Genome evolutionary dynamics followed by diversifying selection explains the complexity of the Sesamum indicum genome
© The Author(s). 2017
Received: 28 January 2016
Accepted: 21 February 2017
Published: 24 March 2017
Whole genome duplication (WGD) and tandem duplication (TD) provide two critical sources of raw genetic material for genome complexity and evolutionary novelty. Little is known about the complexity of the Sesamum indicum genome after it diverged from a common ancestor with the paleodiploid Vitis vinifera and further experienced WGD and TD events.
Here, we analyzed the functional divergence of different classes of inter- and intra-genome gene pairs from ancestral events to uncover multiple-layers of evolutionary dynamics acting during the process of forming the modern S. indicum genome. Comprehensive inter-genome analyses revealed that 60% and 70% of syntenic orthologous gene pairs were retained among the two subgenomes in S. indicum compared to V. vinifera, although there was no evidence of significant differences under selection pressure. For the intra-genomic analyses, 5,932 duplicated gene pairs experienced fractionation, with the remaining 1,236 duplicated gene pairs having undergone functional divergence under diversifying selection. Analysis of the TD events indicated that 2,945 paralogous gene pairs, from 1,089 tandem arrays of 2–16 genes, experienced functional divergence under diversifying selection. Sequence diversification of different classes of gene pairs revealed that most of TD events occurred after the WGD event, with others following the ancestral gene order indicating ancient TD events at some time prior to the WGD event. Our comparison-of-function analyses for different classes of gene pairs indicated that the WGD and TD evolutionary events were both responsible for introducing genes that enabled exploration of novel and complementary functionalities, whilst maintaining individual plant ruggedness.
In this study, we first investigated functional divergence of different classes of gene pairs to characterize the dynamic processes associated with each evolutionary event in S. indicum. The data demonstrated massive and distinct functional divergence among different classes of gene pairs, and provided a genome-scale view of gene function diversification explaining the complexity of the S. indicum genome. We hope this provides a biological model to study the mechanism of plant species formation, particularly in the context of the evolutionary history of flowering plants, and offers novel insights for the study of angiosperm genomes.
KeywordsGenome evolution Dynamics Whole genome duplication Tandem duplication Function divergence
There are many genome-sequenced plant species in the rosid clade, but relatively few in the asterid clade. In the rosid clade, Vitis vinifera was the fourth species for which the complete genome sequence was established in flowering plants. After comparison with its close relatives, V. vinifera was considered as a true diploid, which had not undergone recent genome duplication . So, V. vinifera was thought to contain ancient genomic loci or ancestral gene orders, which could be used to enable the discovery of ancestral traits and genomic features of flowering plants. In the asterid clade, prior to the release of the Sesamum indicum (sesame, Asteraceae) draft genome , several genomes were publicly available, including Solanum tuberosum (potato), Solanum lycopersicon (tomato), Utricularia gibba (floating bladderwort) and Mimulus guttatus (monkey flower), which had experienced WGD or WGT events or near-doubling of chromosome numbers within their genomes [6, 7, 10–12]. Therefore, V. vinifera represents a paleodiploid species that is close to plant species in the asterid clade, and which experienced the older eudicot genome triplication event (γ) [6–8, 10, 13]. As a result, the paleodiploid V. vinifera in the rosid clade has maintained a complement of single-copy genes or single-copy syntenic regions at a whole-genome scale compared to other taxa within the asterid clade. Previous comparison of the two modern genomes, S. indicum and V. vinifera, has led to identification of two non-overlapping subgenomes in the S. indicum genome, which provides a rich source of genomic data to study orthologous genes between V. vinifera and S. indicum, as well as duplicated genes in S. indicum .
