Marylou Mantova

Human activities are intensifying heatwaves and droughts, threatening forest ecosystems worldwide. However, understanding intraspecific variation in physiological traits that confer resistance to hotter drought is critical for predicting tree responses to climate change. In Pinus taeda L., long-term geographic isolation across the Mississippi River Valley after the last glacial maximum has resulted in distinct population genetic structures, likely reflecting historical adaptation to contrasting climatic conditions in western and eastern refugia. However, it remains unclear whether contemporary populations retain meaningful variation in traits that confer tolerance to hotter and drier conditions, such as hydraulic vulnerability and water-use regulation, which are critical for predicting responses to future climate extremes. Here, in a common garden of adult P. taeda trees planted in 2010, we characterized intraspecific variability in 22 physiological traits related to resistance to hotter droughts across 10 provenances originating from either west or east of the Mississippi River Valley. Key traits included xylem vulnerability to embolism, leaf and bark residual conductance, and leaf turgor loss point. We used an integrated indicator, Time to Hydraulic Failure (THF), predicted by a mechanistic hydraulic model, SurEau, to assess how trait combinations contribute to tree resistance to hotter droughts. While we hypothesized that western provenances would be more adapted to hotter drought, we found that THF was lower in western than eastern provenances. The THF values were negatively correlated with residual transpiration and leaf mass per area. These patterns suggest physiological differentiation between populations, although not one strictly determined by drought resistance alone. Overall, our findings demonstrate that intraspecific variation in physiological traits can inform forest management and breeding strategies, underscoring the complex interplay of hydraulic and residual transpiration traits in shaping drought resilience and emphasizing the need to integrate multiple physiological processes when predicting forest responses to climate change.

Identification des bases physiologiques de la mortalité des arbres induite par sécheresse: Les forêts, bien qu’essentielles à la survie de l’Homme du fait de leurs nombreux services écosystémiques, font face à d’importants dépérissements causés par des sécheresses intenses depuis le début de l’Anthropocène. Comme les modèles climatiques globaux prévoient, pour un futur proche, une augmentation de la fréquence et de l’intensité de ces sécheresses qui, par conséquence, accentuera le risque de mortalité des arbres, il apparait alors crucial de mieux comprendre les bases physiologiques de la mortalité des arbres induite par sécheresse afin d’identifier des seuils physiologiques permettant de mieux prédire l’impact de ces changements climatiques sur les écosystèmes forestiers. Si la défaillance hydraulique du xylème a été reconnue comme un facteur omniprésent de la mort des arbres en conditions de sécheresse, des preuves fondamentales du lien mécaniste reliant la défaillance hydraulique, la mortalité des cellules et celle des arbres n’ont pas encore été identifiées. Ainsi, l’objectif principal de cette thèse était d’élucider ce lien tout en identifiant les seuils physiologiques clés au-delà desquels la survie de l’arbre est grandement compromise. Dès lors, en s’intéressant, tout d’abord, à deux espèces, un conifère (Pseudotsuga menziesii M.) et une angiosperme (Prunus lusitanica L.) le travail de thèse a démontré que les niveaux de défaillance hydraulique considérés jusqu’alors comme létaux pour les plantes (P50 pour les conifères et P88 pour les angiospermes) n’étaient pas assez précis pour définir avec certitude le sort d’un arbre après un événement de sécheresse. Cependant, alors que le lien causal entre défaillance hydraulique du xylème et la mortalité cellulaire restait non élucidé, l’interaction entre ces deux phénomènes semblait expliquer la capacité des arbres à récupérer d’un stress hydrique. Ainsi, en combinant, à la fois, la détection des événements de cavitation à l’aide de la méthode optique, des mesures de contenu en eau relatif au niveau tissulaire, et des mesures de lyse cellulaire au niveau d’un organe facilement accessible : la feuille, nous avons mis en évidence que la défaillance hydraulique du xylème, en entrainant une baisse du contenu en eau des tissus en dessous d’un niveau critique, le RWCcrit, provoquait la mort des cellules. Finalement, en partant du postulat que toutes les cellules n’avaient pas la même importance dans la survie des arbres et que cette survie devait certainement être liée au maintien de l’intégrité des cellules responsables de la croissance de la plante, c’est-à-dire des cellules méristématiques, nous avons cherché, en travaillant sur un conifère (Abies concolor (Gordon & Glend) Lindl. Ex Hildebr) et une angiosperme (Fagus sylvatica L.), à montrer que les cellules méristématiques étaient bien des cellules clés lors de l’évaluation du lien mécaniste entre la défaillance hydraulique et la mortalité de l’arbre. Sur cette dernière partie, bien que les analyses statistiques aient à nouveau révélé l’importance du niveau de contenu en eau relatif des tissus de la tige avant réhydratation pour la survie des arbres, des résultats préliminaires obtenus en microscopie électronique à transmission ont montré qu’à niveaux de contenus en eau égaux, des plantes présentant des cellules méristématiques intègres étaient plus à même de survivre à l’événement de sécheresse que les autres et, ce, dès leur ré-arrosage.

