Species Having C4 Single-Cell-Type Photosynthesis in the Chenopodiaceae Family Evolved a Photosynthetic Phosphoenolpyruvate Carboxylase Like That of Kranz-Type C4 Species

Abstract

Abstract Spatial and temporal regulation of phosphoenolpyruvate carboxylase (PEPC) is critical to the function of C4 photosynthesis. The photosynthetic isoform of PEPC in the cytosol of mesophyll cells in Kranz-type C4 photosynthesis has distinctive kinetic and regulatory properties. Some species in the Chenopodiaceae family perform C4 photosynthesis without Kranz anatomy by spatial separation of initial fixation of atmospheric CO2 via PEPC from C4 acid decarboxylation and CO2 donation to Rubisco within individual chlorenchyma cells. We studied molecular and functional features of PEPC in two single-cell functioning C4 species (Bienertia sinuspersici, Suaeda aralocaspica) as compared to Kranz type (Haloxylon persicum, Salsola richteri, Suaeda eltonica) and C3 (Suaeda linifolia) chenopods. It was found that PEPC from both types of C4 chenopods displays higher specific activity than that of the C3 species and shows kinetic and regulatory characteristics similar to those of C4 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 C4 species possesses a Kranz-type C4 isoform with a Ser in the amino terminal. A phylogeny of PEPC shows that isoforms in the two single-cell functioning C4 species are in a clade with the C3 and Kranz C4  Suaeda spp. with high sequence homology. Overall, this study indicates that B. sinuspersici and S. aralocaspica have a C4-type PEPC similar to that in Kranz C4 plants, which likely is required for effective function of C4 photosynthesis.