Whole genome regulatory effect of MoISW2 and consequences for the evolution of the rice plant pathogenic fungus Magnaporthe oryzae

Bibliographic Details
Title: Whole genome regulatory effect of MoISW2 and consequences for the evolution of the rice plant pathogenic fungus Magnaporthe oryzae
Authors: Mengtian Pei, Yakubu Saddeeq Abubakar, Hina Ali, Lianyu Lin, Xianying Dou, Guodong Lu, Zonghua Wang, Stefan Olsson, Ya Li
Source: mBio, Vol 15, Iss 10 (2024)
Publisher Information: American Society for Microbiology, 2024.
Publication Year: 2024
Collection: LCC:Microbiology
Subject Terms: heterochromatin, epigenetics, nucleosomes, avirulence genes, retrotransposons, evolution, Microbiology, QR1-502
More Details: ABSTRACT Isw2 proteins, ubiquitous across eukaryotes, exhibit a propensity for DNA binding and exert dynamic influences on local chromosome condensation in an ATP-dependent fashion, thereby modulating the accessibility of neighboring genes to transcriptional machinery. Here, we report the deletion of a putative MoISW2 gene, yielding substantial ramifications on plant pathogenicity. Subsequent gene complementation and chromatin immunoprecipitation sequencing (ChIP-seq) analyses were conducted to delineate binding sites. RNA sequencing (RNA-seq) assays revealed discernible impacts on global gene regulation along chromosomes in both mutant and wild-type strains, with comparative analyses against 55 external RNA-seq data sets corroborating these findings. Notably, MoIsw2-mediated binding and activities delineate genomic loci characterized by pronounced gene expression variability proximal to MoIsw2 binding sites, juxtaposed with comparatively stable expression in surrounding regions. The contingent genes influenced by MoIsw2 activity predominantly encompass niche-determinant genes, including those encoding secreted proteins, secondary metabolites, and stress-responsive elements, alongside avirulence genes. Furthermore, our investigations unveil a spatial correlation between MoIsw2 binding motifs and known transposable elements (TEs), suggesting a potential interplay wherein TE transposition at these loci could modulate the transcriptional landscape of Magnaporthe oryzae in a strain-specific manner. Collectively, these findings position MoIsw2 as a plausible master regulator orchestrating the delicate equilibrium between genes vital for biomass proliferation, akin to housekeeping genes, and niche-specific determinants crucial for ecological adaptability. Stress-induced TE transposition, in conjunction with MoIsw2 activity, emerges as a putative mechanism fostering enhanced mutagenesis and accelerated evolution of niche-determinant genes relative to housekeeping counterparts.IMPORTANCEIsw2 proteins are conserved in plants, fungi, animals, and other eukaryotes. We show that a fungal Isw2 protein in the rice pathogen Magnaporthe oryzae binds to retrotransposon (RT) DNA motifs and affects the epigenetic gene expression landscape of the fungal genome. Mainly ecological niche determinant genes close to the binding motifs are affected. RT elements occur frequently in DNA between genes in most organisms. They move place and multiply in the genome, especially under physiological stress. We further discuss the Isw2 and RT combined activities as a possible sought-after mechanism that can cause biased mutation rates and faster evolution of genes necessary for reacting to abiotic and biotic challenges. The most important biotic challenges for plant pathogens are the ones from the host plants’ innate immunity. The overall result of these combined activities will be an adaptation-directed evolution of niche-determinant genes.
Document Type: article
File Description: electronic resource
Language: English
ISSN: 2150-7511
Relation: https://doaj.org/toc/2150-7511
DOI: 10.1128/mbio.01590-24
Access URL: https://doaj.org/article/dd13635d57c74474803a0b75039d2a42
Accession Number: edsdoj.13635d57c74474803a0b75039d2a42
Database: Directory of Open Access Journals
More Details
ISSN:21507511
DOI:10.1128/mbio.01590-24
Published in:mBio
Language:English