was resynthesized by the maternal parent ETW and the 297

paternal parent TQ18 (Aegilops tauschii). ETW was ploidy-reversed from hexaploid 298

cultivar wheat TAA10 with high karyotype stability, produced by recurrent 299

backcrossing (Kerber, 1964; Zhang et al., 2014). In total, we identified 8,713 AS 300

events from 4,374 genes in ETW (A subgenome: 2,090; B subgenome: 2,284), 2,536 301

AS events from 1,583 genes in TQ18, and 9,922 AS events from 5,450 genes in 302



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XX329 (A subgenome: 1,863; B subgenome: 2,053; D subgenome: 1,534, Figure 5A). 303

Compared with ETW (AABB) and TQ18 (DD), 2,661 and 587 AS events were lost, 304

whereas 1,394 and 527 AS events were newly formed after polyploidization in 305

XX329. Accordingly, the proportion of AS events in resynthesized allohexaploid 306

wheat reduced by 11.8% compared to the counterpart in the parental lines, with 15.7%, 307

13.5% and 2.4% decreases for subgenomes A, B and D, respectively (Figure 5A). We 308

also examined QDASEs and ATIs in response to polyploidization according to the 309

mentioned criteria above and identified 478 ployploidization responsive QDASEs and 310

39 ployploidization responsive ATIs in wheat (Figure 5B, Supplemental Data set S5). 311

The splicing patterns were also confirmed by RT-PCR in three sets of synthesized 312

wheat accessions. For example, we only detected the band of isoform 1 of RCC1 313

(Regulator of Chromosome Condensation 1, IWGSCv1_B_gene.25853.0) in 314

tetraploid wheat, while both isoform 1 and 2 bands amplified in hexaploid wheat after 315



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polyploidization (Supplemental Figure S8A). Isoform1 of the glycosyltransferase 316

related gene (IWGSCv1_B_gene.137552.0) only amplified in synthetic hexaploid 317

wheat XX329 and SXS (Supplemental Figure S8B). 318

In addition, density curve analysis of PSI of AS events showed that the 319

distribution of PSI was biased to one in subgenome A and B after polyploidization, 320

which was obviously different from the corresponding distribution in subgenome D 321

(Kolmogorov Smirnov test, P-value = 1.4e-12) but similar to the trend in A and B 322

subgenomes (Kolmogorov Smirnov test, P-value = 0.098) during domestication 323

(Figure 5C). Gene Ontology (GO) enrichment analysis also confirmed our 324

observation that AS occurrence distributed unevenly among three subgenomes, since 325

polyploidization responsive ASGs in subgenome D were significantly enriched in two 326

tRNA related terms (GO:0004822 and GO:0006428), whereas the responsive ASGs in 327

subgenome A and B were enriched in ten other terms, including transmembrane 328

transport (GO:0055085) (Figure 5D). These results further suggested that the 329

subgenomes exhibited different AS responses between each other, with two or more 330

predominant transcripts from one ASG in subgenome D after polyploidization but less 331

in subgenome A and B. To better understand why AS occurrence decreased after 332

polyploidization, we examined the expression profile of key AS regulators and found 333

that 13 splicing related factors were differentially expressed after polyploidization. 334

For example, the homologs of U2 small nuclear ribonucleoprotein auxiliary factor 65 335

(U2AF65A, IWGSCv1_A_gene.121408.0) were significantly down-regulated in 336

synthesized hexaploid wheat (XX329/DXY/SXS) compared with the tetraploid 337

(ETW/DM4/SCAUP) parents, which interact with U2AF35 to promote U2snRNP for 338

the recognition of the pre-mRNA 3' splice site during early spliceosome assembly in 339

Arabidopsis (Chusainow et al., 2005; Heiner et al., 2010). In addition, the homolog of 340

RS2Z32 (AT3G53500) in the Ser/Arg-rich (SR) protein family, which controls splice 341

site selection and spliceosome assembly in Arabidopsis (Kalyna et al., 2006; Barta et 342

al., 2010), was also down-regulated after polyploidization in wheat (Supplemental 343

Figure S9). Therefore, we speculate that the differential expression of splicing-related 344

genes after polyploidization, especially the down-regulation of important splicing 345

factors, is one of the causes for the decrease of the number of AS events. This 346

observation is consistent with the functional sharing model that reduced AS events 347

and duplicated genes are complementary in regulating transcriptome plasticity in 348

polyploid crops. 349

Previous studies revealed a complex interplay of subgenomes in the regulation of 350

gene expression in polyploid wheat (Pfeifer et al., 2014). To determine if subgenome 351

interplay influences AS occurrence, we surveyed expression abundance of AS 352

isoforms between XX329 and TAA10, which were predicted to contain > 99.8% 353

identical A and B subgenomic components and only differ from each other in the 354

origin of the D subgenome (Wang et al., 2016). We revealed 16.2% (1,583/9,781) 355

