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Perennial plant dieback is an increasing and complex phenomenon. Perennial plants experience many interacting stressing events leading to final plant mortality. These interactions, and how they may change regarding climatic conditions and plant physiological status, are key in understanding the dieback process. Although dieback events are increasing worldwide, the knowledge on the dieback mechanisms are scarce, given the many technical challenges in studying complex interactions. In this thesis, we studied the interaction between two stresses frequently experienced by grapevines, one of the most important perennial crops: drought and esca (a vascular disease). Esca is a disease in which there are many competing hypotheses regarding its pathogenesis. One of the main hypothesis is that leaf symptoms and plant death are caused by hydraulic failure in xylem vessels. For this reason, drought is thought to contribute synergistically with esca to grapevine dieback. In this context, this thesis has primarily explored the hydraulic failure hypothesis during esca pathogenesis. We found that during leaf symptom expression both leaves and stems suffer from hydraulic failure causing (on average) 69% loss of hydraulic conductance in midribs, 55% in petioles, and 30% in stems. Differing from classical air embolism during drought, we observed that hydraulic failure during esca was caused by the presence of plant-derived vascular occlusions (i.e. tyloses and gels) produced at a distance from the pathogen niche in the trunk. After this discovering, we explored the interaction between esca and drought, subjecting naturally infected plants to drought. We found that drought totally inhibits esca leaf symptoms, as none of the plants under water deficit (at ΨPD ≈ -1MPa for three months) expressed leaf symptoms in two consecutive seasons. At the same time, in order to understand the interaction between esca and drought, we recorded the whole-plant water relations and carbon economy of grapevine under both stresses. We highlight the distinct physiology behind these two stresses, indicating that esca and drought present different underlying mechanisms, and induce different plant responses and physiological consequences. Esca (and subsequent stomatal conductance decline) does not result from decreases in water potential, and generates different gas exchange and non-structural carbohydrate seasonal dynamics compared to drought. Finally, we observed that esca affected the recorded plant physiology only seasonally, and not over the long-term. This thesis highlights the importance in finding the physiological thresholds triggering the different interactions during plant dieback. Together, the results open new scientific and agronomical perspectives on plant-pathogen-environment interactions and vineyard sustainability.; Au cours de leur vie les plantes pérennes sont confrontées à plusieurs stress en interaction qui les entrainent dans un processus de dépérissement. Ces interactions, et leurs changements par rapport aux conditions climatiques et à l’état physiologique de la plante, sont fondamentales pour la compréhension du processus de dépérissement. Malgré l’augmentation des évènements de dépérissement à l’échelle mondiale, les connaissances sur ces mécanismes restent limitées, étant données les difficultés techniques rencontrées dans l’étude des interactions complexes. Dans cette thèse nous avons étudié l’interaction entre deux stress fréquemment vécus par la vigne : la sècheresse et une maladie vasculaire, le mal d’esca. L’esca est une maladie qui soulève plusieurs hypothèses sur sa pathogénèse. Une des principales hypothèses est que les symptômes foliaires et la mort de ceps de vigne soient causés par un dysfonctionnement hydraulique dans les vaisseaux du xylème. Pour cette raison, la sècheresse pourrait contribuer en synergie avec l’esca au dépérissement de la vigne. Compte tenu de ce contexte, nous avons tout d’abord exploré l’hypothèse de dysfonctionnement hydraulique pendant la pathogenèse de l’esca. Nous avons mis en évidence que pendant l’expression des symptômes foliaires plusieurs organes sont atteints par un dysfonctionnement hydraulique qui cause en moyenne une perte de conductivité hydraulique de 69% sur les nervures centrales des feuilles, 55% sur les pétioles et 30% sur les tiges. Contrairement à l’embolie gazeuse classiquement observée pendant la sècheresse, le dysfonctionnement hydraulique pendant l’esca est causé par la présence d’occlusions vasculaires (thylloses et gels) produites par la plante. Après cette découverte, nous avons exploré l’interaction entre l’esca et la sècheresse, en imposant une contrainte hydrique aux plantes naturellement infectées. Nous avons découvert que la sécheresse inhibait complètement l’expression des symptômes d’esca, étant donné qu’aucune plante en stress hydrique (à ΨPD ≈ -1MPa pour trois mois) n’a montré de symptômes foliaires pendant deux saisons consécutives. Nous avons également étudié les relations hydriques et carbonées, à l’échelle de la plante entière au cours de ces expérimentations. Nos résultats soulignent un fonctionnement physiologique distinct lorsque la vigne est soumise à une sécheresse ou exprime des symptômes d’esca. L’esca (et la baisse de la conductance stomatique associée) n’est pas causé par une chute de potentiel hydrique, et génère des dynamiques saisonnières différentes de la sécheresse au regard des échanges gazeux et des teneurs en carbohydrates non-structuraux. Cette thèse souligne l’importance d’identifier les seuils physiologiques sous-jacents aux différentes interactions entre facteurs pendant le processus de dépérissement des plantes. Dans l’ensemble, ces résultats ouvrent des nouvelles perspectives scientifiques et agronomiques pour les interactions plante-pathogène-environnement et pour la durabilité des vignobles.

