Integrating dehydration tolerance and avoidance in drought adaptation

Abstract

Water is a critical limiting resource for the growth and survival of plants. In the context of climate change, drought stress is increasing over many land areas across the globe due to decreased precipitation and/or increased evaporation (Dai 2013). At the same time, drought-induced tree mortality has been documented in every forested land, profoundly affecting forest biodiversity and the carbon and water cycles (Allen et al. 2010; Hammond et al. 2022). However, predicting the patterns of tree drought mortality remains challenging, mainly due to the incomplete understanding of how trees adapt to drought (Brodribb et al. 2020; Trugman et al. 2021). Half a century ago, researchers proposed two divergent strategies for trees to adapt to drought: dehydration tolerance and avoidance (Levitt 1972). Some trees mainly rely on tolerance, such as a more negative turgor loss point, while others depend on avoidance, such as deeper root systems (Volaire 2018). However, all trees possess both dehydration tolerance and avoidance capabilities. Dehydration tolerance and avoidance determine the lethal water threshold and the rate of water loss, respectively. Together, they define the drought survival of a tree (Brodribb et al. 2020). Therefore, how trees coordinate dehydration tolerance and avoidance is the key to their drought adaptation. However, our knowledge in this area remains limited. Here we review the dehydration tolerance and avoidance strategies of trees and propose a research framework that integrates these mechanisms through functional traits. We advocate research on multiple traits that regulate water supply and loss alongside lethal water thresholds. Dehydration tolerance refers to a tree’s ability to withstand tissue water loss (Volaire 2018). This ability is commonly indicated by a set of functional traits, including the lethal water potential (Ψlethal), water potential at 50% or 88% loss of xylem conductivity (P50 or P88), leaf water potential at turgor loss point (Ψtlp) and wood density (Fig. 1). Ψlethal is the most direct metric of dehydration tolerance, representing the ‘point of no return’ beyond which trees cannot recover from drought, even after months of rewatering (Choat 2013). However, determining Ψlethal is particularly time-consuming and labor-intensive. In such cases, wood density can serve as a robust proxy for Ψlethal (Liang et al. 2021). Besides, P50 and P88, which indicate the vulnerability of the xylem to drought-induced cavitation and Ψtlp, which reflects a tree’s ability to maintain cell turgor pressure under water stress, have long been widely used as indicators of dehydration tolerance in the field of plant water relations (Choat et al. 2018). Plants employ two distinct physiological strategies to adapt to drought: dehydration tolerance and avoidance. Dehydration tolerance can be assessed by Ψlethal (lethal water potential), P50 or P88 (water potential at 50% or 88% loss of xylem conductivity), Ψtlp (leaf water potential at turgor loss) and wood density. Dehydration avoidance is influenced by both water conservation, which is a product of stomatal control, gmin (leaf minimum conductance) and transpiring leaf area and water acquisition, which is a function of root depth and water storage. In contrast, dehydration avoidance refers to a tree’s ability to maintain moisture in its leaves or meristematic cells (Volaire 2018), which can be achieved through water conservation and acquisition (Fig. 1). When faced with drought, trees universally close their stomata to reduce water loss, with water potentials that trigger stomatal closure varying substantially across species (Martin-StPaul et al. 2017). However, even after stomatal closure, water continues to transpire through the leaf cuticle. At this stage, the transpiration rate can be described by leaf minimum conductance (gmin). In crop science, gmin has long been recognized as a crucial trait for drought adaptation, but in forest science, it has been largely overlooked (Duursma et al. 2019). In addition to the transpiration rate, the transpiring leaf area, quantifiable through the ratio of leaf area to sapwood area, is another factor determining the overall water transpiration during drought. Besides, root depth and water storage contribute to water supply, thus assisting trees in preventing dehydration of living cells during drought (Oliveira et al. 2021). It is crucial to note that all the traits mentioned above collectively determine the water flux of trees during drought, thus having a direct impact on the dehydration rate. Dehydration tolerance sets the lethal water potential, while avoidance sets the rate of water potential decline. It is the combination of dehydration tolerance and avoidance, rather than either mechanism in isolation, that dictates a tree’s survival during drought (Brodribb et al. 2020). Every tree possesses both dehydration tolerance and avoidance abilities. Therefore, integrating dehydration tolerance and avoidance is essential