Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention

Mandáková, Terezie; Li, Zheng; Barker, Michael S.; Lysak, Martin A.

doi:10.1111/tpj.13553

Cited by 91 publications

(103 citation statements)

References 106 publications

(196 reference statements)

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“…Our observation across multiple species is consistent with post-polyploid genome evolution as dosage-balance may drive the convergent retention of genes. Previous empirical studies supported that gene dosage balance plays an important role in gene retention following gene and genome duplications (Freeling 2009;Session et al 2016;Mandáková et al 2017) . Other hypotheses of duplicate gene retention such as neo-and subfunctionalization are also important in duplicate gene retention, but only the DBH predicts a convergent pattern of gene retention following polyploidy across multiple species (Kondrashov and Kondrashov 2006;Freeling 2009) .…”

Section: Discussionmentioning

confidence: 98%

“…This biased pattern was also found among WGD paralogs in an outgroup species, Ixodes scapularis (deer tick), and suggests that it may be consistent across arthropods. Previous studies in plants have found that similar functional categories of genes have been maintained following different genome duplication events Rody et al 2017) , although there are o en idiosyncratic patterns observed across families (Maere et al 2005;Barker et al 2008;Li et al 2016;Mandáková et al 2017) . The 20 insect transcriptomes included in our GO category analyses represent diverse hexapod (SI 10 .…”

Section: Discussionmentioning

confidence: 99%

“…A common signature of paleopolyploidy is the biased retention and loss of some categories of genes relative to the background pattern of gene turnover. Surviving paralogs from ancient WGDs are o en enriched with idiosyncratic gene ontology (GO) categories in plants (Barker et al 2008;De Smet et al 2013;Li et al 2016;Mandáková et al 2017;Rody et al 2017) , yeasts (Papp et al 2003;Conant 2014) , and animals (Berthelot et al 2014;Lien et al 2016;Session et al 2016) . Among the many hypotheses to explain the retention of paralogs (Kondrashov and Kondrashov 2006;Freeling 2009;Hahn 2009) , the dosage balance hypothesis (DBH) is the only hypothesis that predicts the parallel retention and loss of 7 .…”

Section: Biased Gene Retention and Loss Following Inferred Wgdsmentioning

confidence: 99%

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Multiple large-scale gene and genome duplications during the evolution of hexapods

Tiley

Galuska

et al. 2018

Preprint

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Polyploidy or whole genome duplication (WGD) is a major contributor to genome evolution and diversity. Although polyploidy is recognized as an important component of plant evolution, it is generally considered to play a relatively minor role in animal evolution. Ancient polyploidy is found in the ancestry of some animals, especially fishes, but there is little evidence for ancient WGDs in other metazoan lineages. Here we use recently published transcriptomes and genomes from more than 150 species across the insect phylogeny to investigate whether ancient WGDs occurred during the evolution of Hexapoda, the most diverse clade of animals. Using gene age distributions and phylogenomics, we found evidence for 18 ancient WGDs and six other large-scale bursts of gene duplication during insect evolution. These bursts of gene duplication occurred in the history of lineages such as the Lepidoptera, Trichoptera, and Odonata. To further corroborate the nature of these duplications, we evaluated the pattern of gene retention from putative WGDs observed in the gene age distributions. We found a relatively strong signal of convergent gene retention across many of the putative insect WGDs.Considering the phylogenetic breadth and depth of the insect phylogeny, this observation is consistent with polyploidy as we expect dosage-balance to drive the parallel retention of genes. Together with recent research on plant evolution, our hexapod results suggest that genome duplications contributed to the evolution of two of the most diverse lineages of eukaryotes on Earth.

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Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

Section: Biased Gene Retention and Loss Following Inferred Wgdsmentioning

confidence: 99%

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Multiple large-scale gene and genome duplications during the evolution of hexapods

Tiley

Galuska

et al. 2018

Preprint

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“…In Brassica for example, the variation in base chromosome numbers is the result of multiple and independent diploidizations from the mesohexaploid ancestor (Lysak et al, 2007;Mandáková et al, 2017). Indeed, the stochasticity of polyploid drop, not WGD, is thought to be a major contributor to speciations and radiations (Figure 1).…”

Section: Post-polyploidy Diploidization a Cradle For Diversificationmentioning

confidence: 99%

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

et al. 2018

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The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short-and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as "sponges" accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew.

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“…Successive WGDs have occurred in multiple lineages: As indicated, angiosperms have experienced multiple WGDs, and recursive WGDs among the Brassica crops that include cauliflower, broccoli and cabbages have been precisely mapped recently 58 . The vertebrate animals emerged from the invertebrates approximately 500 Mya via two sequential rounds of WGD (2R-WGD) 59 .…”

Section: Common Themes From Recent Reconstructions Of Ancient Whole-gmentioning

confidence: 99%

Recent advances in understanding the roles of whole genome duplications in evolution

MacKintosh

Ferrier

2017

F1000Res

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Ancient whole-genome duplications (WGDs)— paleopolyploidy events—are key to solving Darwin’s ‘abominable mystery’ of how flowering plants evolved and radiated into a rich variety of species. The vertebrates also emerged from their invertebrate ancestors via two WGDs, and genomes of diverse gymnosperm trees, unicellular eukaryotes, invertebrates, fishes, amphibians and even a rodent carry evidence of lineage-specific WGDs. Modern polyploidy is common in eukaryotes, and it can be induced, enabling mechanisms and short-term cost-benefit assessments of polyploidy to be studied experimentally. However, the ancient WGDs can be reconstructed only by comparative genomics: these studies are difficult because the DNA duplicates have been through tens or hundreds of millions of years of gene losses, mutations, and chromosomal rearrangements that culminate in resolution of the polyploid genomes back into diploid ones (rediploidisation). Intriguing asymmetries in patterns of post-WGD gene loss and retention between duplicated sets of chromosomes have been discovered recently, and elaborations of signal transduction systems are lasting legacies from several WGDs. The data imply that simpler signalling pathways in the pre-WGD ancestors were converted via WGDs into multi-stranded parallelised networks. Genetic and biochemical studies in plants, yeasts and vertebrates suggest a paradigm in which different combinations of sister paralogues in the post-WGD regulatory networks are co-regulated under different conditions. In principle, such networks can respond to a wide array of environmental, sensory and hormonal stimuli and integrate them to generate phenotypic variety in cell types and behaviours. Patterns are also being discerned in how the post-WGD signalling networks are reconfigured in human cancers and neurological conditions. It is fascinating to unpick how ancient genomic events impact on complexity, variety and disease in modern life.

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Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention

Cited by 91 publications

References 106 publications

Multiple large-scale gene and genome duplications during the evolution of hexapods

Multiple large-scale gene and genome duplications during the evolution of hexapods

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

Recent advances in understanding the roles of whole genome duplications in evolution

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