Ancestry Influences the Fate of Duplicated Genes Millions of Years After Polyploidization of Clawed Frogs (Xenopus)

Evans, Ben

doi:10.1534/genetics.106.069690

Cited by 49 publications

(88 citation statements)

References 71 publications

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“…Our model of gene evolution after WGD in X. laevis is illustrated in Fig. 5, which is based on the assumption that the WGD was an allopolyploidization, as is most likely (26,27). Most models to explain gene retention after WGD postulate that the two copies are equal at birth (e.g., refs.…”

Section: Discussionmentioning

confidence: 99%

“…We compare the expression profiles of gene pairs preserved in duplicate after WGD in X. laevis to the expression profiles of orthologous genes in the unduplicated clawed frog S. tropicalis (sometimes also called X. tropicalis). The WGD that has been proposed for X. laevis has not yet been validated by a complete genome sequence, but it is estimated to have occurred 24,25) and it is likely to have been an allopolyploidization because interspecies crosses in Xenopus often produce fertile polyploid offspring and phylogenetic studies have shown that other polyploid clawed frogs are ancient allopolyploids (24,26,27).We used the extensive expressed sequence tag (EST) and cDNA sequence resources available for these species (20,21,25) to detect genes present in one copy in S. tropicalis and in two copies in X. laevis. We inferred the pattern of expression in these triplets and detected events of subfunctionalization.…”

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Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis

Sémon

Wolfe

2008

Proc. Natl. Acad. Sci. U.S.A.

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As paleopolyploid genomes evolve, the expression profiles of retained gene pairs are expected to diverge. To examine this divergence process on a large scale in a vertebrate system, we compare Xenopus laevis, which has retained Ϸ40% of loci in duplicate after a recent whole-genome duplication (WGD), with its unduplicated relative Silurana (Xenopus) tropicalis. This comparison of ingroup pairs to an outgroup allows the direction of change in expression profiles to be inferred for a set of 1,300 X. laevis pairs, relative to their single orthologs in S. tropicalis, across 11 tissues. We identify 68 pairs in which X. laevis is inferred to have undergone a significant reduction of expression in at least two tissues since WGD. Of these pairs, one-third show evidence of subfunctionalization, with decreases in the expression levels of different gene copies in two different tissues. Surprisingly, we find that genes with slow rates of evolution are particularly prone to subfunctionalization, even when the tendency for highly expressed genes to evolve slowly is controlled for. We interpret this result to be an effect of allopolyploidization. We then compare the outcomes of this WGD with an independent one that happened in the teleost fish lineage. We find that if a gene pair was retained in duplicate in X. laevis, the orthologous pair is more likely to have been retained in duplicate in zebrafish, suggesting that similar factors, among them subfunctionalization, determined which gene pairs survived in duplicate after the two WGDs.rate of evolution ͉ Silurana tropicalis ͉ whole-genome duplication P olyploidy, also termed whole-genome duplication (WGD) is a frequent phenomenon in eukaryotes (1). A WGD is followed by extensive and rapid genome restructuring involving many gene losses, so that only one of the two gene copies remains in most genomes that underwent ancient polyploidization [for example, fish and yeast (2, 3)]. Alterations in function are expected among genes retained in duplicate. In some cases, one copy may acquire a new function (neofunctionalization), while the other keeps the ancestral function. The models of Lynch and Force (4, 5) also propose the existence of subfunctionalization, in which each copy retains a subset of the functions of the ancestral gene. Sub and neofunctionalization models make different predictions about the rate and symmetry of sequence evolution in the duplicates.Asymmetry in evolutionary rates between the protein sequences of the two copies is often interpreted as a footprint of neofunctionalization, especially if it is associated with evidence of positive selection in the accelerated copy (6). Several studies of paleopolyploid genomes have shown that rate asymmetry between the two copies can be widespread. For example, asymmetry was seen in 6% of retained gene pairs in Xenopus laevis and in 25-36% of pairs in teleost fishes (6-8). Relatively few examples of subfunctionalization of duplicated genes have been demonstrated so far, the best-known being those of fish mitf (9), sox9 (10), ...

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Section: Discussionmentioning

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Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis

Sémon

Wolfe

2008

Proc. Natl. Acad. Sci. U.S.A.

