1 INTRODUCTION
Water-energy dynamics drive global patterns of plant diversity (Kreft & Jetz, 2007), with the predicted global increase of aridity likely to make plants more vulnerable to a lack of water in the soil (Choat et al., 2018; Olson et al., 2018). In arid and semiarid environments, plant productivity is compromised due to prolonged soil drought. Xerophilous plants that thrive in these ecosystems exhibit anatomical adaptations that reduce rates of water loss, such as smaller leaves, lower stomata index and impermeable coating structures, like cuticles (see Shields, 1950). Surprisingly, some of the structures that prevent evaporative water loss may also facilitate aerial water uptake, decoupling the water status of the canopy from soil water availability (Benzing et al., 1978; Gouvra & Grammatikopoulos, 2003).
Foliar water uptake is a widespread phenomenon of vascular plants, known for three centuries, and evaluated in at least 53 plant families (Dawson & Goldsmith, 2018). Foliar water uptake has direct consequences on plant function, relaxing tension in the water column of the xylem, enhancing turgor-driven growth, and increasing the productivity of agricultural and natural ecosystems (Mayr et al., 2014; Steppe et al., 2018; Aguirre-Gutiérrrez et al., 2019). The key conditions for foliar water uptake are met in fog-dominated environments (Tognetti, 2015; Weathers et al., 2019), where high atmospheric humidity enhances nighttime dew formation on leaf surfaces, thus increasing the possibility of foliar water absorption. Indeed, studies in montane cloud forests of Brazil (Eller et al., 2016), coastal California redwood forests in the USA (Burgess & Dawson, 2004), and cloud forests in Mexico (Gotsch et al., 2014) have demonstrated that aerial water has an important impact on plant functioning, especially during dry periods. Foliar uptake in semiarid areas of the tropics is less studied, despite reports that it can enhance biomass productivity (Díaz & Granadillo, 2005; Limm et al., 2009). Better characterization of the pathways of foliar absorption will enhance understanding of the mechanisms semiarid plants use to hydrate their leaves with aerial water.
Foliar water uptake occurs through a variety of mechanisms and pathways. Some species absorb water through the natural leaf openings, such as stomata (Burkhardt et al., 2012; Berry et al., 2014) or hydathodes (Martin & von Willert, 2000; Boanares et al., 2019). Other structures that are supposedly impermeable to water may participate in aerial water uptake, including cuticles (Vaadia & Waisel, 1963; Yates & Hutley, 1995; Fernández et al., 2017; Schuster et al., 2017), and trichomes (Franke, 1967; Benzing et al., 1978; reviewed by Berry et al., 2019). While the use of these wall-thickened, sealing structures appears as a good strategy to capture atmospheric water condensed on leaf surfaces, demonstration of their hygroscopic capacity requires a careful examination of their cell wall biochemistry, so far lacking for most plant species. Early work in this area showed that the absorptive capacity of leaves is related to the presence of polysaccharides under the cuticle (Kerstiens, 1996). However, the role of ubiquitous compounds of the cell walls, such as pectins and glycoproteins, on foliar water uptake has received little attention (Boanares et al., 2018). It is not known whether trichomes or sclerenchymatous structures display such hygroscopic compounds.
This knowledge gap is particularly severe for xerophylous species, which have leaves with abundant sclerenchymatous tissues, such as idioblasts, highly specialized structures that are understudied from a functional perspective. Idioblasts (Schwendener, 1874) are thick walled cells typically buried in the mesophyll of vascular plants (Bailey & Nast, 1945; Tomlinson & Fisher, 2005), and commonly found in the leaves of xerophilous species (Foster, 1956; Heide Jorgensen, 1990). Traditionally, idioblasts have been explored from the perspective of morphology, ontogeny, and taxonomic value (Foster,1944; 1945a,b; Bloch, 1946; Foster, 1955a,b; Rao & Mody, 1961). However, important functions attributed to idioblasts are typically inferred from their putative stiffness, such as support and defense (Foster, 1947; Tucker, 1964; Rao & Sharma, 1968), or from their topology, such as a possible role in leaf capacitance (Heide-Jorgensen, 1990) or serving as light guides (Karabourniotis, 1998). The diverse array of anatomies of xerophilous species is exemplified in the genus Capparis (Rao & Mody, 1961; Gan et al., 2013). Capparis odoratissima is native to the semiarid tropical environments of the South American continent with a remarkable capacity to produce new biomass in response to canopy irrigation (Díaz & Granadillo, 2005), likely through foliar water uptake. However, the mechanism of foliar water uptake in this species is unknown.
Here we focus on C. odoratissima with the goal of understanding the relationship between anatomy and function. We show that the leaves of C. odoratissima are highly specialized structures that perform a dual function: minimizing water loss when dry and absorbing water when wet. We examine how an intricate network of hygroscopic pathways within the mesophyll enhances water uptake, thus maintaining leaf hydration upon water condensation on the leaf surface.