Molecular Insights Into the Perception of Fungal-Derived Molecular Patterns and Its Impact on Disease Resistance

Abstract

Plant immunity involves complex signaling pathways that detect pathogen-associated molecular patterns (PAMPs) and initiate defense responses. The perception of fungal-derived molecular patterns is crucial for activating plant immune responses and enhancing disease resistance. This research investigates these molecular mechanisms, focusing on chitin, a byproduct of the seafood industry derived from crab exoskeletons, and understanding the molecules derived from the necrotrophic fungal pathogen Botrytis cinerea. We utilized genetic and biochemical approaches to elucidate the molecular details underlying chitin perception and its impact on disease resistance. This included the use of mutants impaired in pattern-triggered immunity (PTI), systemic acquired resistance (SAR), and induced systemic resistance (ISR), as well as micrografting techniques in Arabidopsis. Additionally, we employed co-immunoprecipitation followed by mass spectrometry (IP-MS) to identify novel receptors recognising molecules from the fungal pathogen Botrytis cinerea in an attempt to explore methods for engineering pattern recognition receptors (PRRs) to enhance disease resistance. Our study demonstrates that soil amendment with chitin significantly boosts pattern-triggered immunity (PTI) and systemic disease resistance in a variety of plant species such as lettuce, tomato, Arabidopsis, and wheat. This enhanced resistance proved effective against a range of pathogens, including Pseudomonas syringae pv. tomato DC3000 and the fungal pathogen Blumeria graminis, causing powdery mildew in wheat. Furthermore, chitin application also suppressed the survival of the zoonotic bacterium Salmonella on both lettuce and Arabidopsis leaves, demonstrating its broad-spectrum efficacy. The effectiveness of chitin in enhancing disease resistance is dependent on its perception in the roots, which triggers a systemic immune response in distant tissues. Genetic analyses reveal that induced systemic resistance (ISR) and pattern recognition receptors (PRRs)/co-receptors are involved in chitin's systemic effects. PTI components, including BOTRYTIS-INDUCED KINASE1 (BIK1) and RESPIRATORY BURST OXIDASE HOMOLOGUE D (RBOHD), were upregulated upon soil amendment with chitin. Further investigations into the interaction between plants and the necrotrophic pathogen Botrytis cinerea, which exploits the cerato-platanin protein BcSpl1 to facilitate pathogenicity, were conducted. Using immunoprecipitation coupled with mass spectrometry (IP-MS) with a BAK1-GFP transgenic line, we observed significant enrichment of proteins such as PXY-CORRELATED 3 (PXC3) and IMPAIRED IN GLYCAN PERCEPTION 4 (IGP4) within the BAK1 complex following treatment with BcSpl1. Additional IP-MS experiments with individual BcSpl1 peptides specifically enriched IMPAIRED OOMYCETE SUSCEPTIBILITY1 (IOS1) in response to Peptide 3, suggesting a critical role for IOS1 in the BcSpl1-mediated signaling pathway. Collectively, my PhD work elucidates the molecular mechanisms by which plants perceive and respond to fungal-derived molecular patterns. The findings highlight the potential of chitin soil amendments and engineering plant PRRs, as a sustainable strategy for enhancing durable disease resistance and promoting crop protection.