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Drought is one of the main factors contributing to tree mortality worldwide and drought events are set to become more frequent and intense in the face of a changing climate. Quantifying water stress of forests is crucial in predicting and understanding their vulnerability to drought-induced mortality. Here, we explore the use of high-resolution spectroscopy in predicting water stress indicators of two native Australian tree species, Callitris rhomboidea and Eucalyptus viminalis. Specific spectral features and indices derived from leaf-level spectroscopy were assessed as potential proxies to predict leaf water potential (Ψ leaf ), equivalent water thickness (EWT) and fuel moisture content (FMC) in a dedicated laboratory experiment. New spectral indices were identified that enabled very high confidence linear prediction of Ψ leaf for both species (R 2  > 0.85) with predictive capacity increasing when accounting for a breakpoint in the relationships using segmented regression (E. viminalis, R 2  > 0.89; C. rhomboidea, R 2  > 0.87). EWT and FMC were also linearly predicted to a high accuracy (E. viminalis, R 2  > 0.90; C. rhomboidea, R 2  > 0.80). This study highlights the potential of spectroscopy as a tool for predicting measures of plant water noninvasively, enabling broader applications for monitoring and managing plant water stress., (© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Resolving the position of roots in the whole-plant hierarchy of drought-induced xylem embolism resistance is fundamental for predicting when species become isolated from soil water resources. Published research generally suggests that roots are the most vulnerable organ of the plant vascular system, although estimates vary significantly. However, our knowledge of root embolism excludes the fine roots (< 2 mm diameter) that form the bulk of total absorptive surface area of the root network for water and nutrient uptake. We measured fine root and stem xylem vulnerability in 10 vascular plant species from the major land plant clades (five angiosperms, three conifers, a fern and lycophyte), using standardised in situ methods (Optical Methods and MicroCT). Mean fine root embolism resistance across the network matched or exceeded stems in all study species. In six of these species (one fern, one lycophyte, three conifers and one angiosperm), fine roots were significantly more embolism resistant than stems. No clear relationship was found between root xylem conduit diameter and vulnerability. These results provide insight into the resistance of the plant hydraulic pathway at the site of water and nutrient uptake, and challenge the long-standing assumption that fine roots are more vulnerable than stems., (© 2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.)

Nicotiana benthamiana is predominantly distributed in arid habitats across northern Australia. However, none of six geographically isolated accessions shows obvious xerophytic morphological features. To investigate how these tender-looking plants withstand drought, we examined their responses to water deprivation, assessed phenotypic, physiological, and cellular responses, and analysed cuticular wax composition and wax biosynthesis gene expression profiles. Results showed that the Central Australia (CA) accession, globally known as a research tool, has evolved a drought escape strategy with early vigour, short life cycle, and weak, water loss-limiting responses. By contrast, a northern Queensland (NQ) accession responded to drought by slowing growth, inhibiting flowering, increasing leaf cuticle thickness, and altering cuticular wax composition. Under water stress, NQ increased the heat stability and water impermeability of its cuticle by extending the carbon backbone of cuticular long-chain alkanes from c. 25 to 33. This correlated with rapid upregulation of at least five wax biosynthesis genes. In CA, the alkane chain lengths (c. 25) and gene expression profiles remained largely unaltered. This study highlights complex genetic and environmental control over cuticle composition and provides evidence for divergence into at least two fundamentally different drought response strategies within the N. benthamiana species in < 1 million years., (© 2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.)

Understanding xylem embolism spread in roots is essential for predicting the loss of function across root systems during drought. However, the lasting relevance of root embolism to plant recovery depends on whether roots can refill xylem emboli and resume function after rehydration. Using MicroCT and optical and dye staining methods, we investigated embolism repair in rehydrated intact roots of wheat (Triticum aestivum L.'Krichauff') exposed to a severe water deficit of -3.5 MPa, known to cause approximately 30 % total root network embolism in this species. Air emboli in the xylem vessels of intact roots remained clearly observable using MicroCT after overnight rehydration. This result was verified by xylem staining of the root system and optical quantification of emboli, both of which indicated a lack of functional root xylem recovery 60 hours following soil re-saturation. The absence of root xylem refilling in wheat has substantial implications for how we understand plant recovery after drought. Our findings suggest that xylem embolism causes irreversible damage to the soil-root hydraulic connection in affected parts of the root network., (© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

Stomatal closure under high VPD L (leaf to air vapour pressure deficit) is a primary means by which plants prevent large excursions in transpiration rate and leaf water potential (Ψ leaf ) that could lead to tissue damage. Yet, the drivers of this response remain controversial. Changes in Ψ leaf appear to drive stomatal VPD L response, but many argue that dynamic changes in soil-to-leaf hydraulic conductance (K s-l ) make an important contribution to this response pathway, even in well-hydrated soils. Here, we examined whether the regulation of whole plant stomatal conductance (g c ) in response to typical changes in daytime VPD L is influenced by dynamic changes in K s-l . We use well-watered plants of two species with contrasting ecological and physiological features: the herbaceous Arabidopsis thaliana (ecotype Columbia-0) and the dry forest conifer Callitris rhomboidea. The dynamics of K s-l and g c were continuously monitored by combining concurrent in situ measurements of Ψ leaf using an open optical dendrometer and whole plant transpiration using a balance. Large changes in VPD L were imposed to induce stomatal closure and observe the impact on K s-l . In both species, g c was observed to decline substantially as VPD L increased, while K s-l remained stable. Our finding suggests that stomatal regulation of transpiration is not contingent on a decrease in K s-l . Static K s-l provides a much simpler explanation for transpiration control in hydrated plants and enables simplified modelling and new methods for monitoring plant water use in the field., (© 2024 The Authors New Phytologist © 2024 New Phytologist Foundation.)

