Plasticity in branch water relations and stem hydraulic vulnerability enhances hydraulic safety in mangroves growing along a salinity gradient.

Coping with water stress depends on maintaining cellular function and hydraulic conductance. Yet measurements of vulnerability to drought and salinity do not often focus on capacitance in branch organs that buffer hydraulic function during water stress. The relationships between branch water relations, stem hydraulic vulnerability and stem anatomy were investigated in two co-occurring mangroves Aegiceras corniculatum and Rhizophora stylosa growing at low and high salinity. The dynamics of branch water release acted to conserve water content in the stem at the expense of the foliage during extended drying. Hydraulic redistribution from the foliage to the stem increased stem relative water content by up to 21%. The water potentials at which 12% and 50% loss of stem hydraulic conductivity occurred decreased by ~1.7 MPa in both species between low and high salinity sites. These coordinated tissue adjustments increased hydraulic safety despite declining turgor safety margins at higher salinity sites. Our results highlight the complex interplay of plasticity in organ-level water relations with hydraulic vulnerability in the maintenance of stem hydraulic function in mangroves distributed along salinity gradients. These results emphasise the importance of combining water relations and hydraulic vulnerability parameters to understand vulnerability to water stress across the whole plant.

Heat tolerance of a tropical-subtropical rainforest tree species Polyscias elegans: time-dependent dynamic responses of physiological thermostability and biochemistry.

Heat stress interrupts physiological thermostability and triggers biochemical responses that are essential for plant survival. However, there is limited knowledge on the speed plants adjust to heat in hours and days, and which adjustments are crucial. Tropical-subtropical rainforest tree species (Polyscias elegans) were heated at 40°C for 5 d, before returning to 25°C for 13 d of recovery. Leaf heat tolerance was quantified using the temperature at which minimal chl a fluorescence sharply rose (Tcrit ). Tcrit , metabolites, heat shock protein (HSP) abundance and membrane lipid fatty acid (FA) composition were quantified. Tcrit increased by 4°C (48-52°C) within 2 h of 40°C exposure, along with rapid accumulation of metabolites and HSPs. By contrast, it took > 2 d for FA composition to change. At least 2 d were required for Tcrit , HSP90, HSP70 and FAs to return to prestress levels. The results highlight the multi-faceted response of P. elegans to heat stress, and how this response varies over the scale of hours to days, culminating in an increased level of photosynthetic heat tolerance. These responses are important for survival of plants when confronted with heat waves amidst ongoing global climate change.

Linking water use efficiency with water use strategy from leaves to communities.

Limitations and utility of three measures of water use characteristics were evaluated: water use efficiency (WUE), intrinsic WUE and marginal water cost of carbon gain ( ∂ E / ∂ A ) estimated, respectively, as ratios of assimilation (A) to transpiration (E), of A to stomatal conductance (gs ) and of sensitivities of E and A with variation in gs . Only the measure ∂ E / ∂ A estimates water use strategy in a way that integrates carbon gain relative to water use under varying environmental conditions across scales from leaves to communities. This insight provides updated and simplified ways of estimating ∂ E / ∂ A and adds depth to understanding ways that plants balance water expenditure against carbon gain, uniquely providing a mechanistic means of predicting water use characteristics under changing environmental scenarios.

Revisiting yield in terms of phloem transport to grains suggests phloem sap movement might be homeostatic.

Phloem sap transport, velocity and allocation have been proposed to play a role in physiological limitations of crop yield, along with photosynthetic activity or water use efficiency. Although there is clear evidence that carbon allocation to grains effectively drives yield in cereals like wheat (as reflected by the harvest index), the influence of phloem transport rate and velocity is less clear. Here, we took advantage of previously published data on yield, respiration, carbon isotope composition, nitrogen content and water consumption in winter wheat cultivars grown across several sites with or without irrigation, to express grain production in terms of phloem sucrose transport and compare with xylem water transport. Our results suggest that phloem sucrose transport rate follows the same relationship with phloem N transport regardless of irrigation conditions and cultivars, and seems to depend mostly on grain weight (i.e., mg per grain). Depending on the assumption made for phloem sap sucrose concentration, either phloem sap velocity or its proportionality coefficient to xylem velocity change little with environmental conditions. Taken as a whole, phloem transport from leaves to grains seems to be homeostatic within a narrow range of values and following relationships with other plant physiological parameters across cultivars and conditions. This suggests that phloem transport per se is not a limitation for yield in wheat but rather, is controlled to sustain grain filling.

