The fungus Leptosphaeria maculans has an exceptionally long and complex relationship with its host plant, Brassica napus, during which it switches between different lifestyles, including asymptomatic, biotrophic, necrotrophic, and saprotrophic stages. The fungus is also exemplary of two-speed genome organisms in which gene-rich and repeat-rich regions alternate. Except for a few stages of plant infection under controlled conditions, nothing is known about the genes mobilized by the fungus throughout its life cycle, which may last several years in the field. We show here that about 9% of the genes of this fungus are highly expressed during its interactions with its host plant. These genes are distributed into eight well-defined expression clusters, corresponding to specific infection lifestyles or to tissue-specific genes. All expression clusters are enriched in effector genes, and one cluster is specific to the saprophytic lifestyle on plant residues. One cluster, including genes known to be involved in the first phase of asymptomatic fungal growth in leaves, is re-used at each asymptomatic growth stage, regardless of the type of organ infected. The expression of the genes of this cluster is repeatedly turned on and off during infection. Whatever their expression profile, the genes of these clusters are located in regions enriched in heterochromatin, either constitutive or facultative. These findings provide support for the hypothesis that fungal genes involved in niche adaptation are located in heterochromatic regions of the genome, conferring an extreme plasticity of expression. This work opens up new avenues for plant disease control, by identifying stage-specific effectors that could be used as targets for the identification of novel durable disease resistance genes, or for the in-depth analysis of chromatin remodeling during plant infection, which could be manipulated to interfere with the global expression of effector genes at crucial stages of plant infection.

中文翻译：

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大规模转录组学研究真菌植物病原体与其宿主植物相互作用的两年生命

真菌Leptosphaeria maculans与寄主植物甘蓝型油菜有着极长而复杂的关系，在此过程中，它会在不同的生活方式之间切换，包括无症状，生物营养，坏死和腐生阶段。真菌也是其中基因富集区和重复富集区交替的两速基因组生物的例证。除了在受控条件下植物感染的几个阶段外，对于真菌在其整个生命周期中可能会持续数年的生命周期中动员的基因一无所知。我们在这里显示该真菌与其宿主植物相互作用期间高表达该真菌的基因的约9％。这些基因被分为八个明确定义的表达簇，分别对应于特定的感染生活方式或组织特异性基因。所有表达簇都富含效应子基因，其中一个簇对植物残体的腐生性生活具有特异性。一个簇，包括已知与叶片无症状真菌生长的第一阶段有关的基因，无论感染器官的类型如何，都可以在每个无症状生长阶段重复使用。在感染过程中，该簇基因的表达反复打开和关闭。无论它们的表达谱如何，这些簇的基因都位于组成型或兼性异染色质丰富的区域。这些发现为以下假设提供了支持：与生态位适应有关的真菌基因位于基因组的异色区域中，赋予了极高的表达可塑性。这项工作为控制植物病害开辟了新途径，