Abstract

Summary Extra ATP required in C4 photosynthesis for the CO2‐concentrating mechanism probably comes from cyclic electron transport (CET). As metabolic ATP : NADPH requirements in mesophyll (M) and bundle‐sheath (BS) cells differ among C4 subtypes, the subtypes may differ in the extent to which CET operates in these cells.We present an analytical model for cell‐type‐specific CET and linear electron transport. Modelled NADPH and ATP production were compared with requirements.For malic‐enzyme (ME) subtypes, c. 50% of electron flux is CET, occurring predominantly in BS cells for standard NADP‐ME species, but in a ratio of c. 6 : 4 in BS : M cells for NAD‐ME species. Some C4 acids follow a secondary decarboxylation route, which is obligatory, in the form of ‘aspartate‐malate’, for the NADP‐ME subtype, but facultative, in the form of phosphoenolpyruvate‐carboxykinase (PEP‐CK), for the NAD‐ME subtype. The percentage for secondary decarboxylation is c. 25% and that for 3‐phosphoglycerate reduction in BS cells is c. 40%; but these values vary with species. The ‘pure’ PEP‐CK type is unrealistic because its is impossible to fulfil ATP : NADPH requirements in BS cells.The standard PEP‐CK subtype requires negligible CET, and thus has the highest intrinsic quantum yields and deserves further studies in the context of improving canopy productivity.

Highlights

  • The CO2-concentrating mechanism (CCM) in C4 leaves relies on the coordinated functioning of two distinct photosynthetic cell types, mesophyll (M) cells and bundle-sheath (BS) cells (Hatch, 1987; Kromdijk et al, 2010)

  • The cyclic electron transport (CET) accounted for almost 100% of the electron flux in BS cells and only c. 10% in M cells for the NADP-ME subtype having negligible PSII in BS cells, but c. 60% in BS cells and c. 40% in M cells for the NAD-ME subtype

  • The calculated fractions of NADPH and ATP production in the BS cells were used to match the fractions required for the operation of the Calvin cycle and the CCM cycle

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Summary

Introduction

The CO2-concentrating mechanism (CCM) in C4 leaves relies on the coordinated functioning of two distinct photosynthetic cell types, mesophyll (M) cells and bundle-sheath (BS) cells (Hatch, 1987; Kromdijk et al, 2010). OAA is either reduced to malate or converted into aspartate These C4 acids diffuse to BS cells where they are decarboxylated to deliver CO2 to Rubisco to start the Calvin cycle or the C3 cycle (Hatch, 1987). Operation of the CCM involves the regeneration of PEP in the C4 cycle, which requires ATP (Hatch, 1987; von Caemmerer & Furbank, 1999), in addition to ATP required by the C3 cycle. The full C4 cycle involves both types of cells (Supporting Information Fig. S1), and the amount and location of the ATP required for PEP regeneration depend on the C4 subtypes (Hatch, 1987; Kanai & Edwards, 1999). The subtypes were traditionally classified according to the enzymes that decarboxylate C4 acids in BS compartments: NADP-malic enzyme (ME) in chloroplasts, NAD-ME in mitochondria and PEP carboxykinase (CK) in the cytosol (Hatch, 1987; von Caemmerer & Furbank, 2003)

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