1 running title: a hexaploidization in durian€¦ · 12/11/2018 · 116 (wang et al., 2015; wang...

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Running Title: A hexaploidization in durian 1

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Corresponding author information: 3

Xiyin Wang 4

School of Life Sciences and Center for Genomics and Computational Biology, North 5

China University of Science and Technology, Tangshan, Hebei 063210, China 6

Tel: 86-0315-3721512 7

E-mail: [email protected] 8

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Plant Physiology Preview. Published on November 12, 2018, as DOI:10.1104/pp.18.00921

Copyright 2018 by the American Society of Plant Biologists

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Title: Recursive paleohexaploidization shaped the durian genome 10

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Authors: Jinpeng Wang, Jiaqing Yuan, Jigao Yu, Fanbo Meng, Pengchuan Sun, 12

Yuxian Li, Nanshan Yang, Zhenyi Wang, Yuxin Pan, Weina Ge, Li Wang, Jing Li, 13

Chao Liu, Zhiyan Xi, Yuhao Zhao, Sainan Luo, Dongcen Ge, Xiaobo Cui, 14

Guangdong Feng, Ziwei Wang, Lei Ji, Jun Qin, Xiuqing Li, Xiyin Wang* 15

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School of Life Sciences, North China University of Science and Technology, 17

Caofeidian Dist., Tangshan, Hebei 063210, China (J.W., J.Yuan, J.Yu, F.M., P.S., 18

Y.L., N.Y., Z.Y.W., Y.P., W.G., L.W., J.L., C.L., Y.Z., S.L., D.G., X.C. and X.W.); 19

Center for Genomics and Computational Biology, North China University of Science 20

and Technology, Caofeidian Dist., Tangshan, Hebei 063210, China (J.W., J.Yuan, 21

J.Yu, F.M., Y.L., N.Y., Z.Y.W., Y.P., W.G., L.W., J.L., C.L., Y.Z., G.F., Z.W.W., L.J. 22

and X.W.); Cereal & Oil Crop Institute, Hebei Academy of Agricultural and Forestry 23

Sciences No. 162, Hengshanjie Street, Shijiazhuang, 050035, China (J.Q.); 24

Fredericton Research and Development Centre, Agriculture and Agri-Food Canada, 25

Fredericton, New Brunswick, E3B 4Z7, Canada (X.L.) 26

*Address correspondence to Xi-Yin Wang (Email: [email protected]). 27

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One-sentence summary: Durian genome reanalysis revealed a durian-specific 29

hexaploidization and a decaploidization in the cotton lineage that increased its 30

evolutionary rate, explaining a previous misinterpretation. 31

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mailto:[email protected]


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Footnotes: 33

We appreciate financial support from the Ministry of Science and Technology of the 34

People’s Republic of China (2016YFD0101001), the National Science Foundation of 35

China (31371282 to X.W., 31510333 to J.W. and 31661143009 to X.W.), the 36

National Natural Science Foundation of Hebei Province (C2015209069 to J.W.), the 37

Graduate Student Innovation Fund of North China University of Science and 38

Technology (2018S42 to J.Yuan), and the Tangshan Key Laboratory Project to X.W.. 39

40

Author contributions 41

X.W. conceived and led the research. J.W. implemented and coordinated the analysis. 42

J.Yuan, J.Yu, F.M., P.S., Y.L., N.Y., Z.W., Y.P., W.G., L.W., J.L., C.L., Z.Y.X., Y.Z., 43

S.L., D.G., X.C., G.F., Z.W.W., and L.J. performed the analysis. J.Q. contributed to 44

plant phylogeny reconstruction. X.L. contributed to useful discussion and 45

modification to the manuscript. X.W., J.W., and X.L. wrote the paper. 46

47

Competing interests 48

The authors declare no competing financial interests. 49

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ABSTRACT 51

The durian (Durio zibethinus) genome has recently become available and analysis of 52

this genome reveals two paleopolyploidization events previously inferred as shared 53

with cotton (Gossypium spp.). Here, we reanalyzed the durian genome in comparison 54

with other well-characterized genomes. We found that durian and cotton were actually 55

affected by different polyploidization events: hexaploidization in durian ~19-21 56

million years ago (mya) and decaploidization in cotton ~13-14 mya. Previous 57

interpretations of shared polyploidization events may have resulted from the elevated 58

evolutionary rates in cotton genes due to the decaploidization and insufficient 59

consideration of the complexity of plant genomes. The decaploidization elevated 60

evolutionary rates of cotton genes by ~64% compared to durian and explained a 61

previous ~4 fold over dating of the event. In contrast, the hexaploidization in durian 62

did not prominently elevate gene evolutionary rates likely due to its long generation 63

time. Moreover, divergent evolutionary rates likely explain 98.4% of reconstructed 64

phylogenetic trees of homologous genes being incongruent with expected topology. 65

These findings provide further insight into the roles played by polypoidization in the 66

evolution of genomes and genes and suggests revisiting existing reconstructed 67

phylogenetic trees. 68

69

Keywords: Durian, Genome, Cotton, Cacao, Grape, Polyploid 70

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5

INTRODUCTION 73

Durian (Durio zibethinus), belonging to the Helicteroideae subfamily in the 74

Malvaceae family, grows in Southeast Asia and produces fruits with a unique taste 75

and aroma. Recently, its genome has been deciphered (Teh et al., 2017). Plant 76

genomes often have complex genome structure, mainly due to recursive 77

polyploidization and following genome DNA repatterning (Proost et al., 2011; 78

Schnable et al., 2011; Jiao et al., 2012; Paterson et al., 2012). For a newly sequenced 79

genome, comparison to its well-characterized relative plant genomes helps 80

deconvolute its genome structure and evolutionary history (Schnable et al., 2011; 81

