Recent co-evolution of two pandemic plant diseases in a multi-hybrid swarm

Abstract

Most plant pathogens exhibit host specificity but when former barriers to infection break down, new diseases can rapidly emerge. For a number of fungal diseases, there is increasing evidence that hybridization plays a major role in driving host jumps. However, the relative contributions of existing variation versus new mutations in adapting to new host(s) is unclear. Here we reconstruct the evolutionary history of two recently emerged populations of the fungus Pyricularia oryzae that are responsible for two new plant diseases: wheat blast and grey leaf spot of ryegrasses. We provide evidence that wheat blast/grey leaf spot evolved through two distinct mating episodes: the first occurred ~60 years ago, when a fungal individual adapted to Eleusine mated with another individual from Urochloa. Then, about 10 years later, a single progeny from this cross underwent a series of matings with a small number of individuals from three additional host-specialized populations. These matings introduced non-functional alleles of two key host-specificity factors, whose recombination in a multi-hybrid swarm probably facilitated the host jump. We show that very few mutations have arisen since the founding event and a majority are private to individual isolates. Thus, adaptation to the wheat or Lolium hosts appears to have been instantaneous, and driven entirely by selection on repartitioned standing variation, with no obvious role for newly formed mutations.

Rapid mini‐chromosome divergence among fungal isolates causing wheat blast outbreaks in Bangladesh and Zambia

“…The wheat blast population that has been expanding in South America since before its first discovery in 1985 is genetically complex. Indeed, a recent analysis showed that individual MoT genomes are composed of admixture contributions of chromosome segments derived from five different host-adapted populations of M. oryzae (Rahnama et al, 2023). Rahnama et al suggest the present-day population in South America is structured according to chromosomal haplotypes that were defined when various progeny inherited chromosome segments from different donors through sexual recombination.…”

Tools for pathogen genetic surveillance: Lessons from the ash dieback invasion of Europe

“…Advancing genomic technologies are particularly tractable for the identification of emergent pathogens, especially in cases where culturing requires species-specific knowledge. Sequence-based methods can also be used to understand pathogen populations: to identify sources and important genomic regions, to inform management strategies to reduce transfers between reservoirs of diversity (e.g., [ 14 , 15 ]). Under investigated but equally important, we outline how genomic surveillance can identify haplotypic and structural variation which also facilitate introduction of novel diversity.…”

“…In many fungi, the somatic tissues are haploid and the power to detect the influence of recombination increases as assembly haplotypic contiguity increases, from targeted methods to pangenomics (see Table 1 ). At the species level, hybridisation recombines divergent genetic diversity and has been associated with host jumps [ 23 ] and increased pathogenicity, e.g., Dutch elm disease [ 15 ], and is visible as introgression [ 14 ].…”

“…fraxineus invasion shows that recombination does operate, increasing the potential of any further introduced polymorphism [ 18 ]. Progress in our understanding of the impact of recombination in pathogen invasion may be made by studying pathogen invasions of crops from wild crop relatives (e.g., [ 14 , 25 ]).…”

Distinct genomic contexts predict gene presence–absence variation in different pathotypes of Magnaporthe oryzae

“…Exchange of genetic information between host-specific isolates is thought to be rare, though there is clear evidence of such exchanges ( Gladieux, Condon, et al . 2018 ; Rahnama et al . 2023 ).…”