The WGD event contributed duplicated genes leading to the increase of gene dosage in S. indicum. Previous study indicated that duplicated genes mainly originate as a result of four different processes, that include ectopic recombination, replication slippage, retro-transposition and WGD . Following duplication, these genes may experience different evolutionary fates under diversifying selection pressures, including conserved function, sub-functionalization [15, 16], neo-functionalization [17, 18] and loss . Followed by diversifying selection in an evolutionary process, duplicated genes from the three WGD events in the A. thaliana lineage provided functional divergence and indicated sub- and neo-functionalization, which have been evaluated by protein-protein interaction in modern A. thaliana populations . Moreover, the relative gene expression of paralogous genes across tissues demonstrates that 98% of duplicate pairs have sub-functionalized in a tissue-wise manner following WGD events . Tandem duplication (TD) is a ubiquitous phenomenon in flowering plants, which can also bring about the increase of gene dosage [22, 23]. Compared to other duplication events, TDs occur more frequently and focus on smaller scale duplication within the genome [24, 25]. TD events are prevalent in many flowering plants and are a characteristic feature of many gene families related to key traits or phenotypes, including the genes coding for nucleotide binding site (NBS), cytochrome P450s and receptor-like kinases [26–28]. The tandem duplicated genes generated by TD events have experienced functional divergence under diversifying selection. From expression difference analysis of the NBS-encoding gene family in Brassica rapa and B. oleracea, paralogous genes from tandem arrays contributed more towards functional divergence than orthologous genes between B. rapa and B. oleracea over their evolutionary history .
Both WGD or TD events can contribute to anincrease in gene dosage, which may enhance the biological function of duplicated genes. However, duplicated genes from WGD event or paralogous genes from TD events may subsequently display functional divergence, which was not explained by the gene-dosage balance hypothesis . Several questions therefore arise: How the gene-dosage balance hypothesis influence gene evolution in S. indicum? How is the function of the gene changed in the evolutionary history of the S. indicum genome? What isthe complexity of the S. indicum genome after it diverged from a common ancestor with V. vinifera (species divergence event), and experienced WGD and TD events?
In this study, we first compared two S. indicum subgenomes and the V. vinifera genomes to obtain syntenic orthologous gene pairs. Secondly, we inferred duplicated gene pairs in the S. indicum subgenomes attributable to the WGD event. Thirdly, we identified pairs of genes based on every possible combination from a tandem array to constitute two-gene paralogous gene pairs in a corresponding tandem array within the S. indicum genome. Using different classes of gene pairs from the S. indicum specific ancient evolutionary events, we investigated the functional divergence of different classes of gene pairs by employing InterPro annotation to trace the evolutionary dynamic process of S. indicum genome followed by diversifying selection. From comparison of functional divergence for different classes of gene pairs, we characterized the dynamics associated with each evolutionary event to determine the complexity of the S. indicum genome. The data demonstrate massive and distinct functional divergence among different gene pairs, and provide a genome-scale view of gene function diversification which is able to be traced to ancient evolutionary events. We propose that these insights into the dynamics of S. indicum genome evolution serve as an important model for studying the evolutionary biology of flowering plants.
Influence of whole genome duplication on the S. indicum genome
Summary statistics of syntenic regions on S. indicum subgenomes
No. of syntenic blocks
Genomic length (Mb)
Total syntenic blocks:
Total genomic length:
Total gene numbers:
Genome gene numbers:
Percentage (Total */Genome *)
Functional divergence of syntenic orthologous gene pairs
Based on the syntenic relationships, we identified 5,932 V. vinifera genes that had orthologous genes located within the S. indicum subgenomes. This comparison involved 3,656 and 3,512 syntenic orthologous genes in Subgenome1 and Subgenome2, respectively. InterPro annotation enabled us to annotate these syntenic orthologous genes with functional descriptions . We allocated each of the syntenic orthologous gene pairs to one of three classes, depending on their functional-divergence status: (A) conserved function, with shared identical InterPro entries, (B) sub-functionalization, with shared partially identical InterPro entries, and (C) neo-functionalization, with completely different InterPro entries. The A, B and C functional divergence classes were used as evidence of collinearity between orthologous gene pairs in the S. indicum genome and corresponding ancient genomic loci in the V. vinifera genome.
