Meiotic effects ofMSH4copy number variation support an adaptive role for post-polyploidy gene loss

Abstract

Many eukaryotes descend from polyploid ancestors that experienced massive duplicate gene loss. This genomic erosion is particularly strong for duplicated (meiotic) recombination genes that return to a single copy more rapidly than genome average following polyploidy. To better understand the evolutionary forces underlying duplicate loss, we analysed how varying copy numbers of MSH4, an essential meiotic recombination gene, influences crossover formation in allotetraploid Brassica napus. We show that faithful chromosome segregation and crossover frequencies between homologous chromosomes are unchanged with MSH4 duplicate loss; by contrast, crossovers between homoeologous chromosomes (which result in genomic rearrangements) decrease with reductions in MSH4 copy number. We also found that inter-homoeologue crossovers originate almost exclusively from the MSH4-dependent crossover pathway. Limiting the efficiency of this pathway by decreasing the copy number of key meiotic recombination genes could therefore contribute to adaptation to polyploidy, by promoting regular chromosome segregation and genomic stability. TextGene duplication and gene loss are two driving forces in evolution 1-3 . These two mechanisms are well illustrated by the evolution of the meiotic recombination machinery. At the outset, the emergence of meiosis required key evolutionary breakthroughs 4-6 that were all made possible through iterative gene duplications followed by acquisition of new functions. These include, among others, the formation of programmed DNA double-strand breaks by SPO11 proteins 7 , the promotion of double-strand break repair using homologous templates by DMC1, RAD51 and some other related proteins 8 or the resolution of recombination intermediates as crossovers by MSH and MLH proteins 9 . After this initial phase, genes involved in meiotic recombination (and DNA repair in general) have tended to return preferentially to single copy following subsequent duplications 10,11 , with some