This Article Full Text Full Text (PDF) All Versions of this Article: 141/2/508    most recent pp.105.074765v1 Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (7) Citing Articles via Google Scholar Google Scholar Articles by Sakuragi, Y. Articles by Bryant, D. A. Search for Related Content PubMed PubMed Citation Articles by Sakuragi, Y. Articles by Bryant, D. A. Agricola Articles by Sakuragi, Y. Articles by Bryant, D. A. Related Collections Reactive Oxygen Species

-Tocopherol Plays a Role in Photosynthesis and Macronutrient Homeostasis of the Cyanobacterium Synechocystis sp. PCC 6803 That Is Independent of Its Antioxidant Function¹

Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802 (Y.S., D.A.B.); and Department of Biochemistry and Molecular Biology (H.M., D.D.P.), Cell and Molecular Biology Program (H.M., D.D.P.), and United States Department of Energy Plant Research Laboratory (H.M.), Michigan State University, East Lansing, Michigan 48824–1319

-Tocopherol is synthesized exclusively in oxygenic phototrophs and is known to function as a lipid-soluble antioxidant. Here, we report that -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 -tocopherol biosynthesis are identical, but the mutants exhibit elevated photosynthetic activities and glycogen levels. When grown photomixotrophically with glucose (Glc), 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. Photosystem 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 -tocopherol plays an important role in optimizing photosynthetic activity and macronutrient homeostasis in Synechocystis sp. PCC 6803. Several lines of evidence indicate that increased oxidative stress in the tocopherol mutants is unlikely to be the underlying cause of photosystem II inactivation and Glc-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 Glc-induced lethality. Based on these results, we propose that -tocopherol plays a nonantioxidant regulatory role in photosynthesis and macronutrient homeostasis through a signal transduction pathway that also involves PmgA.

² Present address: Department of Plant Biology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK–1871 Frederiksberg C, Denmark.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Donald A. Bryant (dab14{at}psu.edu).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074765.

^* Corresponding author; e-mail dab14{at}psu.edu; fax 617–738–7664.

Received January 1, 2006; returned for revision March 10, 2006; accepted March 10, 2006.

This article has been cited by other articles:

				H. Takahashi, H. Uchimiya, and Y. Hihara Difference in metabolite levels between photoautotrophic and photomixotrophic cultures of Synechocystis sp. PCC 6803 examined by capillary electrophoresis electrospray ionization mass spectrometry J. Exp. Bot., August 1, 2008; 59(11): 3009 - 3018. [Abstract] [Full Text] [PDF]

				Y. Yang, C. Yin, W. Li, and X. Xu {alpha}-Tocopherol Is Essential for Acquired Chill-Light Tolerance in the Cyanobacterium Synechocystis sp. Strain PCC 6803 J. Bacteriol., March 1, 2008; 190(5): 1554 - 1560. [Abstract] [Full Text] [PDF]

				H. Maeda, T. L. Sage, G. Isaac, R. Welti, and D. DellaPenna Tocopherols Modulate Extraplastidic Polyunsaturated Fatty Acid Metabolism in Arabidopsis at Low Temperature PLANT CELL, February 1, 2008; 20(2): 452 - 470. [Abstract] [Full Text] [PDF]

				S. Lee, J.-Y. Ryu, S. Y. Kim, J.-H. Jeon, J. Y. Song, H.-T. Cho, S.-B. Choi, D. Choi, N. T. de Marsac, and Y.-I. Park Transcriptional Regulation of the Respiratory Genes in the Cyanobacterium Synechocystis sp. PCC 6803 during the Early Response to Glucose Feeding Plant Physiology, November 1, 2007; 145(3): 1018 - 1030. [Abstract] [Full Text] [PDF]

				A.-R. Abbasi, M. Hajirezaei, D. Hofius, U. Sonnewald, and L. M. Voll Specific Roles of {alpha}- and {gamma}-Tocopherol in Abiotic Stress Responses of Transgenic Tobacco Plant Physiology, April 1, 2007; 143(4): 1720 - 1738. [Abstract] [Full Text] [PDF]

				S. E. Sattler, L. Mene-Saffrane, E. E. Farmer, M. Krischke, M. J. Mueller, and D. DellaPenna Nonenzymatic Lipid Peroxidation Reprograms Gene Expression and Activates Defense Markers in Arabidopsis Tocopherol-Deficient Mutants PLANT CELL, December 1, 2006; 18(12): 3706 - 3720. [Abstract] [Full Text] [PDF]