Discovery of additional ancient genome duplications in yeasts

Abstract

Whole genome duplication (WGD) has had profound macroevolutionary impacts on diverse lineages1,2, preceding adaptive radiations in vertebrates3-5, teleost fish6,7, and angiosperms8,9. In contrast to the many known ancient WGDs in animals10,11 and especially plants12-14, we are aware of evidence for only four in fungi15,16. The oldest of these occurred [~]100 million years ago (mya) and is shared by [~]60 extant Saccharomycetales species17,18, including the bakers yeast Saccharomyces cerevisiae (Fig. 1). Notably, this is the only known ancient WGD in the yeast subphylum Saccharomycotina. The dearth of ancient WGD events in fungi remains a mystery15. Some studies have suggested that fungal lineages that experience chromosome19 and genome15 duplication quickly go extinct, leaving no trace in the genomic record, while others contend that the lack of known WGD is due to an absence of data15,16. Under the second hypothesis, additional sampling and deeper sequencing of fungal genomes should lead to the discovery of more WGD events. Coupling hundreds of recently published genomes from nearly every described Saccharomycotina species with three additional long-read assemblies, we discovered three novel WGD events. While the functions of retained duplicate genes originating from these events are broad, they bear many similarities to the well-known WGD that occurred in the Saccharomycetales17. Our results suggest that WGD may be a more common evolutionary force in fungi than previously believed. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=111 SRC="FIGDIR/small/673279v1_fig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@6a8f47org.highwire.dtl.DTLVardef@1e4a790org.highwire.dtl.DTLVardef@b4e0eforg.highwire.dtl.DTLVardef@11b7795_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFigure 1.C_FLOATNO Three additional whole genome duplications in Saccharomycotina yeasts. Rates of gene duplication are mapped onto Saccharomycetales (left) and Dipodascales (right) phylogenies. Whole genome duplications indicated along the lineages in which they are predicted to occur. Trees have been pruned for visualization purposes. C_FIG HighlightsO_LIEvidence for three whole genome duplications (WGDs) in Dipodascales yeasts C_LIO_LIImpacts of WGD are broad but bear many similarities to the known WGD in Saccharomycetales yeasts C_LIO_LIDuplicates with many protein-protein interactions are more likely to be retained over long timescales C_LIO_LIWGD in fungi is likely underreported C_LI