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.