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“…Speciation in Xenopus is accomplished through 'normal' bifurcation as well as hybridization that can result in ploidy elevation [Evans, 2008]. There is no documentation for ploidy reduction, and there is also no indication that polyploid Xenopus utilize, or incorporate, genes or genomes from any diploid species [Evans, 2007[Evans, , 2008. Silurana is a sister pipid genus to Xenopus that contains diploid (S .…”

Section: African Clawed Frogs (Xenopus)mentioning

confidence: 99%

Genetic and Genomic Interactions of Animals with Different Ploidy Levels

Bogart¹,

Bi²

2013

Cytogenet Genome Res

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Polyploid animals have independently evolved from diploids in diverse taxa across the tree of life. We review a few polyploid animal species or biotypes where recently developed molecular and cytogenetic methods have significantly improved our understanding of their genetics, reproduction and evolution. Mitochondrial sequences that target the maternal ancestor of a polyploid show that polyploids may have single (e.g. unisexual salamanders in the genus Ambystoma) or multiple (e.g. parthenogenetic polyploid lizards in the genus Aspidoscelis) origins. Microsatellites are nuclear markers that can be used to analyze genetic recombinations, reproductive modes (e.g. Ambystoma) and recombination events (e.g. polyploid frogs such as Pelophylax esculentus). Hom(e)ologous chromosomes and rare intergenomic exchanges in allopolyploids have been distinguished by applying genome-specific fluorescent probes to chromosome spreads. Polyploids arise, and are maintained, through perturbations of the ‘normal' meiotic program that would include pre-meiotic chromosome replication and genomic integrity of homologs. When possible, asexual, unisexual and bisexual polyploid species or biotypes interact with diploid relatives, and genes are passed from diploid to polyploid gene pools, which increase genetic diversity and ultimately evolutionary flexibility in the polyploid. When diploid relatives do not exist, polyploids can interact with another polyploid (e.g. species of African Clawed Frogs in the genus Xenopus). Some polyploid fish (e.g. salmonids) and frogs (Xenopus) represent independent lineages whose ancestors experienced whole genome duplication events. Some tetraploid frogs (P. esculentus) and fish (Squaliusalburnoides) may be in the process of becoming independent species, but diploid and triploid forms of these ‘species' continue to genetically interact with the comparatively few tetraploid populations. Genetic and genomic interaction between polyploids and diploids is a complex and dynamic process that likely plays a crucial role for the evolution and persistence of polyploid animals. See also other articles in this themed issue.

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“…In addition, interpreting the fate of duplicate genes in polyploids is complicated by the fact that hybridization is often associated with WGD and so it can be difficult to disentangle the effects of combining and duplicating genomes on patterns of duplicate gene expression or dynamics of gene families (e.g., Evans, 2007;Guggisberg et al, 2009;Mable, 2013). Fortunately, rapid advances in sequencing technology and bioinformatic processing mean that the toolbox available to resolve such challenges continues to improve.…”

Section: Introduction Background and Aimsmentioning

confidence: 99%

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

et al. 2018

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Comparative genomics of non-model organisms has resurrected whole genome duplication (WGD) from being viewed as a somewhat obscure process that happens in plants to a primary driver of eukaryotic diversification. The shadow of past ploidy increases has left a strong signature of duplicated genes organized into gene families, even in small genomes that have undergone effectively complete rediploidization. Nevertheless, despite continually advancing technologies and bioinformatics pipelines, resolving the fate of duplicate genes remains a substantial challenge. For example, many important recognition processes are driven not only by allelic expansion through retention of duplicates but also by diversification and copy number variation. This creates technical difficulties with assembly to reference genomes and accurate interpretation of homology. Thus, relatively little is known about the impacts of recent polyploidization and hybridization on the evolution of gene families under selective forces that maintain diversity, such as balancing selection. Here we use a complex of species and ploidy levels in the genus Arabidopsis (A. lyrata and A. arenosa) as a model to investigate the evolutionary dynamics of a large and complicated gene family known to be under strong balancing selection: the receptor-like kinases, which include the female component of genetically controlled self-incompatibility. Specifically, we question: (1) How does diversity of S-receptor kinase (SRK) alleles in tetraploids compare to that in their close diploid relatives? (2) Is there increased trans-specific polymorphism (i.e., sharing of alleles that transcend speciation, characteristic of balancing selection) in tetraploids compared to diploids due to the higher number of copies they carry? (3) Do these highly variable loci show evidence of introgression among extant species/ploidy levels within or outside known zones of hybridization? (4) Is there evidence for copy number variation among paralogs? We use this example to highlight specific issues to consider when interpreting gene family evolution, particularly in relation to polyploids but also more generally in diploids. We conclude with recommendations for strategies to address the challenges of resolving such complex loci in the future, using advances in deep sequencing approaches.

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Ancestry Influences the Fate of Duplicated Genes Millions of Years After Polyploidization of Clawed Frogs (Xenopus)

Cited by 49 publications

References 71 publications

Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis

Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis

Genetic and Genomic Interactions of Animals with Different Ploidy Levels

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

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