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.