Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity-related genes, revealing gene gain and lose dynamics in genome evolution.

Yanhan Dong,Wenwu Ye,Xinyu Liu,Haifeng Zhang,Maofeng Jing,Ying Li,Yongfeng Liu,Ping Wang,Yue Chen,Yuanchao Wang,Miaomiao Zhao,Xiaobo Zheng,Yanhong Liu,Muxing Liu,Xing Zhang,Zhengguang Zhang,Xianxian Guo,Xiaorong Lin

doi:10.1371/journal.ppat.1004801

Abstract

Genome dynamics of pathogenic organisms are driven by pathogen and host co-evolution, in which pathogen genomes are shaped to overcome stresses imposed by hosts with various genetic backgrounds through generation of a variety of isolates. This same principle applies to the rice blast pathogen Magnaporthe oryzae and the rice host; however, genetic variations among different isolates of M. oryzae remain largely unknown, particularly at genome and transcriptome levels. Here, we applied genomic and transcriptomic analytical tools to investigate M. oryzae isolate 98-06 that is the most aggressive in infection of susceptible rice cultivars. A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15. Genome-wide expression profiling revealed the presence of two critical expression patterns of M. oryzae based on 64 known pathogenicity-related (PaR) genes. In addition, 134 candidate effectors with various segregation patterns were identified. Five tested proteins could suppress BAX-mediated programmed cell death in Nicotiana benthamiana leaves. Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity. Moreover, Iug6 and Iug9 are located exclusively in the biotrophic interfacial complex (BIC) and their overexpression leads to suppression of defense-related gene expression in rice, suggesting that they might participate in biotrophy by inhibiting the SA and ET pathways within the host. Thus, our studies identify novel effector and PaR proteins involved in pathogenicity of the highly aggressive M. oryzae field isolate 98-06, and reveal molecular and genomic dynamics in the evolution of M. oryzae and rice host interactions.

Highlights

Rice (Oryza sativa) is one of the most important staple food crops for more than half of the global human population [1]
Genetic variations among different isolates remain largely unknown in M. oryzae, at the genome and transcriptome levels
We provided a systematic genomic and interaction transcriptome profile for a dominant rice blast field isolate, resulting in identification of 134 candidate effectors

Summary

Introduction

Rice (Oryza sativa) is one of the most important staple food crops for more than half of the global human population [1]. Recent advances in genetic and genomic technology have allowed M. oryzae to be a tractable model for studying the plant-microbe interaction [10]. Jantasuriyarat and colleagues used large-scale expressed sequence tag (EST) sequencing to profile gene expression at the early stage of the M. oryzae-rice interaction and identified four genes to be involved in the interaction out of 13,570 uniESTs [11]. 100 pathogenesis-related protein genes specific to infection were identified in other studies using EST analysis [10], and four biotrophy-associated secreted (BAS) proteins were found in M. oryzae using microarray [4]. Several studies have identified the presence of an infection structure, known as the biotrophic interfacial complex (BIC), that is involved in mediating the delivery of pathogen effectors into the rice host cytoplasm [4,12]

Methods

Results

Discussion

Conclusion