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Positionally biased gene loss after whole genome duplication: evidence from human, yeast, and plant.

ABSTRACT: Whole genome duplication (WGD) has made a significant contribution to many eukaryotic genomes including yeast, plants, and vertebrates. Following WGD, some ohnologs (WGD paralogs) remain in the genome arranged in blocks of conserved gene order and content (paralogons). However, the most common outcome is loss of one of the ohnolog pair. It is unclear what factors, if any, govern gene loss from paralogons. Recent studies have reported physical clustering (genetic linkage) of functionally linked (interacting) genes in the human genome and propose a biological significance for the clustering of interacting genes such as coexpression or preservation of epistatic interactions. Here we conduct a novel test of a hypothesis that functionally linked genes in the same paralogon are preferentially retained in cis after WGD. We compare the number of protein-protein interactions (PPIs) between linked singletons within a paralogon (defined as cis-PPIs) with that of PPIs between singletons across paralogon pairs (defined as trans-PPIs). We find that paralogons in which the number of cis-PPIs is greater than that of trans-PPIs are significantly enriched in human and yeast. The trend is similar in plants, but it is difficult to assess statistical significance due to multiple, overlapping WGD events. Interestingly, human singletons participating in cis-PPIs tend to be classified into "response to stimulus." We uncover strong evidence of biased gene loss after WGD, which further supports the hypothesis of biologically significant gene clusters in eukaryotic genomes. These observations give us new insight for understanding the evolution of genome structure and of protein interaction networks.

SUBMITTER: Makino T

PROVIDER: S-EPMC3514672 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Positionally biased gene loss after whole genome duplication: evidence from human, yeast, and plant.

Makino Takashi T McLysaght Aoife A

Genome research 20120726 12

Whole genome duplication (WGD) has made a significant contribution to many eukaryotic genomes including yeast, plants, and vertebrates. Following WGD, some ohnologs (WGD paralogs) remain in the genome arranged in blocks of conserved gene order and content (paralogons). However, the most common outcome is loss of one of the ohnolog pair. It is unclear what factors, if any, govern gene loss from paralogons. Recent studies have reported physical clustering (genetic linkage) of functionally linked ( ...[more]

PMID: 22835904

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Project description:Whole-genome duplication (WGD) occurs broadly and repeatedly across the history of eukaryotes and is recognized as a prominent evolutionary force, especially in plants. Immediately following WGD, most genes are present in two copies as paralogs. Due to this redundancy, one copy of a paralog pair commonly undergoes pseudogenization and is eventually lost. When speciation occurs shortly after WGD; however, differential loss of paralogs may lead to spurious phylogenetic inference resulting from the inclusion of pseudoorthologs-paralogous genes mistakenly identified as orthologs because they are present in single copies within each sampled species. The influence and impact of including pseudoorthologs versus true orthologs as a result of gene extinction (or incomplete laboratory sampling) are only recently gaining empirical attention in the phylogenomics community. Moreover, few studies have yet to investigate this phenomenon in an explicit coalescent framework. Here, using mathematical models, numerous simulated data sets, and two newly assembled empirical data sets, we assess the effect of pseudoorthologs on species tree estimation under varying degrees of incomplete lineage sorting (ILS) and differential gene loss scenarios following WGD. When gene loss occurs along the terminal branches of the species tree, alignment-based (BPP) and gene-tree-based (ASTRAL, MP-EST, and STAR) coalescent methods are adversely affected as the degree of ILS increases. This can be greatly improved by sampling a sufficiently large number of genes. Under the same circumstances, however, concatenation methods consistently estimate incorrect species trees as the number of genes increases. Additionally, pseudoorthologs can greatly mislead species tree inference when gene loss occurs along the internal branches of the species tree. Here, both coalescent and concatenation methods yield inconsistent results. These results underscore the importance of understanding the influence of pseudoorthologs in the phylogenomics era. [Coalescent method; concatenation method; incomplete lineage sorting; pseudoorthologs; single-copy gene; whole-genome duplication.].

Project description:BackgroundAutopolyploidy is a valuable model for studying whole-genome duplication (WGD) without hybridization, yet little is known about the genomic structural and functional changes that occur in autopolyploids after WGD. Cyclocarya paliurus (Juglandaceae) is a natural diploid-autotetraploid species. We generated an allele-aware autotetraploid genome, a chimeric chromosome-level diploid genome, and whole-genome resequencing data for 106 autotetraploid individuals at an average depth of 60 × per individual, along with 12 diploid individuals at an average depth of 90 × per individual.ResultsAutotetraploid C. paliurus had 64 chromosomes clustered into 16 homologous groups, and the majority of homologous chromosomes demonstrated similar chromosome length, gene numbers, and expression. The regions of synteny, structural variation and nonalignment to the diploid genome accounted for 81.3%, 8.8% and 9.9% of the autotetraploid genome, respectively. Our analyses identified 20,626 genes (69.18%) with four alleles and 9191 genes (30.82%) with one, two, or three alleles, suggesting post-polyploid allelic loss. Genes with allelic loss were found to occur more often in proximity to or within structural variations and exhibited a marked overlap with transposable elements. Additionally, such genes showed a reduced tendency to interact with other genes. We also found 102 genes with more than four copies in the autotetraploid genome, and their expression levels were significantly higher than their diploid counterparts. These genes were enriched in enzymes involved in stress response and plant defense, potentially contributing to the evolutionary success of autotetraploids. Our population genomic analyses suggested a single origin of autotetraploids and recent divergence (~ 0.57 Mya) from diploids, with minimal interploidy admixture.ConclusionsOur results indicate the potential for genomic and functional reorganization, which may contribute to evolutionary success in autotetraploid C. paliurus.

Dataset Information

Positionally biased gene loss after whole genome duplication: evidence from human, yeast, and plant.

Publications

Positionally biased gene loss after whole genome duplication: evidence from human, yeast, and plant.

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