Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis

  1. Atsushi Takabayashi*,
  2. Masahiro Kishine*,
  3. Kozi Asada,
  4. Tsuyoshi Endo*,, and
  5. Fumihiko Sato*
  1. *Graduate School of Biostudies, Kyoto University, Sakyo, Kyoto 606-8502, Japan; and Faculty of Life Science and Biotechnology, Fukuyama University, Fukuyama City 729-0292, Japan
  1. Edited by George H. Lorimer, University of Maryland, College Park, MD, and approved October 5, 2005 (received for review August 16, 2005)

Abstract

Whereas linear electron flow (LEF) in photosynthesis produces both ATP and NADPH, the cyclic electron flow (CEF) around photosystem I has been shown to produce only ATP. Two alternative routes have been shown for CEF; NAD(P)H dehydrogenase (NDH)- and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flows, but their physiological relevance has not been elucidated in detail. Meanwhile, because C4 photosynthesis requires more ATP than does C3 photosynthesis to concentrate CO2, it has not been clear how the extra ATP is produced. In this study, to elucidate whether CEF contributes to the additional ATP needed in C4 photosynthesis, we estimated the amounts of PGR5, which participates in FQR-dependent flow, and NDH-H, a subunit of NDH, in four C4 species. Although the expression profiles of PGR5 did not correlate well with the additional ATP requirement, NDH was greatly expressed in mesophyll cells in the NAD-malic enzyme (ME) species, and in bundle-sheath cells in NADP-ME species, where there is a strong need for ATP in the respective cells. Our results indicate that CEF via NDH plays a central role in driving the CO2-concentrating mechanism in C4 photosynthesis.

Footnotes

  • To whom correspondence should be addressed. E-mail: tuendo{at}kais.kyoto-u.ac.jp.

  • Author contributions: A.T., K.A., T.E., and F.S. designed research; A.T. and M.K. performed research; A.T. analyzed data; and A.T., K.A., T.E., and F.S. wrote the paper.

  • Conflict of interest statement: No conflicts declared.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations: CEF, cyclic electron flow; FQR, ferredoxin:plastoquinone oxidoreductase; LEF, linear electron flow; NDH, NAD(P)H dehydrogenase; ME, malic enzyme; PEPC, phosphoenolpyruvate carboxylase; PS, photosystem; qPCR, quantitative real-time RT-PCR.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AB218879-AB218882).

  • § Ohwaki, T. & Asada, K. (2003) Plant Biol. (abstr.).

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