Host Cell Wall Damage during Pathogen Infection: Mechanisms of Perception and Role in Plant-Pathogen Interactions

Abstract

The plant cell wall (CW) is a complex structure that acts as a mechanical barrier, restricting the access to most microbes. Phytopathogenic microorganisms can deploy an arsenal of CW-degrading enzymes (CWDEs) that are required for virulence. In turn, plants have evolved proteins able to inhibit the activity of specific microbial CWDEs, reducing CW damage and favoring the accumulation of CW-derived fragments that act as damage-associated molecular patterns (DAMPs) and trigger an immune response in the host. CW-derived DAMPs might be a component of the complex system of surveillance of CW integrity (CWI), that plants have evolved to detect changes in CW properties. Microbial CWDEs can activate the plant CWI maintenance system and induce compensatory responses to reinforce CWs during infection. Recent evidence indicates that the CWI surveillance system interacts in a complex way with the innate immune system to fine-tune downstream responses and strike a balance between defense and growth.

Impaired Cuticle Functionality and Robust Resistance to Botrytis cinerea in Arabidopsis thaliana Plants With Altered Homogalacturonan Integrity Are Dependent on the Class III Peroxidase AtPRX71

“…Since the cuticle-CW continuum represents the first site of contact with the plant, microbial pathogens have evolved an array of enzymes that degrade the cuticle and CW structural components to assist penetration and colonization, obtain carbon sources, and promote leakage of nutrients from the protoplast (Ziv et al, 2018;Lorrai and Ferrari, 2021). In particular, at early stages of infection, several phytopathogenic fungi synthesize cuticle-degrading enzymes (cutinases, esterases, and lipases) that are thought to prepare the infection site both for adhesion and penetration (Deising et al, 1992;Berto et al, 1999;Nielsen et al, 2000;Garrido et al, 2012).…”

“…In particular, at early stages of infection, several phytopathogenic fungi synthesize cuticle-degrading enzymes (cutinases, esterases, and lipases) that are thought to prepare the infection site both for adhesion and penetration (Deising et al, 1992;Berto et al, 1999;Nielsen et al, 2000;Garrido et al, 2012). Later, tissue penetration and invasion are assisted by microbial CW-degrading enzymes, most notably pectinases, which are among the first to be secreted by many phytopathogens (De Lorenzo et al, 1997;Lorrai and Ferrari, 2021) and are important pathogenicity factors, in particular for those microbes causing soft rot symptoms (Reignault et al, 2008). For instance, the necrotrophic fungus Botrytis cinerea, the causal agent of gray mold in several plant species, secretes large amounts of pectinolytic enzymes, most notably polygalacturonases (PGs), that degrade homogalacturonan (HG), a major pectic component, during the early phases of infection and are crucial for plant invasion, host adaptability, and to determine the type of symptoms caused by this pathogen (Have et al, 1998;Kars et al, 2005).…”

“…The vulnerability that follows CW injury caused by pathogen infection and other stresses can be compensated in the plant by the activation of an array of defense responses, including the strengthening of the altered CW itself (Vaahtera et al, 2019;Gigli-Bisceglia et al, 2020;Lorrai and Ferrari, 2021). Activation of defense responses occurs upon perception of exogenous microbe-associated molecular patterns (MAMPs) and/or CW-derived molecules and fragments that are released in the apoplast by microbial enzymes during infection and are recognized as endogenous damage-associated molecular patterns (DAMPs), thereby activating the so-called patterntriggered immunity (PTI; Gust et al, 2017;Bacete et al, 2018;De Lorenzo et al, 2018).…”

With an Ear Up against the Wall: An Update on Mechanoperception in Arabidopsis

“…The ability of WAK1 to bind OGs in vitro and its upregulation in response to OGs [ 178 ] prompted Brutus et al [ 20 ] to test whether it behaves as an OG receptor in vivo. Released OGs from the cell wall are damage-associated molecular patterns (DAMPs) which activate plant immune responses [ 178 , 179 ]. Since reverse genetic approaches, either because of redundancy or lethal effects [ 180 , 181 ], limited the spectrum of available wak phenotypes, the authors opted to create chimeric receptors to assess whether WAK1 perceives OGs as signal ligands.…”

Membrane Vesicles of Pectobacterium as an Effective Protein Secretion System

“…Pectins are one of the main constituents of a plant cell wall [10]. They are a family of complex polysaccharides that contain α-1,4 galacturonic acid residues [11]. The most abundant in plants is polygalacturonate (PG), a linear chain of α-1,4-linked D-galacturonate residues, methyl-esterified in about 70-80% [10,12].…”