Variation in xylem vessel diameter is one of the most important parameters when evaluating plant water relations. This review provides a synthesis of the ecophysiological implications of variation in ...lumen diameter together with a summary of our current understanding of vessel development and its endogenous regulation. We analyzed inter‐specific variation of the mean hydraulic vessel diameter (Dv) across biomes, intra‐specific variation of Dv under natural and controlled conditions, and intra‐plant variation. We found that the Dv measured in young branches tends to stay below 30 µm in regions experiencing winter frost, whereas it is highly variable in the tropical rainforest. Within a plant, the widest vessels are often found in the trunk and in large roots; smaller diameters have been reported for leaves and small lateral roots. Dv varies in response to environmental factors and is not only a function of plant size. Despite the wealth of data on vessel diameter variation, the regulation of diameter is poorly understood. Polar auxin transport through the vascular cambium is a key regulator linking foliar and xylem development. Limited evidence suggests that auxin transport is also a determinant of vessel diameter. The role of auxin in cell expansion and in establishing longitudinal continuity during secondary growth deserve further study.
Variation in xylem vessel diameter impacts transport efficiency, vulnerability to freezing‐induced embolism, and other aspects of plant biology. This review provides a synthesis of the ecophysiological implications of variation in lumen diameter together with a summary of our current understanding of vessel development and its endogenous regulation. Emphasis is placed on the presumed role of auxin at multiple developmental stages.
Gas exchange is constrained by the whole-plant hydraulic conductance (Kplant). Leaves account for an important fraction of Kplant and may therefore represent a major determinant of plant ...productivity. Leaf hydraulic conductance (Kleaf) decreases with increasing water stress, which is due to xylem embolism in leaf veins and/or the properties of the extra-xylary pathway. Water flow through living tissues is facilitated and regulated by water channel proteins called aquaporins (AQPs). Here we assessed changes in the hydraulic conductance of Populus trichocarpa leaves during a dehydration-rewatering episode. While leaves were highly sensitive to drought, Kleaf recovered only 2 hours after plants were rewatered. Recovery of Kleaf was absent when excised leaves were bench-dried and subsequently xylem-perfused with a solution containing AQP inhibitors. We examined the expression patterns of 12 highly expressed AQP genes during a dehydration-rehydration episode to identify isoforms that may be involved in leaf hydraulic adjustments. Among the AQPs tested, several genes encoding tonoplast intrinsic proteins (TIPs) showed large increases in expression in rehydrated leaves, suggesting that TIPs contribute to reversing drought-induced reductions in Kleaf. TIPs were localized in xylem parenchyma, consistent with a role in facilitating water exchange between xylem vessels and adjacent living cells. Dye uptake experiments suggested that reversible embolism formation in minor leaf veins contributed to the observed changes in Kleaf.
Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration ...and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (,1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.
Conifer needles have been reported to absorb water under certain conditions. Radial water movement across needle tissues is likely influenced by aquaporin (AQP) water channels. Foliar water uptake ...and AQP localization in Picea glauca needles were studied using physiological and microscopic methods. AQP expression was measured using quantitative real‐time PCR. Members of the AQP gene family in spruce were identified using homology search tools. Needles of drought‐stressed plants absorbed water when exposed to high relative humidity (RH). AQPs were present in the endodermis‐like bundle sheath, in phloem cells and in the transfusion parenchyma of needles. Up‐regulation of AQPs in high RH coincided with embolism repair in stem xylem. The present study also provides the most comprehensive functional and phylogenetic analysis of spruce AQPs to date. Thirty putative complete AQP sequences were found. Our findings are consistent with the hypothesis that AQPs facilitate radial water movement from the needle epidermis towards the vascular tissue. Foliar water uptake may occur in late winter when needles are covered by melting snow and may provide a water source for embolism repair before the beginning of the growing season.
Isohydric plants tend to maintain a water potential homeostasis primarily by controlling water loss via stomatal conductance. However, there is accumulating evidence that plants can also modulate ...water uptake in a dynamic manner. The dynamics of water uptake are influenced by aquaporin-mediated changes in root hydraulics. Most studies in this area have been conducted on herbaceous plants, and less is known about responses of woody plants. Here a study was conducted to determine how roots of hybrid poplar plants (Populus trichocarpa×deltoides) respond to a step change in transpirational demand. The main objective was to measure the expression of selected aquaporin genes and to assess how transcriptional responses correspond to changes in root water flow (Q R) and other parameters of water relations. A subset of plants was grown in shade and was subsequently exposed to a 5-fold increase in light level. Another group of plants was grown at ~95% relative humidity (RH) and was then subjected to lower RH while the light level remained unchanged. Both plant groups experienced a transient drop in stem water potentials. At 28h after the increase in transpirational demand, water potentials recovered. This recovery was associated with changes in the expression of PIP1 and PIP2 subfamily genes and an increase in Q R. Stomata of plants growing at high RH were larger and showed incomplete closure after application of abscisic acid. Since stomatal conductance remained high and unchanged in these plants, it is suggested that the recovery in water potential in these plants was largely driven by the increase in Q R.
