Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species

Spatial and temporal regulation of phosphoenolpyruvate carboxylase (PEPC) is critical to the function of C-4 photosynthesis. The photosynthetic isoform of PEPC in the cytosol of mesophyll cells in Kranz-type C-4 photosynthesis has distinctive kinetic and regulatory properties. Some species in the Chenopodiaceae family perform C-4 photosynthesis without Kranz anatomy by spatial separation of initial fixation of atmospheric CO2 via PEPC from C-4 acid decarboxylation and CO2 donation to Rubisco within individual chlorenchyma cells. We studied molecular and functional features of PEPC in two single-cell functioning C-4 species (Bienertia sinuspersici, Suaeda aralocaspica) as compared to Kranz type (Haloxylon persicum, Salsola richteri, Suaeda eltonica) and C-3 (Suaeda linifolia) chenopods. It was found that PEPC from both types of C-4 chenopods displays higher specific activity than that of the C-3 species and shows kinetic and regulatory characteristics similar to those of C-4 species in other families in that they are subject to light/dark regulation by phosphorylation and display differential malate sensitivity. Also, the deduced amino acid sequence from leaf cDNA indicates that the single-cell functioning C-4 species possesses a Kranz-type C-4 isoform with a Ser in the amino terminal. A phylogeny of PEPC shows that isoforms in the two single-cell functioning C-4 species are in a clade with the C-3 and Kranz C-4 Suaeda spp. with high sequence homology. Overall, this study indicates that B. sinuspersici and S. aralocaspica have a C-4-type PEPC similar to that in Kranz C-4 plants, which likely is required for effective function of C-4 photosynthesis.