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

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.

A receptor‐like kinase SlFERL mediates immune responses of tomato to Botrytis cinerea by recognizing BcPG1 and fine‐tuning MAPK signaling

“…It is more likely that SlFERL contributes to the positive regulation of immunity by acting as a scaffold, interacting with microbial signatures and pattern recognition receptors, similar to the function of FER and some other malectin-receptor-like kinases in Arabidopsis. Notably, Lorrai et al (2021) previously reported that Arabidopsis fer-4 mutants were more resistant to B. cinerea, while the present study revealed that Slferl mutants were more sensitive to B. cinerea. It has been demonstrated that homozygous Arabidopsis fer mutants were resistant to Golovinomyces (syn.…”

Cell wall-localized BETA-XYLOSIDASE4 contributes to immunity of Arabidopsis against Botrytis cinerea

“…For example, Arabidopsis reduced wall acetylation 2 mutants, that have reduced pectin acetylation, are more resistant to Botrytis cinerea ( Manabe et al, 2011) . The alteration of HG has also been shown to enhance resistance to B. cinerea ( Lorrai et al, 2021 ). Arabidopsis plants overexpressing PMEI-1 and PMEI-2 show enhanced resistance to the phytopathogens B. cinerea and Pectobacterium carotovorum ( Lionetti et al, 2007 ).…”

Synthesis and import of GDP‐l‐fucose into the Golgi affect plant–water relations

“…We found that the water loss and ion leakage were nearly fully suppressed in qua2‐1 esmd1‐1 double mutant but not in mur1 esmd1‐1 double mutants (Figs 6c, S16). Finally, during the examination of mur1 epidermis by means of cryo‐SEM we did not detect any morphological signs indicative of loss of cell adhesion that are otherwise readily visible in cell adhesion mutants (Verger et al ., 2018; Lorrai et al ., 2021; Dataset S3b,c). We therefore conclude that the lack of GDP‐ l ‐fucose had a minor effect on the adhesion of epidermal cells, and loss of epidermal cell adhesion was not the cause of elevated water loss observed in mur1 mutants.…”

“…Aside from controlling cell wall porosity (Fleischer et al, 1999), RG-II was demonstrated to form borate-dependent linkages with plasma membrane sphingolipids in cultured Rosa cells (Voxeur & Fry, 2014) and boron deficiency affects membrane integrity (Cakmak et al, 1995;Han et al, 2008). Increased ion (Figs 6a, S16) and chlorophyll leakage (Lorrai et al, 2021) observed in mur1 mutants likely stem from the same causes. It is thus possible that elevated membrane permeability, which otherwise does not affect the steady-state leaf conductance, gains significance under conditions of severe water deficit, contributing to high water loss observed in mur1 mutants.…”