Nighttime transpiration has been previously reported as a significant source of water loss in many species; however, there is a need to determine if this trait plays a key role in the response to drought. This study aimed to determine the magnitude, regulation and relative contribution to whole plant water‐use, of nighttime stomatal conductance (g night) and transpiration (E night) in grapevine (Vitis vinifera L.). Our results showed that nighttime water loss was relatively low compared to daytime transpiration, and that decreases in soil and plant water potentials were mainly explained by daytime stomatal conductance (g day) and transpiration (E day). Contrary to E day, E night did not respond to VPD and possible effects of an innate circadian regulation were observed. Plants with higher g night also exhibited higher daytime transpiration and carbon assimilation at midday, and total leaf area, suggesting that increased g night may be linked with daytime behaviors that promote productivity. Modeling simulations indicated that g night was not a significant factor in reaching critical hydraulic thresholds under scenarios of either extreme drought, or time to 20% of soil relative water content. Overall, this study suggests that g night is not significant in exacerbating the risk of water stress and hydraulic failure in grapevine., Our study demonstrates that in grapevine (Vitis vinifera L.), nighttime water loss is not significant in exacerbating the risk of water stress, and in addition, we offer evidence that it may be positively linked to daytime productivity.

Adapting agriculture to climate change is driving the need for the selection and breeding of drought-tolerant crops. The aim of this study was to identify key drought tolerance traits and determine the sequence of their water potential thresholds across three grapevine cultivars with contrasting water use behaviors, Grenache, Syrah, and Semillon. We quantified differences in water use between cultivars and combined this with the determination of other leaf-level traits (e.g. leaf turgor loss point, π TLP), leaf vulnerability to embolism (P50), and the hydraulic safety margin (HSM P50). Semillon exhibited the highest maximum transpiration (Emax), and lowest sensitivity of canopy stomatal conductance (Gc) to vapor pressure deficit (VPD), followed by Syrah and Grenache. Increasing Emax was correlated with more negative water potential at which stomata close (Pgs90), π TLP, and P50, suggesting that increasing water use is associated with hydraulic traits allowing gas exchange under more negative water potentials. Nevertheless, all the cultivars closed their stomata prior to leaf embolism formation. Modeling simulations demonstrated that despite a narrower HSM, Grenache takes longer to reach thresholds of hydraulic failure due to its conservative water use. This study demonstrates that the relationships between leaf hydraulic traits are complex and interactive, stressing the importance of integrating multiple traits in characterizing drought tolerance., The relationships between traits including stomatal regulation, leaf embolism thresholds, and survival time under drought are complex and interactive, stressing the importance of integrating multiple traits in characterizing drought tolerance.

International audience