Comparison of different classes of gene pairs between V. vinifera genome and S. indicum subgenomes
Total No. of Gene Pairs
No. of Gene Pairs with no Annotation
No. of Gene Pairs with Conserved Function
No. of Gene Pairs with Neofunctionalization
No. of Gene Pairs with Subfunctionalization
V. vinifera and Subgenome1
V. vinifera and Subgenome2
Selection pressure on syntenic orthologous gene pairs
For coding sequences, the strength of selection pressure is measured by the ratio of the rates of nonsynonymous substitution over synonymous substitutions (Ka/Ks) [33, 34]. We calculated Ka/Ks of S. indicum and V. vinifera syntenic orthologous gene pairs to determine whether they had experienced different selective pressures during the process of functional divergence. After filtering gene pairs with low sequence similarity, we found that the remaining 3,306 syntenic orthologous gene pairs, representing 90.42% of the total 3,656 syntenic orthologous gene pairs, from each of the A, B, C classes associated with Subgenome1 had a low mean Ka/Ks ratio (0.142, median value: 0.126). This result indicates that they had experienced purifying selection. The A class orthologous gene pairs with identical InterPro entries had the lowest mean Ka/Ks ratio (0.131, median value: 0.118), suggesting relatively strongpurifying selection, whereas the C class orthologous gene pairs had the highest mean Ka/Ks ratio (0.203, median value: 0.181), indicating that they had experienced weaker purifying selection. The Ka/Ks ratio (0.140, median value: 0.121) for the B class gene pairs was intermediate, although overall there were significant differences between each class (Mann-Whitney U test, PA:B = 0.03916 < 0.05; PA:C = 2.2e-16 < 0.05; PB:C = 2.852e-12 < 0.05).
In comparison, we found that overall, 3,116 syntenic orthologous gene pairs from the A, B, C classes associated with Subgenome2 had a mean Ka/Ks ratio of 0.121 (median value: 0.128), which is lower than the mean Ka/Ks ratio observed between Subgenome1 of the S. indicum genome and the V. vinifera genome. However, this difference was not statistically significant (Mann-Whitney U test, P = 0.3371 > 0.05). A similar pattern of Ka/Ks ratios was found (A: 0.131, median value: 0.119; B: 0.142, median value: 0.13 and C: 0.179, median value: 0.166), and a similar inference of purifying selection for any two classes (Mann-Whitney U test, PA:B = 0.003246 < 0.05; PB:C = 1.016e-08 < 0.05; PA:C = 0.0001182 < 0.05) with the consensus evolutionary pattern under diversifying selection among different classes of functional divergence.
Fractionation of duplicated gene pairs
Statistics of fractionation and retention of duplicated genes from S. indicum subgenomes
Total No. of Gene Pairs
No. of retained genes
No. of co-retained genes
No. of fractionated or specific retained genes
Functional divergence of duplicated gene pairs following the whole genome duplication event
Functional divergence of duplicated gene pairs followed by WGD is an important dynamic process for plant genome evolution. WGD events increase gene dosage and provide the opportunity for subsequent functional divergence. Out of 1,236 duplicated gene pairs between the two subgenomes, 110 duplicated gene pairs were not annotated by InterPro entries. After removing these unannotated duplicated gene pairs, we found 74.11% (916 duplicated gene pairs) for the A class shared identical InterPro entries, suggesting that they had maintained common functions following the WGD. We found that these included conserved functional domains for protein kinase domain, Serine/threonine-/dual specificity protein kinase, catalytic domain, tyrosine-protein kinase, catalytic domain, SANT/Myb domain, AAA+ ATPase domain, Myc-type, basic helix-loop-helix (bHLH) domain, Myb domain and homeobox domain, mainly enriched into gene families of protein kinase and transcription factors. For the B class, 130 duplicated gene pairs shared incomplete InterPro entries, indicating that these duplicated gene pairs had undergone partial functional divergence under selection pressure with sub-functionalization in each subgenome. For the 238 InterPro entries referred to Subgenome1, 45 InterPro entries were subgenome1-specific and 193 InterPro entries overlapped with Subgenome2. About 59 of all 252 InterPro entries were subgenome2-specific InterPro entries and the remaining 193 InterPro entries overlapped with Subgenome1. The sub-functionalized duplicated gene pairs annotated with the overlapped InterPro entries between Subgenome1 and Subgenome2 were classified into the gene families of protein kinase and transcription factors, suggesting that although the duplicated gene pairs have undergone sub-functionalization, the important functions of duplicated gene pairs were also maintained and enriched for the same gene families which played an important role in the growth and development processes in S. indicum. For the C class, we detected 80 duplicated gene pairs that shared completely different InterPro entries among the subgenomes. The members of duplicated gene pairs in Subgenome1 were annotated by 54 different InterPro entries, and the members of duplicated gene pairs in Subgenome2 were annotated by 80 different InterPro entries. Of these, 16 common entries were mainly associated with the conserved domains or motifs of zinc finger, RING-type 3 (IPR001841), SANT/Myb domain (IPR001005), pentatricopeptide repeat (IPR002885) and Myb domain (IPR017930) involved in the molecular function of zinc ion binding and chromatin binding (Additional file 4: Table S4).
