Experimental insights into genome reconstruction driven by horizontal transfer of supernumerary chromosomes in Magnaporthe oryzae.

Jianqiang Huang, Guodong Lu, Xiuxiu Li, Guifang Lin, Zonghua Wang, Zhenyu Fang, Yuyong Li, Meilian Chen, Xiali Chen, Xueting Mo, Zhenhui Zhong, Huakun Zheng

Journal: The New phytologist 2025;248(1):140-156

PMID: 40755030

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Abstract

Many pathogenic fungi display 'two-speed genome', with the fast-evolving genomic compartments enriched with repetitive sequences, particularly the transposons, which have been shown to drive the variation of pathogenicity-associated genes. Supernumerary chromosomes (SCs) are known to facilitate genomic variation in fungal pathogens, but their specific role in such processes remains understudied. In this study, we assessed the transferability of SCs between asexual Magnaporthe oryzae strains during co-culture and co-infection, and investigated their role in genome reconstruction through experimental evolution assays. We found that SCs could be horizontally transferred between M. oryzae strains and revealed frequent structural variations facilitated by SCs, including deletions, duplications, translocations, and SC-core chromosome recombinations during and after horizontal transfer. Remarkably, all observed intra- and inter-chromosome rearrangements were confined to core chromosome ends and SCs, indicating a robust role of SCs in facilitating genetic exchange within fast-evolving genomic compartments. Additionally, SC carrying the avirulence gene AvrPik modulates M. oryzae virulence against Pikh rice through horizontal transfer, loss of whole SC, and segmental deletions. Our findings establish SCs as critical players in shaping the diversity and dynamics of the pathogenic fungal genomes, highlighting them as a cradle for the variation of pathogenicity-associated genes.

Address: State Key Laboratory of Agricultural and Forestry Biosecurity, College of Life Sciences, School of Future Technology, and Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.; State Key Laboratory of Agricultural and Forestry Biosecurity, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.; College of Materials and Chemical Engineering, Fujian Key Laboratory on Conservation and Sustainable Utilization of Marine Biodiversity, Minjiang University, Fuzhou, 350108, China.; Basic Forestry and Proteomics Research Center, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.; Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, 610064, China.; State Key Laboratory of Agricultural and Forestry Biosecurity, College of Life Sciences, School of Future Technology, and Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.; Fuzhou Institute of Oceanography, Minjiang University, Fuzhou, 350108, China.; National Engineering Research Center of JUNCAO Technology, College of Juncao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.

DOI: 10.1111/nph.70438

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MeSH Terms: Gene Transfer, Horizontal, Chromosomes, Fungal, Genome, Fungal, Oryza, Virulence, Ascomycota, Magnaporthe