Transition from Csub(3) to proto-Kranz to Csub(3)-Csub(4) intermediate type in the genus Chenopodium (Chenopodiaceae)

The Chenopodiaceae is one of the families including Csub(4) species among eudicots. In this family, the genus Chenopodium is considered to include only Csub(3) species. However, we report here a transition from Csub(3) photosynthesis to proto-Kranz to Csub(3)-Csub(4) intermediate type in Chenopodium. We investigated leaf anatomical and photosynthetic traits of 15 species, of which 8 species showed non-Kranz anatomy and a CO2 compensation point (Γ) typical of Csub(3) plants. However, 5 species showed proto-Kranz anatomy and a Csub(3)-like Γ, whereas C. strictum showed leaf anatomy and a Γ typical of Csub(3)-Csub(4) intermediates. Chenopodium album accessions examined included both proto-Kranz and Csub(3)-Csub(4) intermediate types, depending on locality. Glycine decarboxylase, a key photorespiratory enzyme that is involved in the decarboxylation of glycine, was located predominantly in the mesophyll (M) cells of Csub(3) species, in both M and bundle-sheath (BS) cells in proto-Kranz species, and exclusively in BS cells in Csub(3)-Csub(4) intermediate species. The M/BS tissue area ratio, number of chloroplasts and mitochondria per BS cell, distribution of these organelles to the centripetal region of BS cells, the degree of inner positioning (vacuolar side of chloroplasts) of mitochondria in M cells, and the size of BS mitochondria also changed with the change in glycine decarboxylase localization. All Chenopodium species examined were Csub(3)-like regarding activities and amounts of Csub(3) and Csub(4) photosynthetic enzymes and δsup(13)C values, suggesting that these species perform photosynthesis without contribution of the Csub(4) cycle. This study demonstrates that Chenopodium is not a Csub(3) genus and is valuable for studying evolution of Csub(3)-Csub(4) intermediates.