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J. Biol. Chem., Vol. 283, Issue 23, 15932-15945, June 6, 2008

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MicroRNA-mediated Systemic Down-regulation of Copper Protein Expression in Response to Low Copper Availability in Arabidopsis^*

Salah E. Abdel-Ghany and Marinus Pilon¹

From the Biology Department and Program in Molecular Plant Biology, Colorado State University, Fort Collins, Colorado 80523 and Botany Department, Faculty of Science, Zagazig University, Zagazig 44519, Egypt

In plants, copper is an essential micronutrient required for photosynthesis. Two of the most abundant copper proteins, plastocyanin and copper/zinc superoxide dismutase, are found in chloroplasts. Whereas plastocyanin is essential for photo-autotrophic growth, copper/zinc superoxide dismutase is dispensable and in plastids can be replaced by an iron superoxide dismutase when copper is limiting. The down-regulation of copper/zinc superoxide dismutase expression in response to low copper involves a microRNA, miR398. Interestingly, in Arabidopsis and other plants, three additional microRNA families, miR397, miR408, and miR857, are predicted to target the transcripts for the copper protein plantacyanin and members of the laccase copper protein family. We confirmed the predicted targets of miR397, miR408, and miR857 experimentally by cleavage site analysis. To study the spatial expression pattern of these microRNAs and the effect of copper on their expression, we analyzed Arabidopsis grown hydroponically on different copper regimes. On low amounts of copper the plants accumulated miR397, miR408, and miR857. The microRNA expression pattern was negatively correlated with the accumulation of transcripts for plantacyanin and laccases. Furthermore, the expression of other laccases that are not predicted targets for known microRNAs was similarly regulated in response to copper. For some of these laccases, the regulation was disrupted in a microRNA maturation mutant (hen1-1), suggesting the presence of other copper-regulated microRNAs. Thus, in Arabidopsis, microRNA-mediated down-regulation is a general mechanism to regulate nonessential copper proteins. We propose that this mechanism allows plants to save copper for the most essential functions during limited copper supply.

Received for publication, February 21, 2008 , and in revised form, April 3, 2008.

^* This work was supported by 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 To whom correspondence should be addressed: Biology Dept., CO State University, Fort Collins, CO. 80523-1878. Tel.: 970-491-0803; Fax: 970-491-0649; E-mail: pilon{at}lamar.colostate.edu.

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