Ecophysiology of Phloem Loading in Succulent Leaves With Different Anatomical Patterns of Aizoaceae Species (Caryophyllales).

The mesophyll of succulent leaves of Aizoaceae plants may have specialized water-storing tissue in perennial species (storage succulents), but not in annual species (all-cell succulents). Storage succulents have peripheral minor veins with either outward-facing xylem (exoscopic), restricted to the basal subfamily Sesuvioideae, or inward-facing xylem (endoscopic) with the phloem adjacent to the chlorenchyma ring, as seen in derived subfamilies such as the hyperdiverse Ruschioideae. Here, we investigate the implications of phloem positioning relative to photosynthesizing cells by comparative transmission electron microscopy, aided by immunolocalization of sucrose transporters (SUT1). Both the exoscopic bundles of Sesuvium portulacastrum (L.) L. (Sesuvioideae) and the endoscopic bundles of Delosperma herbeum (N.E.Br.) N.E.Br. (Ruschioideae) have ordinary companion cells. Given their structural similarity, and considering the proximity of the phloem of exoscopic bundles to the chlorenchyma in other Caryophyllales species, we propose that the widespread occurrence of endoscopic bundles in Ruschioideae reflects the maintenance of an adaptively neutral character state during their adaptive radiation. Contrastingly, the all-cell species Mesembryanthemum crystallinum L. (Mesembryanthemoideae) has companion transfer cells, but SUT1 localizes to sieve elements, leaving the exact function of the transfer cells unclear in the context of the increased export of sugars they are known to provide. Nevertheless, because the reproductive phase of this annual species coincides with the dry season, when mesophyll cells must retain osmoprotective solutes simultaneously with flower development, we suggest that its transfer cells are adaptive by mediating a trade-off between source and sink organs, which does not occur in the two perennial storage succulents.