The duplicated genes with conserved function or sub-functionalization in different subgenomes were mainly enriched into conserved domains or motifs of protein kinases and transcription factors, which represented a larger proportion of all duplicated gene pairs. The neo-functionalized duplicated gene pairs experienced severe functional divergence, although these genes still InterPro entries in common which mainly focused on the conserved domains or motifs of zinc finger and transcription factors. These results suggested that WGD events had primarily brought about an increase in protein kinases and transcription factors involved in biological processes of signal transduction system, protein phosphorylation and signal transduction, carbohydrate biosynthesis and metabolism, as well as transcriptional regulation .
Selection underlying the functional divergence of duplicated genes
The analysis of functional annotation for duplicated gene pairs with InterPro entries suggested that about 16.99% of 1,236 duplicated gene pairs have diverged in function after WGD including the duplicated gene pairs in classes of sub-functionalization and neo-functionalization. To investigate the selection pressures of duplicated gene pairs within S. indicum, we analyzed the Ka/Ks ratios of 1,236 duplicated gene pairs having different types of functional divergence as annotated by InterPro entries. Results showed a low mean Ka/Ks ratio (0.193, median value: 0.177) indicating that the duplicated genes had experienced purifying selection. The duplicated gene pairs of the A class of conserved function have the lowest mean Ka/Ks ratio (0.174, median value: 0.163), indicating these genes had undergone the strongest purifying selection compared to the gene pairs of the B and C classes. The mean Ka/Ks ratio of duplicated gene pairs in the B class was 0.212 (median value: 0.191), which was significantly greater than that from the A class. The analysis reveals the B class duplicated genes experienced weaker purifying selection than that of A class, and the mean Ka/Ks ratios for duplicated gene pairs were found to differ significantly between the A and B classes (Mann-Whitney U test, PA:B = 0.001043 < 0.05). The mean Ka/Ks ratio of C class duplicated gene pairs (0.27, median value: 0.252) was significantly greater than that of B class duplicated gene pairs, which indicated that the duplicated gene pairs of C class had been subject to the weakest purifying selection amongst different classes of duplicated gene pairs within syntenic regions in S. indicum. The mean Ks in the A class (0.852, median value: 0.69) was similar to that of the B class (0.845, median value: 0.696), although the average Ks in the C class (1.6, median value: 0.949) was significantly greater than that of A and B classes, suggesting that the C class duplicated genes accumulated more synonymous mutations and showed greater sequence divergence. Another possible interpretation of elevated Ks in class C genes where these genes have substantially lower overall similarity, is that the sequence alignments for these genes were more error prone, which would artificially elevate synonymous substitutions. The mean Ka in the C class (0.452, median value: 0.227) was also significantly higher than that of the A (0.141, median value: 0.119) and B (0.176, median value: 0.142) classes, indicating that the A and B class duplicated gene pairs may have accumulated fewer single base substitutions and experienced weaker purifying selection, thus making the function of duplicated gene pairs more conserved.
Influence of tandem duplication events in the S. indicum genome
Function divergence between the members of tandem array
For each tandem array, we selected two genes based on every possible combination to constitute paralogous gene pairs to investigate functional divergence. For example, one tandem array has three genes (a, b and c), which will generate three paralogous gene pairs (a-b, a-c and b-c). Finally, we obtained 2,945 paralogous gene pairs among all tandem arrays. Based on the annotation by InterPro entries, 197 of the paralogous gene pairs (6.7%) were not represented by InterPro entries. We therefore used the annotation of InterPro entries to determine the functional divergence of 2,748 paralogous gene pairs in tandem arrays, of which 2,308 (78.4%) sharing identical InterPro entries were classified into the A class of conserved function. These were mainly recognized as the members of gene families or conserved domains of Auxin-induced protein, ARG7, Cytochrome P450 and Cytochrome P450, E-class, group I. 425 (14.4%) shared partially identical InterPro entries and were allocated as sub-functionalized between members of paralogous gene pairs, and were grouped into the gene families or conserved domains of Protein kinase domain, Serine/threonine-/dual specificity protein kinase, catalytic domain and Tyrosine-protein kinase, catalytic domain. Only 15 gene pairs were recognized as the gene pairs of complete functional divergence and were also grouped into the gene families of protein kinases. This analysis indicates that the majority of tandem duplicated genes has a conserved function. Irrespective of whether the paralogous genes belonged to the members of gene pairs with sub-functionalization or neo-functionalization, the paralogous gene pairs of functional divergence represented a smaller proportion in all paralogous gene pairs of tandem arrays. This suggests that most of tandem duplicated genes in S. indicum display a bias towards conserved function, suggesting the tandem duplicated genes were subject to weaker selection pressure (Additional file 6: Table S6).