Freeling et al., 2012; Murat et al., 2014; Wang et al., 2016). Before the sequencing of 82

the durian genome, the genomes of two Malvaceae plants had been available, 83

including cotton (Gossypium raimondii, G. hirsutum and G. raimondii ) (Li et al., 84

2012; Paterson et al., 2012; Wang et al., 2012) and cacao (Theobroma cacao) (Argout 85

et al., 2011). Cotton was affected by recursive polyploidization events, including a 86

core-eudicot-common hexaploidization (ECH) and a decaploidization shared by 87

different Gossypium plants (Paterson et al., 2012; Wang et al., 2016). Cacao was not 88

affected by the decaploidization, which means that a cacao (and grape, Vitis vinifera) 89

genomic region would have 5 orthologous regions in cotton diploid (or 90

paleodecaploid) D genome (G. raimondii; orthology ratio 1:5) (Wang et al., 2016). 91

Recently, a comparison of these three genomes showed appreciable gene 92

synteny, and a polyploidization, previously referred to as whole-genome duplication 93

(WGD), was proposed to have occurred during the durian evolution after the ECH 94

(Teh et al., 2017). By characterizing the divergence of syntenic genes produced by the 95

polyploidization in cotton and in durian, orthologous genes were identified between 96

the two genomes and paralogs in each of them. A comparison of sequence divergence 97

showed that the polyploidy-produced paralogs within cotton or durian each predated 98

the cotton-durian orthologs. This was affirmed by a statistical test with posterior 99

probability >= 0.9981. Therefore, it was proposed that durian and cotton share 100 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by

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polyploidization events (other than ECH) that likely occurred before their divergence 101

after ECH and places the known cotton-polyploidization also in the durian lineage 102

(Teh et al., 2017). The authors publishing the durian genome did not mention whether 103

the polyploidization in cotton resulted in decaploidy and used WGD to refer to the 104

event (Teh et al., 2017). 105

Recursive polyploidization could render unexpected complexity of plant 106

genomes and provide enormous evolutionary forces still not fully understood (Charon 107

et al., 2012; Kim et al., 2014; Liu et al., 2014). After each event, there could be 108

whole-genome level repatterning with DNA repacked into smaller numbers of 109

chromosomes (Wang et al., 2016) and large-scale DNA losses with often only a small 110

fraction of duplicated genes retained (Lin et al., 2014; Wang et al., 2017), possibly 111

through a diploidization process. Fortunately, these retained hundreds of duplicates in 112

synteny (or colinearity) often can help infer the event and let us gauge its ploidy 113

nature, occurrence times and dates (Bowers et al., 2003; Abrouk et al., 2010). Because 114

of reducing selective constraint, these duplicated genes often evolve at a faster pace 115

(Wang et al., 2015; Wang et al., 2016; Wang et al., 2017). Recently, a re-analysis of 116

cucurbit genomes using a sophisticated pipeline revealed an overlooked 117

tetraploidization occurred ~92-105 million years ago (mya), likely having contributed 118

to the establishment of the plant family – Cucurbitaceae - one of the largest on Earth 119

(Wang et al., 2018). The pipeline features homologous gene dotplotting and 120

hierarchical identification of homologous genes produced by sequential evolutionary 121

events. 122

Here, we re-analyzed the durian genome using that a recently proposed 123

pipeline in comparison with other Malvaceae species (cacao and cotton [G. 124

raimondii]) and the grape genome, which preserved much of the genome structure of 125

the eudicot-common ancestor. The aim of this study was to investigate whether durian 126

and cotton have shared or unshared polyploidization, to discover factors causing the 127

overlook of certain paleopolyploidization, and to estimate the consequence of the 128 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



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overlook on polyploidization-caused changes of gene evolutionary rates on the 129

credibility of reconstructed phylogenetic trees. 130



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RESULTS 131

Inference of colinear genes 132

By using ColinearScan, we inferred colinear genes within each genome 133

(Supplemental tables S1-2). We inferred 10,465 durian colinear gene pairs, 134

involving 13,062 genes on 451 paralogous blocks, each having at least 4 colinear 135

genes. We characterized the synonymous substitution divergence (Ks) between each 136

colinear gene pair, which showed a clear bimodal structure with two distinct sets, one 137

with Ks distribution peaking at 0.24 (+/-0.03) and another peaking at 1.38 (+/-0.16) 138

(Fig. 1A), indicating at least two large-scale genomic duplication events. We also 139

inferred colinear genes and characterized Ks distribution in other plant genomes 140

(Supplemental table S1 and S2). The Ks distribution of cotton paralogs also showed 141

a bimodal structure, having peaks at 0.52 (+/-0.12) and ~1.57 (+/-0.2) (Fig. 1A and 142

Supplemental table S3). The peaks with larger Ks values in both durian and cotton 143

genomes correspond to the ECH, as repeatedly reported previously (Jaillon et al., 144

2007; Paterson et al., 2012; Wang et al., 2016). Comparatively, the cotton event with 145

Ks ~ 0.52 was previously reported to be decaploidization (Wang et al., 2016) and 146

seems to have occurred much earlier than the durian event with Ks ~ 0.24. 147

We inferred colinear genes between different genomes and the corresponding Ks 148

values (Supplemental table S1 and S2). For example, there were 41,958, 80,299, 149

32,699 colinear genes from 2,630, 5,576, and 2,303 homologous blocks between 150

durian and cacao, cotton, and grape, respectively. The Ks distribution between durian 151

and each of the cacao and cotton genomes had a bimodal structure, with one 152

corresponding to the split between two genomes and the other to the shared ECH 153

event (Fig. 1A). 154

Homologous gene dotplotting 155



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By mapping grape gene sequences onto the durian genome using BLAST, we 156

constructed the homologous dotplot by running genomic dotplotting software. Among 157

the detected homologous genes, orthologs or paralogs were determined jointly by 158