XX329-specifc and 23.9% (2,335/9,781) TAA10-specific AS events on A and B 356



15

subgenomes, respectively (Supplemental Figure S10A). Among the co-existing AS 357

events, 100 and 144 AS events were identified as QDASEs, and 14 and 15 were 358

characterized as ATIs on subgenomes A and B (Figure 5B). We revealed that the 359

homologs of splicing regulators U2AF65A and U2AF35B 360

(IWGSCv1_A_gene.121408.0 and IWGSCv1_A_gene.14304.0) were down-regulated 361

in XX329 compared with TAA10 (Supplemental Figure S10B), which might be 362

involved in the regulation of AS variation between each other. In addition, differential 363

AS types of AS-regulating genes were examined between XX329 and TAA10. For 364

example, the transcripts of IWGSCv1_A_gene.121408.0 deleted the fifth exon in 365

TAA10 but retained in XX329, whereas IWGSCv1_B_gene.67777.0, encoding a 366

DEAD-box ATP-dependent RNA helicase involved in the mRNA splicing process, 367

expressed two transcripts in TAA10 but only one in XX329 (Supplemental Figure 368

S11A). These lines of evidences suggested that the AS profile of subgenome A and B 369

was significantly affected due to substitution of the subgenome D in polyploid wheat, 370

possibly due to differential expression patterns and altered AS profiles of 371

AS-regulating genes. 372

AS partitioning among homeologs in polyploidy wheat 373

To investigate whether AS partitioning occurs among homeologs in hexaploid wheat, 374

we comprehensively assayed AS patterns in hexaploid wheat of TAA10, TKM and 375

CS and identified 10,831 (5,588 genes), 10,797 (6,019 genes) and 8,949 (5,150 genes) 376

AS events, respectively (Figure 6A). Of these AS events, 28.3% (4,679/16,515) were 377

commonly present among the three wheat lines, whereas 43.2% (7,132/16,515) 378

showed accession-specific AS patterns (Supplemental Figure S11B). 379

Next, we focused on the AS variation among homeologous triplets, which have 380

exactly one representative gene on subgenome A, B and D at a similar genomic 381

region. In total, 1,501, 1,518 and 1,386 AS triplets were identified in TAA10, TKM 382

and CS, respectively (Supplemental Data set S8), with at least one of the three 383

homeologs showing AS. We observed that AS patterns were partitioned extensively, 384

with only 14.4% (TAA10:243, TKM:220, CS:181) of triplets showing simultaneous 385

AS in three homeologs. Of these triplets, on average, 89.4% (TAA10:213, TKM:197, 386

CS:166) exhibited the same AS pattern and 10.6% (TAA10:30, TKM:23, CS:15) 387

showed different AS types, respectively (Figure 6B). For example, a triplet cluster 388

(IWGSCv1_A_gene.150363.0, IWGSCv1_B_gene.169279.0, 389

IWGSCv1_D_gene.65226.0) associated with the phosphoglucosamine mutase family 390

has an AS event with the second exon skipped in all A, B and D subgenomes 391

(Supplemental Figure S12A). Another gene with a WW/Rsp5/WWP domain 392

contained triplets showing IR in subgenome A and B but A5 in subgenome D 393

(Supplemental Figure S12B). Among the 89.4% of homeologs displaying 394

conservative AS types, a ternary plot (using a triad’s position based on the proportion 395

of AS events abundance) classified them into seven categories: 1) balanced category 396

with similar proportion of AS transcripts for all three homeologs; 2) 397



16

homeologous-dominant category with a significantly higher PSI value of an AS event 398

in one homeolog than the other two; 3) homeologous-suppressed category with a 399

significantly lower PSI value of an AS event in one homeolog than the other two 400

(Ramirez-Gonzalez et al., 2018). The resulting plot showed that 17.4% (37/213), 24.9% 401

(49/197) and 21.1% (35/166) of homeologous ASGs in TAA10, TKM and CS, 402

respectively, showed partitioned AS patterns among subgenomes (Figure 6C), 403

although most homeologous ASGs were assigned to the AS balanced category. Thus, 404

in total, 87.1% (85.6% + 14.4%*10.6%) of homeologous triplets showed biased or 405

different splicing patterns, suggesting AS changes occur extensively among 406



17

homeologous genes in hexaploid wheat. In addition, we identified 225 homologous 407

AS triplets from WEWv1 and AETv4 reference genomes, of which 198 (88.0%) 408

showed the same AS type. Ternary plots by averaging the PSI value of the 409

corresponding sample showed most of these conservative AS triplets (165/198=83.3%) 410

in WEWv1 and AETv4 are assigned to the balanced category with a similar 411

proportion of AS transcripts for A, B and D homeologs (Supplemental Figure S13). 412

413



18

DISCUSSION 414

Alternative splicing (AS) refers to a mechanism by which multiple mRNA isoforms 415

are generated from one primary type of precursor molecule. Large scale genomics 416

studies have revealed that AS occurs extensively in plants, accounting for 42% to 61% 417

of genes (Marquez et al., 2012; Reddy et al., 2013; Klepikova et al., 2016). AS 418

expands the repertoire of functional complexity in plant genomes by increasing the 419

diversity of the transcriptome, and growing evidence indicates that AS participates in 420

a large fraction of biological pathways in plants (Staiger and Brown, 2013; Wang et 421

al., 2015). Despite increasing interest in how AS is regulated during plant 422

development, limited information is available in wheat. The question of how AS is 423

influenced by subgenome interplay and what trends occur during evolution and 424

domestication history have not been answered. Our results provided interesting 425

suggestions for biologists to better understand how AS responds in plants, that is, 1) 426

