Recombination and repeat-induced point mutation landscapes reveal trade-offs between the sexual and asexual cycles of Magnaporthe oryzae

The fungal disease caused by Magnaporthe oryzae is one of the most devastating diseases that endanger many crops worldwide. Evidence shows that sexual reproduction can be advantageous for fungal diseases as hybridization facilitates host-jumping. However, the pervasive clonal lineages of M. oryzae observed in natural fields contradict this expectation. A better understanding of the roles of recombination and the fungi-specific repeat-induced point mutation (RIP) in shaping its evolutionary trajectory is essential to bridge this knowledge gap. Here we systematically investigate the RIP and recombination landscapes in M. oryzae using a whole genome sequencing data from 252 population samples and 92 cross progenies. Our data reveal that the RIP can robustly capture the population history of M. oryzae, and we provide accurate estimations of the recombination and RIP rates across different M. oryzae clades. Significantly, our results highlight a parent-of-origin bias in both recombination and RIP rates, tightly associating with their sexual potential and variations of effector proteins. This bias suggests a critical trade-off between generating novel allelic combinations in the sexual cycle to facilitate host-jumping and stimulating transposon-associated diversification of effectors in the asexual cycle to facilitate host coevolution. These findings provide unique insights into understanding the evolution of blast fungus. Copyright (c) 2024, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Limited and Science Press. All rights reserved.