BLAST identity and dotplot status. The ratio of the number of probe genes to the 159

number of targeted orthologous genes was defined as the orthology ratio. The ratio of 160

the number of probe genes to the number of targeted outparalogous genes was defined 161

as outparalogy ratio. The rationale of using these ratios to estimate the ploidy levels is 162

as follows: A reference genome is a haploid genome. Therefore, a hexaploid genome 163

has three homologous sequences in the reference genome. If there is no further 164

polyploidization in two eudicot species after the ECH, one of the three sequences in 165

the reference genome is the ortholog and the other two are outparalogs. Therefore, if 166

there was no further polyploidization in durian after the shared hexaploidization (i.e., 167

the ECH), we would expect an orthology ratio 1:1 and an outparalogy ratio 1:2 when 168

we use a grape gene sequence to dotplot with the durian reference genome. The 169

outparalogy was established due to the shared ECH (Fig. 2A and 2B). If there was a 170

durian-specific whole-genome duplication in durian, we would expect an orthology 171

ratio 1:2 and an outparalogy ratio 1:4 (Fig. 2C). If there was a durian-specific 172

whole-genome triplication, we would expect an orthology ratio 1:3 and an 173

outparalogy ratio 1:6 (Fig. 2D). If orthologous region(s) were identified, a transitive 174

paralogy between the grape chromosomes would easily help find outparalogous 175

regions in durian. However, owing to wide-spread gene losses, outparalogous blocks 176

may be much reduced in colinear gene numbers. The other variant situations of 177

polyploidization in durian could also be inferred in a similar manner. In the meantime, 178

inferred colinear genes were mapped onto the homologous gene dotplots with median 179

Ks of each colinear block displayed. This helped distinguish orthologous blocks and 180

outparalogous blocks between different genomes, or paralogous blocks produced by 181

recent events from the ancient ones within each genome. 182



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The actual results that we obtained in the homologous gene dotplotting 183

between grape and durian genomes showed an orthology ratio of 1:3 and outparalogy 184

ratio of 1:6 (Fig. 3A and Supplemental Fig. S1). There were two distinct groups of 185

homologous blocks, with one group with Ks values mostly < 0.95, and the other 186

group mostly > 1.30. A bimodal Ks distribution shown above clearly indicated the 187

former group was produced by orthology and the latter by the shared ECH. For the 188

orthologous blocks, a grape chromosome region often has three independent 189

correspondence in durian (Fig. 3A and Supplemental Fig. S1), implying an 190

orthology ratio of 1:3. This means that a whole-genome triplication or 191

hexaploidization occurred in the durian lineage. This durian lineage whole-genome 192

triplication converted the then likely “diploid” genome to a “hexaploid” genome, and 193

this ancient after-ECH event resulted in a new hexaploidization. The peak on the Ks 194

distribution curve for the paleodecaploidization in cotton is very sharp, suggesting 195

that the decaploidization occurred during a relatively short period. Data in Fig. 1A 196

clearly indicates that this hexaploidization in the durian lineage is obviously not the 197

decaploidization that occurred in the cotton lineage. 198

Furthermore, we drew the homologous dotplotting between durian and two 199

Malvaceae relatives. The durian-cacao gene dotplotting showed a similar observation 200

as in grape, with orthology ratios of 1:3 (Fig. 3B and Supplemental Fig. S2), further 201

supporting a hexaploidization in durian. The durian-cotton (G. raimondii) gene 202

dotplotting showed likely an orthology ratio of 3:5 (Figs 2E-2F and Fig. 3C; 203

Supplemental Fig. S3). 204

In summary, the inference with three reference genomes consistently suggests 205

a durian-specific hexaploidization (DSH), independent of a Gossypium-specific 206

decaploidization (GSD). 207

Evolutionary rates and dates 208



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The GSD-produced duplicated genes had Ks values much larger than those of 209

cotton-cacao (0.41+/-0.08) and cotton-durian (0.38+/-0.06) orthologs. This can only 210

be explained by the possibility that cotton gene evolution became much faster after 211

the GSD. The previous section already concluded that both GSD and DSH events 212

occurred after the split of durian and cotton and after their common ancestor’s split 213

from cacao. Cacao is a close outgroup of durian and cotton, and therefore we used it 214

to evaluate the evolutionary rate difference between the two plants. The Ks 215

distribution of cacao-durian orthologs peaked at 0.25 (+/-0.03), showing that after 216

their split from cacao, cotton evolved ~64% faster than durian. 217

To date the hexaploidization event in the durian lineage, we performed 218

evolutionary rate correction to the evolutionary rates of cotton and durian duplicates 219

(Figs 1C-1D and Supplemental table S4). Here, different from previous practice 220

(Wang et al., 2015; Wang et al., 2017), we performed a two-step rate correction. In 221

the first step, we managed to correct evolutionary rate by aligning the Ks distributions 222

of durian, cotton, and cacao ECH duplicates to that of grape ECH duplicates, which 223

have the smallest Ks values. However, we found the first step correction was not 224

enough, in that the cotton rate was still elevated as compared to durian, which 225

occurred after their split with cacao. Therefore, we performed a second step correction 226

by aligning Ks distribution of cotton-cacao orthologs to that of durian-cacao orthologs 227

(see Methods for details). 228

Eventually, we found that the DSH paralogs had a corrected Ks distribution 229

peaking at 0.17 (+/-0.03). Notably, the cotton decaploidy-produced paralogs had a 230

corrected Ks distribution peaking at 0.12 (+/-0.03), showing that the decaploidy was 231

younger than the recent hexaploidization in durian. Eventually, assuming that the 232

ECH occurred ~115-130 mya (Vekemans et al., 2002; Jiao et al., 2012), the DSH was 233

inferred to have occurred ~19-21 mya, and the GSD ~13-14 mya. In addition, the 234

durian-cotton split was inferred to have occurred ~20-22 mya, and they split ~21-24 235

mya from cacao (Figs 1C-1D). 236 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



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Genome alignment and fractionation 237

