Transposable elements impact the population divergence of rice blast fungus Magnaporthe oryzae

Author:

Lin Lianyu1,Sun Ting1,Guo Jiayuan12,Lin Lili1,Chen Meilian2,Wang Zhe1,Bao Jiandong3,Norvienyeku Justice4ORCID,Zhang Dongmei1,Han Yijuan2,Lu Guodong1,Rensing Christopher5,Zheng Huakun1ORCID,Zhong Zhenhui16ORCID,Wang Zonghua12ORCID

Affiliation:

1. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, China

2. Fuzhou Institute of Oceanography, Minjiang University, Fuzhou, China

3. State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, China

4. Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, College of Plant Protection, Hainan University, Haikou, China

5. Institute of Environmental Microbiology, College of Resource and Environment, Fujian Agriculture and Forestry University, Fuzhou, China

6. Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Sciences, Sichuan University, Chengdu, China

Abstract

ABSTRACT Dynamic transposition of transposable elements (TEs) in fungal pathogens has significant impact on genome stability, gene expression, and virulence to the host. In Magnaporthe oryzae , genome plasticity resulting from TE insertion is a major driving force leading to the rapid evolution and diversification of this fungus. Despite their importance in M. oryzae population 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 11 most abundant TE families in M. oryzae populations. Our results show that these TEs have specifically expanded in recently isolated M. oryzae rice populations, with the presence/absence polymorphism of TE insertions highly concordant with population divergence on Geng/ Japonica and Xian/ Indica rice cultivars. Notably, the genes targeted by clade-specific TEs showed clade-specific expression patterns and are involved in the pathogenic process, suggesting a transcriptional regulation of TEs on targeted genes. Our study provides a comprehensive analysis of TEs in M. oryzae populations and demonstrates a crucial role of recent TE bursts in adaptive evolution and diversification of the M. oryzae rice-infecting lineage. IMPORTANCE Magnaporthe oryzae is 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 of M. oryzae remain largely unknown. In this study, we reported that TEs shape the population divergence of M. oryzae by 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 of M. oryzae population infecting different rice subspecies.

Funder

MOST | National Natural Science Foundation of China

Central Guidance on Local Science and Technology Development Fund of Fujian Province

Publisher

American Society for Microbiology

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