C-4 mechanisms in aquatic angiosperms: comparisons with terrestrial C-4 systems

Aquatic C-4 photosynthesis probably arose in response to dissolved CO2 limitations, possibly before its advent in terrestrial plants. Of over 7600 C-4 species, only about a dozen aquatic species are identified. Amphibious Eleocharis species (sedges) have C-3-C-4 photosynthesis and Kranz anatomy in aerial, but not submersed, leaves. Aquatic grasses have aerial and submersed leaves with C-4 or C-3-C-4 photosynthesis and Kranz anatomy, but some lack Kranz anatomy in the submersed leaves. Two freshwater submersed monocots, Hydrilla verticillata and possibly Egeria densa, are C-4 NADP-malic enzyme (NADP-ME) species. A marine macroalga, Udotea flabellum (Chlorophyta), and possibly a diatom, are C-4, so it is not confined to angiosperms. Submersed C-4 species differ from terrestrial in that beta-carboxylation is cytosolic with chloroplastic decarboxylation and Rubisco carboxylation, so the C-4 and Calvin cycles operate in the same cell without Kranz anatomy. Unlike terrestrial plants, Hydrilla is a facultative C-4 that shifts from C-3 to C-4 in low [CO2]. It is well documented, with C-4 gas exchange and pulse-chase characteristics, enzyme kinetics and localization, high internal [CO2], relative growth rate, and quantum yield studies. It has multiple phosphoenolpyruvate carboxylase isoforms with C-3-like sequences. Hvpepc4 appears to be the photosynthetic form induced in C-4 leaves, but it differs from terrestrial C-4 isoforms in lacking a C-4 signature Serine. The molecular mass of NADP-ME (72 kDa) also resembles a C-3 isoform. Hydrilla belongs to the ancient Hydrocharitaceae family, and gives insight to early C-4 development. Hydrilla is an excellent 'minimalist' system to study C-4 photosynthesis regulation without anatomical complexities.