By checking homologous gene dotplot and Ks values, we separated durian 238

paralogs produced by the ECH and the durian-specific hexaploidization. According to 239

this analysis, the younger event created 10,367 paralogs, forming 6,181 pairs, 240

preserved in the present genome, as compared to the ECH-produced 5,473 forming 241

3,299 pairs. Then, we managed to map the durian colinear genes in homologous 242

blocks on to cacao and grape genomes. This produced whole-genome-level alignment 243

(Fig. 4 and Supplemental Figs S4-S5), which showed wide-spread genomic 244

fractionation in different genomic regions and chromosome rearrangement in each 245

genome. A slice of the genome-level alignment can be closed displayed to highly 246

fractionated homologous regions between genomes and in each genome (Fig. 5). As 247

for the 32,862 cacao genes, 61% had no corresponding colinear genes in all three 248

paralogous durian regions. We also counted missing genes in durian as compared to 249

the other two referenced genomes. Cotton was also involved in the mapping analysis 250

(Fig. 4 and Supplemental Figs S4-S5). 251

As to the referenced 19 grape chromosomes (or 10 cacao chromosomes), we 252

compared the genes colinear to the referenced chromosomes in tripled durian regions 253

(dz1, dz2, dz3) and the penta-pled cotton regions (gr1, gr2, …, gr5). We checked all 3 254

x 5 combinations to see whether durian-cotton pair shared significantly better 255

similarity than others. We adopted a statistic (dz x gr)/gr to measure the similarity. 256

The best-matched regions had only an averaged similarity of 65.6%, a mere 5.8% 257

higher than the secondary matched regions with grape as reference (Supplemental 258

table S5). Similar results were shown with cacao as the reference genome 259

(Supplemental table S6). Grossly, this shows diverged colinear gene content in any 260

compared durian and cotton homoeologous regions. Moreover, this further supports 261

our conclusion above that durian and cotton were independently affected by different 262

recent polyploidization events. If the corresponding durian-cotton regions had shared 263



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an ancestor for a period after recent polyploidy, the statistics would be quite high, 264

even near 1, if little lineage-specific gene loss occurred after their split, and much 265

better than other combinations of comparison. 266

Distorted gene tree topology due to elevated evolutionary rates 267

We constructed evolutionary trees of homologous genes in colinear positions in the 268

involved four genomes, and based on gene colinearity, we inferred their relationship 269

related to speciation and polyploidization. However, we found few trees with an 270

expected tree topology (Fig. 6). Trees were constructed for 511 groups of homologs, 271

and each group had one grape gene as the outgroup, one cacao ortholog, at least three 272

cotton orthologs, and at least 2 durian orthologs. The cacao ortholog was expected to 273

be the outgroup of the durian and cotton orthologs. As to its actual location, the trees 274

can be classified in to four groups (Fig. 6). Astonishingly, we found only 1.6% of 275

constructed trees were of the expected topology, and the majority with the cacao 276

ortholog clustered with the durian (56.9%) or the cotton orthologs (23.5%). This 277

finding that 98.4% of reconstructed trees did not meet the evolutionary phylogeny is 278

surely due to the elevated evolutionary rates after the polyploidization events in cotton 279

and durian lineages. The analysis of these trees provided further evidence of 280

separating occurrence of the DSH and GSD. Shared hexaploidization would likely 281

result in a 1:1 correspondence between cotton and durian genes in a reconstructed 282

phylogenetic tree of syntenic genes. In contrast, separated events, hexaploidization in 283

durian lineage and decaploidization in cotton lineage, would likely result in cotton 284

and durian genes to form different clusters on the tree. We checked trees constructed 285

for cotton and durian genes with cacao and grape genes as references. Considering 286

only branches with >70% bootstrapping percentage, we found cotton or durian genes 287

formed clusters in 53.3% trees (270 of 507), whereas only 0.4% (2/507) had 1:1 288

correspondence. Besides, we used the other four approaches, including maximum 289

likelihood, minimum evolution, UPGMA (Unweighted Pair-group Method With 290 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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Arithmetic Means), and maximum parsimony, provided by using MEGA (Molecular 291

Evolutionary Genetics Analysis), to construct 2028 trees in total, and obtained similar 292

results as above with the neighbor-joining approach (separate clusters: 41.2%, 62.5%, 293

82.4%, and 33.3%, as compared with 0.6%, 0.8%, 1.4%, and 0.4%, respectively). 294

Different means of tree construction resulted in consistent findings. This fact strongly 295

supports a separating occurrence of hexaploidization and decaploidization on different 296

lineages. 297

Polyploidization contributed to aroma gene expansion 298

Methionine γ-lyase (MGL) and aminocyclopropane-1-carboxylic acid 299

synthase (ACS) contribute to the formation of durian aroma (Teh et al., 2017). Here, 300

we found that the two recursive hexaploidization events (both ECH and DSH) 301

contributed to their expansion. The four MGL genes were all in colinear positions 302

with one another. A close check of gene colinearity found that there had been one 303

copy in the common ancestor of durian, cotton, and cacao, which duplicated in the 304

DSH to make triplicated copies in the ancestral durian genome. One of the triplicated 305

copies produced a tandem pair. This means that the DSH contributed to 75% of the 306

MGL expansion. There are 73 ACS genes in the durian genome, and 58 (70.5%) were 307

remnants of the ECH, and 62 (84.93%) resulted from further expansion during the 308

DSH. Comparatively, only 24 (32.9%) were ever affected by single-gene duplication 309

after the DSH. 310

311

DISCUSSION 312

Here, based on the pipeline reported previously to decipher complex genomes (Wang 313

et al., 2018), we inferred hexaploidization in the durian lineage, independent of the 314

decaploidization in the cotton lineage (Wang et al., 2016). The pipeline firstly features 315

the production of homologous gene dotplots within a genome or between genomes. 316

