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.

Keywords: Damage-Associated Molecular Patterns; cell wall-degrading enzymes; plant cell wall; plant innate immunity; plant-pathogen interactions.

Figure 1

Overview of responses induced by cell wall damage during pathogen infection. CW, cell wall; CWDE, cell wall-degrading enzyme; CWI, cell wall integrity; PTI, pattern-triggered immunity; DAMP, Damage-Associated Molecular Pattern; BBEL, berberine bridge enzyme-like protein; oxDAMP, oxidized DAMP; POD, peroxidase; ROS, reactive oxygen species. CWDEs secreted by the pathogen degrade CW structural polysaccharides. CW damage activates the CWI perception system, mediated by dedicated sensors, triggering CWI maintenance responses, that include production of ROS mediated by membrane NADPH oxidases and apoplastic PODs, and reinforcement of the CW. Host-encoded inhibitors reduce CWDE activity, slowing down CW degradation and promoting the accumulation of CW-derived DAMPs. Perception of DAMPs by membrane-localized receptors in turn activates PTI, which leads to antimicrobial defence responses, including production of phytoalexins, PR proteins and ROS, that contribute to restrict infection. Negative and positive crosstalk between CWI and PTI fine-tune defence responses triggered by CW damage. DAMPs can be inactivated by apoplastic BBEL proteins, that oxidize CW-derived oligosaccharides, at the same time producing ROS. Some pathogens can secrete decoy proteins that bind to CWDE inhibitors.