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.