for thorough comprehension and prediction of tree drought adaptation. Recent studies have started to explore both dehydration tolerance and avoidance in understanding tree drought adaptation. For instance, tree species exhibiting higher dehydration tolerance, characterized by more negative P50, P88 and Ψtlp values, have been observed to possess shallower roots within tropical forest communities (Brum et al. 2019; Chitra-Tarak et al. 2021), although this pattern is not consistently observed across global biomes (Laughlin et al. 2023). Additionally, it has also been found that species with greater dehydration tolerance tend to close their stomata earlier (Li et al. 2018; Martin-StPaul et al. 2017) or have smaller water storage capacities (Bartlett et al. 2019; Smith-Martin et al. 2023). These examples provide insight into the diverse and intricate combinations of dehydration tolerance and avoidance that enable trees to adapt to drought conditions. However, a comprehensive framework to grasp the interactions among the diverse traits determining dehydration tolerance and avoidance is still lacking. There are significant knowledge gaps regarding how multiple traits, which govern dehydration tolerance and avoidance, vary under changing drought conditions and how they collectively interact to shape tree drought adaptation. Moreover, there is an urgent need for empirical and quantified data on these multiple traits of forest tree species, as they are pivotal parameters in process-based hydraulic models aimed at predicting tree drought mortality. Bridging these knowledge gaps requires a complete experimental framework and dedicated collaborative efforts within the global scientific community to thoroughly assess all the relevant traits. In detail, we need to figure out how trees effectively coordinate a range of dehydration-tolerant and -avoidant traits to withstand similar levels of drought stress within a community and adapt to various degrees of drought across communities. For example, varying levels of dehydration tolerance, as indicated by different P50 values, have been observed among trees in a given community (Zhu et al. 2013) or among trees experiencing similar precipitation levels (Choat et al. 2012). Consequently, it is reasonable to assume that those trees with lower dehydration tolerance may employ higher dehydration avoidance strategies with various combinations of dehydration-avoidant traits to survive under similar drought conditions. On the other hand, while trees have often been shown to adjust their dehydration-tolerant traits along drought gradients across communities, how they modify their dehydration-avoidant traits remains largely unknown. It is conceivable that both dehydration-tolerant and -avoidant traits were co-selected by water stress, as evidenced by P50 and the ratio of leaf area to xylem area (Sanchez-Martinez et al. 2020). Therefore, trees in drier habitats may exhibit both greater dehydration tolerance and avoidance. Future research should go beyond merely using correlation analysis and principal component analysis. It should aim to uncover the trade-off between dehydration tolerance and avoidance or the continuum spanning from drought tolerance to drought avoidance. To delve deeper into this complex interplay, it is essential to incorporate innovative methodologies, such as trait network analysis (He et al. 2020), to gain more comprehensive insights into trait covariation and its relationship with tree adaptation to drought conditions. In summary, dehydration tolerance and avoidance jointly determine tree survival during drought. Therefore, a comprehensive understanding of tree adaptation to drought requires examining these aspects together rather than in isolation. Future research needs to: Investigate how trees modify multiple dehydration-tolerant and -avoidant traits to adapt to drought. This involves shifting the focus from single organs to multiple organs to gain a holistic view at the whole-plant level. Explore the correlations among these traits across species within communities and across communities experiencing different water stress. Innovative methods like network analysis can be employed for this purpose. Develop a database of key traits to better inform models that aim to predict the impacts of drought on forests, with concerted efforts from scientific communities worldwide. Addressing these points can advance our understanding of tree adaptation to drought and enhance our ability to anticipate and mitigate its effects on forest ecosystems. This work was supported by Guangdong Flagship Project of Basic and Applied Basic Research (2023B0303050001), the National Natural Science Foundation of China (32171503), Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden (2023B1212060046), Science and Technology Projects in Guangzhou (2024A04J4347) and South China Botanical Garden, Chinese Academy of Sciences (QNXM-202303). Conflict of interest statement. The authors declare that they have no conflict of interest.

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