Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas

  1. Pierre Cardola,
  2. Jean Alricb,
  3. Jacqueline Girard-Bascoub,
  4. Fabrice Franckc,
  5. Francis-André Wollmanb,1 and
  6. Giovanni Finazzib,1
  1. aLaboratoire de Génétique des Microorganismes et
  2. cLaboratoire de Photobiologie, Département des Sciences de la Vie, Université de Liège, B-4000 Liège, Belgique; and
  3. bInstitut de Biologie Physico-Chimique, Unité Mixte de Recherche 7141, Centre National de la Recherche Scientifique and Université Pierre et Marie Curie-Paris 6, 75005, Paris, France
  1. Communicated by Pierre A. Joliot, Institut de Biologie Physico-Chimique, Paris, France, July 20, 2009 (received for review April 20, 2009)

Abstract

State transitions correspond to a major regulation process for photosynthesis, whereby chlorophyll protein complexes responsible for light harvesting migrate between photosystem II and photosystem I in response to changes in the redox poise of the intersystem electron carriers. Here we disclose their physiological significance in Chlamydomonas reinhardtii using a genetic approach. Using single and double mutants defective for state transitions and/or mitochondrial respiration, we show that photosynthetic growth, and therefore biomass production, critically depends on state transitions in respiratory-defective conditions. When extra ATP cannot be provided by respiration, enhanced photosystem I turnover elicited by transition to state 2 is required for photosynthetic activity. Concomitant impairment of state transitions and respiration decreases the overall yield of photosynthesis, ultimately leading to reduced fitness. We thus provide experimental evidence that the combined energetic contributions of state transitions and respiration are required for efficient carbon assimilation in this alga.

Footnotes

  • 1To whom correspondence may be addressed. E-mail: francis-andre.wollman{at}ibpc.fr or giovanni.finazzi{at}ibpc.fr
  • Author contributions: P.C., J.A., J.G.-B., F.F., F.-A.W., and G.F. designed research; P.C., J.A., J.G.-B., and G.F. performed research; P.C., J.A., J.G.-B., F.F., F.-A.W., and G.F. analyzed data; and P.C., F.-A.W., and G.F. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0908111106/DCSupplemental.

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