AS evolutionary diverged during wheat domestication and the hexaploidization 427

process; 2) AS and gene duplication might be functionally complementary in 428

hexaploid wheat; 3) Subgenome interplay significantly affects AS occurrence in 429

hexaploid wheat and AS patterns partitioned extensively among homeologs. 430

AS patterns dramatically changed in response to wheat domestication 431

Domestication has been proven to strongly reduce genomic diversity through 432

population bottlenecks in numerous cultivated crop species, resulting in a series of 433

human-preferred syndromes, including loss of rachis brittleness, changes in seed 434

dormancy, increases in seed size, etc. Reduced variation in gene expression patterns 435

was observed in response to domestication by comparative transcriptomes between 436

maize (Zea mays L.) and teosinte (Zea mays ssp parviglumis) as well as between bean 437

and its wild counterpart (Bellucci et al., 2014; Huang et al., 2015). Besides, AS 438

profiles significantly changed during the domestication episode from the wild 439

relatives to the cultivated species, although with different trends: increased AS 440

complexity occurred in domesticated maize, but decreased AS diversity occurred in 441

cultivated sorghum (Huang et al., 2015; Ranwez et al., 2017; Smith et al., 2018). AS 442

participates in the crop domestication process, e.g. a splice-site mutation in the fourth 443

intron of the sh1 gene leads to the removal of the adjacent exon in sorghum and 444

subsequently accelerates its agronomic improvement with the non-shattering trait (Lin 445

et al., 2012), and a C-to-A splice-site mutation of OsSSH1 (SNB) alters the splicing of 446

its mRNA, causing reduced shattering of the ssh1 mutant by altering the development 447

of the abscission layer and vascular bundle in rice (Jiang et al., 2019). 448

In this study, we compared the AS profiles between wild (AbAb) and 449

domesticated diploid wheat species (AmAm) as well as tetraploid wheat species 450

(AABB). Not surprisingly, AS patterns dramatically changed during wheat 451

domestication history, and a significant decrease of AS event abundance occurred in 452

cultivated wheat species compared with wild species, consistent with the findings in 453



19

sorghum (Ranwez et al., 2017). Expression levels of several AS regulators were 454

significantly down-regulated in domesticated wheat species compared with wild ones, 455

which might result in decreased splicing efficiency and reduced AS occurrence in 456

response to domestication in wheat under this circumstance. In addition, AS patterns 457

of RS2Z32 and RSZ22, which are required for the regulation of splicing, were 458

obviously different before and after domestication, indicating another potential 459

contributor to the decreased amount of AS genes after domestication. Interestingly, 460

although previous studies report that rachis brittleness and seed shattering variation 461

are attributed to the presence of mutation at the miRNA binding site and a 161bp 462

transposon insertion of the Q gene (Simons et al., 2006; Debernardi et al., 2017; Jiang 463

et al., 2019), we revealed that the homolog of the Q gene was subjected to differential 464

AS in diploid wheat and tetraploid wheat (Supplemental Figure S7). Furthermore, we 465

found a similar trend for AS variation during domestication events in diploid and 466

tetraploid wheat species, and 16.6% (660/3,983) of AS events exhibited conserved 467

domestication responsive splicing patterns, including AS elimination and new AS 468

formation, which is similar to a previous report (Ranwez et al., 2017). AS loss, in this 469

case, results in a decrease of protein-coding genes in domesticated wheat species 470

(~1.4% and 3.2% for diploids and tetraploids, respectively), and consequently reduces 471

the genomic diversity, which may be negatively corresponded to adaptive ability. 472

However, the “less-is-more” hypothesis proposes that gene loss is recognized as a 473

pervasive source of genetic variation that can cause adaptive phenotypic diversity 474

(Albalat and Canestro, 2016), suggesting that AS may not be just a noisy consequence 475

of domestication. However, the question remains open whether AS actively influences 476

the plant domestication event or if it is just a consequence of this evolution process. 477

Since we do not have convincing biological evidence to support this hypothesis based 478

on this study, the hypothesis merits further investigation in the future. 479

The contribution of AS to specialization during wheat polyploidization 480

Gene duplication (GD) and AS are considered two main contributors involved in the 481

increase of protein diversity during the polyploidization process. The evolutionary 482

relationship between the two processes is far from being understood, although several 483

models have been proposed based on the studies in mammals. Of these, the functional 484

sharing model suggests an asymmetric subfunctionalization of homologous genes 485

such that one homolog would adopt part of the ancestral AS events whereas the other 486

homeolog(s) adopts the rest; thus, on average, the number of AS events per gene 487

decreases after gene duplication (Kopelman et al., 2005; Su et al., 2006; Iniguez and 488

Hernandez, 2017). The accelerated AS model indicates an increased number of AS 489

events per gene probably due to relaxed selection pressure and an acquisition of AS 490

for duplicated genes over time (Iniguez and Hernandez, 2017). In contrast, the 491

independent model is established to explain a lack of relationship between AS and 492

