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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: wangxiyin@vip.sina.com 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: wangxiyin@vip.sina.com). 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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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
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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
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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
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Keywords: Durian, Genome, Cotton, Cacao, Grape, Polyploid 70
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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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16
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
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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
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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
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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
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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
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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
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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
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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
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24
genes; (D) The cacao gene is grouped with but not outgroup to cotton and 530
durian genes. 531
532
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https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.orgDownloaded on December 6, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
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