The Arabidopsis thaliana-Botrytis cinerea pathosystem: from the molecular basis of plant-pathogen interactions to sustainable crop protection

Understanding how plants defend themselves against pathogens is instrumental to develop varieties more resistant to diseases and sustainable methods for crop protection. In this thesis, Arabidopsis thaliana was employed to investigate both the metabolic pathways involved in resistance against Botrytis cinerea, a model for necrotrophic fungi, and to evaluate bio-based methods to control fungal infection. Treatment with different elicitors enhances Arabidopsis resistance to B. cinerea, a process associated with the accumulation of the indolic phytoalexin camalexin. Transcriptomic analyses revealed that elicitor treatments prime the expression of genes involved in the biosynthesis of camalexin but also of indole and aliphatic glucosinolates (IGs and AGs) in response to the pathogen. Reverse genetics showed that, while both indole compounds and AGs are required for elicitor- induced resistance, only indoles are involved in basal resistance to the pathogen. Unexpectedly, mutations in PENETRATION2 (PEN2), a myrosinase converting IGs into antimicrobial products, cause a robust resistance to B. cinerea, correlated with the accumulation of 4-methoxyindol-3-ylmethyl glucosinolate (4MI3G), the main substrate of PEN2, and of camalexin. The enhanced resistance observed in pen2 mutants was lost in mutants unable to synthesize camalexin, suggesting that accumulation of PEN2 substrates reroutes the indole metabolism towards camalexin, enhancing resistance to B. cinerea. These results highlight the importance of feedback mechanisms that modulate special metabolism during pathogen infection, and that must be considered in metabolic engineering of plant resistance. Arabidopsis is an established model to investigate the molecular mechanisms of plant immunity, but it could also be employed to evaluate novel strategies for crop protection before expensing and time-consuming field tests on crop species. Here, we have tested lavender essential oil (LEO) and PhaOP, a novel sustainable elicitor obtained by fermentation of orange peel waste with the white rot fungus Phanerochaete chrysosporium, as sustainable products to control Botrytis infection in Arabidopsis. Our results indicate that LEO has both direct antifungal activity and can prime plant defenses against the pathogen without compromising growth. PhaOP does not show antimicrobial activity but can induced jasmonate- and indole-dependent resistance in Arabidopsis. Notably, both LEO and PhaOP could also restrict B. cinerea infection in crops, indicating that Arabidopsis is a suitable system to test eco-friendly alternatives to chemical pesticides.