Abstract
The Chenopodiaceae is one of the families including C4 species among eudicots. In this family, the genus Chenopodium is considered to include only C3 species. However, we report here a transition from C3 photosynthesis to proto-Kranz to C3–C4 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 C3 plants. However, 5 species showed proto-Kranz anatomy and a C3-like Γ, whereas C. strictum showed leaf anatomy and a Γ typical of C3–C4 intermediates. Chenopodium album accessions examined included both proto-Kranz and C3–C4 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 C3 species, in both M and bundle-sheath (BS) cells in proto-Kranz species, and exclusively in BS cells in C3–C4 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 C3-like regarding activities and amounts of C3 and C4 photosynthetic enzymes and δ13C values, suggesting that these species perform photosynthesis without contribution of the C4 cycle. This study demonstrates that Chenopodium is not a C3 genus and is valuable for studying evolution of C3–C4 intermediates.
Highlights
Photorespiration is an inevitable metabolic process in C 3 plants that use ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) for primary fixation of C O2
In C3–C4 intermediates, at least the P-protein, one of the 4 subunits constituting the glycine decarboxylase (GDC) multi-enzyme system, is absent in the M mitochondria, which renders GDC non-functional, and glycine generated in the M cells must be transported into the BS mitochondria to be decarboxylated by GDC (Rawsthorne 1992; Rawsthorne et al 1988)
Light microscopy revealed a large variation in chloroplast numbers and arrangement in BS cells among Chenopodium species examined (Fig. 1, S1–S3)
Summary
Photorespiration is an inevitable metabolic process in C 3 plants that use ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) for primary fixation of C O2. Leaves of most C3–C4 intermediate plants show Kranz-like anatomy, in which BS cells contain numerous chloroplasts and mitochondria (Edwards and Ku 1987; Sage et al 2014). In these plants, the values of the CO2 compensation point (Г) and O2 inhibition of photosynthesis are intermediate between the values of C3 and C4 plants (Edwards and Ku 1987; Monson and Rawsthorne 2000). Many C3–C4 intermediate species reduce photorespiratory C O2 loss only by using the glycine shuttle (type I intermediates), but in some intermediates a C4 cycle complements the glycine shuttle (type II intermediates; Edwards and Ku 1987)
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