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

Abstract

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 (K surf ). 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. K surf increased with longer durations of leaf wetting and was greater in leaves with more negative water potentials at the initiation of leaf wetting. K surf 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.

Foliar Water Uptake Capacity in Six Mangrove Species

“…As the Sundarbans' salinity conditions are largely determined by the volume of freshwater coming from upstream, both the daily and seasonal (dry or wet season) salinity fluctuations determine the environment in which these trees grow [66]. Given that the salinity levels play a major role in determining the leaf plasticity in mangroves [67,68], the leaf anatomical traits from our study (i.e., the absence of cork warts) can differ from those reported in the study of Evans et al [58] and Bryant et al [25], which were both carried out in Queensland, Australia.…”

“…Caution should be taken when attributing the highest FWU capacity of A. marina solely due to the presence of leaf trichomes, as other water entry points may also be involved in the uptake of water. Recently, a new point of water entry has been elucidated, i.e., cork warts in both S. alba and S. caseolaris [25]. Although this leaf trait was also found in B. gymnorhiza by Evans et al [58], no comparable mode of action for this mechanism has been allocated to this species yet, nor were cork warts observed in our study (Figure 3).…”

“…A clear anatomical distinction of A. marina compared to the other species is the abundance of abaxial, awl-shaped multicellular trichomes, consisting of a top cell, one or two body cells and ending in a basal cell (Figure 3b). Although Bryant et al [25] identified cork warts in Sonneratia sp. and Evans et al [58] in B. gymnorhiza, none were observed on the transverse micrographs (Figure 3d-f).…”

Revisiting plant hydrological niches: The importance of atmospheric resources for ground‐rooted plants

“…This contribution might be particularly important in plant communities where occult precipitation events coincide with soil dry periods, such as in Mediterranean coastal ecosystems (Burgess & Dawson, 2004; Corbin et al, 2005), temperate steppes (Cavallaro et al, 2020) and in the eastern Amazon Forest (Binks et al, 2021). In saline and freshwater wetlands, although soil water is abundant year‐round, the excessive salinity or insufficient oxygenation levels in the soil can impair root water and nutrient uptake, thus likely increasing the relative advantage accrued via aerial uptake (Bryant, Fuenzalida, Zavafer, et al, 2021; Nguyen et al, 2017). In those ecosystems, the competitive advantage of accessing the third layer may vary seasonally, and possibly diurnally, according to the interaction between tidal flows and evaporative demand (Bryant, Fuenzalida, Brothers, et al, 2021).…”

“…mangroves), where high tide can be associated with higher salt‐water inputs. As high‐tide periods in mangroves are also associated with higher risk of inundation of low hanging mature leaves and entire saplings, species in this environment may require ecologically appropriate foliar water uptake pathways (possibly involving active regulation; Bryant, Fuenzalida, Zavafer, et al, 2021) to benefit from occult precipitation events without leading to an unregulated ion entry into leaves.…”