Gene functional differences between duplicated and tandem duplicated genes
Sequence diversification of different classes of gene pairs from evolutionary events
Dating of tandem duplication events in S. indicum
The analysis of sequence divergence of different classes of gene pairs indicates that most of the TD events represented the most recent events in the evolutionary history of S. indicum, and likely occurred after the WGD event. In order to date the evolution of tandem duplicated genes, we combined the different classes of gene pairs from the WGD and TD events. 126 tandem duplicated genes distributed in 63 two-gene tandem arrays were located on the S. indicum subgenomes, which had 118 syntenic orthologous genes in V. vinifera, suggesting that these genes were located on syntenic blocks in the subgenomes compared to V. vinifera genome, and may be inherited from their ancestral gene orders (Additional file 7: Table S7). There was no evidence for the remaining 2,619 tandem duplicated genes being associated with the ancient genomic loci, indicating that these tandem duplicated genes might be generated after the WGD event. With the WGD event recognized as a reference point, tandem duplicated genes can then be divided into two classes: 126 tandem duplicated genes which were generated before the WGD event, and 2,619 after. Of the first set 72 tandem duplicated genes are distributed within 36 two-gene tandem arrays and are located within Subgenome1, with the remainder (54) distributed on 27 two-gene tandem arrays in Subgenome2. From these results, we concluded that the TD events had not occurred at a particular evolutionary stage but had been a continuous process over a long historical period, which is consistent with the description of the Brassica genus .
Evolutionary patterns of certain gene families followed by whole genome duplication and tandem duplication events
Comparison of the members of WRKY, NBS-encoding and Cytochrome P450 gene family after WGD and TD events
Total No. of gene families
Generated by WGD event
Generated by TD event
Functional divergence by diversifying selection
The study of functional-divergence for different classes of gene pairs has been explored in the context of the three ancestral WGD events leading to the contemporary Arabidopsis genome. Different proportions of duplicated gene pairs from these sequential WGD events have indicated functional divergence using the number of identified protein-protein interactions as a proxy. Differences between duplicated gene pairs based on Gene Ontology annotation have reinforced this evidence of functional divergence from protein-protein interactions, and has been interpreted as indicative of adaptation to different cellular components . Comparison of functional divergence between the two S. indicum subgenomes compared to the V. vinifera genome, indicates that 73.3% of Subgenome1 and 72.2% of Subgenome2 have retained a conserved function between members of gene pairs, with the remainder displaying evidence of sub-functionalization or neo-functionalization. Functional analysis of diverged gene pairs indicates enrichment for different functional classes. The analysis of selection pressures indicated that the syntenic orthologous gene pairs can be assigned to those with conserved function, sub-functionalization and neo-functionalization, resulting from different selection pressures. S. indicum has experienced distinct genomic events at different evolutionary stages, with each resulting in extensive changes in composition of gene pairs. Moreover, it appears that some duplicated gene pairs subsequently emerged with a distinct evolutionary fate under diversifying selection, including sub-functionalization and neo-functionalization. Taken together, these results suggest that these classes of genomic event led to the introduction of extensive novel genomic materials resulting in different classes of gene pairs, with evidence of adaptive evolution under diversifying selection. This appears to have provided novel opportunities for species adaptation to changing environments.
Gene functional compensation followed by whole genome duplication and tandem duplication events
Based on the functional differences 1,059 InterPro entries were used to annotate duplicated genes and 634 to annotate tandemly duplicated genes in S. indicum. Of these, 344 had shared InterPro entries, with the remainder allocated to WGD-specific and TD-specific events. This analysis indicated that such gene pairs were mainly grouped into gene families involved in plant development and growth, but the TD-specific InterPro entries were mainly classified into gene families related to environmental influence. Based on genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis, Yu et al. (2014), demonstrated that the TD events led to an increase in gene dosage of NBS-encoding genes resulting in gene amplification, which may have some advantages for plant parasite defense . The TD events giving rise to expansion of the NBS-encoding gene family is also likely to have benefited the resistance of S. indicum to the diseases and pests, and improve the adaptation to a changing environment. The WGD and TD events have brought specific genes with different functional features to the S. indicum genome, which appear to have been essential genomic ingredients for plant growth and development. Where the WGD event has not brought sufficient functional components to meet the need for survival or increased fitness, the TD events have been a valuable mechanism to generate additional genomic ingredients to maintain plant fitness. We infer that this may be due to a critical mechanism for functional compensation in plant evolutionary history, and the mutual compensation of genes, through synergies with each other, jointly maintained the ruggedness of S. indicum.