The homologous gene dotplots help distinguish orthologs from outparalogs, or 317 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


15

separate paralogs produced by sequential polyploidization events in a genome. The 318

homologous gene dotplotting approach was initially used to decipher recursive 319

polyploidization in the Arabidopsis (Arabidopsis thaliana) genome (Bowers et al., 320

2003) and was adopted to understand many other complex plant genomes (Jaillon et 321

al., 2007; Wang et al., 2011; International Tomato Genome Sequencing Consortium, 322

2012; Chalhoub et al., 2014; Wang et al., 2016). The pipeline also features integration 323

of Ks between colinear genes into the homologous dotplot, providing more resolution 324

of homologous blocks produced by different evolutionary events. A use of the 325

pipeline revealed an overlooked tetraploidization in the common ancestor of 326

Cucurbitaceae plants (Wang et al., 2018). The publication of the durian genome did 327

not use homologous dotplotting to distinguish homologous regions between genomes 328

and involving all paralogs in durian genome to estimate Ks (Teh et al., 2017). The 329

conclusion of a shared polyploidization in durian and cotton (Teh et al., 2017) is due 330

to overlooking the divergence in evolutionary rates, observed previously in different 331

plants (Paterson et al., 2012; Wang et al., 2015; Wang et al., 2017). 332

Divergent evolutionary rates of plant genes cause problems in phylogenetic 333

and evolutionary analysis. In the grass family, it was proposed that barley (Hordeum 334

vulgare), sorghum (Sorghum bicolor), and maize (Zea mays) evolved 12-33% faster 335

than rice (Oryza sativa), which preserved the most conservative genome (Wang et al., 336

2015). If assuming a common evolutionary rate of genes, this would have resulted in 337

divergent dating of the shared tetraploidization using duplicated genes in different 338

grasses. With grape orthologs as references, a comparison of cacao and cotton genes 339

showed that the cotton genes evolved 19% and 15% faster than their cacao orthologs 340

at the synonymous and nonsynonymous substitution sites, respectively (Paterson et al., 341

2012). The elevated evolutionary rate in cotton resulted in more divergence between 342

cotton paralogs than their divergence from cacao orthologs. The higher evolutionary 343

rate in cotton than in cacao (no polyploidization after split) was at least partly 344

attributed to the occurrence of the polyploidization in cotton as elevated evolutionary 345 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



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rate of genes was also observed in other paleopolyploidies (Wang et al., 2011). The 346

GSD was inferred to have occurred only ~13-24 mya, rather than~59 mya as reported 347

previously. This was likely caused by insufficient correction to Ks by referencing to 348

the quite anciently diverged grape genes in previous analysis (Paterson et al., 2012; 349

Wang et al., 2016). Besides, we found that, though affected by another 350

hexaploidization after ECH, the durian evolved at similar rate or slightly faster than 351

cacao but much slower than cotton. This might be because durian is a tree with a long 352

generation time, and a long generation time may lead to reduced evolutionary rate, as 353

observed in poplar (Populus trichocarpa) (Tuskan et al., 2006). 354

As to our further analysis, elevated evolutionary rate resulted in problematic 355

reconstruction of phylogenetic trees. As shown above, we inferred 98.4 % of trees of 356

durian and cotton homologs could have a topology failing to reflect their actual 357

relationship. We tested the phylogeny reconstruction using both DNA and protein 358

sequences, and tested different phylogenetic analysis approaches, e.g., 359

neighbor-joining and maximal likelihood, and eventually we obtained similar error 360

rates of tree topology (Supplemental tables S7-S8). This means when genes evolved 361

at divergent rates, no matter which tree construction approach was adopted, one could 362

not reconstruct a credible tree. Here, the inference of gene colinearity provided a 363

precious means to infer a credible tree, showing their true relationship by relating to 364

evolutionary events producing the homology relationship. 365

MATERIALS AND METHODS 366

Materials 367

Genome data was retrieved from public databases: durian (Durio zibethinus) genome 368

(v1.0) was from Genbank (https://www.ncbi.nlm.nih.gov/genome/?term=Durian), 369

grape (Vitis vinifera; v12X) and cotton D (Gossypium raimondii) genomes from 370


https://www.ncbi.nlm.nih.gov/genome/?term=Durian


17

phytozome (v2.1) (https://phytozome.jgi.doe.gov/), and cacao (Theobroma cacao) 371

genome (v2) from CocogenDB (http://cacaogendb.cirad.fr/). 372

Colinearity inference 373

Colinear genes were inferred by using ColinearScan with maximal gap length 374

between neighboring genes in colinearity along a chromosome region < 50 genes, a 375

setting often adopted in previous inferences (Wang et al., 2006). All the homologous 376

blocks with >= 4 colinear gene pairs were output for further analysis (Wang et al., 377

2018). Putative homologous genes based on BLASTP search were used as input 378

(E-value <= 1e-5), and a relatively loose threshold here was used to help find much 379

diverged colinear gene pairs. The significance of colinearity was tested statistically by 380

ColinearScan. 381

Homologous gene dotploting 382

Dotplots were produced by implementing the MCSCAN (Multiple Genome 383

Colinearity Scan) toolkit from the online database PGDD (Plant Genome Duplication 384

Database) (http://www.plantgenome.uga.edu/pgdd/). 385

Ks calculation, distribution fitting, and correction 386

Synonymous nucleotide substitutions on synonymous sites (Ks) were estimated by 387

using the Nei-Gojobori approach (Nei and Gojobori, 1986) implemented using the 388

Bioperl Statistical module. 389

Kernel smoothing density function ksdensity (width is generally set to 0.05) in 390

Matlab was used to estimate the probability density of each Ks list to obtain the 391

density distribution curve. Then, Gaussian multi-peak fitting of the curve was inferred 392

by using the gaussian approximation function Gaussian in the fitting toolbox cftool. 393

