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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.

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.

SUBMITTER: Duan G

PROVIDER: S-EPMC8000120 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the number of studies that have examined the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, we applied experimental evolution and high-throughput pool sequencing to Magnaporthe oryzae, a fungal pathogen that causes massive losses in rice production, to observe the evolution of genome variation. We found that mutations, including single-nucleotide variants (SNVs), insertions and deletions (indels), and transposable element (TE) insertions, accumulated very rapidly throughout the genome of M. oryzae during sequential plant inoculation and preferentially in noncoding regions, while such mutations were not frequently found in coding regions. However, we also observed that new TE insertions accumulated with time and preferentially accumulated at the proximal region of secreted protein (SP) coding genes in M. oryzae populations. Taken together, these results revealed a bias in genetic variation toward noncoding regions and SP genes in M. oryzae and may contribute to the rapid adaptive evolution of the blast fungal effectors under host selection.IMPORTANCE Plants "lose" resistance toward pathogens shortly after their widespread emergence in the field because plant pathogens mutate and adapt rapidly under resistance selection. Thus, the rapid evolution of pathogens is a serious threat to plant health. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the study of the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, by performing an experimental evolution study, we found a bias in genetic variation toward noncoding regions and SPs in the rice blast fungus Magnaporthe oryzae, which explains the ability of the rice blast fungus to maintain high virulence variation to overcome rice resistance in the field.

Project description:Fungi are rich sources of secondary metabolites of pharmaceutical importance, such as antibiotics, antitumor agents, and immunosuppressants, as well as of harmful toxins. Secondary metabolites play important roles in the development and pathogenesis of fungi. LaeA is a global regulator of secondary metabolism and was originally reported in Aspergillus nidulans; however, its role in secondary metabolism in Magnaporthe oryzae has not yet been reported. Here, we investigated the role of a gene homologous to LAEA (loss of AflR expression) of Aspergillus spp. in Magnaporthe oryzae, named M. oryzae LAEA (MoLAEA). Studies on MoLAEA overexpression and knockdown strains have suggested that this gene acts as a negative regulator of sporulation and melanin synthesis. However, it is not involved in the growth and pathogenesis of M. oryzae Transcriptomic data indicated that MoLAEA regulated genes involved in secondary metabolism. Interestingly, we observed (for the first time, to our knowledge) that this gene is involved in benzylpenicillin (penicillin G) synthesis in M. oryzae Overexpression of MoLAEA increased penicillin G production, whereas the silenced strain showed a complete absence of penicillin G compared to its presence in the wild type. We also observed that MoLaeA interacted with MoVeA, a velvet family protein involved in fungal development and secondary metabolism, in the nucleus. This study showed that though MoLAEA may not make any contribution in rice blast fungal pathogenesis, it regulates secondary metabolism in M. oryzae and thus can be further studied for identifying other new uncharacterized metabolites in this fungus.IMPORTANCE M. oryzae causes blast disease, the most serious disease of cultivated rice affecting global rice production. The genome of M. oryzae has been shown to have a number of genes involved in secondary metabolism, but most of them are uncharacterized. In fact, compared to studies of other filamentous fungi, hardly any work has been done on secondary metabolism in M. oryzae It is shown here (for the first time, to our knowledge) that penicillin G is being synthesized in M. oryzae and that MoLAEA is involved in this process. This is the first step in understanding the penicillin G biosynthesis pathway in M. oryzae This study also unraveled the details of how MoLaeA works by forming a nuclear complex with MoVeA in M. oryzae, thus indicating functional conservation of such a gene across filamentous fungi. All these findings open up avenues for more relevant investigations on the genetic regulation of secondary metabolism in M. oryzae.

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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.

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