GD events (Su and Gu, 2012; Iniguez and Hernandez, 2017). 493



20

Hexaploid wheat (AABBDD, Triticum aestivum L.) is a widespread, typical 494

allopolyploid with three distinct subgenomes and has undergone two separate 495

allopolyploidization events. Functional diversification of duplicated genes has widely 496

occurred among homeologous genes in polyploid wheat, probably caused by sequence 497

variation or gene expression pattern change (Bottley et al., 2006; Zhang et al., 2011; 498

Sakuma et al., 2019). In this study, we proposed that AS might also participate in the 499

regulation of subfunctionalization of homeologs, because we revealed that AS 500

patterns were dramatically changed in response to polyploidization at a genome-wide 501

level and the variations in AS patterns diverged significantly among homeologous 502

genes. Furthermore, consistent with the functional sharing model, we observed that 503

the proportion of ASGs dramatically decreased in resynthesized allohexaploid wheat 504

compared with their counterparts in the parental lines. The above results were in 505

accordance with a previous study in resynthesized allotetraploid Brassica napus, 506

which reported that more than one quarter of the duplicated genes showed diverged 507

AS patterns compared with the parents based on RT-PCR validation, with most cases 508

of AS loss from one homeolog after polyploidy (Zhou et al., 2011). However, an 509

increased level of AS was reported in tetraploid watermelon compared with the 510

diploid in all vegetative tissues but fruit (Saminathan et al., 2015), but the authors did 511

not discriminate homeologs in polyploids, which might not be able to differentiate AS 512

changes for each homeolog. In conclusion, we therefore propose that AS and gene 513

duplication may not evolve independently in wheat. Another major outcome from the 514

present study is the finding that subgenome interplay reprograms AS occurrence in 515

polyploid wheat. We took advantage of allopolyploid wheat (wherein chromosome 516

sets are derived from different species), allowing to distinguish subgenome origin of 517

transcripts using SNP information among subgenome sequence. The results show that 518

AS patterns in the subgenomes A and B are substantially dysregulated due to the 519

substitution of subgenome D. However, the molecular mechanisms underlying this 520

observation are still unknown, which is a topic that merits further investigation.521



21

Materials and Methods 522

Plant Materials 523

Wild diploid wheat AA1, AA2, AA4, AA15, AA21 [AbAb, Triticum boeoticum], 524

domesticated diploid wheat AA11, AA19, AA28, AA30, AA31 [AmAm, Triticum 525

monococcum], diploid goatgrass lines TQ18, SQ523 and Y199 [DD, Aegilops 526

tauschii], tetraploid wheat species (AABB, Triticum dicoccoides [IW92, IW95, IW47, 527

IW104, IW136], Triticum dicoccum [DM4, Z39, CX03, CX04, CX05, SCAUP], 528

extracted tetraploid wheat [ETW]) as well as four hexaploid wheat species 529

(AABBDD, Triticum yunnanense King [TKM], Triticum aestivum L. [CS], Triticum 530

aestivum L. [TAA10] and a resynthesized allohexaploid wheat [XX329]) were grown 531

in a growth chamber with 22℃/18℃ (day/night), 16/8h (light/dark) and 50% 532

humidity. TKM (Triticum yunnanense King) is a hexaploid wheat subspecies with 533

wrapped glumes and fragile spikes endemic to Yunnan Province, China. ETW is a 534

ploidy-reversed form of tetraploid wheat from hexaploid wheat TAA10, produced by 535

recurrent backcrossing; The hexaploid wheat XX329 was resynthesized by maternal 536

parent ETW and paternal parent TQ18 (Aegilops tauschii) (Kerber, 1964); The 537

hexaploid SXS was resynthesized by maternal parent SCAUP (Triticum turgidum) 538

and paternal parent SQ523 (Aegilops tauschii); The hexaploid wheat DXY was 539

resynthesized by maternal parent DM4 (Triticum dicoccum) and paternal parent Y199 540

(Aegilops tauschii). 541

RNA Extraction and Sequencing 542

Total RNA of leaf and root tissues from 10-day-old seedings (20 samples × 2 543

replicates) was extracted using TRIzol reagent (Invitrogen Carlsbad, California, USA) 544

according to the manufacturer’s instructions. RNA concentration was measured using 545

a NanoDrop 2000 spectrophotometer (ND-2000, ThermoFisher Scientific, Inc. 546

Waltham, MA, US). RNA integrity was assessed on an Agilent 2100 Bioanalyzer 547

(Agilent Technologies, Inc., Santa Clara, California, US). Then 125bp (ETW, TQ18, 548

XX329, TAA10) or 150bp (AA2, AA11, IW136, DM4, TKM, CS) paired-end 549

sequencing libraries with average insert size of 280 bp were prepared with TruSeq 550

