Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms

Abstract

Gene duplications provide evolutionary potentials for generating novel functions, while polyploidization or whole genome duplication (WGD) doubles the chromosomes initially and results in hundreds to thousands of retained duplicates. WGDs are strongly supported by evidence commonly found in many species-rich lineages of eukaryotes, and thus are considered as a major driving force in species diversification. We performed comparative genomic and phylogenomic analyses of 59 public genomes/transcriptomes and 46 newly sequenced transcriptomes covering major lineages of angiosperms to detect large-scale gene duplication events by surveying tens of thousands of gene family trees. These analyses confirmed most of the previously reported WGDs and provided strong evidence for novel ones in many lineages. The detected WGDs supported a model of exponential gene loss during evolution with an estimated half-life of approximately 21.6 million years, and were correlated with both the emergence of lineages with high degrees of diversification and periods of global climate changes. The new datasets and analyses detected many novel WGDs widely spread during angiosperm evolution, uncovered preferential retention of gene functions in essential cellular metabolisms, and provided clues for the roles of WGD in promoting angiosperm radiation and enhancing their adaptation to environmental changes.

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

“…Using a parsimony-based method to map the location of gene losses onto the P. aurelia phylogeny (Methods), we found that, following a short period of rapid gene loss immediately after the WGD, gene loss rate decreased and entered a phase of linear decline ( Figure 2). This pattern is similar to what has been observed in yeast, teleost fish and plants (Scannell, et al 2006;Inoue, et al 2015;Ren, et al 2018) although the exact shape of the survival curve is disputed (Inoue, et al 2015). Using all of the ancestrally reconstructed duplicated gene survival rates, we found that an exponential decay model provided a better fit (R 2 =0.49) than a linear decay model (R 2 =0.44).…”

“…It is also now widely accepted that two successive rounds of WGDs occurred in the ancestor of vertebrates (Hokamp, et al 2003;Dehal and Boore 2005;Holland and Ocampo Daza 2018) and an additional round of genome duplication in the lineage leading to all teleost fish (Meyer and Schartl 1999;Jaillon, et al 2004;Howe, et al 2013;Glasauer and Neuhauss 2014). Additionally, WGDs are extremely common in land plants, to the point that all angiosperms are believed to have experienced at least one round of genome duplication in their history Ren, et al 2018). Because they create the opportunity for thousands of genes to evolve new functions, WGDs have been suggested to be responsible for the evolutionary success of several lineages Glasauer and Neuhauss 2014).…”

Evolution and genetic control of the floral ground plan

“…Has polyploidy stimulated morphological change? Is it relevant that the origin of the Pentapetalae is associated with the gamma whole genome triplication (Jiao et al, 2012), and later duplications within orders and families are associated with their species richness (Lands et al, 2018;Ren et al, 2018)?…”

Polyploidy promotes species diversification of Allium through ecological shifts

“…Phylogeny-based comparative work has suggested that polyploids diversify more slowly, with higher extinction rates and lower speciation rates than those of their diploid relatives (Mayrose et al, 2011). Nevertheless, recent studies have highlighted a positive correlation of polyploidy with species diversification (Levin & Soltis, 2018;Ren et al, 2018). This is attributed to the advantages of polyploids with respect to genomic plasticity (Leitch & Leitch, 2008), ecological transformation (Ramsey & Ramsey, 2014), or long-term adaptation (Van de Peer et al, 2017).…”