Data_Sheet_3_Mechanisms of Pine Disease Susceptibility Under Experimental Climate Change.DOCX

Climate change (CC) conditions projected for many temperate areas of the world, expressed by way of excessive temperatures and low water availability, will impact forest health directly by means of abiotic stress but also by predisposing trees to pathogenic attack. However, we do not yet know how such environmental conditions alter the physiology and metabolism of trees to render them more susceptible to pathogens. To explore these mechanisms, we conditioned 3-year-old Austrian pine saplings to a simulated CC environment (combined drought and elevated temperatures), followed by pathogenic inoculation with two sister fungal species characterized by contrasting aggressiveness, Diplodia sapinea (aggressive) and D. scrobiculata (less aggressive). Lesion lengths resulting from infection were measured after 3 weeks to determine phenotypes, while dual transcriptomics analysis was conducted on tissues collected from the margins of developing lesions on separate branches 72 h post inoculation. As expected, climate change conditions enhanced host susceptibility to the less aggressive pathogen, D. scrobiculata, to a level that was not statistically different from the more aggressive D. sapinea. Under controlled climate conditions, D. sapinea induced suppression of critical pathways associated with host nitrogen and carbon metabolism, while enhancing its own carbon assimilation. This was accompanied by suppression of host defense-associated pathways. In contrast, D. scrobiculata infection induced host nitrogen and fatty acid metabolism as well as host defense response. The CC treatment, on the other hand, was associated with suppression of critical host carbon and nitrogen metabolic pathways, alongside defense associated pathways, in response to either pathogen. We propose a new working model integrating concurrent host and pathogen responses, connecting the weakened host phenotype under CC treatment with specific metabolic compartments. Our results contribute to a richer understanding of the mechanisms underlying the oft-observed increased susceptibility to fungal infection in trees under conditions of low water availability and open new areas of investigation to further integrate our knowledge in this critical aspect of tree physiology and ecology.

针对全球诸多温带区域预测的气候变化（Climate Change，CC）情景，以极端高温与水分可利用性下降为典型特征，将通过非生物胁迫直接损害森林健康，同时还会使树木更易遭受病原菌侵染。然而，目前学界尚未明确此类环境条件如何改变树木的生理与代谢过程，进而提升其病原菌侵染易感性。为探究此类潜在机制，本研究将3年生奥地利松幼苗驯化于模拟CC环境（干旱与高温复合胁迫），随后采用两种致病性存在显著差异的姊妹真菌进行病原菌接种：强致病性的Diplodia sapinea与弱致病性的D. scrobiculata。接种3周后测量病斑长度以确定宿主表型，同时于接种后72小时采集分离枝条上正在扩展的病斑边缘组织，开展双重转录组学分析。正如预期，CC环境使宿主对弱致病性病原菌D. scrobiculata的易感性显著提升，其易感程度与强致病性的D. sapinea无统计学差异。在可控气候条件下，D. sapinea会抑制宿主与氮、碳代谢相关的关键通路，同时增强自身的碳同化过程；该过程伴随宿主防御相关通路的抑制。与之相反，D. scrobiculata侵染会激活宿主的氮代谢、脂肪酸代谢通路以及宿主防御响应。而在CC处理组中，无论接种哪种病原菌，宿主的关键碳、氮代谢通路以及防御相关通路均受到抑制。本研究提出了一个整合宿主与病原菌同步响应的全新工作模型，将CC处理下宿主的弱化表型与特定代谢区室建立关联。本研究结果有助于更深入地理解树木在水分可利用性下降条件下真菌侵染易感性升高背后的分子机制，并为进一步整合树木生理与生态学这一关键领域的认知开辟了全新的研究方向。