Transposon elements shape population divergence of rice blast fungusMagnaporthe oryzae

Abstract

ABSTRACTDynamic transposition of transposable elements (TEs) in fungal pathogens have been shown to have a significant impact on genome stability, gene expression, and virulence to the host. InMagnaporthe oryzae, genome plasticity resulting from TE insertion polymorphisms is a major driving force leading to the rapid evolution and diversification of this rice blast fungus. Despite their importance inM. oryzaepopulation evolution and divergence, our understanding of TEs in this context remains limited. Here we conducted a genome-wide analysis of TE transposition dynamics in the eleven most abundant TE families and transcriptomic analysis in differentM. oryzaepopulations. Our results show that these TEs have specifically expanded in recently isolatedM. oryzaerice populations, with the presence/absence polymorphism of TE insertions highly concordant with population divergence on Geng/Japonicaand Xian/Indicarice cultivars. Among the TE families, POT2 and Mg-SINE were shown to be overrepresented in clade-specific TE insertion events, indicating their essential roles in population divergence. Notably, the genes targeted by clade-specific TEs showed clade-specific expression patterns, suggesting a transcriptional regulation of TEs on targeted genes. Furthermore, population transcriptomic analysis revealed that genes disrupted by POT2 and Mg-SINE insertions exhibited significantly lower expression, implying a silencing function of these TEs on the targeted genes. Our study provides a comprehensive analysis of TEs inM. oryzaepopulations and demonstrates a crucial role of recent TE bursts in adaptive evolution and diversification of theM. oryzaerice-infecting lineage.IMPORTANCEM. oryzaeis the causal agent of the destructive blast disease, which caused massive loss of yield annually worldwide. The fungus diverged into distinct clades during adaptation toward the two rice subspecies, Xian/indica and Geng/japonica. Although the role of TEs in the adaptive evolution was well established, mechanisms underlying how TEs promote the population divergence ofM. oryzaeremains largely unknown. In this study, we reported that TEs shape the population divergence ofM. oryzaeby differentially regulating gene expression between Xian/Indica-infecting and Geng/Japonica-infecting populations. Our results revealed a TE insertion mediated gene expression adaption that led to the divergence ofM. oryzaepopulation infecting different rice subspecies.