Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ

BACKGROUND AND AIMS: Previous work has shown that Borszczowia aralocaspica (Chenopodiaceae) accomplishes C4 photosynthesis in a unique, polarized single-cell system in leaves. Mature cotyledons have the same structure as leaves, with chlorenchyma cells having biochemical polarization of dimorphic chloroplasts and C4 functions at opposite ends of the cell. KEY RESULTS: Development of the single-celled C4 syndrome in cotyledons was characterized. In mature seeds, all cell layers are already present in the cotyledons, which contain mostly lipids and little starch. The incipient chlorenchyma cells have a few plastids towards the centre of the cell. Eight days after germination and growth in the dark, small plastids are evenly distributed around the periphery of the expanding cells. Immunolocalization studies show slight labelling of Rubisco in plastids in seeds, including chlorenchyma, hypodermal and water storage, but not epidermal, cells. After imbibition and 8 d of growth in the dark labelling for Rubisco progressively increased, being most prominent in chlorenchyma cells. There was no immunolabelling for the plastid C4 enzyme pyruvate, Pi dikinase under these conditions. Cotyledons developing in light show formation of chlorenchyma tissue, induction of the cytosolic enzyme phosphoenolpyruvate carboxylase and development of dimorphic chloroplasts at opposite ends of the cells. Proximal chloroplasts have well-developed grana, store starch and contain Rubisco; those located distally have reduced grana, lack starch and contain pyruvate, Pi dikinase. CONCLUSIONS: The results show cotyledons developing in the dark have a single structural plastid type which expresses Rubisco, while light induces formation of dimorphic chloroplasts from the single plastid pool, synthesis of C4 enzymes, and biochemical and structural polarization leading to the single-cell C4 syndrome.