Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae)

Abstract

Portulacaceae is one of 19 families of terrestrial plants in which species having C₄ photosynthesis have been found. Representative species from major clades of the genus Portulaca were studied to characterize the forms of photosynthesis structurally and biochemically. The species P. amilis, P. grandiflora, P. molokiniensis, P. oleracea, P. pilosa, and P. umbraticola belong to the subgenus Portulaca and are C₄ plants based on leaf carbon isotope values, Kranz anatomy, and expression of key C₄ enzymes. Portulaca umbraticola, clade Umbraticola, is NADP-malic enzyme (NADP-ME)-type C₄ species, while P. oleracea and P. molokiniensis in clade Oleracea are NAD-ME-type C₄ species, all having different forms of Atriplicoid-type leaf anatomy. In clade Pilosa, P. amilis, P. grandiflora, and P. pilosa are NADP-ME-type C₄ species. They have Pilosoid-type anatomy in which Kranz tissues enclose peripheral vascular bundles with water storage in the centre of the leaf. Portulaca cf. bicolor, which belongs to subgenus Portulacella, is an NADP-ME C₄ species with Portulacelloid-type anatomy; it has well-developed Kranz chlorenchyma surrounding lateral veins distributed in one plane under the adaxial epidermis with water storage cells underneath. Portulaca cryptopetala (clade Oleracea), an endemic species from central South America, was identified as a C₃–C₄ based on its intermediate CO₂ compensation point and selective localization of glycine decarboxylase of the photorespiratory pathway in mitochondria of bundle sheath cells. The C₄Portulaca species which were examined also have cotyledons with Kranz-type anatomy, while the stems of all species have C₃-type photosynthetic cells. The results indicate that multiple structural and biochemical forms of C₄ photosynthesis evolved in genus Portulaca.