Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

Abstract

Supernumerary mini-chromosomes-a unique type of genomic structural variation-have been implicated in the emergence of virulence traits in plant pathogenic fungi. However, the mechanisms that facilitate the emergence and maintenance of mini-chromosomes across fungi remain poorly understood. In the blast fungus Magnaporthe oryzae, mini-chromosomes have been first described in the early 1990s but, until very recently, have been overlooked in genomic studies. Here we investigated structural variation in four isolates of the blast fungus M. oryzae from different grass hosts and analyzed the sequences of mini-chromosomes in the rice, foxtail millet and goosegrass isolates. The mini-chromosomes of these isolates turned out to be highly diverse with distinct sequence composition. They are enriched in repetitive elements and have lower gene density than core-chromosomes. We identified several virulence-related genes in the mini-chromosome of the rice isolate, including the polyketide synthase Ace1 and the effector gene AVR-Pik. Macrosynteny analyses around these loci revealed structural rearrangements, including inter-chromosomal translocations between core-and mini-chromosomes. Our findings provide evidence that mini-chromosomes independently emerge from structural rearrangements of core-chromosomes and might contribute to adaptive evolution of the blast fungus. Author summaryThe genomes of plant pathogens often exhibit an architecture that facilitates high rates of dynamic rearrangements and genetic diversification in virulence associated regions. These regions, which tend to be gene sparse and repeat rich, are thought to serve as a cradle for adaptive evolution. Supernumerary chromosomes, i.e. chromosomes that are only present in some but not all individuals of a species, are a special type of structural variation that have been observed in plants, animals, and fungi. Here we identified and studied supernumerary mini-chromosomes in the blast fungus Magnaporthe oryzae, a pathogen that causes some of the most destructive plant diseases. We found that rice, foxtail millet and goosegrass isolates of this pathogen contain mini-chromosomes with distinct sequence composition. All minichromosomes are rich in repetitive genetic elements and have lower gene densities than core-chromosomes. Further, we identified virulence-related genes on the mini-chromosome of the rice isolate. We observed large-scale genomic rearrangements around these loci, indicative of a role of mini-chromosomes in facilitating genome dynamics. Taken together, our results indicate that mini-chromosomes facilitate genome rearrangements and possibly adaptive evolution of the blast fungus.

Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain

“…Given that the rice-infecting lineage of M. oryzae is estimated to have arisen about 7,000-9,000 years ago (Couch et al, 2005;Latorre et al, 2020), our findings are consistent with the view that Pik-1 alleles evolved during rice domestication as previously suggested (Kanzaki et al, 2012;Zhai et al, 2011). In addition, AVR-Pik is widespread in rice-infecting isolates but absent in other blast fungus lineages (Langner et al, 2020;Latorre et al, 2020;Yoshida et al, 2016). Therefore, it is tempting to speculate that the rice agroecosystem has created the ecological context that led to Pik neofunctionalization towards recognition of the new pathogen threat imposed by the blast fungus.…”

Differential loss of effector genes in three recently expanded pandemic clonal lineages of the rice blast fungus

“…Future experiments will tease out the degree to which the distinct effector repertoires of the clonal lineages of M. oryzae reflect their adaptation to the rice host and their evolutionary history. Such analyses will require new genomic resources that permit a more accurate identification of effectors in canonical chromosomes and minichromosomes [60,61]. To this aim, it will be fundamental to generate multiple reference genomes sequenced with long-read technologies in conjunction with a detailed characterization of structural variation and genomic rearrangements, which will include a per isolate inventory of mini-chromosome repertoires.…”

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

“…Future experiments will tease out the degree to which the distinct effector repertoires of the clonal lineages of M. oryzae reflect their adaptation to the rice host and their evolutionary history. Such analyses will require new genomic resources that permit a more accurate identification of effectors in canonical chromosomes and mini-chromosomes [58] . To this aim, it will be fundamental to generate multiple reference genomes sequenced with long-read technologies in conjunction with a detailed characterization of structural variation and genomic rearrangements, which will include a per isolate inventory of mini-chromosome repertoires.…”