RNA Sample Preparation Kit v2 (Illumina, San Diego, CA) and sequenced on 551

Illumina HiSeq2500 (125bp) or Illumina Novaseq6000 (150bp) according to the 552

manufacturer’s standard protocols. Raw data obtained from Illumina sequencing were 553

processed and filtered using the Illumina pipeline (https://www.Illumina.com) to 554

generate Fastq files. Finally, approximately 304.4G high-quality clean reads were 555

generated from 40 libraries after quality detection (FastQC v0.11.5; 556

http://www.bioinformatics.babraham.ac.uk) and filtering (Trimmomatic, v0.36) 557

(Bolger et al., 2014). Next, the high-quality reads were aligned to the respective 558

reference genomes using the STAR program, and then the Scallop program (Shao and 559

Kingsford, 2017; De Clerck et al., 2018) was employed to perform transcriptome 560

assembly from merged mapping results by samtools (Li et al., 2009). Illumina reads 561



22

of all samples were deposited in the Bioproject at the National Center for 562

Biotechnology Information (https://www.ncbi.nlm.nih.gov/bioproject) under the 563

accession number PRJNA553311. 564

Reads mapping, transcript structure assembly and gene expression analysis 565

An overview of the bioinformatics pipeline used for data analysis is shown in 566

Supplemental Figure S2. High-quality paired-end RNA-Seq reads from each library 567

were mapped to the appropriate reference genome with transcriptome GTF annotation 568

files using the STAR program (version 2.5.3a) with stringent parameters 569

‘--alignEndsType EndToEnd --outFilterMultimapNmax 1 --alignIntronMax 20000 570

--alignIntronMin 20 --outSJfilterCountUniqueMin 4 2 2 2 --outSJfilterCountTotalMin 571

4 2 2 2 --alignSJoverhangMin 8 --alignSJDBoverhangMin 2’ (Dobin et al., 2013). 572

Due to lack of a uniform reference genome for AA2, AA11 and DM4, we first 573

mapped all their sequencing reads to IWGSCv1, WEWv1 and Tuv2 genomes using 574

the STAR program and chose the best according to the unique mapping rate 575

(Supplemental Figure S1). Finally, the WEWv1_A genome was used as a reference 576

for AA2 and AA11, the WEWv1_A&B genome was used for IW136 and DM4, the 577

IWGSCv1_A&B genome was used for ETW, AETv4 was used for TQ18, 578

IWGSCv1_A&B&AETv4 was used for XX329, and IWGSCv1 was used for TAA10, 579

TKM and CS. 580

The mapped reads were merged according to the mapping location of different 581

reference subgenomes by SAMtools (version 0.1.19) (Li et al., 2009). Merged 582

mapping results were assembled into putative transcripts by scallop (version v0.10.2) 583

with parameters ‘--min_transcript_coverage 5 --min_single_exon_coverage 50 584

--min_flank_length 6’ (Shao and Kingsford, 2017). Next, transcripts with exons or 585

introns less than 20bp were filtered out, and only those transcripts with more than five 586

normalized junction supporting reads for each junction in at least two biological 587

replicates of one sample were retained for the following analysis using custom Perl 588

scripts. The number of genes or ASGs per 1Mb on the genome were counted and R 589

was used (https://www.r-project.org/) to perform statistical tests. The number of 590

mapping reads and FPKM (Fragments per Kilobase Million) on each gene were 591

calculated by featureCount (v1.5.2) and an in-house script, respectively. The 592

differentially expressed genes were characterized by the R package DESeq2 (version 593

1.24.0) (Love et al., 2014) with an absolute value of log2-fold change ≥ 1 and a false 594

discovery rate < 0.05 as cutoffs. Moreover, only the reads of AABB or DD 595

subgenome in XX329 were counted to compare with ETW and TQ18, respectively, to 596

analyze the differentially expressed genes before and after polyploidization. 597

AS event, QDASE and ATI identification 598

To identify AS events, exon-exon and exon-intron junction information was 599

extracted from the GTF file generated by scallop and filtered via custom Perl scripts. 600

AS events in all reference genomes, consisting of IR, A3, A5, ES, FE, LE and ME, 601



23

were identified based on the junction information by custom Perl scripts using the 602

methods described by Brooks et al (Brooks et al., 2011). Then, custom Perl scripts 603

were used to count the number of supporting reads for each detected junction based 604

on BAM files generated by STAR, and this number was multiplied by the normalized 605

coefficient (average sequencing base / the sample sequencing base) based on the 606

sequencing bases of the sample. To minimize artifacts, only unique mapped reads 607

with <= 5 mismatches and >= 5 overhang bases were considered. The number of 608

normalized junction supporting reads in these AS events was used to measure the 609

percentage of a gene’s mRNA transcript that include a specific exon or splice site, 610

namely, PSI (Percent spliced in index) (Supplemental Figure S2) (Katz et al., 2010; 611

Liu et al., 2018; Park et al., 2018): 612 𝑃𝑆𝐼 = 𝐽𝑆𝑅𝑖𝐽𝑆𝑅𝑖 + 𝐽𝑆𝑅𝑒 × 100%. JSRi represents the number of junction reads that support inclusion of alternative 613

exons (ES, IR) or longer exons (A3, A5, FE, LE, ME) in an AS event, where the JSRi 614

in IR type AS events was normalized according to the length of reads and introns: 615 𝐽𝑆𝑅𝑖 of IR = × ×( × ); 616

