Plasticfruits, part 8: the case of Ziziphus/Paliurus (Rhamnaceae)

Gemini

Q. Consider Paliurus and Ziziphus to be congeneric. Describe the ontogeny of the fruits in this clade, accounting for the remarkable distinction between fleshy fruits in some species and dry, winged fruits in others. The point is to explain how such clear adaptations for endozoochory vs anemochory can arise from a single ancestral fruit, without generic differentiation.

The shared template. Floral ontogeny in this clade begins with a perigynous to semi-epigynous arrangement. Both genera have a pentamerous flower with a prominent intrastaminal nectar disc frequently adnate to the ovary base, and a gynoecium of 2–3 carpels forming a multi-locular ovary. The distinction between the two forms emerges after anthesis, dictated by the differential growth of the mesocarp and of the extralocular tissue — the floral cup or hypanthium.

The fleshy drupe (Ziziphus). The inner ovary wall undergoes rapid sclerification, forming a hard stone that protects the seeds during digestion. The mid-layer undergoes massive parenchyma proliferation, the cells accumulating sugars, mucilage and water to create the reward for vertebrate dispersers. The epidermis develops a cuticle and pigments, anthocyanins or carotenoids, that signal ripeness to visual foragers.

The dry, winged fruit (Paliurus). The central portion of the ovary lignifies as in Ziziphus, but the peripheral tissue, derived from the upper margin of the hypanthium and the mesocarp, does not become succulent. Instead it undergoes meristematic activity that pushes outward horizontally, expanding into a circular, leathery or woody wing. During maturation the cells undergo programmed senescence and air-space formation, giving a lightweight, aerodynamic structure. The stone remains central for protection, but the flesh is replaced by a structural extension that increases drag for dispersal by wind.

Transition without generic divergence. The shift from a succulent drupe to a winged fruit, or the reverse, can occur through relatively minor heterochronic shifts in the expression of genes governing cell proliferation and expansion in the floral cup. If the instruction for parenchyma expansion is localised to a peripheral ring rather than the whole mesocarp, and is coupled with early desiccation, a samaroid fruit results. Because these changes modify existing structures rather than creating new organs, the transition is morphologically fluid — supporting the view that Paliurus is merely a specialised anemochorous branch of the Ziziphus lineage.

References given. Brizicky, G. K. (1964), Journal of the Arnold Arboretum 45(4): 439–463; Hauenschild, F., et al. (2016), Taxon 65(4): 766–778; Medan, D. & Schirarend, C. (2004), in Kubitzki (ed.), The Families and Genera of Vascular Plants VI: 320–338; Schirarend, C. (1991), IAWA Bulletin 12(4): 359–400; Islam, M. B. & Simmons, M. P. (2006), Systematic Botany 31(4): 826–839.