National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India.
Plant Pathology Research Institute, Agricultural Research Center (ARC), 9 Gamaa St, Giza, 12619, Egypt.
Plant J. 2020 Jul;103(2):561-583. doi: 10.1111/tpj.14750. Epub 2020 Apr 20.
Pathogen-/microbe-associated molecular patterns (PAMPs/MAMPs) initiate complex defense responses by reorganizing the biomolecular dynamics of the host cellular machinery. The extracellular matrix (ECM) acts as a physical scaffold that prevents recognition and entry of phytopathogens, while guard cells perceive and integrate signals metabolically. Although chitosan is a known MAMP implicated in plant defense, the precise mechanism of chitosan-triggered immunity (CTI) remains unknown. Here, we show how chitosan imparts immunity against fungal disease. Morpho-histological examination revealed stomatal closure accompanied by reductions in stomatal conductance and transpiration rate as early responses in chitosan-treated seedlings upon vascular fusariosis. Electron microscopy and Raman spectroscopy showed ECM fortification leading to oligosaccharide signaling, as documented by increased galactose, pectin and associated secondary metabolites. Multiomics approach using quantitative ECM proteomics and metabolomics identified 325 chitosan-triggered immune-responsive proteins (CTIRPs), notably novel ECM structural proteins, LYM2 and receptor-like kinases, and 65 chitosan-triggered immune-responsive metabolites (CTIRMs), including sugars, sugar alcohols, fatty alcohols, organic and amino acids. Identified proteins and metabolites are linked to reactive oxygen species (ROS) production, stomatal movement, root nodule development and root architecture coupled with oligosaccharide signaling that leads to Fusarium resistance. The cumulative data demonstrate that ROS, NO and eATP govern CTI, in addition to induction of PR proteins, CAZymes and PAL activities, besides accumulation of phenolic compounds downstream of CTI. The immune-related correlation network identified functional hubs in the CTI pathway. Altogether, these shifts led to the discovery of chitosan-responsive networks that cause significant ECM and guard cell remodeling, and translate ECM cues into cell fate decisions during fusariosis.
病原体/微生物相关分子模式 (PAMPs/MAMPs) 通过重排宿主细胞机制的生物分子动力学来启动复杂的防御反应。细胞外基质 (ECM) 充当物理支架，防止植物病原体的识别和进入，而保卫细胞则在代谢上感知和整合信号。尽管壳聚糖是一种已知的参与植物防御的 MAMP，但壳聚糖触发免疫 (CTI) 的精确机制尚不清楚。在这里，我们展示了壳聚糖如何赋予植物对真菌病的免疫力。形态组织学检查显示，在血管镰刀菌病中，壳聚糖处理的幼苗早期会出现气孔关闭，同时气孔导度和蒸腾速率降低。电子显微镜和拉曼光谱显示 ECM 强化导致寡糖信号，这表现为半乳糖、果胶和相关次生代谢物的增加。使用定量 ECM 蛋白质组学和代谢组学的多组学方法鉴定了 325 种壳聚糖触发的免疫反应蛋白 (CTIRP)，特别是新型 ECM 结构蛋白 LYM2 和类受体激酶，以及 65 种壳聚糖触发的免疫反应代谢物 (CTIRM)，包括糖、糖醇、脂肪醇、有机和氨基酸。鉴定出的蛋白质和代谢物与活性氧 (ROS) 产生、气孔运动、根瘤发育和根结构有关，与寡糖信号有关，从而导致对镰刀菌的抗性。累积数据表明，ROS、NO 和 eATP 控制 CTI，除了诱导 PR 蛋白、CAZymes 和 PAL 活性以及 CTI 下游酚类化合物的积累外。免疫相关的相关网络确定了 CTI 途径中的功能枢纽。总之，这些变化导致了壳聚糖反应网络的发现，这些网络导致 ECM 和保卫细胞的显著重塑，并将 ECM 线索转化为镰刀菌病期间的细胞命运决定。