A theoretical trade-off between the efficiency and safety of water transport systems in plants is used to explain diverse ecological patterns, from tree size to community structure. Despite its pervasive influence, this theory has marginal empirical support. This may be partially due to obfuscation of associations by wide phylogenetic sampling or non-standard sampling between studies. To address this, we examine the coordination of structural and anatomical traits linked to hydraulic safety and efficiency in the leaves of an ecologically diverse group of eucalypts. We introduce a new trait for characterising leaf water transport function measured as the cross-sectional XA at the petiole divided by the downstream leaf area (XLA petiole ). Variation in XLA petiole revealed support for a safety-efficiency trade-off in eucalypt leaves. XLA petiole was negatively correlated with theoretical petiole xylem conductivity (K s&#95;petiole ) and strongly negatively correlated with leaf cavitation vulnerability (Ψ50 leaf ). Species with lower Ψ50 leaf exhibited petiole xylem with narrower vessels and greater fibre wall area fractions. Our findings highlight XLA petiole as a novel integrative trait that provides insights into the evolution of leaf form and function in eucalypts and holds promise for wider use among diverse species., (© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Tropical rainforest woody plants have been thought to have uniformly low resistance to hydraulic failure and to function near the edge of their hydraulic safety margin (HSM), making these ecosystems vulnerable to drought; however, this may not be the case. Using data collected at 30 tropical forest sites for three key traits associated with drought tolerance, we show that site-level hydraulic diversity of leaf turgor loss point, resistance to embolism (P 50 ), and HSMs is high across tropical forests and largely independent of water availability. Species with high HSMs (>1 MPa) and low P 50 values (< -2 MPa) are common across the wet and dry tropics. This high site-level hydraulic diversity, largely decoupled from water stress, could influence which species are favoured and become dominant under a drying climate. High hydraulic diversity could also make these ecosystems more resilient to variable rainfall regimes., (© 2023 The Authors. Ecology Letters published by John Wiley & Sons Ltd.)

Vapour pressure deficit (VPD) plays a crucial role in regulating plant carbon and water fluxes due to its influence on stomatal behaviour and transpiration. Yet, characterising stomatal responses of the whole plant to VPD remains challenging due to methodological limitations. Here, we develop a novel method for in situ assessment of whole-plant stomatal responses (g c ) to VPD in the herbaceous plant Tanacetum cinerariifolium. To do this, we examine the relationship between daytime VPD and the corresponding soil-stem water potential gradient (ΔΨ) monitored using the optical dendrometry in well-hydrated plants under nonlimiting light in both glasshouse and field conditions. In glasshouse plants, ΔΨ increased proportionally with the VPD up to a threshold of 1.53 kPa, beyond which the slope decreased, suggesting a two-phase response in g c . This pattern aligned with corresponding gravimetrically measured g c behaviour, which also showed a decline when VPD exceeded a similar threshold. This response was then compared with that of field plants monitored using the optical dendrometry technique over a growing season under naturally variable VPD conditions and nonlimiting light and water supply. Field plants exhibited a similar threshold-type response to VPD but were more sensitive than glasshouse individuals with a VPD threshold of 0.74 kPa. The results showed that whole-plant g c responses to VPD can be characterised optically in T. cinerariifolium, introducing a new tool for the monitoring and characterisation of stomatal behaviour in situ., (© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Perennial plant species from water-limiting environments (including climates of extreme drought, heat and freezing temperatures) have evolved traits that allow them to tolerate these conditions. As such, traits that are associated with water stress may show evidence of adaptation to climate when compared among closely related species inhabiting contrasting climatic conditions. In this study, we tested whether key hydraulic traits linked to drought stress, including the vulnerability of leaves to embolism (P50 leaf) and the minimum diffusive conductance of shoots (gmin), were associated with climatic characteristics of 14 Tasmanian eucalypt species from sites that vary in precipitation and temperature. Across species, greater cavitation resistance (more negative P50 leaf) was associated with increasing aridity and decreasing minimum temperature. By contrast, gmin showed strong associations with aridity only. Among these Tasmanian eucalypts, evidence suggests that trait variation is influenced by both cold and dry conditions, highlighting the need to consider both aspects when exploring adaptive trait-climate relationships., (© The Author(s) 2023. Published by Oxford University Press.)

Flowers are critical for angiosperm reproduction and the production of food, fiber, and pharmaceuticals, yet for unknown reasons, they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a vascular system that has a low capacity to supply water and is prone to failure under water stress. These characteristics may render reproductive structures more susceptible than leaves to runaway cavitation-an uncontrolled feedback cycle between rising water stress and declining water transport efficiency that can rapidly lead to lethal tissue desiccation. We provide modeling and empirical evidence to demonstrate that flower damage in the perennial crop pyrethrum (Tanacetum cinerariifolium), in the form of irreversible desiccation, corresponds with runaway cavitation in the flowering stem after a combination of heat and water stress. We show that tissue damage is linked to greater evaporative demand during high temperatures rather than direct thermal stress. High floral transpiration dramatically reduced the soil water deficit at which runaway cavitation was triggered in pyrethrum flowering stems. Identifying runaway cavitation as a mechanism leading to heat damage and reproductive losses in pyrethrum provides different avenues for process-based modeling to understand the impact of climate change on cultivated and natural plant systems. This framework allows future investigation of the relative susceptibility of diverse plant species to reproductive failure under hot and dry conditions., Competing Interests: Conflict of interest statement. None declared., (© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

Premise: Acmopyle (Podocarpaceae) comprises two extant species from Oceania that are physiologically restricted to ever-wet rainforests, a confirmed fossil record based on leaf adpressions and cuticles in Australia since the Paleocene, and a few uncertain reports from New Zealand, Antarctica, and South America. We investigated fossil specimens with Acmopyle affinities from the early Eocene Laguna del Hunco site in Patagonia, Argentina., Methods: We studied 42 adpression leafy-shoot fossils and included them in a total evidence phylogenetic analysis., Results: Acmopyle grayae sp. nov. is based on heterophyllous leafy shoots with three distinct leaf types. Among these, bilaterally flattened leaves uniquely preserve subparallel, linear features that we interpret as accessory transfusion tissue (ATT, an extra-venous water-conducting tissue). Some apical morphologies of A. grayae shoots are compatible with the early stages of ovuliferous cone development. Our phylogenetic analysis recovers the new species in a polytomy with the two extant Acmopyle species. We report several types of insect-herbivory damage. We also transfer Acmopyle engelhardti from the middle Eocene Río Pichileufú flora to Dacrycarpus engelhardti comb. nov., Conclusions: We confirm the biogeographically significant presence of the endangered West Pacific genus Acmopyle in Eocene Patagonia. Acmopyle is one of the most drought-intolerant genera in Podocarpaceae, possibly due to the high collapse risk of the ATT, and thus the new fossil species provides physiological evidence for the presence of an ever-wet rainforest environment at Laguna del Hunco during the Early Eocene Climatic Optimum., (© 2023 Botanical Society of America.)

