Origins of Host-Specific Populations of the Blast Pathogen Magnaporthe oryzae in Crop Domestication With Subsequent Expansion of Pandemic Clones on Rice and Weeds of Rice

Abstract

Rice, as a widely and intensively cultivated crop, should be a target for parasite host shifts and a source for shifts to co-occurring weeds. Magnaporthe oryzae, of the M. grisea species complex, is the most important fungal pathogen of rice, with a high degree of host specificity. On the basis of 10 loci from six of its seven linkage groups, 37 multilocus haplotypes among 497 isolates of M. oryzae from rice and other grasses were identified. Phylogenetic relationships among isolates from rice (Oryza sativa), millet (Setaria spp.), cutgrass (Leersia hexandra), and torpedo grass (Panicum repens) were predominantly tree like, consistent with a lack of recombination, but from other hosts were reticulate, consistent with recombination. The single origin of rice-infecting M. oryzae followed a host shift from a Setaria millet and was closely followed by additional shifts to weeds of rice, cutgrass, and torpedo grass. Two independent estimators of divergence time indicate that these host shifts predate the Green Revolution and could be associated with rice domestication. The rice-infecting lineage is characterized by high copy number of the transposable element MGR586 (Pot3) and, except in two haplotypes, by a loss of AVR-Co39. Both mating types have been retained in ancestral, well-distributed rice-infecting haplotypes 10 (mainly temperate) and 14 (mainly tropical), but only one mating type was recovered from several derived, geographically restricted haplotypes. There is evidence of a common origin of both ACE1 virulence genotypes in haplotype 14. Host-haplotype association is evidenced by low pathogenicity on hosts associated with other haplotypes. W IDELY distributed, high-density populations, such commonly follows (Tibayrenc et al. 1991; Maynard as those of cultivated crops or humans, are large Smith et al. 1993; Brasier and Buck 2001). While we targets for host shifts by parasites. After crossing host would expect that virulence determinants in a pandemic species boundaries, successful shifts culminate with speclone would remain associated and modified only cialization and genetic divergence on the new host through mutation, any genetic exchange with recombi- (Antonovics et al. 2002). If the parasite crosses a species nation would shuffle these determinants into novel combarrier only once, virulence determinants would derive binations across the parasite population. Within large from this common origin. In contrast, if the target host pathogen populations, recombination would increase species is invaded in multiple, independent host shifts, the rate at which multiple virulence factors could comvirulence could have multiple, fundamentally different bine to generate "super parasite" genotypes (Crow and determinants among host populations (MacLeod et al. Kimura 1970). 2001.The rice blast pathosystem is a model system not only After successful establishment on a new host, espefor plant-pathogen interactions (Valent 1990; Talbot cially one that is abundant and relatively genetically 2003), but also for host ...

Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi

“…Additionally, in a single species, clonal and recombining reproduction can be temporally or spatially separated. In some fungi causing disease of crop plants, reproduction is clonal in agricultural environments, but elsewhere populations retain the ancestral capacity for sexual recombination (Taylor et al 1999;Couch et al 2005). Clonal or inbreeding fungi should be able to invade more distant regions more easily because only one individual is needed to establish a population.…”

“…Conversely, for fungi whose gametes can disperse long distances, e.g. among the many fungi showing host preference, Armillaria (Basidiomycota; Anderson & Ullrich 1979), Heterobasidion (Basidiomycota; Chase & Ullrich 1990), Sclerotinia (Ascomycota; Carbone & Kohn 2001) or Magnaporthe (Ascomycota; Couch et al 2005), allopatry would seem to be the most effective premating reproductive barrier. If everything were everywhere, it is difficult to see how new species could form in these fungi, or in fungi without host preference, like Schizophyllum or Neurospora.…”

Translocation ofMagnaporthe oryzaeEffectors into Rice Cells and Their Subsequent Cell-to-Cell Movement

“…For the eukaryotic pathogens, which are less-studied than prokaryotic pathogens, this raises the major question of how effectors are delivered across the plasma membrane to reach the host cytoplasm. We are addressing this question by studying rice blast disease, which is caused by the hemibiotrophic, ascomycetous fungus Magnaporthe oryzae (Couch et al, 2005;Dean et al, 2005;Ebbole, 2007;Wilson and Talbot, 2009). Rice blast continues to pose a threat to global food supplies despite decades of effort to control this disease (Wang and Valent, 2009).…”

Regulatory network of genes associated with stimuli sensing, signal transduction and physiological transformation of appressorium inMagnaporthe oryzae

“…After gaining entry into host cells, M. oryzae invades in a hemibiotrophic lifestyle. Invasive hyphae are enclosed by the host extra-invasive-hyphal membrane within 36 hours of biotrophic growth and extend into the neighbouring cells via the plasmodesmata to cause the necrosis of host tissues (Couch et al 2005; Kankanala et al 2007; Nishizawa et al 2016). Although the genetic determinants facilitating this hemi-biotrophic transition are mostly unknown, there are suggestions that effector proteins secreted by M. oryzae play a prominent role in suppressing host immunity during this transition (Zhang et al 2014b).…”