JSRe represents the number of junction reads that support exclusion of alternative 617

exons (ES, IR) or shorter exons (A3, A5, FE, LE, ME) in an AS event. Only those 618

with the value of PSI between 0.05 and 0.95, and > 5 normalized junction-supporting 619

reads for each junction in both biological replicates were considered as AS events in 620

this study. If the PSI value was close to 0 or 1, the ASG possessed one major 621

transcript; if the PSI value was close to 0.5, the ASG tended to express both splicing 622

transcripts. 623

To identify domestication-responsive and polyploidization-responsive AS events, 624

Fisher’s exact tests in R (https://www.r-project.org/) were performed on the 625

comparison of junction read counts supporting different splice isoforms. Next, ∆PSI 626

(∆PSI = |PSIsample1-PSIsample2|×100%) representing the degree of deviation in the AS 627

events between different samples was calculated. Finally, AS events with ∆PSI > 20%, 628

FDR-adjusted P-values (Benjamini and Hochberg’s method) < 0.05 in two biological 629

replicates were identified as quantitative differential alternative splicing events 630

(QDASE) or altering transcript isoforms (ATIs) (Dong et al., 2018; Liu et al., 2018). 631

Functional annotation and enrichment 632

The longest transcripts of assembled genes were aligned against IWGSCv1 reference 633

genes with fairly good functional annotations by a local BLASTN program (Camacho 634

et al., 2009). The functional description of the IWGSCv1 gene was derived from the 635



24

functional description of the homologous genes of rice (Oryza sativa ssp. Japonica) 636

(IRGSP1.0, https://rapdb.dna.affrc.go.jp/) and Arabidopsis (Arabidopsis thaliana) 637

(TAIR, https://www.arabidopsis.org/) by local BLASTP program. The best hit with 638

e-value less than 1e-5 and percentage of alignment amino acid length more than 50% 639

(BLASTP) was retained for functional annotation. Gene Ontology (GO) annotations 640

of IWGSCv1 genes were obtained from Ensembl Plant Biomart 641

(http://plants.ensembl.org/). Significantly overrepresented GO terms were 642

implemented by goseq (version v1.30.0), and all ASGs or assembled genes were used 643

as background genes for domestication and ployploidization responsive ASGs or 644

differentially expressed genes, respectively. Translation prediction of transcripts was 645

realized by Transcoder program (version 5.3.0, 646

https://github.com/TransDecoder/TransDecoder), and supplemented by the search of 647

the Pfam 32.0 database. Pfam annotations were built and annotated by HMMER from 648

Pfam 32.0 (Johnson et al., 2010) (https://pfam.xfam.org/). Pfam enrichment analysis 649

of ASGs was carried out by a custom Python script. 650

Identification of homeologous triplets and AS triplets in wheat 651

Wheat homeologous genes were first compared against each other using BLASTN 652

with e-value cutoff of 1e-5, and only candidate alignments with a minimum of 200 bp 653

sequence coverage and >90 % sequence identity were considered. Next, all the 654

aligned sequences were clustered, and only clusters that had exactly one 655

representative member from each subgenome and were located on similar position on 656

three chromosomes (triplets) were considered. Then, the AS types of triplet members 657

were analyzed, and if all three homeologous members possessed the same AS type at 658

similar sequence position, the triplet was classified as having the conservative AS 659

type. Otherwise, AS events occurring in all three triplet genes but showing 660

inconsistent type of splicing event or similar AS type but different splicing site 661

location were classified as different types of AS triplet. Visualization of homeologous 662

triplets was achieved by using circos version v0.69 (http://circos.ca/) and R package 663

ggtern (https://cran.r-project.org/web/packages/ggtern/index.html). 664

RT-PCR, Semi-RT-qPCR and RT-qPCR validation of AS events or genes 665

Total RNA treated with DNase I was reverse-transcribed with oligo-dT primers using 666

Reverse Transcriptase M-MLV (TaKaRa, Kusatsu, Shiga, Japan) following the 667

manufacturer’s instructions. RT-PCR was performed in a 10 μL reaction volume and 668

a primer pair for each gene was designed to amplify both splice variants (isoforms 1 669

and 2) in a single reaction. Then 2% w/v agarose gel electrophoresis was used to 670

demonstrate different isoforms. For semi-quantitative reverse transcription and 671

polymerase chain reaction, gene-specific primers across junctions were used to 672

amplify WEWv1_A_gene.90708.0 (Q), WEWv1_A_gene.112770.0 673

(AT4G31580/RSZ22) and WEWv1_A_gene.1336.0 (AT3G53500/RS2Z32). Wheat 674

β-ACTIN gene (WEWv1_A_gene.7189.0 /TraesCS1A02G179000) was chosen as an 675



25

internal control for normalization. The PCR conditions for the amplification were as 676

follows: 5 min at 94℃, followed by 32 cycles of 20s at 94℃, 30s at 58℃, and 20s at 677

72℃. RT-qPCR was performed using a CFX96 real-time PCR detection system and 678

SYBR Green Supermix solution (Bio-Rad, http://www.bio-rad.com/). Each sample 679

was quantified at least in triplicate and normalized using β-ACTIN as an internal 680

control. The gene-specific primers used in this research are listed in Supplemental 681