R-squared, a parameter to evaluate the goodness of fit, was set to at least 95%, the 394 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by


https://phytozome.jgi.doe.gov/

http://cocoagendb.cirad.fr/


18

smallest number of normal distributions was used to represent the complex Ks 395

distribution, and the principle one was used to represent the corresponding 396

evolutionary event. 397

To correct the evolutionary rates of ECH-produced duplicated genes, the 398

maximum likelihood estimate μ from

inferred Ks means of ECH-produced 399

duplicated genes were aligned to have the same value of that of grape, which evolved 400

the slowest. Supposing a grape duplicated gene pair to have Ks value is a random 401

variable ),(:2

GGGX ，and for a duplicated gene pair in another genome the Ks to 402

be ),(:2

iiiX , the relative difference was: 403

( ) i G Gr μ μ / μ . 404

To get the corrected 2,:

correctionicorrectionicorrectioniX ，the correction 405

coefficient was defined as: 406

i correction Gi

i i

μ μλ

μ μ, 407

and 1

1

Gi correction i i

i

μμ μ μ

μ r. 408

If 409

1=

1+iλ

r

410

then 411

2,:

ii iicorrectioniX 412

To calculate Ks of homologous gene pairs between two plants, i, j ，and 413

supposing the Ks distribution was 2,:

ijijjiX , the algebraic mean of the 414

correction coefficients from two plants was adopted as 415

( ) 2 ij i jλ λ λ / ， 416



19

then, 417

22,:

ijij ijijcorrectionjiX . 418

Specifically, when one the plant is grape, for the other plant, i 419

22,:

iGi iGicorrectionGiX . 420

Cotton genes evolved much faster than durian genes due to 421

paleodecaploidization. Even after a correction of Ks of ECH-produced genes, 422

durian-cacao and cotton-cacao homologs still had very divergent distribution. 423

Therefore, a further round of corrections was applied by aligning cotton-cacao and 424

durian-cacao distributions to have the same distribution means. Supposing GSD 425

duplicates had ECH-corrected Ks distribution of 2,:

CCCX , as compared to the 426

DSH duplicates’ Ks distribution of 2,:

DDDX , the correction coefficient would 427

be sλ . Aligning the cotton-cacao and durian-cacao ECH-corrected distributions 428

resulted in 429

1

2

sTC TD

λμ μ 430

2 1 TDs

TC

μλ

μ 431

then: 432

22,: CSCScorrectionCX 433

Similar to the above correction, 434

22

2

1,

2

1: TC

sTC

scorrectionTCX

, 435

and

22

2

1,

2

1: CD

sDC

scorrectionGDX

436

1

2

scd correction cd

ck k

. 437



20

438

439

Tree construction 440

Trees of homologous genes in four genomes were constructed by implementing the 441

maximal likelihood approach in PHYML (Guindon et al., 2005) and the 442

neighboring-joining approach in PHYLIP using default parameter settings. 443

444

Accession Numbers 445

Sequence data from this article can be found in Materials. 446

447



21

SUPPLEMENTAL DATA 448

The following supplemental materials are available. 449

Supplemental Figure S1. Homologous dotplot between grape and durian genomes. 450

Supplemental Figure S2. Homologous dotplot between cacao and durian genomes. 451

Supplemental Figure S3. Homologous dotplot between cotton and durian genomes. 452

Supplemental Figure S4. Alignment of cacao and durian genomes. 453

Supplemental Figure S5. Alignment of grape and durian genomes. 454

Supplemental Table S1. Number of homologous blocks and gene pairs within a 455

genome or between genomes. 456

Supplemental Table S2. Number of homologous genes residing in blocks within a 457

genome or between genomes. 458

Supplemental Table S3. Kernel function analysis of Ks distribution related to 459

duplication events within each genome and between genomes (before evolutionary 460

rate correction). 461

Supplemental Table S4. Kernel function analysis of Ks distribution related to 462

duplication events within each genome and between genomes (after evolutionary rate 463

correction). 464

Supplemental Table S5. The similarity between tripled durian regions and 465

penta-pled cotton regions with grape as reference. 466

Supplemental Table S6. The similarity between tripled durian regions and 467

penta-pled cotton regions with cacao as reference. 468

Supplemental table S7. The tree topology in cotton and durian genes with cacao and 469

grape genes as references using five approaches. 470

Supplemental table S8. The tree topology rates in cotton and durian genes with 471

cacao and grape genes as references using five approaches. 472

473

ACKNOWLEDGEMENTS 474 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



22

We thank the researchers at iGeno Co. Ltd, China for their helpful discussion. 475

476

FIGURE LEGENDS 477

Figure 1. Original and corrected synonymous nucleotide substitutions (Ks) 478

between colinear genes. DSH: durian-specific hexaploidization; GSD: 479

Gossypium-specific decaploidization; ECH: core-eudicot-common 480

hexaploidization; Mya: million years ago. Continuous lines are used to show 481

Ks distribution in a genome, and dashed lines are between genomes. (A) 482

Distributions fitted by using original Ks values; (B) Inferred means; (C) 483

Distributions fitted by using corrected Ks values; (D) Inferred evolutionary 484

dates. 485

486

Figure 2. Species phylogeny and polyploidization occurrence models using 487

haploid reference genomes. For example, in subfigure C, the triplicated cacao 488

paralogs, C1, C2, C3, would each have one grape ortholog and two durian 489

orthologs. Non-orthology homologs between genomes were defined as 490

outparalogs. Between cacao (or grape) and durian, this results in a orthology 491

ratio 1:2 and outparalogy ratio 1:4. (A) Species phylogeny; (B) Assuming no 492

durian-specific event; (C) Assuming a durian-specific tetraploidization; (D) 493

Assuming a durian-specific paleohexaploidization; (E) If cotton is added to the 494

phylogeny; (F) Assuming a durian-specific paleohexaploidization and a 495

Gossypium-specific paleodecaploidization. 496

497

Figure 3. Examples of homologous gene dotplots between durian, cotton, 498

grape and cacao. Durian scaffold numbers and grape, cacao and cotton 499

chromosome numbers were shown on the tops and sides of plots, segment 500

regions showed in megabyte (Mbp). Best-hit genes are shown in red dots, 501 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



