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.
Esca critically affects xylem water movement in grapevine perennial organs by the presence of plant-derived tyloses.
Abstract
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. Xylem occlusions (tyloses) and subsequent loss of stem hydraulic conductivity (ks) occurred in all shoots with severe symptoms (apoplexy) and in more than 60% of shoots with moderate symptoms (tiger-stripe), with no tyloses in asymptomatic shoots. In vivo stem observations demonstrated that tyloses occurred only when leaf symptoms appeared, and resulted in more than 50% loss of hydraulic conductance in 40% of symptomatic stems, unrelated to symptom age. The impact of esca on xylem integrity was only seasonal, with no long-term impact of disease history. Our study demonstrated how and to what extent a vascular disease such as esca, affecting xylem integrity, could amplify plant mortality through hydraulic failure.
Summary
Hydraulic failure resulting from drought‐induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult ...to achieve at scale, leading to alternative metrics and correlations with more easily measured traits. These efforts have led to the longstanding and pervasive assumed mechanistic link between vessel diameter and vulnerability in angiosperms. However, there are at least two problems with this assumption that requires critical re‐evaluation: (1) our current understanding of drought‐induced embolism does not provide a mechanistic explanation why increased vessel width should lead to greater vulnerability, and (2) the most recent advancements in nanoscale embolism processes suggest that vessel diameter is not a direct driver. Here, we review data from physiological and comparative wood anatomy studies, highlighting the potential anatomical and physicochemical drivers of embolism formation and spread. We then put forward key knowledge gaps, emphasising what is known, unknown and speculation. A meaningful evaluation of the diameter–vulnerability link will require a better mechanistic understanding of the biophysical processes at the nanoscale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought.
The synergy between drought-responsive traits across different organs is crucial in the whole-plant mechanism influencing drought resilience. These organ interactions, however, are poorly understood, ...limiting our understanding of drought response strategies at the whole-plant level. Therefore, we need more integrative studies, especially on herbaceous species that represent many important food crops but remain underexplored in their drought response. We investigated inflorescence stems and rosette leaves of six Arabidopsis thaliana genotypes with contrasting drought tolerance, and combined anatomical observations with hydraulic measurements and gene expression studies to assess differences in drought response. The soc1ful double mutant was the most drought-tolerant genotype based on its synergistic combination of low stomatal conductance, largest stomatal safety margin, more stable leaf water potential during non-watering, reduced transcript levels of drought stress marker genes, and reduced loss of chlorophyll content in leaves, in combination with stems showing the highest embolism resistance, most pronounced lignification, and thickest intervessel pit membranes. In contrast, the most sensitive Cvi ecotype shows the opposite extreme of the same set of traits. The remaining four genotypes show variations in this drought syndrome. Our results reveal that anatomical, ecophysiological, and molecular adaptations across organs are intertwined, and multiple (differentially combined) strategies can be applied to acquire a certain level of drought tolerance.
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 (gnight) and transpiration (Enight) 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 (gday) and transpiration (Eday). Contrary to Eday, Enight did not respond to VPD and possible effects of an innate circadian regulation were observed. Plants with higher gnight also exhibited higher daytime transpiration and carbon assimilation at midday, and total leaf area, suggesting that increased gnight may be linked with daytime behaviors that promote productivity. Modeling simulations indicated that gnight 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 gnight 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.
Abstract
Climate change is challenging the resilience of grapevine (Vitis), one of the most important crops worldwide. Adapting viticulture to a hotter and drier future will require a multifaceted ...approach including the breeding of more drought-tolerant genotypes. In this study, we focused on plant hydraulics as a multi-trait system that allows the plant to maintain hydraulic integrity and gas exchange rates longer under drought. We quantified a broad range of drought-related traits within and across Vitis species, created in silico libraries of trait combinations, and then identified drought tolerant trait syndromes. By modeling the maintenance of hydraulic integrity of current cultivars and the drought tolerant trait syndromes, we identified elite ideotypes that increased the amount of time they could experience drought without leaf hydraulic failure. Generally, elites exhibited a trait syndrome with lower stomatal conductance, earlier stomatal closure, and a larger hydraulic safety margin. We demonstrated that, when compared with current cultivars, elite ideotypes have the potential to decrease the risk of hydraulic failure across wine regions under future climate scenarios. This study reveals the syndrome of traits that can be leveraged to protect grapevine from experiencing hydraulic failure under drought and increase drought tolerance.
Global viticulture has seen decreases in fruit yield and vine longevity over the past two decades. Our understanding of the underlying causes is limited by the complex interactions among the ...different factors involved and the technical challenges that limit investigations of these interactions. In Bortolami et al. (2021a) we investigated the interaction between two main drivers of grapevine decline, drought and vascular disease (esca), monitoring esca leaf symptom development and vine physiology in Sauvignon blanc during both stresses. We found that drought conditions inhibited esca leaf symptom development revealing the key role of plant water status in esca pathogenesis and opening new perspectives into water use management in the context of climate change.
Global viticulture has seen decreases in fruit yield and vine longevity over the past two decades. Our understanding of the underlying causes is limited by the complex interactions among the ...different factors involved and the technical challenges that limit investigations of these interactions. In Bortolami et al. (2021a) we investigated the interaction between two main drivers of grapevine decline, drought and vascular disease (esca), monitoring esca leaf symptom development and vine physiology in Sauvignon blanc during both stresses. We found that drought conditions inhibited esca leaf symptom development revealing the key role of plant water status in esca pathogenesis and opening new perspectives into water use management in the context of climate change.
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., CO
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.
PDF