Ghosts of dry seasons past: Legacy of severe drought enhances mangrove salinity tolerance through coordinated cellular osmotic and elastic adjustments.

The incidence and severity of global mangrove mortality due to drought is increasing. Yet, little is understood of the capacity of mangroves to show long-term acclimation of leaf water relations to severe drought. We tested for differences between mid-dry season leaf water relations in two cooccurring mangroves, Aegiceras corniculatum and Rhizophora stylosa before a severe drought (a heatwave combined with low rainfall) and after its relief by the wet season. Consistent with ecological stress memory, the legacy of severe drought enhanced salinity tolerance in the subsequent dry season through coordinated adjustments that reduced the leaf water potential at the turgor loss point and increased cell wall rigidity. These adjustments enabled maintenance of turgor and relative water content with increasing salinity. As most canopy growth occurs during the wet season, acclimation to the 'memory' of higher salinity in the previous dry season enables greater leaf function with minimal adjustments, as long-lived leaves progress from wet through dry seasons. However, declining turgor safety margins - the difference between soil water potential and leaf water potential at turgor loss - implied increasing limitation to water use with increasing salinity. Thus, plasticity in leaf water relations contributes fundamentally to mangrove function under varying salinity regimes.

Good vibrations: Raman spectroscopy enables insights into plant biochemical composition.

Non-invasive techniques are needed to enable an integrated understanding of plant metabolic responses to environmental stresses. Raman spectroscopy is one such technique, allowing non-destructive chemical characterisation of samples in situ and in vivo and resolving the chemical composition of plant material at scales from microns to metres. Here, we review Raman band assignments of pigments, structural and non-structural carbohydrates, lipids, proteins and secondary metabolites in plant material and consider opportunities this technology raises for studies in vascular plant physiology.

Foliar water uptake enables embolism removal in excised twigs of Avicennia marina.

Embolism refilling is thought to require relaxation of xylem tension, and it is unclear whether and how tall trees or plants growing in arid or saline soils recover from embolism. We tested whether foliar water uptake could enable embolism refilling in dehydrated twigs of the grey mangrove (Avicennia marina). Four dehydrated twigs were imaged by laboratory-based micro-computed tomography before and after wetting leaves. Emboli were observed in dehydrated stems and leaves. Embolism decreased with increasing distance from the cut end of stems, suggesting that stem emboli were caused by cutting. A significant (P = 0.026) c. 80% reduction in the embolised area was observed in leaves between the start and the end of the experiment (29 ± 10 h after wetting). Embolus diameter was unaffected by wetting. Embolism refilling occurred slowly, in stems embolised by cutting and leaves embolised by cutting and/or dehydration. The lack of response of embolus diameter to wetting suggests that capillarity was not the main mechanism for refilling. Results show that excised twigs of A. marina are able to recover from embolism by absorption of atmospheric water and call for studies under natural conditions.

Mangroves provide blue carbon ecological value at a low freshwater cost.

