In the context of climate change, plant mortality is increasing worldwide in both natural and agroecosystems. However, our understanding of the underlying causes is limited by the complex interactions between abiotic and biotic factors and the technical challenges that limit investigations of these interactions. Here, we studied the interaction between two main drivers of mortality, drought and vascular disease (esca), in one of the world’s most economically valuable fruit crops, grapevine. We found that drought totally inhibited esca leaf symptom expression. We disentangled the plant physiological response to the two stresses by quantifying whole-plant water relations (i.e., water potential and stomatal conductance) and carbon balance (i.e., CO2 assimilation, chlorophyll, and nonstructural carbohydrates). Our results highlight the distinct physiology behind these two stress responses, indicating that esca (and subsequent stomatal conductance decline) does not result from decreases in water potential and generates different gas exchange and nonstructural carbohydrate seasonal dynamics compared to drought.

Hydraulic failure has been extensively studied during drought-induced plant dieback, but its role in plant-pathogen interactions is under debate. During esca, a grapevine (Vitis vinifera) disease, symptomatic leaves are prone to irreversible hydraulic dysfunctions but little is known about the hydraulic integrity of perennial organs over the short- and long-term. We investigated the effects of esca on stem hydraulic integrity in naturally infected plants within a single season and across season(s). We coupled direct (ks) and indirect (kth) hydraulic conductivity measurements, and tylose and vascular pathogen detection with in vivo X-ray microtomography visualizations. We found xylem occlusions (tyloses), and subsequent loss of stem ks, in all of the shoots with severe symptoms (apoplexy) and in more than 60% of the shoots with moderate symptoms (tiger-stripe), and no tyloses in shoots that were currently asymptomatic. In vivo stem observations demonstrated that tyloses were observed only when leaf symptoms appeared, and resulted in more than 50% PLC in 40% of symptomatic stems, unrelated to symptom age. The impact of esca on xylem integrity was only seasonal and no long-term impact of disease history was recorded. Our study demonstrated how and to what extent a vascular disease such as esca, affecting xylem integrity, could amplify plant mortality by hydraulic failure.

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