The propagation of xylem embolism throughout the root systems of drought-affected plants remains largely unknown, despite this process being comparatively well characterized in aboveground tissues. We used optical and X-ray imaging to capture xylem embolism propagation across the intact root systems of bread wheat (Triticum aestivum L. 'Krichauff') plants subjected to drying. Patterns in vulnerability to xylem cavitation were examined to investigate whether vulnerability may vary based on root size and placement across the entire root system. Individual plants exhibited similar mean whole root system vulnerabilities to xylem cavitation but showed enormous 6 MPa variation within their component roots (c. 50 roots per plant). Xylem cavitation typically initiated in the smallest, peripheral parts of the root system and moved inwards and upwards towards the root collar last, although this trend was highly variable. This pattern of xylem embolism spread likely results in the sacrifice of replaceable small roots while preserving function in larger, more costly central roots. A distinct pattern of embolism-spread belowground has implications for how we understand the impact of drought in the root system as a critical interface between plant and soil., (© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.)

The ideal plant water transport system is one that features high efficiency and resistance to drought-induced damage (xylem cavitation), however, species rarely possess both. This may be explained by trade-offs between traits, yet thus far, no proposed trade-off has offered a universal explanation for the lack of water transport systems that are both highly drought-resistant and highly efficient. Here, we find evidence for a new trade-off, between growth rate and resistance to xylem cavitation, in the canopies of a drought-resistant tree species (Callitris rhomboidea). Wide variation in cavitation resistance (P50) was found in distal branch tips (<2 mm in diameter), converging to low variation in P50 in larger diameter stems (>2 mm). We found a significant correlation between cavitation resistance and distal branchlet internode length across branch tips in C. rhomboidea canopies. Branchlets with long internodes (8 mm or longer) were significantly more vulnerable to drought-induced xylem cavitation than shorter internodes (4 mm or shorter). This suggests that varying growth rates, leading to differences in internode length, drive differences in cavitation resistance in C. rhomboidea trees. The only distinct anatomical difference found between internodes was the pith size, with the average pith to xylem area in long internodes being five times greater than in short internodes. Understanding whether this trade-off exists within and between species will help us to uncover what drives and limits drought resistance across the world's flora., (© The Author(s) 2023. Published by Oxford University Press.)

Background and Aims: Many annual grasses exhibit drought-avoiding life cycles in which rapid reproduction must be completed before soil water is exhausted. This strategy would seem to require a hydraulic system capable of sustaining reproduction at all costs to the rest of the plant, yet little is known about the whole-plant structure of hydraulic vulnerability in grasses., Methods: We examine vulnerability to water-stress-induced xylem cavitation in roots, flag leaves, and basal and apical regions of peduncles of wheat (Triticum aestivum L. 'Krichauff') to understand the staged failure of xylem function in severe drought. The functionality of segmented vulnerabilities is tested by conducting rehydration experiments after acute dehydration., Key Results: We show that water supply to peduncles is more drought resistant than in leaves due to greater xylem cavitation resistance, ensuring a pathway of water can be maintained from the roots to the reproductive tissues even after severe water deficit. Differential rehydration of peduncles compared to leaves following drought confirmed the functionality of xylem supply from roots to seed after water stress sufficient to completely cavitate flag leaf vessels., Conclusions: These results demonstrate that a proportion of the hydraulic pathway between roots and seeds remains functional under extreme dehydration, suggesting that vulnerability traits in this key grass species reflect its reproductive strategy., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Annals of Botany Company.)

Xylem cavitation during drought is proposed as a major driver of canopy collapse, but the mechanistic link between hydraulic failure and leaf damage in trees is still uncertain. Here, we used the tree species manna gum (Eucalyptus viminalis) to explore the connection between xylem dysfunction and lethal desiccation in leaves. Cavitation damage to leaf xylem could theoretically trigger lethal desiccation of tissues by severing water supply under scenarios such as runaway xylem cavitation, or the local failure of terminal parts of the leaf vein network. To investigate the role of xylem failure in leaf death, we compared the timing of damage to the photosynthetic machinery (Fv/Fm decline) with changes in plant hydration and xylem cavitation during imposed water stress. The water potential at which Fv/Fm was observed to decline corresponded to the water potential marking a transition from slow to very rapid tissue dehydration. Both events also occurred simultaneously with the initiation of cavitation in leaf high-order veins (HOV, veins from the third order above) and the analytically derived point of leaf runaway hydraulic failure. The close synchrony between xylem dysfunction and the photosynthetic damage strongly points to water supply disruption as the trigger for desiccation of leaves in this hardy evergreen tree. These results indicate that runaway cavitation, possibly triggered by HOV network failure, is the tipping agent determining the vulnerability of E. viminalis leaves to damage during drought and suggest that HOV cavitation and runaway hydraulic failure may play a general role in determining canopy damage in plants., Competing Interests: Conflict of interest statement. None declared., (© American Society of Plant Biologists 2023. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Forest mortality during drought has been attributed to hydraulic failure, which can be challenging to measure. A limited number of alternative proxies for incipient leaf death exist. Here we investigate whether a terminal increase in abscisic acid (ABA) levels in leaves occurs across vascular land plants and is an indicator of imminent leaf death. For different species across vascular plants, we monitored ABA levels during lethal drought as well as leaf embolism resistance, across the canopy as leaves die following senescence, or when leaves are exposed to a heavy, lethal frost late in the growing season. We observed a considerable increase in foliage ABA levels once leaves showed signs of incipient leaf death. This increase in ABA levels upon incipient leaf death, could be induced by embolism during drought, by freezing or as leaves age naturally, and was observed in species spanning the phylogeny of vascular land plants as well as in an ABA biosynthetic mutant plant. A considerable increase in foliage ABA levels may act as an indicator of impending leaf death., (© 2022 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands.)

