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Published on October 31, 2008; 10.1104/pp.108.128124

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Received August 15, 2008
Accepted October 26, 2008

Chlororespiration and grana hyperstacking - How an Arabidopsis thaliana double mutant can survive, which is defective in both starch biosynthesis and daily carbon export from chloroplasts (adg1-1/tpt-1)

Rainer E. Hausler *, Stefan Geimer , H. Henning Kunz , Jessica Schmitz , Peter Dormann , Kirsten Bell , Sonja Hetfeld , Andre Guballa , and Ulf-Ingo Flugge

Universitat zu Koln, Botanisches Institut, Gyrhofstrasse 15, D-50931 Koln (Cologne), Germany; Universitat Bayreuth, Biologie/Elektronenmikroskopie NW I / B1, D-95440 Bayreuth, Germany; Universitat Bonn, Institut fur Molekulare Physiologie und Biotechnologie der Pflanzen, Karlrobert-Kreiten-Strase 13, D-53115 Bonn, Germany

* Corresponding author; email: rainer.haeusler{at}uni-koeln.de.

An Arabidopsis thaliana double mutant impaired in starch biosynthesis and the triose phosphate/phosphate translocator (adg1-1/tpt-1) is characterized by a diminished utilization of photoassimilates and the concomitant consumption of reducing power and energy produced in the photosynthetic light reaction. In order to guarantee survival, the double mutant responds to this metabolic challenge with growth retardation, an 80% decline in photosynthetic electron transport, diminished chlorophyll contents, an enhanced reduction state of plastoquinone in the dark (up to 50%), a perturbation of the redox poise in the leaves (increased NADPH/NADP ratios; decreased ascorbate/dehydroascorbate ratios), hyperstacking of grana thylakoids, and an increased number of plastoglobules. Enhanced oxygen consumption and applications of inhibitors of alternative mitochondrial and chloroplast oxidases (AOX, PTOX) suggest that chlororespiration as well as mitochondrial respiration are involved in the enhanced plastoquinone reduction state in the dark. Transcript amounts of PTOX and AOX were diminished and nuclear-encoded components related to plastidic NADH reductase (NDH1) were increased in adg1-1/tpt-1 compared to the wild-type. Cytochrome b559, proposed to be involved in the re-oxidation of photosystem II, was not regulated at the transcriptional level. The hyperstacking of grana thylakoids mimicks adaptation to low light and increased plastoglobule numbers suggest a response to enhanced oxidative stress. Altered chloroplast organization combined with perturbations in the redox poise suggests that adg1-1/tpt-1 could be a tool for the in vivo study of retrograde signaling mechnisms controlling the co-ordinated expression of nuclear- and plastome-encoded photosynthetic genes.




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