Data set S9. The visualization of gene structure and RNA-seq reads alignment results 682

was accomplished using IGV software (version 2.4.10) (Robinson et al., 2011). 683

Accession Numbers 684

Genes referenced in this article can be found in the Ensembl Plants 685 (https://plants.ensembl.org/index.html) under the following accession numbers in 686 Supplemental Data set S10. 687

Supplemental Data 688

Supplemental Figure S1. Determination of reference genome for different wheat 689

species based on unique read mapping rate. 690

Supplemental Figure S2. Schematic diagram representing the procedure of 691

alternative splicing identification. 692

Supplemental Figure S3. Structural sketches of different alternative splicing events 693

and their corresponding number and proportion in different wheat species. 694

Supplemental Figure S4. Expression analysis of AS-regulating genes after 695

domestication in diploid and tetraploid wheat. 696

Supplemental Figure S5. GO enrichment analysis of AS genes responsive to 697

domestication in diploid and tetraploid wheat. 698

Supplemental Figure S6. Verification of AS differences of splicing regulating genes 699

before and after domestication in diploid and tetraploid wheat. 700

Supplemental Figure S7. Display and validation of AS changes of the Q gene 701

(WEWv1_A_gene.90708.0) in response to domestication in diploid and tetraploid 702

wheat species. 703

Supplemental Figure S8. Display and validation of AS changes in response to wheat 704


Supplemental Figure S9. Expression variation of AS-regulating genes in response to 706

polyploidization in wheat. 707

Supplemental Figure S10. Comparison of alternative splicing events between 708

TAA10 and XX329. 709



26

Supplemental Figure S11. Differential expression level and alternative splicing 710

patterns of AS genes in wheat caused by the substitution of the D subgenome in 711

hexaploid wheat. 712

Supplemental Figure S12. AS conservation and partitioning among homeologs in 713

hexaploid wheat. 714

Supplemental Figure S13. Ternary plot showing AS partitioning among 715

homeologous genes with same AS type in triplets using WEWv1 and AETv4 as 716

reference genomes. 717

Supplemental Data set S1. Overview of RNA-seq data and reads mapping. 718

Supplemental Data set S2. Identified alternative splicing events from merged 719

RNA-seq mapping results. 720

Supplemental Data set S3. Alternative splicing events in each sample. 721

Supplemental Data set S4. PFAM and GO enrichment of alternative splicing genes. 722

Supplemental Data set S5. Domestication or polyploidization response AS events 723

and genes in wheat. 724

Supplemental Data set S6. Differentially expressed genes in this study. 725

Supplemental Data set S7. Pfam changes of domestication or polyploidization 726

responsive ASGs by IR. 727

Supplemental Data set S8. Homologous genes with only one copy on each 728

subgenome (triplet cluster) and their AS type in hexaploid wheat. 729

Supplemental Data set S9. Primers used in this research. 730

Supplemental Data set S10. Accession numbers of major genes mentioned in this 731

paper. 732

Acknowledgements 733

This work was supported by the Major Program of the National Natural Science 734

Foundation of China (31991210 and 91935304). 735



27

Figure legend and Supplemental Data set 736

Figure 1. Alternative splicing event identification in wheat species with different 737

ploidies. (A) Column diagram shows the number of assembled genes (yellow), 738

transcripts (light gray), alternative spliced genes (orange), and alternative splicing 739

transcripts (dark gray) on each subgenome. Pie charts represent the proportion of total 740

assembled genes with single-transcript or multi-transcripts. Green, blue, yellow, 741

brown and purple indicate genes with one, two, three, four and greater than five 742

transcripts. (B) Structural sketches of different alternative splicing events and their 743

corresponding number and proportion on each subgenome. IR: intron retention, ES: 744

exon skipping, A5: alternative 5’ donor site, A3: alternative 3’ acceptor site, FE: 745

alternative first exon, LE: alternative last exon, ME: mutually exclusive exons. AS: 746

alternative splicing. 747

Figure 2. Characterization of alternative splicing genes in wheat species with 748

different ploidies. (A) Density distribution of PSI of alternative splicing events. A 749

large portion of ASGs with low PSI values indicate that these genes express one 750

major transcript. (B) The top ten significantly enriched Pfam domains in AS genes 751

ranked by hypergeometric test. Red broken line represents calculated –log10 752

(P-value). Dark gray and light gray bars represent the observed and the expected AS 753

gene number, respectively. (C) Density distribution of GC content between skipped 754

exons (1,395) and other exons (328,525), as well as between retained introns (9,226) 755

and other introns (249,641) (Student's t-test, P-value < 0.001, marked with “***”). 756

The vertical dashed lines represent the average value of the data corresponding to 757

each color. (D) The comparison of length of skipped exons (1,395) and other exons 758

(328,525) as well as retained introns (9,226) and other introns (249,641) (Student's 759

t-test, P-value < 0.001, marked with “***”). The horizontal solid line represents the 760

median length of the exon or intron in the AS event, and the horizontal dashed line 761

represents the median length of counterparts. 762

Figure 3. Chromosome distribution of AS genes in wheat species with different 763

ploidies. (A-B): Chromosome distribution of AS genes in hexaploid wheat (A) as well 764

as in diploid and tetraploid wheat species (B). Lane a: chromosome visualization; 765