Background and Aims: Hydraulic failure is considered a main cause of drought-induced forest mortality. Yet, we have a limited understanding of how the varying intensities and long time scales of natural droughts induce and propagate embolism within the xylem., Methods: X-ray computed tomography (microCT) images were obtained from different aged branch xylem to study the number, size and spatial distribution of in situ embolized conduits among three dominant tree species growing in a woodland community., Key Results: Among the three studied tree species, those with a higher xylem vulnerability to embolism (higher water potential at 50 % loss of hydraulic conductance; P50) were more embolized than species with lower P50. Within individual stems, the probability of embolism was independent of conduit diameter but associated with conduit position. Rather than the occurrence of random or radial embolism, we observed circumferential clustering of high and low embolism density, suggesting that embolism spreads preferentially among conduits of the same age. Older xylem also appeared more likely to accumulate embolisms than young xylem, but there was no pattern suggesting that branch tips were more vulnerable to cavitation than basal regions., Conclusions: The spatial analysis of embolism occurrence in field-grown trees suggests that embolism under natural drought probably propagates by air spreading from embolized into neighbouring conduits in a circumferential pattern. This pattern offers the possibility to understand the temporal aspects of embolism occurrence by examining stem cross-sections., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Plant transpiration is an inevitable consequence of photosynthesis and has a huge impact on the terrestrial carbon and water cycle, yet accurate and continuous monitoring of its dynamics is still challenging. Under well-watered conditions, canopy transpiration (Ec) could potentially be continuously calculated from stem water potential (Ψstem), but only if the root to stem hydraulic conductance (Kr-s) remains constant and plant capacitance is relatively small. We tested whether such an approach is viable by investigating whether Kr-s remains constant under a wide range of daytime transpiration rates in non-water-stressed plants. Optical dendrometers were used to continuously monitor tissue shrinkage, an accurate proxy of Ψstem, while Ec was manipulated in three species with contrasting morphological, anatomical, and phylogenetic identities: Tanacetum cinerariifolium, Zea mays, and Callitris rhomboidea. In all species, we found Kr-s to remain constant across a wide range of Ec, meaning that the dynamics of Ψstem could be used to monitor Ec. This was evidenced by the close agreement between measured Ec and that predicted from optically measured Ψstem. These results suggest that optical dendrometers enable both plant hydration and Ec to be monitored non-invasively and continuously in a range of woody and herbaceous species. This technique presents new opportunities to monitor transpiration under laboratory and field conditions in a diversity of woody, herbaceous, and grassy species., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Plant function arises from a complex network of structural and physiological traits. Explicit representation of these traits, as well as their connections with other biophysical processes, is required to advance our understanding of plant-soil-climate interactions. We used the Terrestrial Regional Ecosystem Exchange Simulator (TREES) to evaluate physiological trait networks in maize. Net primary productivity (NPP) and grain yield were simulated across five contrasting climate scenarios. Simulations achieving high NPP and grain yield in high precipitation environments featured trait networks conferring high water use strategies: deep roots, high stomatal conductance at low water potential ("risky" stomatal regulation), high xylem hydraulic conductivity and high maximal leaf area index. In contrast, high NPP and grain yield was achieved in dry environments with low late-season precipitation via water conserving trait networks: deep roots, high embolism resistance and low stomatal conductance at low leaf water potential ("conservative" stomatal regulation). We suggest that our approach, which allows for the simultaneous evaluation of physiological traits, soil characteristics and their interactions (i.e., networks), has potential to improve our understanding of crop performance in different environments. In contrast, evaluating single traits in isolation of other coordinated traits does not appear to be an effective strategy for predicting plant performance., (© 2022 John Wiley & Sons Ltd.)

The hydraulic vulnerability segmentation (HVS) hypothesis implies the existence of differences in embolism resistance between plant organs along the xylem pathway and has been suggested as an adaptation allowing the differential preservation of more resource-rich tissues during drought stress. Compound leaves in trees are considered a low-cost means of increasing leaf area and may thus be expected to show evidence of strong HVS, given the tendency of compound-leaved tree species to shed their leaf units during drought. However, the existence and role of HVS in compound-leaved tree species during drought remain uncertain. We used an optical visualization technique to estimate embolism occurrence in stems, petioles, and leaflets of shoots in two compound-leaved tree species, Manchurian ash (Fraxinus mandshurica) and Manchurian walnut (Juglans mandshurica). We found higher (less negative) water potentials corresponding to 50% loss of conductivity (P50) in leaflets and petioles than in stems in both species. Overall, we observed a consistent pattern of stem > petiole > leaflet in terms of xylem resistance to embolism and hydraulic safety margins (i.e. the difference between mid-day water potential and P50). The coordinated variation in embolism vulnerability between organs suggests that during drought conditions, trees benefit from early embolism and subsequent shedding of more expendable organs such as leaflets and petioles, as this provides a degree of protection to the integrity of the hydraulic system of the more carbon costly stems. Our results highlight the importance of HVS as an adaptive mechanism of compound-leaved trees to withstand drought stress., (© American Society of Plant Biologists 2022. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

The mechanisms by which woody plants recover xylem hydraulic capacity after drought stress are not well understood, particularly with regard to the role of embolism refilling. We evaluated the recovery of xylem hydraulic capacity in young Eucalyptus saligna plants exposed to cycles of drought stress and rewatering. Plants were exposed to moderate and severe drought stress treatments, with recovery monitored at time intervals from 24 h to 6 months after rewatering. The percentage loss of xylem vessels due to embolism (PLV) was quantified at each time point using microcomputed tomography with stem water potential (Ψ x ) and canopy transpiration (E c ) measured before scans. Plants exposed to severe drought stress suffered high levels of embolism (47.38% ± 10.97% PLV) and almost complete canopy loss. No evidence of embolism refilling was observed at 24 h, 1 week, or 3 weeks after rewatering despite rapid recovery in Ψ x . Recovery of hydraulic capacity was achieved over a 6-month period by growth of new xylem tissue, with canopy leaf area and E c recovering over the same period. These findings indicate that E. saligna recovers slowly from severe drought stress, with potential for embolism to persist in the xylem for many months after rainfall events., (© 2022 John Wiley & Sons Ltd.)

Vulnerability to xylem cavitation is a strong predictor of drought-induced damage in forest communities. However, biotic features of the community itself can influence water availability at the individual tree-level, thereby modifying patterns of drought damage. Using an experimental forest in Tasmania, Australia, we determined the vulnerability to cavitation (leaf P 50 ) of four tree species and assessed the drought-induced canopy damage of 2944 6-yr-old trees after an extreme natural drought episode. We examined how individual damage was related to their size and the density and species identity of neighbouring trees. The two co-occurring dominant tree species, Eucalyptus delegatensis and Eucalyptus regnans, were the most vulnerable to drought-induced xylem cavitation and both species suffered significantly greater damage than neighbouring, subdominant species Pomaderris apetala and Acacia dealbata. While the two eucalypts had similar leaf P 50 values, E. delegatensis suffered significantly greater damage, which was strongly related to the density of neighbouring P. apetala. Damage in E. regnans was less impacted by neighbouring plants and smaller trees of both eucalypts sustained significantly more damage than larger trees. Our findings demonstrate that natural drought damage is influenced by individual plant physiology as well as the composition, physiology and density of the surrounding stand., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

