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Plant Cell Advance Online Publication
Published on November 7, 2008; 10.1105/tpc.108.061341

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Received June 10, 2008
Returned for revision October 5, 2008
Accepted October 22, 2008

A Heterocomplex of Iron Superoxide Dismutases Defends Chloroplast Nucleoids against Oxidative Stress and Is Essential for Chloroplast Development in Arabidopsis

Fumiyoshi Myouga 1, Chieko Hosoda 2, Taishi Umezawa 3, Haruko Iizumi 1, Takashi Kuromori 1, Reiko Motohashi 4, Yuriko Shono 5, Noriko Nagata 5, Masahiko Ikeuchi 6, and Kazuo Shinozaki 1*

1 Gene Discovery Research Group, RIKEN Plant Science Center, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan
2 Gene Discovery Research Group, RIKEN Plant Science Center, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Komaba, Meguro-ku, Tokyo 153-8902, Japan
3 Gene Discovery Research Team, RIKEN Plant Science Center, Tsukuba, Ibaraki 305-0074, Japan
4 Department of Biological Science, Faculty of Agriculture, Shizuoka University, Ohya, Shizuoka 422-8529, Japan
5 Department of Chemical Biological Sciences, Japan Women's University, Bunkyo-ku, Tokyo 112-8681, Japan
6 Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Komaba, Meguro-ku, Tokyo 153-8902, Japan

* To whom correspondence should be addressed. E-mail: sinozaki{at}rtc.riken.jp.

There are three iron superoxide dismutases in Arabidopsis thaliana: FE SUPEROXIDE DISMUTASE1 (FSD1), FSD2, and FSD3. Their biological roles in chloroplast development are unknown. Here, we show that FSD2 and FSD3 play essential roles in early chloroplast development, whereas FSD1, which is found in the cytoplasm, does not. An fsd2-1 fsd3-1 double mutant had a severe albino phenotype on agar plates, whereas fsd2 and fsd3 single knockout mutants had pale green phenotypes. Chloroplast development was arrested in young seedlings of the double mutant. The mutant plants were highly sensitive to oxidative stress and developed increased levels of reactive oxygen species (ROS) during extended darkness. The FSD2 and FSD3 proteins formed a heteromeric protein complex in the chloroplast nucleoids. Furthermore, transgenic Arabidopsis plants overexpressing both the FSD2 and FSD3 genes showed greater tolerance to oxidative stress induced by methyl viologen than did the wild type or single FSD2- or FSD3-overexpressing lines. We propose that heteromeric FSD2 and FSD3 act as ROS scavengers in the maintenance of early chloroplast development by protecting the chloroplast nucleoids from ROS.




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