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.

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.

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.

Secondary leaves of an outbreak-adapted tree species are both more resource acquisitive and more herbivore resistant than primary leaves.

The magnitude and frequency of insect outbreaks are predicted to increase in forests, but how trees cope with severe outbreak defoliation is not yet fully understood. Winter deciduous trees often produce a secondary leaf flush in response to defoliation (i.e., compensatory leaf regrowth or refoliation), which promotes fast replenishment of carbon (C) storage and eventually tree survival. However, secondary leaf flushes may imply a high susceptibility to insect herbivory, especially in the event of an ongoing outbreak. We hypothesized that in winter deciduous species adapted to outbreak-driven defoliations, secondary leaves are both more C acquisitive and more herbivore resistant than primary leaves. During an outbreak by Ormiscodes amphimone F. affecting Nothofagus pumilio (Poepp. & Endl.) Krasser forests, we (i) quantified the defoliation and subsequent refoliation by analyzing the seasonal dynamics of the normalized difference vegetation index (NDVI) and (ii) compared the physiological traits and herbivore resistance of primary and secondary leaves. Comparisons of the NDVI of the primary and second leaf flushes relative to the NDVI of the defoliated forest indicated 31% refoliation, which is close to the leaf regrowth reported by a previous study in juvenile N. pumilio trees subjected to experimental defoliation. Primary leaves had higher leaf mass per area, size, carbon:nitrogen ratio and soluble sugar concentration than secondary leaves, along with lower nitrogen and starch concentrations, and similar total polyphenol and phosphorus concentrations. In both a choice and a non-choice bioassay, the leaf consumption rates by O. amphimone larvae were significantly higher (>50%) for primary than for secondary leaves, indicating higher herbivore resistance in the latter. Our study shows that secondary leaf flushes in outbreak-adapted tree species can be both C acquisitive and herbivore resistant, and suggests that these two features mediate the positive effects of the compensatory leaf regrowth on the tree C balance and forest resilience.

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.