Premise: Tip-to-base conduit widening is considered a key mechanism that enables vascular plants to grow tall by decreasing the hydraulic resistance imposed by increasing height. Widening of hydraulic anatomy (larger conducting elements toward the base of the vascular system) minimizes gradients in leaf-specific hydraulic conductance with plant height, allowing uniform photosynthesis across the crown of trees. Tip-to-base conduit widening has also been associated with changes in conduit number. However, in bryophytes, despite having representatives with internal water-conducting tissue, conduit widening has been scarcely investigated., Methods: Here, we examined the changes in hydroid diameter and number with distance from plant tip in Dawsonia superba and D. polytrichoides, two representatives of the genus containing the tallest extant bryophytes., Results: The position of these moss species on the global scale of conduit size and plant size was consistent with a general scaling among plants with internal water transport. Within plants, patterns of conduit widening and number with distance from plant tip in endohydric mosses were similar to those observed in vascular plants., Conclusions: This study demonstrated that land plants growing upward in the atmosphere show analogous conduit widening of hydraulic structures, suggesting that efficient internal water transport is a convergent adaptation for photosynthesis on land., (© 2021 Botanical Society of America.)

Reproductive success largely defines the fitness of plant species. Understanding how heat and drought affect plant reproduction is thus key to predicting future plant fitness under rising global temperatures. Recent work suggests reproductive tissues are highly vulnerable to water stress in perennial plants where reproductive sacrifice could preserve plant survival. However, most crop species are annuals where such a strategy would theoretically reduce fitness. We examined the reproductive strategy of tomato (Solanum lycopersicum var. Rheinlands Ruhm) to determine whether water supply to fruits is prioritized above vegetative tissues during drought. Using optical methods, we mapped xylem cavitation and tissue shrinkage in vegetative and reproductive organs during dehydration to determine the priority of water flow under acute water stress. Stems and peduncles of tomato showed significantly greater xylem cavitation resistance than leaves. This maintenance of intact water supply enabled tomato fruit to continue to expand during acute water stress, utilizing xylem water made available by tissue collapse and early cavitation of leaves. Here, tomato plants prioritize water supply to reproductive tissues, maintaining fruit development under drought conditions. These results emphasize the critical role of water transport in shaping life history and suggest a broad relevance of hydraulic prioritization in plant ecology., (© 2021 John Wiley & Sons Ltd.)

Damage to the plant water transport system through xylem cavitation is known to be a driver of plant death in drought conditions. However, a lack of techniques to continuously monitor xylem embolism in whole plants in vivo has hampered our ability to investigate both how this damage propagates and the possible mechanistic link between xylem damage and tissue death. Using optical and fluorescence sensors, we monitored drought-induced xylem embolism accumulation and photosynthetic damage in vivo throughout the canopy of a drought-resistant conifer, Callitris rhomboidea, during drought treatments of c. 1 month duration. We show that drought-induced damage to the xylem can be monitored in vivo in whole trees during extended periods of water stress. Under these conditions, vulnerability of the xylem to cavitation varied widely among branchlets, with photosynthetic damage only recorded once > 90% of the xylem was cavitated. The variation in branchlet vulnerability has important implications for understanding how trees like C. rhomboidea survive drought, and the high resistance of branchlets to tissue damage points to runaway cavitation as a likely driver of tissue death in C. rhomboidea branch tips., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

Leaf habit has been hypothesized to define a linkage between the slow-fast plant economic spectrum and the drought resistance-avoidance trade-off in tropical forests ('slow-safe vs fast-risky'). However, variation in hydraulic traits as a function of leaf habit has rarely been explored for a large number of species. We sampled leaf and branch functional traits of 97 tropical dry forest tree species from four sites to investigate whether patterns of trait variation varied consistently in relation to leaf habit along the 'slow-safe vs fast-risky' trade-off. Leaf habit explained from 0% to 43.69% of individual trait variation. We found that evergreen and semi-deciduous species differed in their location along the multivariate trait ordination when compared to deciduous species. While deciduous species showed consistent trait values, evergreen species trait values varied as a function of the site. Last, trait values varied in relation to the proportion of deciduous species in the plant community. We found that leaf habit describes the strategies that define drought avoidance and plant economics in tropical trees. However, leaf habit alone does not explain patterns of trait variation, which suggests quantifying site-specific or species-specific uncertainty in trait variation as the way forward., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

We introduce the AusTraits database - a compilation of values of plant traits for taxa in the Australian flora (hereafter AusTraits). AusTraits synthesises data on 448 traits across 28,640 taxa from field campaigns, published literature, taxonomic monographs, and individual taxon descriptions. Traits vary in scope from physiological measures of performance (e.g. photosynthetic gas exchange, water-use efficiency) to morphological attributes (e.g. leaf area, seed mass, plant height) which link to aspects of ecological variation. AusTraits contains curated and harmonised individual- and species-level measurements coupled to, where available, contextual information on site properties and experimental conditions. This article provides information on version 3.0.2 of AusTraits which contains data for 997,808 trait-by-taxon combinations. We envision AusTraits as an ongoing collaborative initiative for easily archiving and sharing trait data, which also provides a template for other national or regional initiatives globally to fill persistent gaps in trait knowledge., (© 2021. The Author(s).)

Plants from arid environments display covarying traits to survive or resist drought. Plant drought resistance and ability to survive long periods of low soil water availability should involve leaf phenology coordination with leaf and stem functional traits related to water status. This study tested correlations between phenology and functional traits involved in plant water status regulation in 10 Sonoran Desert tree species with contrasting phenology. Species seasonal variation in plant water status was defined by calculating their relative positions along the iso/anisohydric regulation continuum based on their hydroscape areas (HA)-a metric derived from the relationship between predawn and midday water potentials-and stomatal and hydraulic traits. Additionally, functional traits associated with plant water status regulation, including lamina vessel hydraulic diameter (DHL), stem-specific density (SSD) and leaf mass per area (LMA) were quantified per species. To characterize leaf phenology, leaf longevity (LL) and canopy foliage duration (FD) were determined. Hydroscape area was strongly correlated with FD but not with leaf longevity (LL); HA was significantly associated with SSD and leaf hydraulic traits (DHL, LMA) but not with stem hydraulic traits (vulnerability index, relative conductivity); and FD was strongly correlated with LMA and SSD. Leaf physiological characteristics affected leaf phenology when it was described as canopy FD better than when described as LL. Stem and leaf structure and hydraulic functions were not only relevant for categorizing species along the iso/anisohydric continuum but also allowed identifying different strategies of desert trees within the 'fast-slow' plant economics spectrum. The results in this study pinpoint the set of evolutionary pressures that shape the Sonoran Desert Scrub physiognomy., (© The Author(s) 2021. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com.)

