Abstract
Wounded leaves of Arabidopsis thaliana show transient immunity to Botrytis cinerea, the causal agent of grey mould. Using a fluorescent probe, histological staining and a luminol assay, we now show that reactive oxygen species (ROS), including H2O2 and O2 −, are produced within minutes after wounding. ROS are formed in the absence of the enzymes Atrboh D and F and can be prevented by diphenylene iodonium (DPI) or catalase. H2O2 was shown to protect plants upon exogenous application. ROS accumulation and resistance to B. cinerea were abolished when wounded leaves were incubated under dry conditions, an effect that was found to depend on abscisic acid (ABA). Accordingly, ABA biosynthesis mutants (aba2 and aba3) were still fully resistant under dry conditions even without wounding. Under dry conditions, wounded plants contained higher ABA levels and displayed enhanced expression of ABA-dependent and ABA-reporter genes. Mutants impaired in cutin synthesis such as bdg and lacs2.3 are already known to display a high level of resistance to B. cinerea and were found to produce ROS even when leaves were not wounded. An increased permeability of the cuticle and enhanced ROS production were detected in aba2 and aba3 mutants as described for bdg and lacs2.3. Moreover, leaf surfaces treated with cutinase produced ROS and became more protected to B. cinerea. Thus, increased permeability of the cuticle is strongly linked with ROS formation and resistance to B. cinerea. The amount of oxalic acid, an inhibitor of ROS secreted by B. cinerea could be reduced using plants over expressing a fungal oxalate decarboxylase of Trametes versicolor. Infection of such plants resulted in a faster ROS accumulation and resistance to B. cinerea than that observed in untransformed controls, demonstrating the importance of fungal suppression of ROS formation by oxalic acid. Thus, changes in the diffusive properties of the cuticle are linked with the induction ROS and attending innate defenses.
Highlights
The cuticle is mainly considered as a constitutive barrier against water loss, irradiation, xenobiotics or pathogens [1,2]
This study provides an explanation for the strong resistance to B. cinerea observed in wounded plants or plants with cuticular defects
This study demonstrates how a cuticle-degrading pathogen avoids the generation of reactive oxygen species (ROS) by producing an effector that interferes with ROS production
Summary
The cuticle is mainly considered as a constitutive barrier against water loss, irradiation, xenobiotics or pathogens [1,2]. The structure of this lipid boundary layer covering aerial parts of plants is made of waxes covering and interspersed in cutin, a polymer layer formed by a network of esterified V-hydroxylated fatty acids that are produced and secreted by the epidermis cells [3]. The fatty acids in the cutin can be hydroxylated at midchains (C8, C9, or C10) or in V-positions and are linked together or to glycerol by ester bonds It is still unclear if the cutin polymers exist as free polymers or if they are anchored in some ways to the cell wall [8]. While considerable knowledge is available on single components, the detailed chemical structure of the entire cuticle is still not known and the relation between the structure and the biological function of the individual components remains to be defined
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