Gene evolutionary dynamics arising from evolutionary events
The ancestral S. indicum genome has diverged from a common ancestor with the ancestral V. vinifera and inherited evolutionary evidence of ancestral gene orders. Subsequently, the ancestral S. indicum genome has experienced a WGD event around 71 (±19) Mya, which introduced extensive additional genomic materials leading to genome-wide chromosome fragmentation and rearrangement. TD events, which increase gene dosage and contribute to the expansion of gene families, have occurred over a long historical evolutionary period, although most of them have occurred mainly after the WGD event. The WGD and TD events increased gene dosage and improved the corresponding gene function, which will increase the likelihood of plant survival in changing environments. This can be explained by the gene-dosage balance hypothesis . Subsequently, some duplicated genes or tandem duplicated genes experienced sub-functionalization or neo-functionalization under diversifying selection, which did not fit the gene-dosage balance hypothesis. So, the gene-dosage balance hypothesis might influence certain periods in the evolutionary history of S. indicum genome. Following each evolutionary event, functional components of the S. indicum genome have undergone subsequent gene functional divergence, and meanwhile also generated novel functional components. The WGD and TD events have independently supplied novel genomic materials, each complementing the other in terms of functional components, and both contributing to the additional functional features and ruggedness of the species.
The availability of the S. indicum genome sequence provides an opportunity to investigate the characterization of S. indicum genome, and to compare with genomic analogues in its closely relatives through a comparative genomics approach. By tracing the evolutionary history of S. indicum it appears that WGD and TD events occurred after the divergence of the predecessors of S. indicum and V. vinifera from a common ancestor. These evvents have also provided an extensive genomic resource to investigate the complexity of the S. indicum genome. According to syntenic relationship between S. indicum and V. vinifera, 60% and 70% of syntenic orthologous gene pairs were retained among Subgenome1 and Subgenome2 in S. indicum compared to V. vinifera. Based on selection pressure analysis, there was no evidence of significant differences between different subgenomes in S. indicum compared to V. vinifera. For the intra-genomic analyses, 5,932 duplicated gene pairs were retained 3,656 and 3,512 single-copy genes in Subgenome1 and Subgenome2 compared to V. vinifera respectively, which meant that duplicated gene pairs in S. indicum have experienced fractionation. The co-retained 1,236 duplicated gene pairs in different subgenomes in S. indicum have undergone functional divergence under diversifying selection. From comparison of WGD and TD events, most of tandem duplicated genes were generated after the WGD, with others following the ancestral gene order indicating ancient tandem duplication at some time prior to the WGD. Our comparison of function analyses revealed that the WGD and TD evolutionary events were both responsible for introducing genes that enabled exploration of novel and complementary functionalities. Importantly, the comparison of gene families related to certain traits or phenotypes and their further exploitation may help us to uncover the intriguing evolutionary process of special traits or phenotypes in S. indicum, which can explore the phenotypic diversity due to the complexity of S. indicum genome. We hope this provides a valuable biological model to study the mechanism of plant species formation, particularly in the context of the evolutionary history of flowering plants, and offers a novel insight for the study of angiosperm genomes.
S. indicum and V. vinifera genomic and annotation data were downloaded from the Sinbase (http://ocri-genomics.org/Sinbase/)  and Genoscope (http://www.genoscope.cns.fr) , respectively. The putative tandem duplicated genes in S. indicum genome were downloaded from the PTGBase (http://ocri-genomics.org/PTGBase/) .
InterPro annotation Analysis
In order to provide functional analysis of protein sequences by classifying them into families and predict the presence of domains and important sites, the functional domains or conserved sites classification for a gene was determined by the InterPro database . All records were derived from member databases of the InterPro consortium by using predictive models, known as signatures. Gene function divergence in the members of gene pairs is defined by sharing partially identical or complete differences InterPro entries between different classes of gene pairs.
