Chitosan‐triggered immunity to Fusarium in chickpea is associated with changes in the plant extracellular matrix architecture, stomatal closure and remodeling of the plant metabolome and proteome

Abstract

Summary 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.

Boosting photosynthetic machinery and defense priming with chitosan application on tomato plants infected withFusarium oxysporumf. sp.lycopersici

“…On the one hand, the oxidative cascades of the defense response, added to the accumulation of free radicals in the chloroplast after stomatal closure, can induce membrane damage by lipid peroxidation; these damages include the components of the photosynthetic apparatus such as thylakoid membranes and photosystems. Furthermore, the production of fungal toxins such as fusaric acid increases ROS production, and the degradation of membranes exacerbates oxidative damage and also damages to chloroplasts (Narula et al, 2020;Singh et al, 2017). All these components could contribute to damaging the photosystems of the plants infected with Fol, as observed in the results of the fluorescence parameters reported in this work.…”

Biodiversity of Fusarium oxysporum Isolated from Diseased Chickpea and Detection of Resistance Sources to Some Egyptian Chickpea Cultivars

“…Biochemical analysis is important to understand the resistant mechanism before and after infection of plant and to isolate the resistance sources (Jyothi et al, 2018 andNarula et al, 2020). It is considered as a direct control tactic in integrated plant disease management that involve the use of additive or synergistic combinations of biotic, cultural, and chemical control measures (Jiménez et al, 2015 andLanda et al, 2004).…”

Network organization of the plant immune system: from pathogen perception to robust defense induction

“…However, integrative analysis of defense protein networks has rarely been performed. Using protein expression data produced in the context of chickpea (Cicer arietinum L.) interaction with Fusarium, chitosan-responsive networks were reported (Narula et al, 2020). PPI networks were also investigated by looking for partners or targets of candidate proteins.…”