"Blue carbon" wetland vegetation has a limited freshwater requirement. One type, mangroves, utilizes less freshwater during transpiration than adjacent terrestrial ecoregions, equating to only 43% (average) to 57% (potential) of evapotranspiration ([Formula: see text]). Here, we demonstrate that comparative consumptive water use by mangrove vegetation is as much as 2905 kL H2O ha-1 year-1 less than adjacent ecoregions with [Formula: see text]-to-[Formula: see text] ratios of 47-70%. Lower porewater salinity would, however, increase mangrove [Formula: see text]-to-[Formula: see text] ratios by affecting leaf-, tree-, and stand-level eco-physiological controls on transpiration. Restricted water use is also additive to other ecosystem services provided by mangroves, such as high carbon sequestration, coastal protection and support of biodiversity within estuarine and marine environments. Low freshwater demand enables mangroves to sustain ecological values of connected estuarine ecosystems with future reductions in freshwater while not competing with the freshwater needs of humans. Conservative water use may also be a characteristic of other emergent blue carbon wetlands.

Monitoring plant water status via static uniaxial compression of the leaf lamina.

Turgor pressure is an essential, but difficult to measure indicator of plant water status. Turgor has been quantified by localized compression of cells or tissues, but a simple method to perform these measurements is lacking. We hypothesized that changes in leaf turgidity can be monitored by uniaxially compressing the leaf lamina and measuring the mechanical stress under a constrained thickness (stress relaxation) and that changes in leaf water content can be monitored by measuring the leaf thickness under constant mechanical stress. Using a simple, custom-built leaf squeeze-flow rheometer, we performed different compression tests on leaves from 13 plant species. The mechanical stress measured during stress relaxation was correlated with leaf bulk turgor pressure (R2 > 0.95) and thus with balancing pressure (R2 > 0.94); the leaf thickness measured under constant mechanical stress was correlated with relative water content (R2 > 0.74). The coefficients of these relationships were related to the leaf bulk osmotic pressure at the turgor-loss point. An idealized average-cell model suggests that, under isothermal conditions, the stationary bulk modulus during compression is largely determined by the bulk osmotic pressure. Our study presents an inexpensive, accessible and automatable method to monitor plant water status noninvasively.

Foliar water uptake via cork warts in mangroves of the Sonneratia genus.

Foliar water uptake (FWU) occurs in plants of diverse ecosystems; however, the diversity of pathways and their associated FWU kinetics remain poorly resolved. We characterized a novel FWU pathway in two mangrove species of the Sonneratia genus, S. alba and S. caseolaris. Further, we assessed the influence of leaf wetting duration, wet-dry seasonality and leaf dehydration on leaf conductance to surface water (Ksurf ). The symplastic tracer dye, disodium fluorescein, revealed living cells subtending and encircling leaf epidermal structures known as cork warts as a pathway of FWU entry into the leaf. Rehydration kinetics experiments revealed a novel mode of FWU, with slow and steady rates of water uptake persistent over a duration of 12 hr. Ksurf increased with longer durations of leaf wetting and was greater in leaves with more negative water potentials at the initiation of leaf wetting. Ksurf declined by 68% between wet and dry seasons. Our results suggest that FWU via cork warts in Sonneratia sp. may be rate limited and under active regulation. We conclude that FWU pathways in halophytes may require ion exclusion to avoid uptake of salt when inundated, paralleling the capacity of halophyte roots for ion selectivity during water acquisition.

Shifting access to pools of shoot water sustains gas exchange and increases stem hydraulic safety during seasonal atmospheric drought.

Understanding how plants acclimate to drought is crucial for predicting future vulnerability, yet seasonal acclimation of traits that improve drought tolerance in trees remains poorly resolved. We hypothesized that dry season acclimation of leaf and stem traits influencing shoot water storage and hydraulic capacitance would mitigate the drought-associated risks of reduced gas exchange and hydraulic failure in the mangrove Sonneratia alba. By late dry season, availability of stored water had shifted within leaves and between leaves and stems. While whole shoot capacitance remained stable, the symplastic fraction of leaf water increased 86%, leaf capacitance increased 104% and stem capacitance declined 80%. Despite declining plant water potentials, leaf and whole plant hydraulic conductance remained unchanged, and midday assimilation rates increased. Further, the available leaf water between the minimum water potential observed and that corresponding to 50% loss of stem conductance increased 111%. Shifting availability of pools of water, within and between organs, maintained leaf water available to buffer periods of increased photosynthesis and losses in stem hydraulic conductivity, mitigating risks of carbon depletion and hydraulic failure during atmospheric drought. Seasonal changes in access to tissue and organ water may have an important role in drought acclimation and avoidance.