23

secondary hits with blue dots, and others in grey. Arrows show complement 502

correspondence produced by chromosome breakages during evolution. (A) 503

Grape vs. durian; (B) Cacao vs. durian; (C) Cotton vs. durian. 504

505

Figure 4. Alignment of durian, cotton, cacao, and grape genomes. The 506

alignment was constructed by using inferred colinear genes between genomes 507

with the grape genome as reference. The grape chromosomes form the 508

innermost circle, and their paralogous genes in colinearity are linked curves. A 509

grape chromosome region has 1, 5, and 3 orthologous regions in cacao, 510

cotton, and durian genomes, respectively. The homologous regions form the 511

other circles, displayed by short lines to show colinear genes. The short lines 512

in grape chromosomes were coloured as the 7 core-eudicot-common ancestral 513

chromosomes inferred previously (Jaillon et al., 2007). The short lines forming 514

chromosomes in other genomes were coloured as to their respective source 515

chromosome numbers. The colour scheme is shown at the bottom. V: grape; 516

G: cotton; D: durian. 517

518

Figure 5. Alignment of homologous regions from durian, cotton, cacao, and 519

grape genomes. A slice of genome-wide alignment shown in Fig. 4 is shown 520

here in details. This displays alignment in homologous local regions from 521

considered genomes. 522

523

Figure 6. Types of reconstructed phylogeny of homologous genes. Each 524

reconstructed tree has one grape gene as the outgroup and its cacao ortholog. 525

The reconstructed trees are divided into four types based on the location of the 526

cacao gene or on genes with which plant species it grouped on the 527

phylogenetic tree. (A) The tree is of expected phylogeny; (B) The cacao gene 528

is grouped with durian homologs; (C) The cacao genes is grouped with cotton 529 https://plantphysiol.orgDownloaded on December 6, 2020. - Published by



24

genes; (D) The cacao gene is grouped with but not outgroup to cotton and 530

durian genes. 531

532



25

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https://www.ncbi.nlm.nih.gov/pubmed?term=Li Q%2C Jin X%2C Zhu YX %282012%29 Identification and analyses of miRNA genes in allotetraploid Gossypium hirsutum fiber cells based on the sequenced diploid G%2E raimondii genome%2E J Genet Genomics&dopt=abstract

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https://scholar.google.com/scholar?as_q=Journey through the past: 150 million years of plant genome evolution&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Proost&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schnable&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=The draft genome of tropical fruit durian (Durio zibethinus)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Teh&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

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Wang J, Sun P, Li Y, Liu Y, Yu J, Ma X, Sun S, Yang N, Xia R, Lei T, Liu X, Jiao B, Xing Y, Ge W, Wang L, Wang Z, Song X, Yuan M, GuoD, Zhang L, Zhang J, Jin D, Chen W, Pan Y, Liu T, Jin L, Sun J, Yu J, Cheng R, Duan X, Shen S, Qin J, Zhang MC, Paterson AH, Wang X(2017) Hierarchically Aligning 10 Legume Genomes Establishes a Family-Level Genomics Platform. Plant Physiol 174: 284-300


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Wang X, Shi X, Li Z, Zhu Q, Kong L, Tang W, Ge S, Luo J (2006) Statistical inference of chromosomal homology based on genecolinearity and applications to Arabidopsis and rice. BMC Bioinformatics 7: 447


Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M,Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, DuranC, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, BonnemaG, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J,Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M,Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, ChoiSR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z,Xiong Z, Zhang Z (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43: 1035-1039


Wang X, Wang J, Guo H, Lee T, Liu T, Jin D, Paterson AH (2015) Genome Alignment Spanning Major Poaceae Lineages RevealsHeterogeneous Evolutionary Rates and Alters Inferred Dates for Key Evolutionary Events. Molecular Plant 8: 14


Wang X, Wang Z, Guo H, Zhang L, Wang L, Li J, Jin D, Paterson AH (2016) Telomere-centric genome repatterning determines recurringchromosome number reductions during the evolution of eukaryotes. New Phytol 205: 12



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https://scholar.google.com/scholar?as_q=Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size&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=Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vekemans&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang J%2C Sun P%2C Li Y%2C Liu Y%2C Yang N%2C Yu J%2C Ma X%2C Sun S%2C Xia R%2C Liu X%2C Ge D%2C Luo S%2C Liu Y%2C Kong Y%2C Cui X%2C Lei T%2C Wang L%2C Wang Z%2C Ge W%2C Zhang L%2C Song X%2C Yuan M%2C Guo D%2C Jin D%2C Chen W%2C Pan Y%2C Liu T%2C Yang G%2C Xiao Y%2C Sun j%2C Zhang C%2C Li Z%2C Xu H%2C Duan X%2C Shen S%2C Zhang Z%2C Huang S%2C Wang X %282018%29 An overlooked paleo%2Dtetraploidization in Cucurbitaceae Molecular and Biological Evolution&dopt=abstract

