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

Riccardo Lorrai,Simone Ferrari,Christiane Nawrath,Fedra Francocci,Giulia De Lorenzo,Kay Gully,Helle J Martens

doi:10.3389/fpls.2021.696955

Abstract

Pectin is a major cell wall component that plays important roles in plant development and response to environmental stresses. Arabidopsis thaliana plants expressing a fungal polygalacturonase (PG plants) that degrades homogalacturonan (HG), a major pectin component, as well as loss-of-function mutants for QUASIMODO2 (QUA2), encoding a putative pectin methyltransferase important for HG biosynthesis, show accumulation of reactive oxygen species (ROS), reduced growth and almost complete resistance to the fungal pathogen Botrytis cinerea. Both PG and qua2 plants show increased expression of the class III peroxidase AtPRX71 that contributes to their elevated ROS levels and reduced growth. In this work, we show that leaves of PG and qua2 plants display greatly increased cuticle permeability. Both increased cuticle permeability and resistance to B. cinerea in qua2 are suppressed by loss of AtPRX71. Increased cuticle permeability in qua2, rather than on defects in cuticle ultrastructure or cutin composition, appears to be dependent on reduced epidermal cell adhesion, which is exacerbated by AtPRX71, and is suppressed by the esmeralda1 mutation, which also reverts the adhesion defect and the resistant phenotype. Increased cuticle permeability, accumulation of ROS, and resistance to B. cinerea are also observed in mutants lacking a functional FERONIA, a receptor-like kinase thought to monitor pectin integrity. In contrast, mutants with defects in other structural components of primary cell wall do not have a defective cuticle and are normally susceptible to the fungus. Our results suggest that disrupted cuticle integrity, mediated by peroxidase-dependent ROS accumulation, plays a major role in the robust resistance to B. cinerea of plants with altered HG integrity.

Highlights

The cell wall (CW) is crucial for various important aspects of plant biology, providing mechanical support to the protoplast, modulating cell growth and shape, and mediating cell adhesion and cell-to-cell communication (McCann and Roberts, 1991; Carpita and Gibeaut, 1993; Somerville et al, 2004; Humphrey et al, 2007)
It was previously reported that PG and qua2 plants display a robust resistance to B. cinerea (Ferrari et al, 2008; Verger, 2014), that resembles that of Arabidopsis plants with altered cuticle (Bessire et al, 2007; Chassot et al, 2007; Tang et al, 2007)
Rosette leaves of WT, PG, and qua2 plants were sprayed with a control solution or with abscisic acid (ABA), and cuticle permeability was evaluated after 24 h using two different assays: toluidine blue staining of the leaf surface (Figure 1A) and measurement of chlorophyll leakage in ethanol (Figure 1B)

Summary

Introduction

The cell wall (CW) is crucial for various important aspects of plant biology, providing mechanical support to the protoplast, modulating cell growth and shape, and mediating cell adhesion and cell-to-cell communication (McCann and Roberts, 1991; Carpita and Gibeaut, 1993; Somerville et al, 2004; Humphrey et al, 2007). In the epidermal cells of the aerial parts of the plant, the outermost surface of the CW is in continuation with the cuticle, a multi-layered hydrophobic structure that limits the diffusion of water, regulates the exchange of gases with the environment, and provides protection against pathogens (Yeats and Rose, 2013). The cuticle contains waxes, mixtures of hydrophobic material containing very long-chain fatty acids, and other secondary metabolites (Kunst and Samuels, 2009; Yeats and Rose, 2013). As for the CW components, the wax and cutin compositions of the plant cuticle widely vary among plant species, organs, and during development (Yeats and Rose, 2013)

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