C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems

Abstract

Aquatic C4 photosynthesis probably arose in response to dissolved CO2 limitations, possibly before its advent in terrestrial plants. Of over 7600 C4 species, only about a dozen aquatic species are identified. Amphibious Eleocharis species (sedges) have C3-C4 photosynthesis and Kranz anatomy in aerial, but not submersed, leaves. Aquatic grasses have aerial and submersed leaves with C4 or C3-C4 photosynthesis and Kranz anatomy, but some lack Kranz anatomy in the submersed leaves. Two freshwater submersed monocots, Hydrilla verticillata and possibly Egeria densa, are C4 NADP-malic enzyme (NADP-ME) species. A marine macroalga, Udotea flabellum (Chlorophyta), and possibly a diatom, are C4, so it is not confined to angiosperms. Submersed C4 species differ from terrestrial in that β-carboxylation is cytosolic with chloroplastic decarboxylation and Rubisco carboxylation, so the C4 and Calvin cycles operate in the same cell without Kranz anatomy. Unlike terrestrial plants, Hydrilla is a facultative C4 that shifts from C3 to C4 in low [CO2]. It is well documented, with C4 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 C3-like sequences. Hvpepc4 appears to be the photosynthetic form induced in C4 leaves, but it differs from terrestrial C4 isoforms in lacking a C4 signature Serine. The molecular mass of NADP-ME (72 kDa) also resembles a C3 isoform. Hydrilla belongs to the ancient Hydrocharitaceae family, and gives insight to early C4 development. Hydrilla is an excellent 'minimalist' system to study C4 photosynthesis regulation without anatomical complexities.