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Published on March 24, 2006; 10.1104/pp.105.074765

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Received January 1, 2006
Returned for revision January 30, 2006
Accepted March 10, 2006

{alpha}-Tocopherol plays a role in photosynthesis and macronutrient homeostasis of the cyanobacterium Synechocystis sp. PCC 6803 that is independent of its antioxidant function

Yumiko Sakuragi , Hiroshi Maeda , Dean DellaPenna , and Donald A. Bryant *

Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802
Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824-1319; Cell and Molecular Biology Program, Michigan State University, East Lansing, MI, 48824-1319; DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI, 48824-1319
Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824-1319; Cell and Molecular Biology Program, Michigan State University, East Lansing, MI, 48824-1319

* Corresponding author; email: dab14{at}psu.edu.

{alpha}-Tocopherol is synthesized exclusively in oxygenic phototrophs and is known to function as a lipid-soluble antioxidant. Here we report that {alpha}-tocopherol also has a novel function independent of its antioxidant properties in the cyanobacterium Synechocystis sp. PCC 6803. The photoautotrophic growth rates of wild type and mutants impaired in {alpha}-tocopherol biosynthesis are identical, but the mutants exhibit elevated photosynthetic activities and glycogen levels. When grown photomixotrophically with glucose, however, these mutants cease growth within 24 h and exhibit a global macronutrient starvation response associated with nitrogen, sulfur, and carbon, as shown by decreased phycobiliprotein content (35% of the wild-type level) and accumulation of the nblA1-nblA2, sbpA, sigB, sigE, and sigH transcripts. PS II activity and carboxysome synthesis are lost in the tocopherol mutants within 24 h of photomixotrophic growth, and the abundance of carboxysome gene (rbcL, ccmK1, ccmL) and ndhF4 transcripts decreases to undetectable levels. These results suggest that {alpha}-tocopherol plays an important role in optimizing photosynthetic activity and macronutrient homeostasis in Synechocystis sp. PCC 6803. Several lines of evidence indicate increased oxidative stress in the tocopherol mutants is unlikely to be the underlying cause of PS II inactivation and glucose-induced lethality. Interestingly, insertional inactivation of the pmgA gene, which encodes a putative serine/threonine kinase similar to RsbW and RsbT in Bacillus subtilis, results in a similar increase in glycogen and glucose-induced lethality. Based on these results, we propose that {alpha}-tocopherol plays a non-antioxidant regulatory role in photosynthesis and macronutrient homeostasis through a signal transduction pathway that also involves PmgA.




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