Harvesting water from unsaturated atmospheres: deliquescence of salt secreted onto leaf surfaces drives reverse sap flow in a dominant arid climate mangrove, Avicennia marina.

The mangrove Avicennia marina adjusts internal salt concentrations by foliar salt secretion. Deliquescence of accumulated salt causes leaf wetting that may provide a water source for salt-secreting plants in arid coastal wetlands where high nocturnal humidity can usually support deliquescence whereas rainfall events are rare. We tested the hypotheses that salt deliquescence on leaf surfaces can drive top-down rehydration, and that such absorption of moisture from unsaturated atmospheres makes a functional contribution to dry season shoot water balances. Sap flow and water relations were monitored to assess the uptake of atmospheric water by branches during shoot wetting events under natural and manipulated microclimatic conditions. Reverse sap flow rates increased with increasing relative humidity from 70% to 89%, consistent with function of salt deliquescence in harvesting moisture from unsaturated atmospheres. Top-down rehydration elevated branch water potentials above those possible from root water uptake, subsidising transpiration rates and reducing branch vulnerability to hydraulic failure in the subsequent photoperiod. Absorption of atmospheric moisture harvested through deliquescence of salt on leaf surfaces enhances water balances of Avicennia marina growing in hypersaline wetlands under arid climatic conditions. Top-down rehydration from these frequent, low intensity wetting events contributes to prevention of carbon starvation and hydraulic failure during drought.

Night and day: Shrinking and swelling of stems of diverse mangrove species growing along environmental gradients.

Tree stems swell and shrink daily, which is thought to reflect changes in the volume of water within stem tissues. We observed these daily patterns using automatic dendrometer bands in a diverse group of mangrove species over five mangrove forests across Australia and New Caledonia. We found that mangrove stems swelled during the day and shrank at night. Maximum swelling was highly correlated with daily maxima in air temperature. Variation in soil salinity and levels of tidal inundation did not influence the timing of stem swelling over all species. Medium-term increases in stem circumference were highly sensitive to rainfall. We defoliated trees to assess the role of foliar transpiration in stem swelling and shrinking. Defoliated trees showed maintenance of the pattern of daytime swelling, indicating that processes other than canopy transpiration influence the temporary stem diameter increments, which could include thermal swelling of stems. More research is required to understand the processes contributing to stem shrinking and swelling. Automatic Dendrometer Bands could provide a useful tool for monitoring the response of mangroves to extreme climatic events as they provide high-frequency, long-term, and large-scale information on tree water status.

Shoot surface water uptake enables leaf hydraulic recovery in Avicennia marina.

The significance of shoot surface water uptake (SSWU) has been debated, and it would depend on the range of conditions under which it occurs. We hypothesized that the decline of leaf hydraulic conductance (Kleaf ) in response to dehydration may be recovered through SSWU, and that the hydraulic conductance to SSWU (Ksurf ) declines with dehydration. We quantified effects of leaf dehydration on Ksurf and effects of SSWU on recovery of Kleaf in dehydrated leaves of Avicennia marina. SSWU led to overnight recovery of Kleaf , with recovery retracing the same path as loss of Kleaf in response to dehydration. SSWU declined with dehydration. By contrast, Ksurf declined with rehydration time but not with dehydration. Our results showed a role of SSWU in the recovery of leaf hydraulic conductance and revealed that SSWU is sensitive to leaf hydration status. The prevalence of SSWU in vegetation suggests an important role for atmospheric water sources in maintenance of leaf hydraulic function, with implications for plant responses to changing environments.

Mangrove dieback during fluctuating sea levels.

