4.2 Asymmetric foliar water uptake and anatomical specializations in Capparis odoratissima
Our experiments with water droplets on each leaf surface revealed an asymmetry in the water uptake. Both surfaces of the C. odoratissima leaves loaded with water droplets showed an initial positive gain of water with time. However, when water was applied to the adaxial surface only, water gains were only possible for the initial six hours of exposure, and then water losses occurred. In contrast, when the abaxial surface was loaded, water uptake was linear, and followed a rate of 0.033 mg cm-2 h-1, an order or magnitude lower than submerged leaves, due to evaporative losses of the exposed leaf surfaces. Previous work with the Australian subtropical species Sloanea woollsii (Yates and Hutley, 1995) showed similar rates for sprayed leaves, although these results were questioned by Kerstiens (1996), who suggested that small cracks in the cuticle could explain the extremely high leaf permeances. Natural openings (i.e. not created by microorganisms) are unusual in the upper leaf surface, except in amphistomous leaves, or leaves with hydathodes (Martin & von Willert, 2000). However, we found thousands of micropores per cm area projecting toward concave areas on the adaxial leaf surfaces inCapparis odoratissima , which likely correlate with apoplastic water transport from the atmosphere to the leaf. These openings connect with the lumen of columnar idioblasts, pointing to these structures as significant players in the leaf water budgets.
Idioblasts have rarely been demonstrated as contributing to foliar water uptake in angiosperms, with some exceptions such as Hakea suaveolens (Heide-Jorgensen, 1990). However, their topology in the numerous forest species where they have been described, including gymnosperms (Hooker, 1864; Sterling, 1947), and more than eighty eudicot families (Solereder, 1908; Foster, 1955a,b; Rao & Mody, 1961; Zhang et al., 2009; Vitarelli et al., 2016), suggested a role in the storage of water in leaves. As thick-walled sclerenchymatous tissues (Evert, 2006), idioblasts evolved multiple shapes and dispositions within leaves, but the columnar type of idioblasts displayed in the leaves of C. odortatissima have only been described in two species so far,Hakea suaveolens (Heide-Jorgensen, 1990), and Mouriria huberi (Foster, 1947). These adaptations cannot be related to xeric environments, as other species from the same genus and adapted to dry climates have completely different anatomies, such as the MediterraneanCapparis spinosa (Rhizopoulou, 1990; Rhizopoulou & Psaras, 2003; Gan et al., 2013).
In nature, water condenses most likely on the adaxial surface of leaves, and, indeed, most studies of foliar water uptake suggest that the upper side is more permeable to water (Gardingen & Grace, 1992; Fernández et al., 2014). In C. odoratissima , the reasons behind the asymmetric water uptake correlate with the markedly distinct anatomy between leaf surfaces. Although uptake from the adaxial surface is modest compared with the abaxial one, this dual possibility is unique among flowering plants. Indeed, this correlates with the unique anatomy of leaves, in which the lumen of the idioblasts formed a continuum with the peltate hairs located in the abaxial surface, traversing the cross sectional area of the leaves. As a result, an intricate network of micro channels linked both surfaces with the mesophyll. Trichome-idioblast associations are commonly found in species from arid environments such as those from the family Euphorbiaceae (Solereder, 1908; Metcalfe & Chalk, 1950),Olea europaea (Arzeee, 1953), or Androstachys johnsoni(Alvin, 1987). The presence of peltate hairs is not indicative of foliar water uptake (Bickford, 2016), since species with peltate hairs such as in Olea europaea showed no evidence of water absorption (Arzeee, 1953). Our results revealed a high hygroscopicity of the peltate hairs of C. odoratissima . Hygroscopic peltate hairs have been reported in some angiosperm species (Gramatikopoulos & Manetas, 1994; Bickford, 2016; Eller et al., 2016; Pina et al., 2016; Vitarelli et al., 2016), with the best studied being epiphytic bromeliads (Benzing & Burt, 1970; Benzing, 1976; Benzing et al., 1978; Benz & Martin, 2006; Ohrui et al., 2007; Raux et al., 2020). While a tradeoff between epidermal evaporation and water entrance from the atmosphere might exist, in C .odoatissima, this tradeoff favors the uptake of water from the trichomes of the lower surface, and from the idioblast tips when water condenses in the upper surface. Strikingly, loading the leaves of a seedling in vivo revealed that the droplet disappearance from the adaxial surface was similar to that of the abaxial one.