Decoding lipid signaling in grapevine – Plasmopara viticola interaction: from host membrane remodeling to oomycete-derived lipid elicitors

Abstract

Over the past decades, lipids and fatty acids have emerged as pivotal regulators of plant–pathogen interactions. Their functions span a broad spectrum, ranging from the formation of structural barriers to the activation of signaling pathways and immune priming. Increasing evidence also identifies specific lipid species as potential biomarkers of resistance or susceptibility to diverse pathogens. Furthermore, studies examining extracellular dynamics during plant–pathogen interactions have highlighted the role of lipids in mediating intercellular communication and contributing to the establishment of systemic acquired resistance. In the context of grapevine downy mildew, lipid signalling plays a surprisingly central role in determining the outcome of the interaction, despite the biotrophic lifestyle of Plasmopara viticola. We have demonstrated that jasmonic acid biosynthesis is rapidly induced during the early hours of infection in tolerant grapevine genotypes. This response is associated with enhanced membrane lipid biosynthesis, elevated levels of C18:3, and the activation of fatty acid desaturation processes, along with increased chloroplast membrane lipid hydrolysis. Key lipid-processing enzyme gene families have also been characterized in grapevine, including phospholipases A, C, and D, as well as fatty acid desaturases and stearoyl-ACP desaturases. Ultimately, we showed that the specific activation of lipid signalling pathways may be linked to the resistance locus Resistance to Plasmopara viticola locus 3 (RPV3), suggesting a mechanistic connection between lipid-mediated signalling and genetically determined resistance.

From the pathogen’s perspective, several lipid species accumulate during infection, playing pivotal roles in life cycle completion and pathogenicity. Moreover, we have demonstrated that selected P. viticola-derived lipids can prime grapevine immune responses both in pot and in field trials. The use of these lipids as elicitors represents a promising strategy to address disease management through more sustainable, non-chemical approaches.

Acknowledgements

This work was supported by the European Commission in the frame of the Horizon Europe program, project ‘Shield4Grape’ (grant agreement number 101135088). Views and opinions expressed are those of the authors only and do not necessarily reflect those of the European Union. Neither the European Union nor the granting authority can be held responsible for them.