Abstract
Most asexual species of fungi have either lost sexuality recently, or they experience recombination by cryptic sexual reproduction. Verticillium dahliae is a plant-pathogenic, ascomycete fungus with no known sexual stage, even though related genera have well-described sexual reproduction. V. dahliae reproduces mitotically and its population structure is highly clonal. However, previously described discrepancies in phylogenetic relationships among clonal lineages may be explained more parsimoniously by recombination than mutation; therefore, we looked for evidence of recombination within and between clonal lineages. Genotyping by sequencing was performed on 141 V. dahliae isolates from diverse geographic and host origins, resulting in 26,748 single-nucleotide polymorphisms (SNPs). We found a strongly clonal population structure with the same lineages as described previously by vegetative compatibility groups (VCGs) and molecular markers. We detected 443 recombination events, evenly distributed throughout the genome. Most recombination events detected were between clonal lineages, with relatively few recombinant haplotypes detected within lineages. The only three isolates with mating type MAT1-1 had recombinant SNP haplotypes; all other isolates had mating type MAT1-2. We found homologs of eight meiosis-specific genes in the V. dahliae genome, all with conserved or partially conserved protein domains. The extent of recombination and molecular signs of sex in (mating-type and meiosis-specific genes) suggest that V. dahliae clonal lineages arose by recombination, even though the current population structure is markedly clonal. Moreover, the detection of new lineages may be evidence that sexual reproduction has occurred recently and may potentially occur under some circumstances. We speculate that the current clonal population structure, despite the sexual origin of lineages, has arisen, in part, as a consequence of agriculture and selection for adaptation to agricultural cropping systems.
Highlights
Asexual reproduction has evolved from sexually reproducing ancestors in almost all major groups of eukaryotes, except birds and mammals, and confers several short-term advantages [1]
We refer to lineages inferred from single-nucleotide polymorphisms (SNPs) genotyping as 2A, 4B, etc., after their respective vegetative compatibility groups (VCGs), but we drop the VCG designation because lineages are defined by SNP haplotypes, not heterokaryon incompatibility
We conclude that SNPs identified by genotyping by sequencing (GBS) are distributed throughout the V. dahliae genome, and are appropriate for analyzing genome-wide patterns of recombination
Summary
Asexual reproduction has evolved from sexually reproducing ancestors in almost all major groups of eukaryotes, except birds and mammals, and confers several short-term advantages [1]. Asexuality has evolved independently many times from sexual ancestors [6]. The sexual stage is either unknown or has been observed only rarely in the laboratory, and inferences of recombination and cryptic sex have been made indirectly from population-genetic analyses [9,10,11,12] and, more recently, from the analysis of genomes showing molecular signs of sex [5,13,14,15,16]
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