Dampening the DAMPs: How Plants Maintain the Homeostasis of Cell Wall Molecular Patterns and Avoid Hyper-Immunity.

Daniela Pontiggia,Felice Cervone,Sara Costantini,Giulia De Lorenzo,Manuel Benedetti

doi:10.3389/fpls.2020.613259

Daniela Pontiggia, Felice Cervone + Show 3 more

Open Access

https://doi.org/10.3389/fpls.2020.613259

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Abstract

Several oligosaccharide fragments derived from plant cell walls activate plant immunity and behave as typical damage-associated molecular patterns (DAMPs). Some of them also behave as negative regulators of growth and development, and due to their antithetic effect on immunity and growth, their concentrations, activity, time of formation, and localization is critical for the so-called “growth-defense trade-off.” Moreover, like in animals, over accumulation of DAMPs in plants provokes deleterious physiological effects and may cause hyper-immunity if the cellular mechanisms controlling their homeostasis fail. Recently, a mechanism has been discovered that controls the activity of two well-known plant DAMPs, oligogalacturonides (OGs), released upon hydrolysis of homogalacturonan (HG), and cellodextrins (CDs), products of cellulose breakdown. The potential homeostatic mechanism involves specific oxidases belonging to the family of berberine bridge enzyme-like (BBE-like) proteins. Oxidation of OGs and CDs not only inactivates their DAMP activity, but also makes them a significantly less desirable food source for microbial pathogens. The evidence that oxidation and inactivation of OGs and CDs may be a general strategy of plants for controlling the homeostasis of DAMPs is discussed. The possibility exists of discovering additional oxidative and/or inactivating enzymes targeting other DAMP molecules both in the plant and in animal kingdoms.

Highlights

The cell wall represents the interface between plants and the environment and acts as a physical barrier to protect plants against biotic and abiotic stresses
damage-associated molecular patterns (DAMPs) are likely to be released upon cell wall remodeling that occurs during plant growth and development
Endogenous cell wall degrading enzymes (CWDEs) can release, at low levels, oligosaccharide fragments of the same nature as those accumulated in larger quantities during more destructive mechanical injuries or plant cell wall degradation caused by pathogen-encoded CWDEs (De Lorenzo et al, 2018, 2019)

Summary

INTRODUCTION

The cell wall represents the interface between plants and the environment and acts as a physical barrier to protect plants against biotic and abiotic stresses. Microlesions caused, for example, by cell expansion, lateral root formation, or organ abscission, may cause cell wall damage and affect the so-called cell wall integrity (CWI; Anderson and Kieber, 2020; Gigli-Bisceglia et al, 2020) In these cases, endogenous cell wall degrading enzymes (CWDEs) can release, at low levels, oligosaccharide fragments of the same nature as those accumulated in larger quantities during more destructive mechanical injuries or plant cell wall degradation caused by pathogen-encoded CWDEs (De Lorenzo et al, 2018, 2019). We discuss how several extracellular DAMPs released from the polysaccharides of the plant cell wall may be kept under homeostatic control by oxidizing/inactivating enzymes (Figure 1) and how a similar mechanism may have general relevance for other DAMPs

DYNAMICS OF THE CELL WALL AND RELEASE OF REGULATORY FRAGMENTS

THE MODE OF ACTION OF CELL WALL DAMPs

Eschscholzia californica

Microdochium nivale Chondrus crispus

OF SIGNAL HOMEOSTASIS AND