Root systems play a major role in supplying the canopy with water, enabling photosynthesis and growth. Yet, much of the dynamic response of root hydraulics and its influence on gas exchange during soil drying and recovery remains uncertain. We examined the decline and recovery of the whole root hydraulic conductance (Kr) and canopy diffusive conductance (gc) during exposure to moderate water stress in two species with contrasting root systems: Tanacetum cinerariifolium (herbaceous Asteraceae) and Callitris rhomboidea (woody conifer). Optical dendrometers were used to record stem water potential at high temporal resolution and enabled non-invasive measurements of Kr calculated from the rapid relaxation kinetics of water potential in hydrating roots. We observed parallel declines in Kr and gc to <20% of unstressed levels during the early stages of water stress in both species. The recovery of Kr after rewatering differed between species. T. cinerariifolium recovered quickly, with 60% of Kr recovered within 2 h, while C. rhomboidea was much slower to return to its original Kr. Recovery of gc followed a similar trend to Kr in both species, with C. rhomboidea slower to recover. Our findings suggest that the pronounced sensitivity of Kr to drought is a common feature among different plant species, but recovery may vary depending on root type and water stress severity. Kr dynamics are proposed to modulate gc response during and following drought., (© American Society of Plant Biologists 2021. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Desiccation tolerant plants can survive extreme water loss in their vegetative tissues. The fern Anemia caffrorum produces desiccation tolerant (DT) fronds in the dry season and desiccation sensitive (DS) fronds in the wet season, providing a unique opportunity to explore the physiological mechanisms associated with desiccation tolerance. Anemia caffrorum plants with either DT or DS fronds were acclimated in growth chambers. Photosynthesis, frond structure and anatomy, water relations and minimum conductance to water vapour were measured under well-watered conditions. Photosynthesis, hydraulics, frond pigments, antioxidants and abscisic acid contents were monitored under water deficit. A comparison between DT and DS fronds under well-watered conditions showed that the former presented higher leaf mass per area, minimum conductance, tissue elasticity and lower CO 2 assimilation. Water deficit resulted in a similar induction of abscisic acid in both frond types, but DT fronds maintained higher stomatal conductance and upregulated more prominently lipophilic antioxidants. The seasonal alternation in production of DT and DS fronds in A. caffrorum represents a mechanism by which carbon gain can be maximized during the rainy season, and a greater investment in protective mechanisms occurs during the hot dry season, enabling the exploitation of episodic water availability., (© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.)

Plants control water-use efficiency (WUE) by regulating water loss and CO 2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to water stress. Here, we compared the response of gas exchange to decreasing leaf water potential among four ferns and nine seed plant species exposed to a gradually intensifying water deficit. The data collected were combined with those from 339 phylogenetically diverse species obtained from previous studies. In well-watered angiosperms, the maximum stomatal conductance was high and greater than that required for maximum WUE, but drought stress caused a rapid reduction in stomatal conductance and an increase in WUE in response to elevated concentrations of abscisic acid. However, in ferns, stomata did not open beyond the optimum point corresponding to maximum WUE and actually exhibited a steady WUE in response to dehydration. Thus, seed plants showed improved photosynthetic WUE under water stress. The ability of seed plants to increase WUE could provide them with an advantage over ferns under drought conditions, thereby presumably increasing their fitness under selection pressure by drought., (© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.)

The key role of cell walls in setting mesophyll conductance to CO2 (gm) and, consequently, photosynthesis is reviewed. First, the theoretical properties of cell walls that can affect gm are presented. Then, we focus on cell wall thickness (Tcw) reviewing empirical evidence showing that Tcw varies strongly among species and phylogenetic groups in a way that correlates with gm and photosynthesis; that is, the thicker the mesophyll cell walls, the lower the gm and photosynthesis. Potential interplays of gm, Tcw, dehydration tolerance, and hydraulic properties of leaves are also discussed. Dynamic variations of Tcw in response to the environment and their implications in the regulation of photosynthesis are discussed, and recent evidence suggesting an influence of cell wall composition on gm is presented. We then propose a hypothetical mechanism for the influence of cell walls on photosynthesis, combining the effects of thickness and composition, particularly pectins. Finally, we discuss the prospects for using biotechnology for enhancing photosynthesis by altering cell wall-related genes., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Variation in resistance of xylem to embolism among flowers, leaves, and stems strongly influences the survival and reproduction of plants. However, little is known about the vulnerability to xylem embolism under drought stress and their relationships to the anatomical traits of pits among reproductive and vegetative organs. In this study, we investigated the variation in xylem vulnerability to embolism in peduncles, petioles, and stems in a woody plant, Magnolia grandiflora . We analyzed the relationships between water potentials that induced 50% embolism (P 50 ) in peduncles, petioles, and stems and the conduit pit traits hypothesized to influence cavitation resistance. We found that peduncles were more vulnerable to cavitation than petioles and stems, supporting the hypothesis of hydraulic vulnerability segmentation that leaves and stems are prioritized over flowers during drought stress. Moreover, P 50 was significantly correlated with variation in the dimensions of inter-vessel pit apertures among peduncles, petioles and stems. These findings highlight that measuring xylem vulnerability to embolism in reproductive organs is essential for understanding the effect of drought on plant reproductive success and mortality under drought stress., Competing Interests: The authors declare no conflict of interest., (© 2020 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.)

Hydraulic failure of the plant vascular system is a principal cause of forest die-off under drought. Accurate quantification of this process is essential to our understanding of the physiological mechanisms underpinning plant mortality. Imaging techniques increasingly are applied to estimate xylem cavitation resistance. These techniques allow for in situ measurement of embolism formation in real time, although the benefits and trade-offs associated with different techniques have not been evaluated in detail. Here we compare two imaging methods, microcomputed tomography (microCT) and optical vulnerability (OV), to standard hydraulic methods for measurement of cavitation resistance in seven woody species representing a diversity of major phylogenetic and xylem anatomical groups. Across the seven species, there was strong agreement between cavitation resistance values (P 50 ) estimated from visualization techniques (microCT and OV) and between visual techniques and hydraulic techniques. The results indicate that visual techniques provide accurate estimates of cavitation resistance and the degree to which xylem hydraulic function is impacted by embolism. Results are discussed in the context of trade-offs associated with each technique and possible causes of discrepancy between estimates of cavitation resistance provided by visual and hydraulic techniques., (© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.)

