Large-Scale Genome Scanning within Exonic Regions Revealed the Contributions of Selective Sweep Prone Genes to Host Divergence and Adaptation in Magnaporthe oryzae Species Complex.

Guohua Duan,Xiaomin Chen,Huiquan Chen,Jiahui Xie,Zonghua Wang,Wei Tang,Yuchan Liu,Huakun Zheng,Jiandong Bao

doi:10.3390/microorganisms9030562

Guohua Duan, Xiaomin Chen + Show 7 more

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https://doi.org/10.3390/microorganisms9030562

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Abstract

Magnaporthe oryzae, one of the most notorious plant pathogens in the agronomic ecosystem, causes a destructive rice blast disease around the world. The blast fungus infects wide arrays of cultivated and non-cultivated plants within the Poaceae. Studies have shown that host speciation exerts selection pressure that drives the evolution and divergence of the M. oryzae population. Population genetic relationship deducted by genome-wide single nucleotide polymorphisms showed that M. oryzae differentiation is highly consistent with the host speciation process. In particular, the rice-infecting population of M. oryzae is distinct from populations from other hosts. However, how genome regions prone to host-mediated selection pressures associated with speciation in M. oryzae, especially at a large-scale population level, has not been extensively characterized. Here, we detected strong evidence of sweep selection throughout the genomes of rice and non-rice pathotypes of M. oryzae population using integrated haplotype score (iHS), cross population extended haplotype homozygosity (XPEHH), and cross population composite likelihood ratio (XPCLR) tests. Functional annotation analyses of the genes associated with host-mediated selection pressure showed that 14 pathogenicity-related genes are under positive selection pressure. Additionally, we showed that 17 candidate effector proteins are under positive and divergent selection among the blast fungus population through sweep selection analysis. Specifically, we find that a divergent selective gene, MGG_13871, is experiencing host-directed mutation in two amino acid residues in rice and non-rice infecting populations. These results provide a crucial insight into the impact of selective sweeping on the differentiation of M. oryzae populations and the dynamic influences of genomic regions in promoting host adaptation and speciation among M. oryzae species.

Highlights

Phylogenetic analysis, principal component analysis (PCA), and population structure component analysis unraveled the relationship between different host-infecting M. oryzae populations
Host specificity is a noticeable genetic characteristic that has been the focus of whole-genome sequencing and multi-locus analysis in previous studies to decipher the genomic parameters of the host diversity of isolates within the M. oryzae spepathotypes from multiple lineages favored the formation of identical isolates with no common cryptic lineages [8]
Host specificity is a noticeable genetic characteristic that has been the focus of whole-genome sequencing and multi-locus analysis in previous studies to decipher the genomic parameters of the host diversity of isolates within the M. oryzae species complex [17,21]

Summary

Introduction

Rice is cultivated globally and feeds more than a half of the world’s people [1]. Magnaporthe oryzae, the causal agent of rice blast disease, is a pathogenic filamentous fungus that causes a 10–30% loss of harvest each year [2,3]. M. oryzae is a multihost pathogen that can infect approximately 50 species of both wild and cultivated plants, especially cereals from the Poaceae family, such as rice, wheat, foxtail millet, and finger millet crops [4], posing a huge threat to global food security [5,6]. Since the whole genomic sequence of M. oryzae laboratory strain 70–15 was first deciphered in 2005 [7], many more

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