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https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang J%2C Sun P%2C Li Y%2C Liu Y%2C Yu J%2C Ma X%2C Sun S%2C Yang N%2C Xia R%2C Lei T%2C Liu X%2C Jiao B%2C Xing Y%2C Ge W%2C Wang L%2C Wang Z%2C Song X%2C Yuan M%2C Guo D%2C Zhang L%2C Zhang J%2C Jin D%2C Chen W%2C Pan Y%2C Liu T%2C Jin L%2C Sun J%2C Yu J%2C Cheng R%2C Duan X%2C Shen S%2C Qin J%2C Zhang MC%2C Paterson AH%2C Wang X %282017%29 Hierarchically Aligning 10 Legume Genomes Establishes a Family%2DLevel Genomics Platform%2E Plant Physiol&dopt=abstract


https://scholar.google.com/scholar?as_q=Hierarchically Aligning 10 Legume Genomes Establishes a Family-Level Genomics Platform&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=Hierarchically Aligning 10 Legume Genomes Establishes a Family-Level Genomics Platform&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang K%2C Wang Z%2C Li F%2C Ye W%2C Wang J%2C Song G%2C Yue Z%2C Cong L%2C Shang H%2C Zhu S%2C Zou C%2C Li Q%2C Yuan Y%2C Lu C%2C Wei H%2C Gou C%2C Zheng Z%2C Yin Y%2C Zhang X%2C Liu K%2C Wang B%2C Song C%2C Shi N%2C Kohel RJ%2C Percy RG%2C Yu JZ%2C Zhu YX%2C Wang J%2C Yu S %282012%29 The draft genome of a diploid cotton Gossypium raimondii%2E Nat Genet&dopt=abstract


https://scholar.google.com/scholar?as_q=The draft genome of a diploid cotton Gossypium raimondii&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=The draft genome of a diploid cotton Gossypium raimondii&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Guo H%2C Wang J%2C Lei T%2C Liu T%2C Wang Z%2C Li Y%2C Lee TH%2C Li J%2C Tang H%2C Jin D%2C Paterson AH %282016%29 Comparative genomic de%2Dconvolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation%2E New Phytol&dopt=abstract


https://scholar.google.com/scholar?as_q=Comparative genomic de-convolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation&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=Comparative genomic de-convolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Shi X%2C Li Z%2C Zhu Q%2C Kong L%2C Tang W%2C Ge S%2C Luo J %282006%29 Statistical inference of chromosomal homology based on gene colinearity and applications to Arabidopsis and rice%2E BMC Bioinformatics&dopt=abstract


https://scholar.google.com/scholar?as_q=Statistical inference of chromosomal homology based on gene colinearity and applications to Arabidopsis and rice.&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=Statistical inference of chromosomal homology based on gene colinearity and applications to Arabidopsis and rice.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Wang H%2C Wang J%2C Sun R%2C Wu J%2C Liu S%2C Bai Y%2C Mun JH%2C Bancroft I%2C Cheng F%2C Huang S%2C Li X%2C Hua W%2C Wang J%2C Wang X%2C Freeling M%2C Pires JC%2C Paterson AH%2C Chalhoub B%2C Wang B%2C Hayward A%2C Sharpe AG%2C Park BS%2C Weisshaar B%2C Liu B%2C Li B%2C Liu B%2C Tong C%2C Song C%2C Duran C%2C Peng C%2C Geng C%2C Koh C%2C Lin C%2C Edwards D%2C Mu D%2C Shen D%2C Soumpourou E%2C Li F%2C Fraser F%2C Conant G%2C Lassalle G%2C King GJ%2C Bonnema G%2C Tang H%2C Wang H%2C Belcram H%2C Zhou H%2C Hirakawa H%2C Abe H%2C Guo H%2C Wang H%2C Jin H%2C Parkin IA%2C Batley J%2C Kim JS%2C Just J%2C Li J%2C Xu J%2C Deng J%2C Kim JA%2C Li J%2C Yu J%2C Meng J%2C Wang J%2C Min J%2C Poulain J%2C Wang J%2C Hatakeyama K%2C Wu K%2C Wang L%2C Fang L%2C Trick M%2C Links MG%2C Zhao M%2C Jin M%2C Ramchiary N%2C Drou N%2C Berkman PJ%2C Cai Q%2C Huang Q%2C Li R%2C Tabata S%2C Cheng S%2C Zhang S%2C Zhang S%2C Huang S%2C Sato S%2C Sun S%2C Kwon SJ%2C Choi SR%2C Lee TH%2C Fan W%2C Zhao X%2C Tan X%2C Xu X%2C Wang Y%2C Qiu Y%2C Yin Y%2C Li Y%2C Du Y%2C Liao Y%2C Lim Y%2C Narusaka Y%2C Wang Y%2C Wang Z%2C Li Z%2C Wang Z%2C Xiong Z%2C Zhang Z %282011%29 The genome of the mesopolyploid crop species Brassica rapa%2E Nat Genet&dopt=abstract


https://scholar.google.com/scholar?as_q=The genome of the mesopolyploid crop species Brassica rapa&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=The genome of the mesopolyploid crop species Brassica rapa&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Wang J%2C Guo H%2C Lee T%2C Liu T%2C Jin D%2C Paterson AH %282015%29 Genome Alignment Spanning Major Poaceae Lineages Reveals Heterogeneous Evolutionary Rates and Alters Inferred Dates for Key Evolutionary Events%2E Molecular Plant&dopt=abstract


https://scholar.google.com/scholar?as_q=Genome Alignment Spanning Major Poaceae Lineages Reveals Heterogeneous Evolutionary Rates and Alters Inferred Dates for Key Evolutionary Events.&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 Alignment Spanning Major Poaceae Lineages Reveals Heterogeneous Evolutionary Rates and Alters Inferred Dates for Key Evolutionary Events.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Wang Z%2C Guo H%2C Zhang L%2C Wang L%2C Li J%2C Jin D%2C Paterson AH %282016%29 Telomere%2Dcentric genome repatterning determines recurring chromosome number reductions during the evolution of eukaryotes%2E New Phytol&dopt=abstract


https://scholar.google.com/scholar?as_q=Telomere-centric genome repatterning determines recurring chromosome number reductions during the evolution of eukaryotes.&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=Telomere-centric genome repatterning determines recurring chromosome number reductions during the evolution of eukaryotes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1


1 running title: a hexaploidization in durian€¦ · 12/11/2018 · 116 (wang et al., 2015; wang...

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