Global transcriptome of the fungal pathogen Sclerotinia sclerotiorum (strain 1980) during the colonization of 23 Accessions of Arabidopsis thaliana

Quantitative disease resistance (QDR) is an almost universal and often broad-spectrum process in plants, serving to limit the damage caused by pathogen infections. It represents the primary form of plant immunity that reduces disease symptoms induced by numerous pathogens actively killing host cells during infection, including the necrotrophic pathogen Sclerotinia sclerotiorum. Investigating the evolutionary origins of QDR against necrotrophic fungi is crucial for comprehending how plant resistance evolves. To explore the diversity of local responses to S. sclerotiorum within a plant species level, we conducted a comprehensive analysis of the entire transcriptomes from 23 accessions of Arabidopsis thaliana, mainly distributed across Europe. More than half on the pan-transcriptome displayed local responses toS. sclerotiorum, including similar transcriptome patterns. Notably, core S. sclerotiorum-responsive genes exhibited a clear gene age pattern, dominated by older genes forming protein-protein networks that continuously acquiring new hubs. Comparative transcriptome analyses revealed QDR is associated with quantitative expression variations specific to accession subsets. By comparison of promoter sequences, we have shown evidence that accession subsets independently evolved and acquired specific cis-regulatory elements, confering Sclerotinia resistance. This scenario suggests multiple exaptation trajectories of novel QDR genes through species-level cis-regulation. This study sheds light on the regulation of QDR-associated genes within a species, contributing to our understanding of the molecular mechanisms of plant fungal resistance. Overall design: Periphery of S. sclerotiorum disease lesions (Ss) and uninfected plants grown together (control), Ss and control samples collected simultaneously in three independent replicates

定量抗病性（Quantitative disease resistance, QDR）是植物中近乎普遍存在且通常具有广谱性的防御机制，可限制病原菌侵染所造成的损伤。其作为植物免疫的主要形式，能够减轻诸多在侵染过程中主动杀死宿主细胞的病原菌所引发的病害症状，其中包括死体营养型病原菌核盘菌（Sclerotinia sclerotiorum）。解析针对死体营养型真菌的QDR演化起源，对于理解植物抗病性的演化机制至关重要。为探究植物物种层面下拟南芥（Arabidopsis thaliana）对核盘菌的局部应答多样性，我们对23份主要分布于欧洲的拟南芥种质株系的全转录组（transcriptome）进行了综合分析。泛转录组（pan-transcriptome）中超过一半的基因呈现出对核盘菌的局部应答，包括相似的转录组表达模式。值得注意的是，核盘菌核心应答基因呈现出清晰的基因年龄分布模式：古老基因占比更高，它们所构建的蛋白质互作网络（protein-protein networks）会持续获得新的枢纽节点。比较转录组分析结果表明，QDR与仅存在于特定种质亚组的定量表达变异密切相关。通过启动子序列比较分析，我们发现不同种质亚组独立演化并获得了特异性顺式调控元件（cis-regulatory elements），从而赋予植株对核盘菌的抗性。该结果表明，通过物种水平的顺式调控，新的QDR基因可通过多条外适应演化路径形成。本研究阐明了物种水平下QDR相关基因的调控机制，有助于我们深入理解植物抗真菌病害的分子机理。实验设计方案：采集核盘菌病害病斑边缘组织（Ss组）与同期种植的未侵染对照植株组织（对照组），两组样本均设置三次独立生物学重复。