Arabidopsis thaliana Cuticle Composition Contributes to Differential Defense Response to Botrytis cinerea

Abstract

The chemical composition of a plant cuticle can change in response to various abiotic or biotic stresses and plays essential functions in disease resistance responses. Arabidopsis thaliana mutants altered in cutin content are resistant to Botrytis cinerea, presumably because of increased cuticular water and solute permeability, allowing for faster induction of defense responses. Within this context, our knowledge of wax mutants is limited against this pathogen. We tested the contribution of cuticular components to immunity to B. cinerea using mutants altered in either cutin or wax alone, or in both cutin and wax contents. We found that even all the tested mutants showed increased permeability and reactive oxygen species (ROS) accumulation in comparison with wild-type plants and that only cutin mutants showed resistance. To elucidate the early molecular mechanisms underlying cuticle-related immunity, we performed a transcriptomic analysis. A set of upregulated genes involved in cell wall integrity and accumulation of ROS were shared by the cutin mutants bdg, lacs2-3, and eca2, but not by the wax mutants cer1-4 and cer3-6. Interestingly, these genes have recently been shown to be required in B. cinerea resistance. In contrast, we found the induction of genes involved in abiotic stress shared by the two wax mutants. Our study reveals new insight that the faster recognition of a pathogen by changes in cuticular permeability is not enough to induce resistance to B. cinerea, as has previously been hypothesized. In addition, our data suggest that mutants with resistant phenotype can activate other defense pathways, different from those canonical immune ones.

Could a cuticle be an active component of plant immunity?

“…Higher susceptibility of A. thaliana to Pseudomonas syringae pv. tomato DC3000 (Pto DC3000) was described in DEWAX-Ox, lacs2, att1, acp4, cer3-6, cer1-1 even though CER1ox1 and CER1ox2 mutants (Tang et al 2007, Xia et al 2009, Bourdenx et al 2011, Aragón et al 2021. Higher resistance to Pto DC3000 was observed in dewax and myb96 mutants (Ju et al 2017, Seo and Park 2010) (Table 1).…”

“…Increased resistance of A. thaliana to biotrophic fungus Golovinomyces orontii was observed in cer1-1, cer3-6, and cer3-8 mutant with reduced wax content (Table 1). On the other hand, the same mutant (cer1-1) exhibited higher susceptibility to the necrotrophic fungus Sclerotinia sclerotiorum (Bourdenx et al 2011, Aragón et al 2021. Similarly, A. thaliana plants expressing a fungal cutinase called CUTE were more susceptible to S. sclerotiorum (Table 1).…”

“…Most work focusing on the effects of cuticle changes on plant resistance to pathogens was done using necrotrophic fungi Botrytis cinerea (Table 1). Surprisingly, A. thaliana mutants with increased cuticle permeability (lacs2, lacs2.3, lcr, bdg or DEWAX-Ox) were more resistant to B. cinerea (Sieber et al 2000, Bessire et al 2007, Tang et al 2007, Voisin et al 2009, L'Haridon et al 2011, Aragón et al 2021) (Table 1). This was confirmed also by treatment with cutinase or by mechanical damage which both increased cuticle permeability and improved resistance to B. cinerea (L'Haridon et al 2011).…”

“…This was confirmed also by treatment with cutinase or by mechanical damage which both increased cuticle permeability and improved resistance to B. cinerea (L'Haridon et al 2011). In all cases (genetic mutation, cutinase treatment, mechanical damage) was observed induction of plant immune responses such as reactive oxygen species (ROS) production and faster callose accumulation, which was put into the connection with observed higher transcription of genes encoding two co-receptors BAK1 (Brassinosteroid-associated kinase 1) and BIK1 (Botrytis-induced kinase 1) that play an important role in plant immunity (Liu et al 2017, Aragón et al 2021. Enhanced immune response is the explanation for A. thaliana increased resistance to B. cinerea.…”

Water permeability of different aerial tissues of carnations is related to cuticular wax composition

“…The aboveground tissues of higher plants are covered by a thin and continuous hydrophobic cuticle (Samuels et al, 2008). The functions of the cuticle are well established; it serves as a barrier against uncontrolled water loss (Seufert et al, 2022), regulates the exchange of gas and chemicals (Ray et al, 2022), attenuates ultraviolet irradiation and protects against pathogen invasion and extreme temperatures (Arag on et al, 2021;Xue et al, 2017), and prevents organ fusion during development (Müller & Riederer, 2005). Cutin and waxes are the main constituents of the plant cuticle, and their chemical composition, relative amounts, and structural arrangement determine the various functions of the cuticle.…”