Plant Cell Wall Integrity Perturbations and Priming for Defense

Abstract

A plant cell wall is a highly complex structure consisting of networks of polysaccharides, proteins, and polyphenols that dynamically change during growth and development in various tissues. The cell wall not only acts as a physical barrier but also dynamically responds to disturbances caused by biotic and abiotic stresses. Plants have well-established surveillance mechanisms to detect any cell wall perturbations. Specific immune signaling pathways are triggered to contrast biotic or abiotic forces, including cascades dedicated to reinforcing the cell wall structure. This review summarizes the recent developments in molecular mechanisms underlying maintenance of cell wall integrity in plant-pathogen and parasitic interactions. Subjects such as the effect of altered expression of endogenous plant cell-wall-related genes or apoplastic expression of microbial cell-wall-modifying enzymes on cell wall integrity are covered. Targeted genetic modifications as a tool to study the potential of cell wall elicitors, priming of signaling pathways, and the outcome of disease resistance phenotypes are also discussed. The prime importance of understanding the intricate details and complete picture of plant immunity emerges, ultimately to engineer new strategies to improve crop productivity and sustainability.

Keywords: cell wall integrity (CWI); cell-wall-digesting enzymes (CWDEs); cell-wall-modifying enzymes (CWMEs); damage-associated molecular patterns (DAMPs); pattern triggered immunity; plant cell wall; polysaccharides; signaling cascade; surveillance.

Figure 1

An overview of plant defense pathway triggered by perturbation of cell wall integrity during biotic stresses. The DAMPs, MAMPs, or HAMPs elicitors released due to biotic stresses are sensed through the plasma-membrane-localized pattern-recognition receptors (PRR) that activate the host defense pathway. The elicitor binding to PRRs activates a series of events, such as activation of Ca-channels and Ca influx, activation of reactive oxygen species production (ROS burst; H₂O₂), and protein kinases (MAPKs) cascade activation, and these are inter-linked with each other. The MAPK and Ca-dependent kinase (CDPKs, CCaMKs, and CIPKs) cascades further activate transcriptional reprogramming, defense-related PTI genes, reinforcement of cell wall (callose and lignin deposition), generation of anti-microbial secondary metabolites, and activation of ET, SA, and JA hormone synthesis. Locally activated immunity is amplified through these hormones. Immunity may also involve the spread of defense responses to distal tissues, resulting in systemic acquired resistance (SAR). It should be emphasized that a general view of only the pattern triggered immunity is described here and that each pathosystem may involve specific molecular interactions.

Figure 2

Induced CW perturbations and related signaling. A targeted modification of the CW structures (polysaccharides, phenolics, and proteins) can be achieved by apoplastic overexpression/mutation/silencing the plant endogenous CW synthesizing enzymes, CWMEs, and their inhibitors. As an alternative strategy, exogenous microbial CWDEs can be expressed in the apoplast as well. This results in a different extent of CW perturbations that can result in production of a plethora of DAMPs. DAMPs are perceived by specific receptors to trigger single or multiple defense signaling pathways, which results in different levels of immunity and tolerance/resistance to pathogens. Targeted modification of CW components in planta represents a useful tool to learn about the molecular mechanisms behind CWI maintenance during stress. This knowledge can be exploited to improve crop protection against pathogens.

Figure 3

Defense pathways involved against the CWI alterations triggered by CWMEs or CWDEs. (A) Plant LPMO-oxidized cellulose oligosaccharides activated a signaling pathway, which resulted in resistance to B. cinerea in Arabidopsis. (B) Released CW pectin OGs activated an immune pathway that resulted in Arabidopsis resistance to B. cinerea and P. syringae pv. tomato DC3000. (C) Mixed-linked glucans (MLGs) DAMPs from digested rice CW triggered PTI, and, as a result, the Arabidopsis plants became resistant to H. arabidopsidis. (D) CW-MLGs released from pathogen endoglucanases-overexpressor rice plants activated immune responses, resulting in enhanced resistance to M. oryzae.