Gene Ontology annotation
Gene Ontology was employed to determine the functional enrichment analysis for the members of different classes of gene pairs by predicting the presence of conserved domains or important sites .
Calculation of Ka, Ks and Ka/Ks Values
Protein sequences of different classes of gene pairs were aligned using ClustalW . Coding sequence alignments of different classes of gene pairs were guided by protein sequence alignment using PAL2NAL . Nonsynonymous substitutions per sites (Ka) and synonymous substitutions per sites (Ks) values were calculated using the yn00 program in the PAML package .
We thank Dr. Xin Zhou in Washington University in St. Louis and Dr. Komivi Dossa in Oil Crops Research Institute in Chinese Academy of Agricultural Sciences for the critical reading of the manuscript.
This work was supported by the National Natural Science Foundation of China (no. 31271766), the Agricultural Science and Technology Innovation Program, CAAS,the National Basic Research Program of China (973 Program; no. 2011CB109304), and China Agriculture Research System (no. CARS-15).
JY analyzed the data and prepared the manuscript. GK revised the manuscript. LW, HG, BL and XZ participated in data analysis and the manuscript preparation. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Stephens SG. Possible significances of duplication in evolution. Adv Genet. 1951;4:247–65.PubMedGoogle Scholar
- Bowers JE, Chapman BA, Rong J, Paterson AH. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature. 2003;422(6930):433–8.View ArticlePubMedGoogle Scholar
- Blanc G, Wolfe KH. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell. 2004;16(7):1667–78.View ArticlePubMedPubMed CentralGoogle Scholar
- Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011;473(7345):97–100.View ArticlePubMedGoogle Scholar
- Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278):178–83.View ArticlePubMedGoogle Scholar
- Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, et al. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475(7355):189–95.View ArticlePubMedGoogle Scholar
- Consortium TTG. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485(7400):635–41.View ArticleGoogle Scholar
- Wang L, Yu S, Tong C, Zhao Y, Liu Y, Song C, Zhang Y, Zhang X, Wang Y, Hua W, et al. Genome sequencing of the high oil crop sesame provides insight into oil biosynthesis. Genome Biol. 2014;15(2):R39.View ArticlePubMedPubMed CentralGoogle Scholar
- Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449(7161):463–7.View ArticlePubMedGoogle Scholar
- Ibarra-Laclette E, Lyons E, Hernandez-Guzman G, Perez-Torres CA, Carretero-Paulet L, Chang TH, Lan T, Welch AJ, Juarez MJ, Simpson J, et al. Architecture and evolution of a minute plant genome. Nature. 2013;498(7452):94–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Hellsten U, Wright KM, Jenkins J, Shu S, Yuan Y, Wessler SR, Schmutz J, Willis JH, Rokhsar DS. Fine-scale variation in meiotic recombination in Mimulus inferred from population shotgun sequencing. Proc Natl Acad Sci U S A. 2013;110(48):19478–82.View ArticlePubMedPubMed CentralGoogle Scholar
- Fishman L, Willis JH, Wu CA, Lee YW. Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae). Heredity. 2014;112(5):562–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Di Genova A, Almeida AM, Muñoz-Espinoza C, et al. Whole genome comparison between table and wine grapes reveals a comprehensive catalog of structural variants. BMC Plant Biology. 2014;14:7. doi:10.1186/1471-2229-14-7.
