1077 I. 1078 II. 1079 III. 1080 IV. 1081 V. 1084 VI. 1087 VII. 1088 1089 References 1089 SUMMARY: The rate of CO₂ assimilation by plants is directly influenced by the concentration of CO₂ in the ...atmosphere, cₐ. As an environmental variable, cₐ also has a unique global and historic significance. Although relatively stable and uniform in the short term, global cₐ has varied substantially on the timescale of thousands to millions of years, and currently is increasing at seemingly an unprecedented rate. This may exert profound impacts on both climate and plant function. Here we utilise extensive datasets and models to develop an integrated, multi‐scale assessment of the impact of changing cₐ on plant carbon dioxide uptake and water use. We find that, overall, the sensitivity of plants to rising or falling cₐ is qualitatively similar across all scales considered. It is characterised by an adaptive feedback response that tends to maintain 1 − cᵢ/cₐ, the relative gradient for CO₂ diffusion into the leaf, relatively constant. This is achieved through predictable adjustments to stomatal anatomy and chloroplast biochemistry. Importantly, the long‐term response to changing cₐ can be described by simple equations rooted in the formulation of more commonly studied short‐term responses.
Summary
Plant responses to elevated atmospheric carbon dioxide (eCO2) have been hypothesized as a key mechanism that may ameliorate the impact of future drought. Yet, despite decades of experiments, ...the question of whether eCO2 reduces plant water use, yielding ‘water savings’ that can be used to maintain plant function during periods of water stress, remains unresolved. In this Viewpoint, we identify the experimental challenges and limitations to our understanding of plant responses to drought under eCO2. In particular, we argue that future studies need to move beyond exploring whether eCO2 played ‘a role’ or ‘no role’ in responses to drought, but instead more carefully consider the timescales and conditions that would induce an influence. We also argue that considering emergent differences in soil water content may be an insufficient means of assessing the impact of eCO2. We identify eCO2 impact during severe drought (e.g. to the point of mortality), interactions with future changes in vapour pressure deficit and uncertainty about changes in leaf area as key gaps in our current understanding. New insights into CO2 × drought interactions are essential to better constrain model theory that governs future climate model projections of land–atmosphere interactions during periods of water stress.
The role of time in ecology has a long history of investigation, but ecologists have largely restricted their attention to the influence of concurrent abiotic conditions on rates and magnitudes of ...important ecological processes. Recently, however, ecologists have improved their understanding of ecological processes by explicitly considering the effects of antecedent conditions. To broadly help in studying the role of time, we evaluate the length, temporal pattern, and strength of memory with respect to the influence of antecedent conditions on current ecological dynamics. We developed the stochastic antecedent modelling (SAM) framework as a flexible analytic approach for evaluating exogenous and endogenous process components of memory in a system of interest. We designed SAM to be useful in revealing novel insights promoting further study, illustrated in four examples with different degrees of complexity and varying time scales: stomatal conductance, soil respiration, ecosystem productivity, and tree growth. Models with antecedent effects explained an additional 18–28% of response variation compared to models without antecedent effects. Moreover, SAM also enabled identification of potential mechanisms that underlie components of memory, thus revealing temporal properties that are not apparent from traditional treatments of ecological time‐series data and facilitating new hypothesis generation and additional research.
Plant survival during drought requires adequate hydration in living tissues and carbohydrate reserves for maintenance and recovery. We hypothesized that tree growth and hydraulic strategy determines ...the intensity and duration of the ‘physiological drought’, thereby affecting the relative contributions of loss of hydraulic function and carbohydrate depletion during mortality.
We compared patterns in growth rate, water relations, gas exchange and carbohydrate dynamics in three tree species subjected to prolonged drought.
Two Eucalyptus species (E. globulus, E. smithii) exhibited high growth rates and water-use resulting in rapid declines in water status and hydraulic conductance. In contrast, conservative growth and water relations in Pinus radiata resulted in longer periods of negative carbon balance and significant depletion of stored carbohydrates in all organs. The ongoing demand for carbohydrates from sustained respiration highlighted the role that duration of drought plays in facilitating carbohydrate consumption.
Two drought strategies were revealed, differentiated by plant regulation of water status: plants maximized gas exchange, but were exposed to low water potentials and rapid hydraulic dysfunction; and tight regulation of gas exchange at the cost of carbohydrate depletion. These findings provide evidence for a relationship between hydraulic regulation of water status and carbohydrate depletion during terminal drought.
