Delplace Florent, Khafif Mehdi, Stam Remco, Barbacci Adelin, Raffaele Sylvain
Laboratoire des Interactions Plantes-Microbes Environnement (LIPME), INRAE, CNRS, Université de Toulouse, Castanet-Tolosan 31326, France.
Faculty of Agricultural and Nutritional Sciences, Department of Phytopathology and Crop Protection, Institute of Phytopathology, Christian-Albrechts-University, Kiel 24118, Germany.
Plant Cell. 2025 Jun 4;37(6). doi: 10.1093/plcell/koaf105.
Quantitative disease resistance (QDR) is an immune response limiting pathogen damage in plants. It involves transcriptomic reprogramming of numerous genes, each having a small contribution to plant immunity. Despite the broad-spectrum nature of QDR, the evolution of its underlying transcriptome reprogramming remains largely uncharacterized. Here, we analyzed global gene expression in response to the necrotrophic fungus Sclerotinia sclerotiorum in 23 Arabidopsis (Arabidopsis thaliana) accessions of diverse origin and contrasting QDR phenotypes. Over half of the species pan-transcriptome displayed local responses to S. sclerotiorum, with global reprogramming patterns incongruent with accession phylogeny. Due to frequent small-amplitude variations, only ∼11% of responsive genes were common across all accessions, defining a core transcriptome enriched in highly responsive genes. Coexpression and correlation analyses showed that QDR phenotypes result from the integration of the expression of numerous genes. Promoter sequence comparisons revealed that variation in DNA-binding sites within cis-regulatory regions contributes to gene expression rewiring. Finally, transcriptome-phenotype maps revealed abundant neutral networks connecting diverse QDR transcriptomes with no loss of resistance, hallmarks of robust and evolvable traits. This navigability associated with regulatory variation in core genes highlights their role in QDR evolvability. This work provides insights into the evolution of complex immune responses, informing models for plant disease dynamics.
定量抗病性（QDR）是植物中限制病原体损害的一种免疫反应。它涉及众多基因的转录组重编程，每个基因对植物免疫的贡献都很小。尽管QDR具有广谱性，但其潜在转录组重编程的进化在很大程度上仍未得到表征。在这里，我们分析了来自不同来源且具有不同QDR表型的23个拟南芥（Arabidopsis thaliana）种质对坏死营养型真菌核盘菌（Sclerotinia sclerotiorum）的全基因组基因表达。超过一半的物种泛转录组对核盘菌表现出局部反应，其全局重编程模式与种质系统发育不一致。由于频繁的小幅度变化，所有种质中只有约11%的响应基因是共同的，从而定义了一个富含高响应性基因的核心转录组。共表达和相关性分析表明，QDR表型是众多基因表达整合的结果。启动子序列比较显示，顺式调控区域内DNA结合位点的变异有助于基因表达的重新连接。最后，转录组-表型图谱揭示了丰富的中性网络，这些网络连接着不同的QDR转录组且不损失抗性，这是稳健且可进化性状的标志。这种与核心基因调控变异相关的可导航性突出了它们在QDR可进化性中的作用。这项工作为复杂免疫反应的进化提供了见解，为植物病害动态模型提供了信息。
