NDH-Mediated Cyclic Electron Flow Around Photosystem I is Crucial for C4 Photosynthesis

Plant Cell Physiol. 2016 Oct;57(10):2020-2028. doi: 10.1093/pcp/pcw127. Epub 2016 Aug 6.

Abstract

C4 photosynthesis exhibits efficient CO2 assimilation in ambient air by concentrating CO2 around ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) through a metabolic pathway called the C4 cycle. It has been suggested that cyclic electron flow (CEF) around PSI mediated by chloroplast NADH dehydrogenase-like complex (NDH), an alternative pathway of photosynthetic electron transport (PET), plays a crucial role in C4 photosynthesis, although the contribution of NDH-mediated CEF is small in C3 photosynthesis. Here, we generated NDH-suppressed transformants of a C4 plant, Flaveria bidentis, and showed that the NDH-suppressed plants grow poorly, especially under low-light conditions. CO2 assimilation rates were consistently decreased in the NDH-suppressed plants under low and medium light intensities. Measurements of non-photochemical quenching (NPQ) of Chl fluorescence, the oxidation state of the reaction center of PSI (P700) and the electrochromic shift (ECS) of pigment absorbance indicated that proton translocation across the thylakoid membrane is impaired in the NDH-suppressed plants. Since proton translocation across the thylakoid membrane induces ATP production, these results suggest that NDH-mediated CEF plays a role in the supply of ATP which is required for C4 photosynthesis. Such a role is more crucial when the light that is available for photosynthesis is limited and the energy production by PET becomes rate-determining for C4 photosynthesis. Our results demonstrate that the physiological contribution of NDH-mediated CEF is greater in C4 photosynthesis than in C3 photosynthesis, suggesting that the mechanism of PET in C4 photosynthesis has changed from that in C3 photosynthesis accompanying the changes in the mechanism of CO2 assimilation.

Keywords: ATP production; C4 photosynthesis; Chloroplast NADH dehydrogenase-like complex; Cyclic electron flow around PSI; Low-light condition; Proton translocation across the thylakoid membrane.

MeSH terms

  • Carbon / metabolism*
  • Carbon Dioxide / metabolism
  • Electron Transport / radiation effects
  • Flaveria / enzymology*
  • Flaveria / growth & development
  • Flaveria / radiation effects
  • Light
  • NADH Dehydrogenase / metabolism*
  • Photosynthesis* / radiation effects
  • Photosystem I Protein Complex / metabolism*
  • Plant Leaves / metabolism
  • Plant Leaves / radiation effects
  • Plant Proteins / metabolism*
  • RNA Interference
  • Spectrum Analysis
  • Suppression, Genetic / radiation effects
  • Transformation, Genetic / radiation effects

Substances

  • Photosystem I Protein Complex
  • Plant Proteins
  • Carbon Dioxide
  • Carbon
  • NADH Dehydrogenase