Variation in xylem structure and function has been extensively studied across different species with a wide taxonomic, geographical, and ecological coverage. In contrast, our understanding of how ...xylem of a single species can adjust to different growing condition remains limited. Here phenotypic and developmental plasticity in xylem traits of hybrid poplar (Populus trichocarpa×deltoides) was studied. Clonally propagated saplings were grown under experimental drought, nitrogen fertilization, and shade for >30 d. Xylem hydraulic and anatomical traits were subsequently examined in stem segments taken from two different vertical positions along the plant’s main axis. The experimental treatments affected growth and development and induced changes in xylem phenotype. Across all treatments, the amount of leaf area supported by stem segments (AL) scaled linearly with stem native hydraulic conductivity (K native), suggesting that the area of assimilating leaves is constrained by the xylem transport capacity. In turn, K native was mainly driven by the size of xylem cross-sectional area (AX). Moreover, the structural and functional properties of xylem varied significantly. Vulnerability to cavitation, measured as the xylem pressure inducing 50% loss of conductivity (P50), ranged from –1.71MPa to –0.15MPa in saplings subjected to drought and nitrogen fertilization, respectively. Across all treatments and stem segment positions, P50 was tightly correlated with wood density. In contrast, no relationship between P50 and xylem-specific conductivity (K S) was observed. The results of this study enhance our knowledge of plant hydraulic acclimation and provide insights into common trade-offs that exist in xylem structure and function.
Xylem embolism is a limiting factor for woody species worldwide. Conifers at the alpine timberline are exposed to drought and freeze-thaw stress during winter, which induce potentially lethal ...embolism. Previous studies indicated that timberline trees survive by xylem refilling. In this study on Picea abies, refilling was monitored during winter and spring seasons and analyzed in the laboratory and in situ experiments, based on hydraulic, anatomical, and histochemical methods. Refilling started in late winter, when the soil. was frozen and soil water not available for the trees. Xylem embolism caused up to 86.2% ± 3.1% loss of conductivity and was correlated with the ratio of closed pits. Refilling of xylem as well as recovery in shoot conductance started in February and corresponded with starch accumulation in secondary phloem and in the mesophyll of needles, where we also observed increasing aquaporin densities in the phloem and endodermis. This indicates that active, cellular processes play a role for refilling even under winter conditions. As demonstrated by our experiments, water for refilling was thereby taken up via the branches, likely by foliar water uptake. Our results suggest that refilling is based on water shifts to embolized tracheids via intact xylem, phloem, and parenchyma, whereby aquaporins reduce resistances along the symplastic pathway and aspirated pits facilitate isolation of refilling tracheids. Refilling must be taken into account as a key process in plant hydraulics and in estimating future effects of climate change on forests and alpine tree ecosystems.
The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem ...conduits, thus impeding sap transport to the leaves. A well‐known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety–efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r² < 0.086), no species had high efficiency and high safety, supporting the idea for a safety–efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r² < 0.02 in most cases) with higher wood density, lower leaf‐ to sapwood‐area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.
Forest mortality constitutes a major uncertainty in projections of climate impacts on terrestrial ecosystems and carbon‐cycle feedbacks. Recent drought‐induced, widespread forest die‐offs highlight ...that climate change could accelerate forest mortality with its diverse and potentially severe consequences for the global carbon cycle, ecosystem services, and biodiversity. How trees die during drought over multiple years remains largely unknown and precludes mechanistic modeling and prediction of forest die‐off with climate change. Here, we examine the physiological basis of a recent multiyear widespread die‐off of trembling aspen (Populus tremuloides) across much of western North America. Using observations from both native trees while they are dying and a rainfall exclusion experiment on mature trees, we measure hydraulic performance over multiple seasons and years and assess pathways of accumulated hydraulic damage. We test whether accumulated hydraulic damage can predict the probability of tree survival over 2 years. We find that hydraulic damage persisted and increased in dying trees over multiple years and exhibited few signs of repair. This accumulated hydraulic deterioration is largely mediated by increased vulnerability to cavitation, a process known as cavitation fatigue. Furthermore, this hydraulic damage predicts the probability of interyear stem mortality. Contrary to the expectation that surviving trees have weathered severe drought, the hydraulic deterioration demonstrated here reveals that surviving regions of these forests are actually more vulnerable to future droughts due to accumulated xylem damage. As the most widespread tree species in North America, increasing vulnerability to drought in these forests has important ramifications for ecosystem stability, biodiversity, and ecosystem carbon balance. Our results provide a foundation for incorporating accumulated drought impacts into climate–vegetation models. Finally, our findings highlight the critical role of drought stress accumulation and repair of stress‐induced damage for avoiding plant mortality, presenting a dynamic and contingent framework for drought impacts on forest ecosystems.
The wide size range of conifer tracheids and angiosperm vessels has important consequences for function. In both conduit types, bigger is better for conducting efficiency. The gain in efficiency with ...size is maximized by the control of conduit shape, which balances end-wall and lumen resistances. Although vessels are an order of magnitude longer than tracheids of the same diameter, they are not necessarily more efficient because they lack the low end-wall resistance of tracheids with torus-margo pits. Instead, vessels gain conducting efficiency over tracheids by achieving wider maximum diameters. End-walls contributed 56-64% to total xylem resistance in both conduit types, indicating that length limits conducting efficiency. Tracheid dimensions may be more limited by unicellularity and the need to supply strength to homoxylous wood than by the need to protect against cavitation. In contrast, the greater size of the multicellular vessel is facilitated by fibers that strengthen heteroxylous wood. Vessel dimensions may be most limited by the need to restrict intervessel pitting and cavitation by air-seeding. Stressful habitats that promote narrow vessels should favor coexistence of conifers and angiosperms. The evolution of vessels in angiosperm wood may have required early angiosperms to survive a phase of mechanic and hydraulic instability.
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