Chapter 5 Single-Cell C4 Photosynthesis in Aquatic Plants

In water with low free [CO2] a common strategy of submersed plants is to use HCO 3 − , but some ­species utilize a C4 photosynthetic system that surprisingly lacks the Kranz dual-cell compartmentation of most terrestrial C4 plants. Instead, the C4 and C3 cycles are in the same cell, with phosphoenolpyruvate ­carboxylase (PEPC) and ribulose bisphosphate carboxylase–oxygenase (rubisco) sequestered in the cytosol and chloroplasts, respectively. Malate decarboxylation by NADP malic enzyme (NADP-ME) in the chloroplasts produces a chloroplastic CO2 concentrating mechanism (CCM). It occurs in the ­submersed monocots Hydrilla verticillata and Egeria densa (Hydrocharitaceae), and in these species it is facultative because low [CO2] induces a metabolic shift in the leaves from C3 to single-cell C4 photosynthesis. ­Submersed leaves of other species also perform single-cell C4 photosynthesis, including Sagittaria ­subulata (Alismataceae), the grasses Orcuttia californica and O. viscida (Poaceae), and the sedge ­Eleocharis acicularis. A marine macroalga (Udotea flabellum, Chlorophyta) and a diatom (Thalassiosira weissflogii) likewise show evidence of its occurrence, so it is not restricted to higher plants. The change from C3 to C4 photosynthetic gas exchange and pulse-chase characteristics is well documented in Hydrilla, along with enzyme kinetics and localization; high internal [CO2], and improved growth. ­Multiple isoforms of PEPC, NADP-ME and pyruvate orthophosphate dikinase (PPDK) exist in Hydrilla and Egeria, but specific forms, including hvpepc4, hvme1 and hvppdk1are up-regulated in the C4 leaves of Hydrilla and encode proteins with C4 photosynthetic characteristics. Interestingly, the photosynthetic hvpepc4 differs from its terrestrial C4 counterparts in lacking a “C4-signature” serine near the carboxy terminus. The C3 leaf must maximize CO2 conductance to rubisco, but as the C4 system is induced, ­chloroplast conductance is probably minimized to reduce leakage from the CCM. Further study of the facultative system of Hydrilla could determine if down-regulation of chloroplast-envelope aquaporins is involved in reducing CO2 conductance. Hydrilla and Egeria are in the ancient Hydrocharitaceae ­family, and can give insights into early C4 photosynthesis, which likely originated in water prior to its advent on land.