High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae

Abstract

Microbial populations depend on genetic variation to respond to novel environmental challenges. Plant pathogens are notorious for their ability to overcome pesticides and host resistance genes as a result of genetic changes. We report here that in particular hybrid strains of Phytophthora sojae, an oomycete pathogen of soybean, high frequency mitotic gene conversion rapidly converts heterozygous loci to homozygosity, resulting in heterokaryons containing highly diverse populations of diploid nuclei. In hybrids involving strain P7076, conversion rates of up to 3 ؋ 10 ؊2 per locus per nucleus per generation were observed. In other hybrids, rates were of the order of 5 ؋ 10 ؊5 . Independent gene conversion was observed within a selected linkage group including loci as close as 0.7 kb apart and in unlinked markers throughout the genome. Gene conversions continued throughout vegetative growth and were stimulated by further sexual reproduction. At many loci, conversion showed extreme disparity, with one allele always being lost, suggesting that conversion was initiated by allele-specific double-stranded breaks. Pedigree analysis indicated that individual loci undergo multiple independent conversions within the nuclei of a vegetative clone and that conversion may be preceded by a heritable ''activation'' state.

Deleterious Mutations and Selection for Sex in Finite Diploid Populations

“…Nevertheless, mitotic recombination is thought to occur at rate $0.8 3 10 À4 per cell per generation in yeast (Mandegar and Otto 2007 and references therein), while LOH is often observed at a frequency of 10 À4 -10 À5 in normal cells in vivo, in mice and in humans (Tischfield 1997;Holt et al 1999;Shao et al 1999;Carr and Gottschling 2008). Furthermore, Chamnanpunt et al (2001) measured rates of mitotic gene conversion ranging from 3 3 10 À2 to 10 À5 in hybrids of the oomycete Phytophthora sojae. Finally, LOH has been estimated to occur at rate $10 À4 per locus per generation in an experiment involving mutation-accumulation lines of asexual Daphnia (Omilian et al 2006).…”

Molecular Genetics of Pathogenic Oomycetes

“…Many oomycetes, including P. infestans and several other Phytophthora species, are known to exhibit tremendous phenotypic variation, both in the field and in culture, even during asexual reproduction (9,10,16,22,34). The genetic basis of this phenomenon is not clear, but it could be due to genome instability, perhaps caused by transposable elements, gene conversion, mitotic recombination, and/or dispensable chromosomes (10,22,34,57). Sequences similar to transposable elements are abundant in Phytophthora genomes.…”

“…Recently, mitotic gene conversion was observed to occur in hybrid strains of P. sojae at remarkably high frequencies, as high as 3 ϫ 10 2 conversions per locus per nucleus per generation (10). The conversion tracts were shorter than 1 kb, with no evidence for crossing over or mitotic recombination (10).…”

“…Recently, mitotic gene conversion was observed to occur in hybrid strains of P. sojae at remarkably high frequencies, as high as 3 ϫ 10 2 conversions per locus per nucleus per generation (10). The conversion tracts were shorter than 1 kb, with no evidence for crossing over or mitotic recombination (10). Mitotic gene conversion resulted in the reassortment of loci that show close linkage during meiotic recombination, suggesting that in nature this mechanism could rapidly generate unique genetic types (10).…”

Developmental and environmental variation in genomes

“…During development, the genome also undergoes processes such as the high gene conversion rate detected in Phytophthora sojae (Chamnanpunt et al, 2001) or immunoglobulin gene diversification in animals (McCormack et al, 1991). However, these changes appear unlikely to contribute significantly to the increase or decease of genomic DNA content.…”