Recent evidence indicates that climate change and intensification of the El Niño Southern Oscillation (ENSO) has increased variation in sea level. Although widespread impacts on intertidal ecosystems are anticipated to arise from the sea level seesaw associated with climate change, none have yet been demonstrated. Intertidal ecosystems, including mangrove forests are among those ecosystems that are highly vulnerable to sea level rise, but they may also be vulnerable to sea level variability and extreme low sea level events. During 16 years of monitoring of a mangrove forest in Mangrove Bay in north Western Australia, we documented two forest dieback events, the most recent one being coincident with the large-scale dieback of mangroves in the Gulf of Carpentaria in northern Australia. Diebacks in Mangrove Bay were coincident with periods of very low sea level, which were associated with increased soil salinization of 20-30% above pre-event levels, leading to canopy loss, reduced Normalized Difference Vegetation Index (NDVI) and reduced recruitment. Our study indicates that an intensification of ENSO will have negative effects on some mangrove forests in parts of the Indo-Pacific that will exacerbate other pressures.

Leaf water storage increases with salinity and aridity in the mangrove Avicennia marina: integration of leaf structure, osmotic adjustment and access to multiple water sources.

Leaf structure and water relations were studied in a temperate population of Avicennia marina subsp. australasica along a natural salinity gradient [28 to 49 parts per thousand (ppt)] and compared with two subspecies grown naturally in similar soil salinities to those of subsp. australasica but under different climates: subsp. eucalyptifolia (salinity 30 ppt, wet tropics) and subsp. marina (salinity 46 ppt, arid tropics). Leaf thickness, leaf dry mass per area and water content increased with salinity and aridity. Turgor loss point declined with increase in soil salinity, driven mainly by differences in osmotic potential at full turgor. Nevertheless, a high modulus of elasticity (ε) contributed to maintenance of high cell hydration at turgor loss point. Despite similarity among leaves in leaf water storage capacitance, total leaf water storage increased with increasing salinity and aridity. The time that stored water alone could sustain an evaporation rate of 1 mmol m-2  s-1 ranged from 77 to 126 min from subspecies eucalyptifolia to ssp. marina, respectively. Achieving full leaf hydration or turgor would require water from sources other than the roots, emphasizing the importance of multiple water sources to growth and survival of Avicennia marina across gradients in salinity and aridity.

Plumbing the depths: extracellular water storage in specialized leaf structures and its functional expression in a three-domain pressure -volume relationship.

A three-domain pressure-volume relationship (PV curve) was studied in relation to leaf anatomical structure during dehydration in the grey mangrove, Avicennia marina. In domain 1, relative water content (RWC) declined 13% with 0.85 MPa decrease in leaf water potential, reflecting a decrease in extracellular water stored primarily in trichomes and petiolar cisternae. In domain 2, RWC decreased by another 12% with a further reduction in leaf water potential to -5.1 MPa, the turgor loss point. Given the osmotic potential at full turgor (-4.2 MPa) and the effective modulus of elasticity (~40 MPa), domain 2 emphasized the role of cell wall elasticity in conserving cellular hydration during leaf water loss. Domain 3 was dominated by osmotic effects and characterized by plasmolysis in most tissues and cell types without cell wall collapse. Extracellular and cellular water storage could support an evaporation rate of 1 mmol m-2 s-1 for up to 54 and 50 min, respectively, before turgor loss was reached. This study emphasized the importance of leaf anatomy for the interpretation of PV curves, and identified extracellular water storage sites that enable transient water use without substantive turgor loss when other factors, such as high soil salinity, constrain rates of water transport.

Plant hydraulics as a central hub integrating plant and ecosystem function: meeting report for 'Emerging Frontiers in Plant Hydraulics' (Washington, DC, May 2015).

