Transcriptome and Metabolite Profiling of the Infection Cycle of Zymoseptoria tritici on Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifestyle Definition
Transcriptome and Metabolite Profiling of the Infection Cycle of Zymoseptoria tritici on Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifestyle Definition
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DOI：
10.1104/pp.114.255927
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发表时间：
2015-03-01
期刊：
影响因子：
7.4
通讯作者：
Courbot, Mikael
中科院分区：
文献类型：
--
作者：
Rudd, Jason J.;Kanyuka, Kostya;Courbot, Mikael
半生物营养真菌ZymosepVictoria tritici引起小麦(Triticum Aestivum)斑点病。病原菌在小麦上的繁殖没有细胞穿透，这表明在整个病害周期中，真菌和植物之间发生了动态和密切的细胞间通讯。本研究采用深层RNA测序和代谢组学方法，对小麦叶片上小麦发酵菌的无性繁殖周期中的植物生理和病原菌进行了研究。3000多个病原基因、7000多个小麦基因和300多个代谢物被差异调控。有趣的是，单个真菌染色体对整个基因表达变化的贡献并不相同。在接种的叶片中检测到可能的寄主防御基因的早期转录下调。在小麦酵母菌无症状的定植过程中，几乎没有证据表明真菌从植物中获得营养，相反，它可能利用脂肪和脂肪酸储存来生长。然而，真菌随后在转向坏死性生长和繁殖的过程中操纵特定的植物碳水化合物，包括果聚糖代谢物。这一转变与茉莉酸生物合成基因的表达增加和其他植物防御反应的大规模激活相吻合。真菌编码次生代谢物簇和分泌的效应蛋白的基因具有不同的侵染阶段特异性表达模式，尽管功能分析表明许多基因在毒力方面具有重叠/冗余功能。通过本研究揭示了小麦发酵菌对小麦的致病方式，包括一种生长缓慢的胞外和营养有限的病原菌对小麦的最初防御抑制，然后在繁殖过程中激活防御(HYPER)，揭示了对半生物营养植物感染的概念定义的微妙修改。
The hemibiotrophic fungus Zymoseptoria tritici causes Septoria tritici blotch disease of wheat (Triticum aestivum). Pathogen reproduction on wheat occurs without cell penetration, suggesting that dynamic and intimate intercellular communication occurs between fungus and plant throughout the disease cycle. We used deep RNA sequencing and metabolomics to investigate the physiology of plant and pathogen throughout an asexual reproductive cycle of Zymoseptoria tritici on wheat leaves. Over 3,000 pathogen genes, more than 7,000 wheat genes, and more than 300 metabolites were differentially regulated. Intriguingly, individual fungal chromosomes contributed unequally to the overall gene expression changes. Early transcriptional down-regulation of putative host defense genes was detected in inoculated leaves. There was little evidence for fungal nutrient acquisition from the plant throughout symptomless colonization by Zymoseptoria tritici, which may instead be utilizing lipid and fatty acid stores for growth. However, the fungus then subsequently manipulated specific plant carbohydrates, including fructan metabolites, during the switch to necrotrophic growth and reproduction. This switch coincided with increased expression of jasmonic acid biosynthesis genes and large-scale activation of other plant defense responses. Fungal genes encoding putative secondary metabolite clusters and secreted effector proteins were identified with distinct infection phase-specific expression patterns, although functional analysis suggested that many have overlapping/redundant functions in virulence. The pathogenic lifestyle of Zymoseptoria tritici on wheat revealed through this study, involving initial defense suppression by a slow-growing extracellular and nutritionally limited pathogen followed by defense (hyper) activation during reproduction, reveals a subtle modification of the conceptual definition of hemibiotrophic plant infection.