Root vulnerability to cavitation is challenging to measure and under-represented in current datasets. This gap limits the precision of models used to predict plant responses to drought because roots comprise the critical interface between plant and soil. In this study, we measured vulnerability to drought-induced cavitation in woody roots and stems of five tree species (Acacia aneura, Cedrus deodara, Eucalyptus crebra, Eucalytus saligna, and Quercus palustris) with a wide range of xylem anatomies. X-ray microtomography was used to visualize the accumulation of xylem embolism in stems and roots of intact plants that were naturally dehydrated to varying levels of water stress. Vulnerability to cavitation, defined as the water potential causing a 50% loss of hydraulic function (P50), varied broadly among the species (-4.51 MPa to -11.93 MPa in stems and -3.13 MPa to -9.64 MPa in roots). The P50 of roots and stems was significantly related across species, with species that had more vulnerable stems also having more vulnerable roots. While there was strong convergence in root and stem vulnerability to cavitation, the P50 of roots was significantly higher than the P50 of stems in three species. However, the difference in root and stem vulnerability for these species was small; between 1% and 31% of stem P50. Thus, while some differences existed between organs, roots were not dramatically more vulnerable to embolism than stems, and the differences observed were less than those reported in previous studies. Further study is required to evaluate the vulnerability across root orders and to extend these conclusions to a greater number of species and xylem functional types., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Xylem cavitation resulting in air embolism is a major cause of plant death during drought, yet the spread of embolism throughout the plant water transport system is poorly understood. Our study used optical visualization and x-ray microcomputed tomography imaging to capture the spread of emboli in stems of three drought-resistant angiosperm trees: drooping she-oak ( Allocasuarina verticillata ), black wattle ( Acacia mearnsii ), and blue gum ( Eucalyptus globulus ). These species have similar degrees of xylem network connectivity (vessel grouping) with largely solitary vessels. The high temporal resolution of the optical vulnerability technique revealed that in current year branches, >80% of the cavitation events were discrete, temporally separated events in single vessels. This suggests that in xylem networks with low connectivity, embolism spread between conduits leading to multiple conduit cavitation events is uncommon. A. mearnsii showed both the highest number of multivessel cavitation events and the highest degree of vessel connectivity, suggesting a link between vessel arrangement and embolism spread. Knowledge of embolism spread will help us to uncover the links between xylem anatomy, arrangement, and the path of water flow in the xylem in diverse species to ultimately understand the drivers of cavitation and plant vulnerability to drought., (© 2020 American Society of Plant Biologists. All Rights Reserved.)

Tight coordination in the photosynthetic, gas exchange and water supply capacities of leaves is a globally conserved trend across land plants. Strong selective constraints on leaf carbon gain create the opportunity to use quantitative optimization theory to understand the connected evolution of leaf photosynthesis and water relations. We developed an analytical optimization model that maximizes the long-term rate of leaf carbon gain, given the carbon costs in building and maintaining stomata, leaf hydraulics and osmotic pressure. Our model demonstrates that selection for optimal gain should drive coordination between key photosynthetic, gas exchange and water relations traits. It also provides predictions of adaptation to drought and the relative costs of key leaf functional traits. Our results show that optimization in terms of carbon gain, given the carbon costs of physiological traits, successfully unites leaf photosynthesis and water relations and provides a quantitative framework to consider leaf functional evolution and adaptation.

The photosynthetic efficiency of plants in different environments is controlled by stomata, hydraulics, biochemistry, and mesophyll conductance (gm). Recently, gm was demonstrated to be the key limitation of photosynthesis in gymnosperms. Values of gm across gymnosperms varied over 20-fold, but this variation was poorly explained by robust structure-bound integrated traits such as leaf dry mass per area. Understanding how the component structural traits control gm is central for identifying the determinants of variability in gm across plant functional and phylogenetic groups. Here, we investigated the structural traits responsible for gm in 65 diverse gymnosperms. Although the integrated morphological traits, shape, and anatomical characteristics varied widely across species, the distinguishing features of all gymnosperms were thick mesophyll cell walls and low chloroplast area exposed to intercellular airspace (Sc/S) compared with angiosperms. Sc/S and cell wall thickness were the fundamental traits driving variations in gm across gymnosperm species. Chloroplast thickness was the strongest limitation of gm among liquid-phase components. The variation in leaf dry mass per area was not correlated with the key ultrastructural traits determining gm. Thus, given the absence of correlating integrated easy-to-measure traits, detailed knowledge of underlying component traits controlling gm across plant taxa is necessary to understand the photosynthetic limitations across ecosystems., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Flowers underpin plant evolution, genetic legacy and global food supply. They are exposed to similar evaporative conditions as leaves, yet floral physiology is a product of different selective forces. We used Tanacetum cinerariifolium, a perennial daisy, to examine the response of flowers to whole-plant water stress, determining if flowers constitute a liability during drought, and how this species has adapted to minimize risk associated with reproduction. We determined the relative transpiration cost of flowers and leaves and confirmed that flowers in this species are xylem-hydrated. The relative water stress tolerance of leaves and flowers then was compared using xylem vulnerability measurements linked with observed tissue damage during an acute drought treatment. Flowers were a major source of water loss during drought but the xylem supplying them was much more vulnerable to cavitation than leaves. This xylem vulnerability segmentation was confirmed by observations that most flowers died whereas leaves were minimally affected during drought. Early cavitation and hydraulic isolation of flowers during drought benefits the plant by slowing the dehydration of perennial vegetative organs and delaying systemic xylem damage. Our results highlight the need to understand flower xylem vulnerability as a means of predicting plant reproductive failure under future drought., (© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.)

