Abstract
Cuticular defects trigger a battery of reactions including enhanced reactive oxygen species (ROS) production and resistance to necrotrophic pathogens. However, the source of ROS generated by such impaired cuticles has remained elusive. Here, we report the characterization of Arabidopsis thaliana ohy1 mutant, a Peroxidase 57 (PER57) – overexpressing line that demonstrates enhanced defense responses that result both from increased accumulation of ROS and permeability of the leaf cuticle. The ohy1 mutant was identified in a screen of A. thaliana seedlings for oligogalacturonides (OGs) insensitive/hypersensitive mutants that exhibit altered growth retardation in response to exogenous OGs. Mutants impaired in OG sensitivity were analyzed for disease resistance/susceptibility to the necrotrophic phytopathogens Botrytis cinerea and Pectobacterium carotovorum. In the ohy1 line, the hypersensitivity to OGs was associated with resistance to the tested pathogens. This PER57 overexpressing line exhibited a significantly more permeable leaf cuticle than wild-type plants and this phenotype could be recapitulated by overexpressing other class III peroxidases. Such peroxidase overexpression was accompanied by the suppressed expression of cutin biosynthesis genes and the enhanced expression of genes associated with OG-signaling. Application of ABA completely removed ROS, restored the expression of genes associated with cuticle biosynthesis and led to decreased permeability of the leaf cuticle, and finally, abolished immunity to B. cinerea. Our work demonstrates that increased peroxidase activity increases permeability of the leaf cuticle. The loss of cuticle integrity primes plant defenses to necrotrophic pathogens via the activation of DAMP-responses.
Highlights
To fight off pathogens, animals depend on mobile defender cells and the adaptive immune system, while plants rely on the innate immunity of individual cells
A co-segregation analysis of progeny obtained from backcrosses of ohy1 and wild-type plants indicated that the mutation linked to the observed phenotypes was dominant and that the phenotype was dependent on the inserted T-DNA
The overexpression of Peroxidase 57 (PER57) in Col-0 background resulted in similar responses as those observed in the ohy1 mutants, confirming the contribution of this peroxidase to the phenotype of the ohy1 plants (Figure 1)
Summary
Animals depend on mobile defender cells and the adaptive immune system, while plants rely on the innate immunity of individual cells. In plants, these systems are activated by cell surface or intracellular receptors (Jones and Dangl, 2006). The recognition of PAMPs and DAMPs leads to the activation of plant defenses and pattern-triggered immunity (PTI), which provide resistance to most non-adapted pathogens in a phenomenon called non-host resistance (Zipfel, 2009, 2014). This type of perception involves intracellular receptors that directly or indirectly recognize pathogen effectors (Zipfel, 2014). Recognition of PAMPs, DAMPs and effectors triggers overlapping signaling responses in the plant and indicate a difference in the speed, persistence and robustness rather than the quality of response between PTI and ETI (Espinosa and Alfano, 2004; Tsuda and Katagiri, 2010)
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