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.
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.
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DOI：
10.1371/journal.ppat.1004801
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发表时间：
2015-04
期刊：
影响因子：
6.7
通讯作者：
Zhang Z
中科院分区：
文献类型：
--
作者：
Dong Y;Li Y;Zhao M;Jing M;Liu X;Liu M;Guo X;Zhang X;Chen Y;Liu Y;Liu Y;Ye W;Zhang H;Wang Y;Zheng X;Wang P;Zhang Z
病原生物的基因组动力学是由病原体和宿主共同进化驱动的，在这种进化中，病原体基因组通过产生各种分离物来克服具有不同遗传背景的宿主施加的压力。同样的原理也适用于稻瘟病菌和水稻寄主；然而，不同分离株之间的遗传变异在很大程度上仍然未知，特别是在基因组和转录组水平上。本研究应用基因组学和转录组学分析工具对稻瘟病分枝杆菌98-06进行了研究。与参考菌株70-15相比，分离菌株98-06有独特的1.4 Mb基因组序列。基于64个已知的致病性相关（PaR）基因，全基因组表达谱揭示了M. oryzae存在两种关键表达模式。此外，还鉴定了134个具有不同偏析模式的候选效应体。5种被测蛋白可抑制bax介导的烟叶细胞程序性死亡。分离特异性效应候选物Iug6、Iug9和PaR候选物Iug18的特性表明它们在真菌繁殖和致病性中发挥作用。此外，Iug6和Iug9仅位于生物营养界面复合物（BIC）中，它们的过表达会抑制水稻防御相关基因的表达，这表明它们可能通过抑制寄主体内的SA和ET通路参与生物营养。因此，我们的研究发现了与高侵袭性m.o ryzae田间分离物98-06的致病性有关的新的效应蛋白和PaR蛋白，并揭示了m.o ryzae与水稻宿主相互作用进化的分子和基因组动力学。病原体的遗传变异，例如稻瘟病的致病因子，经常导致抗病品种的规避。先前对模式生物的全基因组分析表明，病原体效应物也在快速进化，特别是在基因组可塑性高的区域。然而，不同分离株之间的遗传变异在很大程度上仍然未知，特别是在基因组和转录组水平上。在这项研究中，我们提供了水稻稻瘟病田优势分离物的系统基因组和相互作用转录组图谱，从而鉴定出134个候选效应物。两个效应物Iug6和Iug9以及一个致病性相关（PaR）基因产物Iug18进行了功能表征。我们发现Iug6和Iug9位于生物营养界面复合物（BIC）中，它们的过表达会抑制水稻防御相关基因的表达，而Iug18可能是一种新的PaR蛋白。我们的研究支持了一个假设，即分离的独特基因可能是m.o ryzae群体遇到不同环境时遗传变异的一个来源。我们的研究也有助于进一步了解M. oryzae致病性的效应因子和基因组变异。
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. Genetic variations in pathogens, such as the causal agent of rice blast Magnaporthe oryzae, often lead to circumvention of disease-resistance cultivars. Previous genome-wide analyses of model organisms suggest that pathogen effectors are also rapidly evolving, especially in regions with high genome plasticity. However, genetic variations among different isolates remain largely unknown in M. oryzae, particularly at the genome and transcriptome levels. In this study, we provided a systematic genomic and interaction transcriptome profile for a dominant rice blast field isolate, resulting in identification of 134 candidate effectors. Two effectors, Iug6 and Iug9, and one pathogenicity-related (PaR) gene product, Iug18, were subjected to functional characterization. We found that Iug6 and Iug9 are located in the biotrophic interfacial complex (BIC) and their overexpression leads to suppression of defense-related gene expression in rice, while Iug18 appears to be a novel PaR protein. Our studies support the hypothesis that isolate-unique genes may serve as a source of genetic variability in the M. oryzae population encountering different environments. Our studies also facilitate further understanding of effectors and genomic variations in pathogenicity of M. oryzae.
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