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J. Biol. Chem., Vol. 282, Issue 22, 16369-16378, June 1, 2007

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Regulation of Copper Homeostasis by Micro-RNA in Arabidopsis^*

Hiroaki Yamasaki¹, Salah E. Abdel-Ghany¹, Christopher M. Cohu, Yoshichika Kobayashi, Toshiharu Shikanai², and Marinus Pilon³

From the Graduate School of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashiku, Fukuoka 812-8581, Japan and the Biology Department and Program in Molecular Plant Biology, Colorado State University, Fort Collins, Colorado 80523

Major copper proteins in the cytoplasm of plant cells are plastocyanin, copper/zinc superoxide dismutase, and cytochrome c oxidase. Under copper limited conditions, expression of copper/zinc superoxide dismutase is down-regulated and the protein is replaced by iron superoxide dismutase in chloroplasts. We present evidence that a micro-RNA, miR398, mediates this regulation in Arabidopsis thaliana, by directing the degradation of copper/zinc superoxide dismutase mRNA when copper is limited. Sequence analysis indicated that the transcripts encoding cytosolic copper/zinc superoxide dismutase and COX5b-1, a subunit of the mitochondrial cytochrome c oxidase, are also targeted by miR398. This regulation via miR398 takes place in response to changes in a low range of copper levels (0.2-0.5 µM), indicating that miR398 is involved in a response to copper limitation. On the other hand, another major copper protein, plastocyanin, which is involved in photosynthetic electron flow and is essential in higher plants, was not regulated via miR398.We propose that miR398 is a key factor in copper homeostasis in plants and regulates the stability of mRNAs of major copper proteins under copper-limited conditions.

Received for publication, January 5, 2007 , and in revised form, March 12, 2007.

^* This work was supported by grant-in-aids for Creative Scientific Research (17GS0316) and for Scientific Research on Priority Areas (16085206) (to T. S.) and United States National Science Foundation Grant NSF-IBN-0418993 (to M. P.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Both authors contributed equally to this manuscript.

² To whom correspondence may be addressed. Tel./Fax: 81-92-642-2882; E-mail: shikanai{at}agr.kyushu-u.ac.jp. ³ To whom correspondence may be addressed.

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