Multiple, simultaneous abiotic stresses differentially impact downy mildew infection in grapevine

Maintaining grapevine health and resilience under climate change demands an understanding of how multiple stresses interact. Climate change has led to more frequent and intense droughts and heat waves, which often occur together and may affect disease pressure. Here, we explored a complex multi-stress framework by combining drought and heat stress with downy mildew infection in grapevine, determining their possible interactions (synergistic or antagonistic) on pathogenesis, and detailing their effects on grapevine leaf physiology. We subjected grapevines (Vitis vinifera L.) to drought, heat stress or a combination of both, subsequently inoculating leaves with Plasmopara viticola (Berk. & Curt. Ex de Bary). In these same leaves we quantified their physiological responses and changes in defense-related metabolite (H2O2 and phenols) concentrations. Our results revealed common and distinct responses to the multi-stress interactions. Drought and drought-heat treatments led to low stomatal conductance (a reduction in stomatal aperture), which acted as a biophysical mechanism restricting P. viticola entry and resulting in a lower P. viticola sporulation rate. Defense-related metabolites were differentially regulated according to the stress combination, suggesting a role in the biochemical mechanism against the P. viticola infection. Stilbene concentration increased by 36, 57 and 113% in response to drought, heat and drought-heat, respectively. Flavonoids and phenolic acids exhibited distinct patterns in response to different stress treatments. These results shed light on the mechanisms that drive complex interactions between abiotic and biotic stressors, enhancing our understanding of multi-stress resilience and allowing us to better predict how grapevines will respond to the changing climate.