4.3 The biochemistry of foliar water uptake in Capparis odoratissima
The pathway of atmospheric water entry in the leaves of C. odoratissima involves hygroscopic materials deposited in the leaf coatings (Gouvra & Gamatipoulus, 2003). In the current work, we first describe the thick walled structures composing the multicellular peltate hairs, which project pectins to the external part, suggesting their involvement in the initial water capture when condensation happens in the abaxial side. A few reports have revealed the presence of pectins in trichomes, such as species from semi-arid forests like Crombretum leprosum (Pina et al., 2016), the tropical species Drymis brasiliensis (Eller et al., 2013), or in the trichomes of Fagus(Schreel et al., 2020). In addition, we revealed that both epidermal and spongy mesophyll cells show a high concentration of un-esterified pectins in their cell walls. This is in line with the ubiquity of pectins within the leaf mesophyll. In the leaves of C. odoratissima , the tight association of mesophyll cells and their exposed pectins with the numerous idioblasts may imply a pulling force for water deposited on the leaf surfaces, using idioblasts as carriers.
The idioblasts of C. odoratissima are highly hygroscopic, with cellulosic walls that contain polar molecules for water attachment, but also partially lignified, suggesting a secondary role in defense and structural support. A finely tuned water uptake in C. odoratissima is revealed by our experiments with the apoplastic dye tracer Lucifer Yellow. Water entering from the surrounding atmosphere to the idioblasts flows through an intricate network of crenations and branches within the idioblasts that connect all leaf tissues and the exterior. Most strikingly is the fact that epitopes belonging to arabinogalacatan proteins are specifically located within these channels. AGPs are highly branched proteins with a short amino acid backbone attached to the plasma membrane of cells, and a large saccharidic part that has been related with nutritive and/or signaling functions between cells (Ellis et al., 2010). AGPs play different roles in plant development, including mate recognition and support during reproduction, proper early seedling development, and many others (Majewska-Sawka & Nothnagel, 2000; Vaughn et al., 2007; Pereira et al., 2016). However, the role of AGPs in plant hydration has been scarcely studied. Remarkably, works evaluating the composition of the cell walls in the resurrection plant Craterostigma wilmsii , which can completely dry out and subsequently regain water, point to the hygroscopic properties of AGPs as critical players in this rapid and effective rehydration (Vicré et al, 2004). AGP-related proteins have been previously related with the tensile strength of stems due to their participation in secondary cell wall composition, such as in the vessels or fibers (Ito et al., 2005; Liu et al., 2013). But the presence of AGPs have never been reported before in idioblasts with such specific pattern as in the current work. What this reveals are the biochemical complexity of sclerenchymatous tissues, which are possible effectors enabling hydration of tissues during periods where water deficits in the soil combines with water saturation in the atmosphere (Figure 8). Thus, AGPs may be secreted to the lumen of the idioblasts during development, serving as bridges of water uptake between the atmosphere and the leaf mesophyll. Future works should explore the presence of AGPs in sclerenchymatous tissues of other species, as well as their putative role in leaf capacitance.