Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually

Abstract

Sexual reproduction may be cryptic or facultative in fungi and therefore difficult to detect. Magnaporthe oryzae, which causes blast, the most damaging fungal disease of rice, is thought to originate from southeast Asia. It reproduces asexually in all rice-growing regions. Sexual reproduction has been suspected in limited areas of southeast Asia, but has never been demonstrated in contemporary populations. We characterized several M. oryzae populations worldwide both biologically and genetically, to identify candidate populations for sexual reproduction. The sexual cycle of M. oryzae requires two strains of opposite mating types, at least one of which is female-fertile, to come into contact. In one Chinese population, the two mating types were found to be present at similar frequencies and almost all strains were female-fertile. Compatible strains from this population completed the sexual cycle in vitro and produced viable progenies. Genotypic richness and linkage disequilibrium data also supported the existence of sexual reproduction in this population. We resampled this population the following year, and the data obtained confirmed the presence of all the biological and genetic characteristics of sexual reproduction. In particular, a considerable genetic reshuffling of alleles was observed between the 2 years. Computer simulations confirmed that the observed genetic characteristics were unlikely to have arisen in the absence of recombination. We therefore concluded that a contemporary population of M. oryzae, pathogenic on rice, reproduces sexually in natura in southeast Asia. Our findings provide evidence for the loss of sexual reproduction by a fungal plant pathogen outside its centre of origin.

Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae

“…Loss of sexual fertility also appears to have a role in lineage maintenance. The rice lineage, in particular, is single mating type and female sterile throughout most of its range, which would reduce the chance of outcrossing sex with members of other lineages (50). Our analyses rejected the null hypothesis of clonality in all lineages, but they provided no time frame for the detected recombination events.…”

Wheat blast disease: danger on the move

“…Although most rice pathogens isolated around the world have low levels of sexual fertility, there is growing evidence that some MoO populations still reproduce sexually in their putative center of origin in the Himalayan foothills of India and China (Zeigler 1998;Saleh et al 2012b). Again, this is based on occurrence of frequent female-fertile rice isolates with both mating types, and on evidence of recombination in isolates sampled in consecutive years (Saleh et al 2012b). In contrast, migration of MoO strains around the world has been accompanied by loss of female fertility and mating ability.…”

What does the geography of parthenogenesis teach us about sex?

“…Being an agricultural pest has also been shown often to be associated with parthenogenesis [12,130]. Some globally spreading pest species of fungi are known to use only vegetative reproduction outside their native range, where they are normally only facultative asexuals, despite several independent introductions being documented [43].…”

“…in plants [38], animals, [39], fungi [40]), and with vegetative reproduction, where the new individual stems from a collection of somatic cells which usually results in relatively lower dispersal compared with the production of zygotes (e.g. plants [41], animals [42], fungi [43], algae [44]). The founder of the term geographic parthenogenesis himself remarked that a northerly distribution of asexuality was probably not restrained to parthenogenetic species: Vandel cites instances of aquatic angiosperms that reproduce solely via bulbils in the north of Europe [1].…”