Water plays a central role in plant biology and the efficiency of water transport throughout the plant affects both photosynthetic rate and growth, an influence that scales up deterministically to the productivity of terrestrial ecosystems. Moreover, hydraulic traits mediate the ways in which plants interact with their abiotic and biotic environment. At landscape to global scale, plant hydraulic traits are important in describing the function of ecological communities and ecosystems. Plant hydraulics is increasingly recognized as a central hub within a network by which plant biology is connected to palaeobiology, agronomy, climatology, forestry, community and ecosystem ecology and earth-system science. Such grand challenges as anticipating and mitigating the impacts of climate change, and improving the security and sustainability of our food supply rely on our fundamental knowledge of how water behaves in the cells, tissues, organs, bodies and diverse communities of plants. A workshop, 'Emerging Frontiers in Plant Hydraulics' supported by the National Science Foundation, was held in Washington DC, 2015 to promote open discussion of new ideas, controversies regarding measurements and analyses, and especially, the potential for expansion of up-scaled and down-scaled inter-disciplinary research, and the strengthening of connections between plant hydraulic research, allied fields and global modelling efforts.

Diurnal and seasonal variation in light and dark respiration in field-grown Eucalyptus pauciflora.

Respiration from vegetation is a substantial part of the global carbon cycle and the responses of plant respiration to daily and seasonal fluctuations in temperature and light must be incorporated in models of terrestrial respiration to accurately predict these CO2 fluxes. We investigated how leaf respiration (R) responded to changes in leaf temperature (T(leaf)) and irradiance in field-grown saplings of an evergreen tree (Eucalyptus pauciflora Sieb. ex Spreng). Seasonal shifts in the thermal sensitivity of leaf R in the dark (R(dark)) and in the light (R(light)) were assessed by allowing T(leaf) to vary over the day in field-grown leaves over a year. The Q10 of R (i.e., the relative increase in R for a 10 °C increase in T(leaf)) was similar for R(light) and R(dark) and had a value of ∼ 2.5; there was little seasonal change in the Q10 of either R(light) or R(dark), indicating that we may be able to use similar functions to model short-term temperature responses of R in the dark and in the light. Overall, rates of R(light) were lower than those of R(dark), and the ratio of R(light)/R(dark) tended to increase with rising T(leaf), such that light suppression of R was reduced at high T(leaf) values, in contrast to earlier work with this species. Our results suggest we cannot assume that R(light)/R(dark) decreases with increasing T(leaf) on daily timescales, and highlights the need for a better mechanistic understanding of what regulates light suppression of R in leaves.

Easy Come, Easy Go: Capillary Forces Enable Rapid Refilling of Embolized Primary Xylem Vessels.

Protoxylem plays an important role in the hydraulic function of vascular systems of both herbaceous and woody plants, but relatively little is known about the processes underlying the maintenance of protoxylem function in long-lived tissues. In this study, embolism repair was investigated in relation to xylem structure in two cushion plant species, Azorella macquariensis and Colobanthus muscoides, in which vascular water transport depends on protoxylem. Their protoxylem vessels consisted of a primary wall with helical thickenings that effectively formed a pit channel, with the primary wall being the pit channel membrane. Stem protoxylem was organized such that the pit channel membranes connected vessels with paratracheal parenchyma or other protoxylem vessels and were not exposed directly to air spaces. Embolism was experimentally induced in excised vascular tissue and detached shoots by exposing them briefly to air. When water was resupplied, embolized vessels refilled within tens of seconds (excised tissue) to a few minutes (detached shoots) with water sourced from either adjacent parenchyma or water-filled vessels. Refilling occurred in two phases: (1) water refilled xylem pit channels, simplifying bubble shape to a rod with two menisci; and (2) the bubble contracted as the resorption front advanced, dissolving air along the way. Physical properties of the protoxylem vessels (namely pit channel membrane porosity, hydrophilic walls, vessel dimensions, and helical thickenings) promoted rapid refilling of embolized conduits independent of root pressure. These results have implications for the maintenance of vascular function in both herbaceous and woody species, because protoxylem plays a major role in the hydraulic systems of leaves, elongating stems, and roots.