- Zhang J. Evolution by gene duplication: an update. Trends Ecol Evol. 2003;18(6):292–8.View ArticleGoogle Scholar
- Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999;151(4):1531–45.PubMedPubMed CentralGoogle Scholar
- Stoltzfus A. On the possibility of constructive neutral evolution. J Mol Evol. 1999;49(2):169–81.View ArticlePubMedGoogle Scholar
- Lynch VJ. Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol. 2007;7:2.View ArticlePubMedPubMed CentralGoogle Scholar
- Conant GC, Wolfe KH. Turning a hobby into a job: How duplicated genes find new functions. Nat Rev Genet. 2008;9(12):938–50.View ArticlePubMedGoogle Scholar
- Lee JA, Lupski JR. Genomic rearrangements and gene copy-number alterations as a cause of nervous system disorders. Neuron. 2006;52(1):103–21.View ArticlePubMedGoogle Scholar
- Guo H, Lee TH, Wang X, Paterson AH. Function relaxation followed by diversifying selection after whole-genome duplication in flowering plants. Plant Physiol. 2013;162(2):769–78.View ArticlePubMedPubMed CentralGoogle Scholar
- Pophaly SD, Tellier A. Population Level Purifying Selection and Gene Expression Shape Subgenome Evolution in Maize. Mol Biol Evol. 2015;32(12):3226–35.PubMedGoogle Scholar
- Initiative TAG. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408(6814):796–815.View ArticleGoogle Scholar
- Kane J, Freeling M, Lyons E. The evolution of a high copy gene array in Arabidopsis. J Mol Evol. 2010;70(6):531–44.View ArticlePubMedPubMed CentralGoogle Scholar
- Davis JC, Petrov DA. Do disparate mechanisms of duplication add similar genes to the genome? Trends Genet. 2005;21(10):548–51.View ArticlePubMedGoogle Scholar
- Hakes L, Pinney JW, Lovell SC, Oliver SG, Robertson DL. All duplicates are not equal: the difference between small-scale and genome duplication. Genome Biol. 2007;8(10):R209.View ArticlePubMedPubMed CentralGoogle Scholar
- Yu J, Tehrim S, Zhang F, Tong C, Huang J, Cheng X, Dong C, Zhou Y, Qin R, Hua W, et al. Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genomics. 2014;15:3.View ArticlePubMedPubMed CentralGoogle Scholar
- Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell. 2004;16(5):1220–34.View ArticlePubMedPubMed CentralGoogle Scholar
- Doddapaneni H, Chakraborty R, Yadav JS. Genome-wide structural and evolutionary analysis of the P450 monooxygenase genes (P450ome) in the white rot fungus Phanerochaete chrysosporium: evidence for gene duplications and extensive gene clustering. BMC Genomics. 2005;6:92.View ArticlePubMedPubMed CentralGoogle Scholar
- Birchler JA, Veitia RA. The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell. 2007;19(2):395–402.View ArticlePubMedPubMed CentralGoogle Scholar
- Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7):e49.View ArticlePubMedPubMed CentralGoogle Scholar
- Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33(Web Server issue):W116–120.View ArticlePubMedPubMed CentralGoogle Scholar
- Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997;13(5):555–6.PubMedGoogle Scholar
- Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24(8):1586–91.View ArticlePubMedGoogle Scholar
- Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25(1):25–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Ohno S. Evolution by gene duplication. Springer-Verlag; 1970. ISBN 0-04-575015-7.Google Scholar
- Yu J, Ke T, Tehrim S, Sun F, Liao B, Hua W. PTGBase: an integrated database to study tandem duplicated genes in plants. Database the Journal of Biological Databases & Curation. 2015;2015. doi:10.1093/database/bav017.
- Freeling M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Plant Biology. 2009;60(60):433–53.View ArticleGoogle Scholar
- Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA, Zhao M, Ma J, Yu J, Huang S, et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun. 2014;5:3930.PubMedPubMed CentralGoogle Scholar
- Rushton PJ, Somssich IE, Ringler P, Shen QJ. WRKY transcription factors. Trends Plant Sci. 2010;15(5):247–58.View ArticlePubMedGoogle Scholar
- van Ooijen G, van den Burg HA, Cornelissen BJ, Takken FL. Structure and function of resistance proteins in solanaceous plants. Annu Rev Phytopathol. 2007;45:43–72.View ArticlePubMedGoogle Scholar
- Werck-Reichhart D, Feyereisen R. Cytochromes P450: a success story. Genome Biol. 2000;1(6):REVIEWS3003.View ArticlePubMedPubMed CentralGoogle Scholar
- Schuler MA, Werck-Reichhart D. Functional genomics of P450s. Annu Rev Plant Biol. 2003;54:629–67.View ArticlePubMedGoogle Scholar
- Guttikonda SK, Trupti J, Bisht NC, Chen H, An YQ, Pandey S, Xu D, Yu O. Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases. BMC Plant Biol. 2010;10:243.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang L, Yu J, Li D, Zhang X. Sinbase: an integrated database to study genomics, genetics and comparative genomics in Sesamum indicum. Plant Cell Physiol. 2015;56(1):e2.View ArticlePubMedGoogle Scholar
- Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33(suppl_2):116–20.View ArticleGoogle Scholar
- Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–8.View ArticlePubMedGoogle Scholar
- Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34(Web Server issue):W609–612.View ArticlePubMedPubMed CentralGoogle Scholar