The plant epidermis or cuticle is constantly exposed to external and internal environmental factors, including an enriched and diverse community of bacteria, yeast, fungi, viruses, and mites. It is not only where the plant has its first physical barrier, but also where organisms can be recognized and potentially where the plant defense responses can be triggered. The plant cuticle is a polymeric composite formed by an array of structurally and chemically heterogeneous compounds, including cutin and wax. A few studies have shown that cuticular components are essential and important drivers of the structure and size of the bacterial community. On the other hand, cuticular components are also important for both pathogens and plants, to initiate the pre-invasion and infection process and to activate the innate immune response, respectively. In this review, we explore current knowledge on the role of the cuticle during the intimate interactions between plants and microorganisms, in particular pathogenic and non-pathogenic bacteria and fungi. Finally, we propose new perspectives on the potential use of this information for agriculture.

Plant diseases induced by fungi are among the most important limiting factors during pre- and post-harvest food production. For decades, synthetic chemical fungicides have been used to control these diseases, however, increase on worldwide regulatory policies and the demand to reduce their application, have led to searching for new ecofriendly alternatives such as the biostimulants. The commercial application of yeasts as biocontrol agents, has shown low efficacy compared to synthetic fungicides, mostly due to the limited knowledge of the molecular mechanisms of yeast-induced responses. To date, only two genome-wide transcriptomic analyses have characterized the mode of action of biocontrols using the plant model Arabidopsis thaliana, missing, in our point of view, all its molecular and genomic potential. Here we describe that compounds released by the biocontrol yeast Hanseniaspora opuntiae (HoFs) can protect Glycine max and Arabidopsis thaliana plants against the broad host-range necrotrophic fungi Corynespora cassiicola and Botrytis cinerea. We show that HoFs have a long-lasting, dose-dependent local, and systemic effect against Botrytis cinerea. Additionally, we performed a genome-wide transcriptomic analysis to identify genes differentially expressed after application of HoFs in Arabidopsis thaliana. Our work provides novel and valuable information that can help researchers to improve HoFs efficacy in order for it to become an ecofriendly alternative to synthetic fungicides.

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.

Plant food production is severely affected by fungi; to cope with this problem, farmers use synthetic fungicides. However, the need to reduce fungicide application has led to a search for alternatives, such as biostimulants. Rare-earth elements (REEs) are widely used as biostimulants, but their mode of action and their potential as an alternative to synthetic fungicides have not been fully studied. Here, the biostimulant effect of gadolinium (Gd) is explored using the plant-pathosystem Arabidopsis thaliana–Botrytis cinerea. We determine that Gd induces local, systemic, and long-lasting plant defense responses to B. cinerea, without affecting fungal development. The physiological changes induced by Gd have been related to its structural resemblance to calcium. However, our results show that the calcium-induced defense response is not sufficient to protect plants against B. cinerea, compared to Gd. Furthermore, a genome-wide transcriptomic analysis shows that Gd induces plant defenses and modifies early and late defense responses. However, the resistance to B. cinerea is dependent on JA/ET-induced responses. These data support the conclusion that Gd can be used as a biocontrol agent for B. cinerea. These results are a valuable tool to uncover the molecular mechanisms induced by REEs.