Heatwaves are likely to increase in frequency and intensity with climate change, which may impair tree function and forest C uptake. However, we have little information regarding the impact of ...extreme heatwaves on the physiological performance of large trees in the field. Here, we grew Eucalyptus parramattensis trees for 1 year with experimental warming (+3°C) in a field setting, until they were greater than 6 m tall. We withheld irrigation for 1 month to dry the surface soils and then implemented an extreme heatwave treatment of 4 consecutive days with air temperatures exceeding 43°C, while monitoring whole‐canopy exchange of CO2 and H2O, leaf temperatures, leaf thermal tolerance, and leaf and branch hydraulic status. The heatwave reduced midday canopy photosynthesis to near zero but transpiration persisted, maintaining canopy cooling. A standard photosynthetic model was unable to capture the observed decoupling between photosynthesis and transpiration at high temperatures, suggesting that climate models may underestimate a moderating feedback of vegetation on heatwave intensity. The heatwave also triggered a rapid increase in leaf thermal tolerance, such that leaf temperatures observed during the heatwave were maintained within the thermal limits of leaf function. All responses were equivalent for trees with a prior history of ambient and warmed (+3°C) temperatures, indicating that climate warming conferred no added tolerance of heatwaves expected in the future. This coordinated physiological response utilizing latent cooling and adjustment of thermal thresholds has implications for tree tolerance of future climate extremes as well as model predictions of future heatwave intensity at landscape and global scales.
Heatwaves are likely to increase in frequency and intensity, but we know relatively little about how trees will respond. Here, we documented that large trees growing in the field responded to an extreme heatwave with a coordinated physiological response involving continued leaf cooling from transpiration and a rapid increase in leaf thermal tolerance. The Eucalyptus trees that we studied were remarkably capable of tolerating an extreme heatwave via mechanisms that have implications for future heatwave intensity and forest resilience in a warmer world.
Abstract
Drought-induced tree mortality alters forest structure and function, yet our ability to predict when and how different species die during drought remains limited. Here, we explore how ...stomatal control and drought tolerance traits influence the duration of drought stress leading to critical levels of hydraulic failure. We examined the growth and physiological responses of four woody plant species (three angiosperms and one conifer) representing a range of water-use and drought tolerance traits over the course of two controlled drought–recovery cycles followed by an extended dry-down. At the end of the final dry-down phase, we measured changes in biomass ratios and leaf carbohydrates. During the first and second drought phases, plants of all species closed their stomata in response to decreasing water potential, but only the conifer species avoided water potentials associated with xylem embolism as a result of early stomatal closure relative to thresholds of hydraulic dysfunction. The time it took plants to reach critical levels of water stress during the final dry-down was similar among the angiosperms (ranging from 39 to 57 days to stemP88) and longer in the conifer (156 days to stemP50). Plant dry-down time was influenced by a number of factors including species stomatal-hydraulic safety margin (gsP90 – stemP50), as well as leaf succulence and minimum stomatal conductance. Leaf carbohydrate reserves (starch) were not depleted at the end of the final dry-down in any species, irrespective of the duration of drought. These findings highlight the need to consider multiple structural and functional traits when predicting the timing of hydraulic failure in plants.
Phosphorus (P) is often one of the most limiting nutrients in highly weathered soils of humid tropical forests and may regulate the responses of carbon (C) feedback to climate warming. However, the ...response of P to warming at the ecosystem level in tropical forests is not well understood because previous studies have not comprehensively assessed changes in multiple P processes associated with warming. Here, we detected changes in the ecosystem P cycle in response to a 7‐year continuous warming experiment by translocating model plant‐soil ecosystems across a 600‐m elevation gradient, equivalent to a temperature change of 2.1°C. We found that warming increased plant P content (55.4%) and decreased foliar N:P. Increased plant P content was supplied by multiple processes, including enhanced plant P resorption (9.7%), soil P mineralization (15.5% decrease in moderately available organic P), and dissolution (6.8% decrease in iron‐bound inorganic P), without changing litter P mineralization and leachate P. These findings suggest that warming sustained plant P demand by increasing the biological and geochemical controls of the plant‐soil P‐cycle, which has important implications for C fixation in P‐deficient and highly productive tropical forests in future warmer climates.
The response of phosphorus cycle to warming in tropical forests is not well understood. Our study found that warming increased plant P content and decreased foliar N:P. Increased plant P content was supplied by multiple processes, including enhanced plant P resorption, soil P mineralization, and dissolution, without changing litter P mineralization and leachate P. These findings suggest that warming sustained plant P demand by increasing the biological and geochemical controls of the plant‐soil P‐cycle, which has important implications for C fixation in P‐deficient and highly productive tropical forests in future warmer climates.