Hydraulic failure has been causally linked to cellular damage at the leaf level, yet the functional pathway connecting xylem dysfunction to whole-tree mortality remains unresolved. One recent hypothesis is that tree death ultimately depends on the loss of meristem vitality. However, because meristems are difficult to access and assess, their response to drought has rarely been investigated. Here, we aimed to identify whether reduced water supply resulting from hydraulic dysfunction directly compromises cambial integrity and determines tree survival. We subjected potted saplings of a gymnosperm species, Abies concolor, and an angiosperm species, Fagus sylvatica L. to severe drought by withholding water, generating different levels of loss of hydraulic functioning ranging from 30% to complete loss of conductivity (PLC 100). Prior to rewatering, water potential, percentage of embolism, relative water content, and level of cellular damage were quantified at the stem level, while cambial cell integrity was assessed using transmission electron microscopy. Sapling survival was monitored for one year following drought release.Surprisingly, saplings of both species could display similar water potentials, relative water content status or level of hydraulic failure at the time of rewatering but exhibited different survival capacities. Saplings that maintained structurally intact cambial cells recovered, whereas those showing cambial damage died, regardless of their level of hydraulic status. Thus, our results provide direct evidence that cambium integrity represents a critical bottleneck linking hydraulic failure to tree mortality. They also evinced that the mechanisms behind loss of cambial cell integrity are mainly explained by the consequences of tree dehydration after hydraulic failure. Focusing on the water relocation towards cambial cells during a drought event could help understand the mechanisms associated with cambial cell death, and identify potential thresholds for improving the precisions of the mechanistic models aiming at predicting tree mortality.

Human activities are increasing temperatures and reducing water availability, intensifying climate variability and extremes including heat waves and droughts, which threaten forest ecosystems. Here, we characterize and model intraspecific variability in physiological traits related to resistance to hotter droughts in loblolly pine (P. taeda). For this, we use complementary approaches to evaluate trait variation and potential differences between two populations that have been geographically and spatially separated since the last glacial maximum (21,000–5,000 years before present). Adaptive variation was investigated by phenotyping provenances originating east and west of the Mississippi River Valley, where long-term geographic separation has resulted in distinct population genetic structure. We used an integrated indicator, time to hydraulic failure (THF), predicted by a mechanistic hydraulic model, SurEau, to assess how trait combinations contribute to tree resistance to hotter droughts. Measured physiological traits included xylem vulnerability to cavitation, leaf and bark residual conductance, and leaf turgor loss point, each of which is known to be essential for tree drought resistance. Surprisingly, results indicate a tendency for THF to be lower in western provenances compared to eastern ones. Time to Hydraulic Failure was negatively correlated with residual stomatal conductance and leaf mass per area. This pattern suggests a physiological differentiation between populations, although it is not only determined by traits associated with drought resistance. Ongoing work aims to leverage this intraspecific variation to guide selection within and among tree species for more drought-resistant forests under continued climate change.

Summary: Drought‐induced tree mortality is associated with hydraulic failure and subsequent cell death. Leaf vitality is a critical indicator of tree water stress; however, current methods for assessing cell death are destructive and unsuitable for large‐scale measurements. The optical method, which detects changes in leaf light transmittance, has been traditionally used to monitor vein cavitation. However, emerging studies have reported transmittance changes extending beyond veins, suggesting a potential link with mesophyll cell death. In this study, we investigated whether the loss of light transmittance in leaves reflects underlying cellular mortality. We subjected seedlings from six tree species with contrasting drought resistance to progressive water stress. Changes in leaf light transmittance were continuously monitored using the optical method while cell mortality was quantified using classical methods. Cryo‐SEM imaging provided anatomical insights into cell structural degradation and its influence on transmittance. Our results revealed a strong synchronicity between transmittance loss and cell mortality increases across species, supporting the use of light transmittance as a nondestructive proxy for cellular damage. Overall, our results highlight the potential of the optical method for early detection of drought‐induced stress and mortality in trees and offer a promising, scalable, and noninvasive tool for monitoring tree health under drought.

Summary: Plant hydraulics is crucial for assessing the plants' capacity to extract and transport water from the soil up to their aerial organs. Along with their capacity to exchange water between plant compartments and regulate evaporation, hydraulic properties determine plant water relations, water status and susceptibility to pathogen attacks. Consequently, any variation in the hydraulic characteristics of plants is likely to significantly impact various mechanisms and processes related to plant growth, survival and production, as well as the risk of biotic attacks and forest fire behaviour. However, the integration of hydraulic traits into disciplines such as plant pathology, entomology, fire ecology or agriculture can be significantly improved. This review examines how plant hydraulics can provide new insights into our understanding of these processes, including modelling processes of vegetation dynamics, illuminating numerous perspectives for assessing the consequences of climate change on forest and agronomic systems, and addressing unanswered questions across multiple areas of knowledge.

Summary: Xylem hydraulic failure (HF) has been identified as a ubiquitous factor in triggering drought‐induced tree mortality through the damage induced by the progressive dehydration of plant living cells. However, fundamental evidence of the mechanistic link connecting xylem HF to cell death has not been identified yet. The main aim of this study was to evaluate, at the leaf level, the relationship between loss of hydraulic function due to cavitation and cell death under drought conditions and discern how this relationship varied across species with contrasting resistances to cavitation. Drought was induced by withholding water from potted seedlings, and their leaves were sampled to measure their relative water content (RWC) and cell mortality. Vulnerability curves to cavitation at the leaf level were constructed for each species. An increment in cavitation events occurrence precedes the onset of cell mortality. A variation in cells tolerance to dehydration was observed along with the resistance to cavitation. Overall, our results indicate that the onset of cellular mortality occurs at lower RWC than the one for cavitation indicating the role of cavitation in triggering cellular death. They also evidenced a critical RWC for cellular death varying across species with different cavitation resistance.