Lane b: chromosome distribution of high-confidence annotated genes per Mb from 766

reference genome; Lane c: density histogram of assembled genes per 500kb from our 767

transcriptome sequencing data; Lane d: distribution of AS genes per 500Kb along 768

chromosome; Lane e. Conservation of alternative splicing between homeologous 769

genes. Yellow line in panel A indicates that AS patterns are conserved among all 770

three homoelogs of hexaploid. Gray line in panel A indicates that AS patterns are 771

conserved in only two homeologs of hexaploid. Yellow line in panel B represents that 772

AS patterns are conserved in tetraploid wheat. AS: alternative splicing. 773

Figure 4. AS changes in diploid and tetraploid wheat. (A) Histogram showing the 774

number of AS events in Triticum boeoticum (AA2), Triticum monococcum (AA11), 775



28

Triticum dicoccoides (IW136) and Triticum dicoccum (DM4). The Venn diagram at 776

the top shows the comparison of ASGs between diploid or tetraploid wheat. (B) The 777

number of AS events in response to domestication in diploid and tetraploid wheat, 778

including lost AS events (red), new AS events (blue), QDASE (green) and ATI 779

(yellow) after domestication. QDASE: quantitative differential alternative splicing 780

event, ATI: altering transcript isoform, ASE: alternative splicing event. (C): Display 781

and validation of AS changes in response to domestication in diploid wheat. AA2, 782

AA4, AA15, AA21 and AA1 represent wild diploid accessions, whereas AA11, 783

AA19, AA28, AA30 and AA31 represent domesticated diploid wheat accessions. (D): 784

Display and validation of AS changes in response to domestication in tetraploid wheat. 785

IW136, IW92, IW95, IW47, IW104 represent wild tetraploid accessions, whereas 786

DM4, Z39, CX03, CX04 and CX05 represent domesticated tetraploid wheat. The gray 787

(isoform1) and black (isoform2) squares in the upper panel represent the structure and 788

transcriptional direction of different isoforms of AS genes. The lower panel shows the 789

results of RNA-seq data mapping at gene splicing sites and the number of normalized 790

junction supporting reads of different isoforms. The red arrows represent the location 791

and direction of primers (F: forward, R: reverse) designed for RT-PCR, and agarose 792

gel electrophoresis on the right verifies the alternative splicing. (E-F): Comparison of 793

density distribution of PSI before and after domestication in diploid (E) and tetraploid 794

(F) wheat. P-value was calculated using the Kolmogorov-Smirnov test. Blue: wild 795

wheat, red: cultivated wheat. PSI: Percent spliced index measures expressed 796

proportion of transcripts that include a specific exon or splice site. 797

Figure 5. AS changes in response to wheat polyploidization. (A) The number of AS 798

events in TAA10, ETW, TQ18 and XX329. Allohexaploid XX329 was resynthesized 799

by the maternal parent ETW and the paternal parent TQ18. ETW was ploidy-reversed 800

from hexaploid cultivar wheat TAA10 with high karyotype stability, produced by 801

recurrent backcrossing. (B) The number of polyploidization responsive AS events in 802

wheat, including lost AS events, new AS events, QDASE and ATI. QDASE: 803

quantitative differential alternative splicing event, ATI: altering transcript isoform, 804

ASE: alternative splicing event, AS: alternative splicing. (C) Comparison of density 805

distribution of PSI before and after wheat polyploidization. PSI: Percent spliced index. 806

P-value was calculated using the Kolmogorov-Smirnov test. Blue: before 807

polyploidization, red: after polyploidization. (D) GO enrichment analysis of AS genes 808

responsive to polyploidization. The color scale from white (low) to dark red (high) 809

represents differential log10(P-value) of GO enrichment , and only significantly 810

enriched terms (P-value < 0.05) are indicated. 811

Figure 6. AS partitioning among homeologs in hexaploid wheat. (A) The number of 812

AS events identified in TAA10 (green), TKM (blue) and CS (red). A, B and D 813

represent subgenomes in wheat. (B) Comparison of AS patterns of homeologs among 814

TAA10, TKM, and CS. Light gray: triplet with only one or two AS homeologs; light 815

green or light blue or light red: AS triplets with different splicing types; green or blue 816



29

or red: AS triplets with same splicing types. Venn diagram shows conservation of AS 817

triplets with same splicing type in three genotypes of hexaploid wheat. (C): Ternary 818

plots show AS partitioning among homeologous genes with same AS type in 819

hexaploid wheat (TAA10: 243, TKM: 220, CS: 181). Each dot represents a triad’s 820

coordinate based on the PSI value. Dark brown: balanced triplets; Dark green: A 821

subgenome dominant; Bright green: A subgenome suppressed; Deep red: B 822

subgenome dominant; Light red: B subgenome suppressed; Dark purple: D 823

subgenome dominant; Light purple: D subgenome suppressed. AS: alternative 824

splicing. 825

826

827



30

828

829



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Short title: Alternative splicing in wheatOct 13, 2020 · 106 observed in polyploidization...

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