Sodium (Na+) is a beneficial element for most plants that may replace potassium (K+) in osmoregulatory process to a certain extent, increasing plant water-use efficiency. Thus, understanding ...coordinated mechanisms underlying the combined use of K+ and Na+ in tree drought tolerance is a key challenge for the agricultural industry in dealing with forest productivity and water limitations. A pot experiment with three ratios of K/Na (K-supplied, partial K replacement by Na and K-deficient plants) and two water regimes, well-watered (W+) and water-stressed (W-), was conducted on saplings of two Eucalyptus species with contrasting drought sensitivities. We evaluated the point of stomatal closure (Pgs90), xylem embolism thresholds (P12, P50, P88), hydraulic safety margin (HSM), leaf gas exchange (A, E, gs and dark respiration), leaf water potential (ΨPD and ΨMD), long-term water use efficiency (WUEL) and total dry mass (TDM). Partial K replacement by Na increased the leaf gas exchange, WUEL and TDM, while Pgs90, P12, P50, P88 and ΨMD decreased (more negative), compared to plants exclusively supplied with K and K-deficient plants of both species. Fertilized plants had narrower HSMs than K-deficient plants, indicating that these Eucalyptus species adopt the functional adaptive strategy of operating close to their hydraulic limits to maximize carbon uptake while increasing the risk of hydraulic failure under drought-stress.
Mesophyll conductance increased with increasing CO2 from glacial to ambient CO2 levels, then declined at super-elevated CO2 for both well-watered and water-limited treatments. These responses may ...have a structural basis.
Abstract
Mesophyll conductance (gm) is an important factor limiting photosynthesis. However, gm response to long-term growth in variable CO2 is not well understood, particularly in crop plants. Here, we grew two cultivars of wheat (Halberd and Cranbrook), known to differ in gm under current environmental conditions, in four CO2 treatments: glacial (206 μmol mol−1), pre-industrial (344 μmol mol−1), current ambient (489 μmol mol−1), and super-elevated (1085 μmol mol−1), and two water treatments (well-watered and moderate water limitation), to develop an evolutionary and future climate perspective on gm control of photosynthesis and water-use efficiency (WUE). In the two wheat genotypes, gm increased with rising CO2 from glacial to ambient CO2, but declined at super-elevated CO2. The responses of gm to different growth CO2 also depend on water stress; however, the specific mechanism of gm response to CO2 remains unclear. Although gm and gm/gsc (mesophyll conductance/stomatal conductance) were strongly associated with the variability of photosynthetic rates (A) and WUE, we found that plants with higher gm may increase A without increasing gsc, which increased WUE. These results may be useful to inform plant breeding programmes and cultivar selection for Australian wheat under future environmental conditions.
statement: Mesophyll conductance (
) was negatively correlated with wheat leaf age but was positively correlated with the surface area of chloroplasts exposed to intercellular airspaces (
). The rate ...of decline in photosynthetic rate and
as leaves aged was slower for water-stressed than well-watered plants. Upon rewatering, the degree of recovery from water-stress depended on the age of the leaves, with the strongest recovery for mature leaves, rather than young or old leaves. Diffusion of CO
from the intercellular airspaces to the site of Rubisco within C
plant chloroplasts (
) governs photosynthetic CO
assimilation (
). However, variation in
in response to environmental stress during leaf development remains poorly understood. Age-dependent changes in leaf ultrastructure and potential impacts on
,
, and stomatal conductance to CO
(
) were investigated for wheat (
L.) in well-watered and water-stressed plants, and after recovery by re-watering of droughted plants. Significant reductions in
and
were found as leaves aged. The oldest plants (15 days and 22 days) in water-stressed conditions showed higher A and gm compared to irrigated plants. The rate of decline in
and
as leaves aged was slower for water-stressed compared to well-watered plants. When droughted plants were rewatered, the degree of recovery depended on the age of the leaves, but only for
. The surface area of chloroplasts exposed to intercellular airspaces (
) and the size of individual chloroplasts declined as leaves aged, resulting in a positive correlation between
and
. Leaf age significantly affected cell wall thickness (
), which was higher in old leaves compared to mature/young leaves. Greater knowledge of leaf anatomical traits associated with
partially explained changes in physiology with leaf age and plant water status, which in turn should create more possibilities for improving photosynthesis using breeding/biotechnological strategies.
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