Dynamic variation of the stomatal pore in response to changes in leaf-air vapour pressure difference (VPD) constitutes a critical regulation of daytime gas exchange. The stomatal response to VPD has been associated with both foliage abscisic acid (ABA) and leaf water potential (Ψ  l ); however, causation remains a matter of debate. Here, we seek to separate hydraulic and hormonal control of stomatal aperture by manipulating the osmotic potential of sunflower leaves. In addition, we test whether stomatal responses to VPD in an ABA-deficient mutant ( w-1 ) of sunflower are similar to the wild type. Stomatal apertures during VPD transitions were closely linked with foliage ABA levels in sunflower plants with contrasting osmotic potentials. In addition, we observed that the inability to synthesize ABA at high VPD in w-1 plants was associated with no dynamic or steady-state stomatal response to VPD. These results for sunflower are consistent with a hormonal, ABA-mediated stomatal responses to VPD rather than a hydraulic-driven stomatal response to VPD., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company.)

The hydraulic implications of stomatal positioning across leaf surfaces and the impact on internal water flow through amphistomatic leaves are not currently well understood. Amphistomaty potentially provides hydraulic efficiencies if the majority of hydraulic resistance in the leaf exists outside the xylem in the mesophyll. Such a scenario would mean that the same xylem network could equally supply a hypostomatic or amphistomatic leaf. Here we examine leaves of Helianthus annuus to determine whether amphistomaty in this species is associated with higher hydraulic efficiency compared with hypostomatic leaves. We identified asymmetry in the positioning of minor veins which were significantly closer to the abaxial than the adaxial leaf surface, combined with lower Kleaf when transpiration was driven through the adaxial rather than the abaxial surface. We also identified a degree of coordination in stomatal behaviour driven by leaf hydraulics, where the hydraulic conditions experienced by an individual leaf surface affected the stomatal behaviour on the opposite surface. We found no advantage to amphistomaty based on efficiencies in construction costs of the venous system, represented by vein density:stomatal density, only limited hydraulic independence between leaf surfaces. These results suggest that amphistomaty does not substantially increase whole-leaf hydraulic efficiency., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Drought-related tree mortality is now a widespread phenomenon predicted to increase in magnitude with climate change. However, the patterns of which species and trees are most vulnerable to drought, and the underlying mechanisms have remained elusive, in part due to the lack of relevant data and difficulty of predicting the location of catastrophic drought years in advance. We used long-term demographic records and extensive databases of functional traits and distribution patterns to understand the responses of 20-53 species to an extreme drought in a seasonally dry tropical forest in Costa Rica, which occurred during the 2015 El Niño Southern Oscillation event. Overall, species-specific mortality rates during the drought ranged from 0% to 34%, and varied little as a function of tree size. By contrast, hydraulic safety margins correlated well with probability of mortality among species, while morphological or leaf economics spectrum traits did not. This firmly suggests hydraulic traits as targets for future research., (© 2020 John Wiley & Sons Ltd.)

Trees are the living foundations on which most terrestrial biodiversity is built. Central to the success of trees are their woody bodies, which connect their elevated photosynthetic canopies with the essential belowground activities of water and nutrient acquisition. The slow construction of these carbon-dense, woody skeletons leads to a slow generation time, leaving trees and forests highly susceptible to rapid changes in climate. Other long-lived, sessile organisms such as corals appear to be poorly equipped to survive rapid changes, which raises questions about the vulnerability of contemporary forests to future climate change. The emerging view that, similar to corals, tree species have rather inflexible damage thresholds, particularly in terms of water stress, is especially concerning. This Review examines recent progress in our understanding of how the future looks for forests growing in a hotter and drier atmosphere., (Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

The evolution of terrestrial plants capable of growing upwards into the dry atmosphere profoundly transformed the Earth. A transition from small, 'non-vascular' bryophytes to arborescent vascular plants during the Devonian period is partially attributed to the evolutionary innovation of an internal vascular system capable of functioning under the substantial water tension associated with vascular water transport. Here, we show that vascular function in one of the most widespread living bryophytes (Polytrichum commune) exhibits strong functional parallels with the vascular systems of higher plants. These parallels include vascular conduits in Polytrichum that resist buckling while transporting water under tension, and leaves capable of regulating transpiration, permitting photosynthetic gas exchange without cavitation inside the vascular system. The advanced vascular function discovered in this tallest bryophyte family contrasts with the highly inefficient water use found in their leaves, emphasizing the importance of stomatal evolution enabling photosynthesis far above the soil surface.

The best predictor of leaf level photosynthetic rate is the porosity of the leaf surface, as determined by the number and aperture of stomata on the leaf. This remarkable correlation between stomatal porosity (or diffusive conductance to water vapour g s ) and CO 2 assimilation rate (A) applies to all major lineages of vascular plants (Figure 1) and is sufficiently predictable that it provides the basis for the model most widely used to predict water and CO 2 fluxes from leaves and canopies. Yet the Ball-Berry formulation is only a phenomenological approximation that captures the emergent character of stomatal behaviour. Progressing to a more mechanistic prediction of plant gas exchange is challenging because of the diversity of biological components regulating stomatal action. These processes are the product of more than 400 million years of co-evolution between stomatal, vascular and photosynthetic tissues. Both molecular and structural components link the abiotic world of the whole plant with the turgor pressure of the epidermis and guard cells, which ultimately determine stomatal pore size and porosity to water and CO 2 exchange (New Phytol., 168, 2005, 275). In this review we seek to simplify stomatal behaviour by using an evolutionary perspective to understand the principal selective pressures involved in stomatal evolution, thus identifying the primary regulators of stomatal aperture. We start by considering the adaptive process that has locked together the regulation of water and carbon fluxes in vascular plants, finally examining specific evidence for evolution in the proteins responsible for regulating guard cell turgor., (© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.)

The size of plant stomata (adjustable pores that determine the uptake of CO 2 and loss of water from leaves) is considered to be evolutionarily important. This study uses fossils from the major Southern Hemisphere family Proteaceae to test whether stomatal cell size responded to Cenozoic climate change. We measured the length and abundance of guard cells (the cells forming stomata), the area of epidermal pavement cells, stomatal index and maximum stomatal conductance from a comprehensive sample of fossil cuticles of Proteaceae, and extracted published estimates of past temperature and atmospheric CO 2 . We developed a novel test based on stochastic modelling of trait evolution to test correlations among traits. Guard cell length increased, and stomatal density decreased significantly with decreasing palaeotemperature. However, contrary to expectations, stomata tended to be smaller and more densely packed at higher atmospheric CO 2 . Thus, associations between stomatal traits and palaeoclimate over the last 70 million years in Proteaceae suggest that stomatal size is significantly affected by environmental factors other than atmospheric CO 2 . Guard cell length, pavement cell area, stomatal density and stomatal index covaried in ways consistent with coordinated development of leaf tissues.