Abstract
The well supported gene dosage hypothesis predicts that genes encoding proteins engaged in dose–sensitive interactions cannot be reduced back to single copies once all interacting partners are simultaneously duplicated in a whole genome duplication. The genomes of extant flowering plants are the result of many sequential rounds of whole genome duplication, yet the fraction of genomes devoted to encoding complex molecular machines does not increase as fast as expected through multiple rounds of whole genome duplications. Using parallel interspecies genomic comparisons in the grasses and crucifers, we demonstrate that genes retained as duplicates following a whole genome duplication have only a 50% chance of being retained as duplicates in a second whole genome duplication. Genes which fractionated to a single copy following a second whole genome duplication tend to be the member of a gene pair with less complex promoters, lower levels of expression, and to be under lower levels of purifying selection. We suggest the copy with lower levels of expression and less purifying selection contributes less to effective gene-product dosage and therefore is under less dosage constraint in future whole genome duplications, providing an explanation for why flowering plant genomes are not overrun with subunits of large dose–sensitive protein complexes.
Highlights
Plants have been colorfully labeled the “big kahuna of polyploidization” (Sémon and Wolfe, 2007)
We addressed the issue of mitigation of gene dosage-constraints with two experimental systems, the grasses, and the crucifers
Genes syntenically conserved through the crucifiers or grasses were categorized as (1) those without a homeologous duplicate from the older polyploidy in each lineage (2) those with a retained homeolog from the older polyploidy in each lineage
Summary
Plants have been colorfully labeled the “big kahuna of polyploidization” (Sémon and Wolfe, 2007). The lineages leading to the two preeminent models for plant genetics – Arabidopsis (a eudicot) and maize (a monocot) – each show evidence of multiple independent whole genome duplications (Figure 1) since monocots and eudicots diverged approximately 120 million years ago (Soltis et al, 2009). Whole genome duplication creates duplicate, potentially redundant, copies of all the genes within a genome. The loss of these duplicate copies from the genomes of ancient polyploid species is known as fractionation (Langham et al, 2004) and – over evolutionary time scales – the majority of genes duplicated by polyploidy will be reduced back to a single copy. If fractionation did not occur, an ancestral genome of 10,000 genes would grow to an unrealistically large 640,000 genes in maize, and 1.44 million genes in Brassica rapa
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