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J. Biol. Chem., Vol. 280, Issue 47, 39229-39237, November 25, 2005

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A Dual Upstream Open Reading Frame-based Autoregulatory Circuit Controlling Polyamine-responsive Translation^*

From the Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA, United Kingdom

A novel form of translational regulation is described for the key polyamine biosynthetic enzyme S-adenosylmethionine decarboxylase (AdoMetDC). Plant AdoMetDC mRNA 5' leaders contain two highly conserved overlapping upstream open reading frames (uORFs): the 5' tiny and 3' small uORFs. We demonstrate that the small uORF-encoded peptide is responsible for constitutively repressing downstream translation of the AdoMetDC proenzyme ORF in the absence of increased polyamine levels. This first example of a sequence-dependent uORF to be described in plants is also functional in Saccharomyces cerevisiae. The tiny uORF is required for normal polyamine-responsive AdoMetDC mRNA translation, and we propose that this is achieved by control of ribosomal recognition of the occluded small uORF, either by ribosomal leaky scanning or by programmed -1 frameshifting. In vitro expression demonstrated that both the tiny and the small uORFs are translated. This tiny/small uORF configuration is highly conserved from moss to Arabidopsis thaliana, and a more diverged tiny/small uORF arrangement is found in the AdoMetDC mRNA 5' leader of the single-celled green alga Chlamydomonas reinhardtii, indicating an ancient origin for the uORFs.

Received for publication, August 24, 2005 , and in revised form, September 21, 2005.

This paper is dedicated to the memories of our fathers, Christopher C. Hanfrey and John W. Michael.

^* This work was funded in part by a Biotechnology and Biological Sciences Research Council Core Strategic Grant from the British Food Standards Agency. 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 Supported by European Union Marie Curie Post-doctoral Fellowship MCF 2000-02029. Present address: Dept. of Biology, University of Bologna, Via Irnerio 42, 40126 Bologna, Italy.

² Present address: Dept. of Cytogenetics, Sheffield Children's Hospital, Western Bank, Sheffield, S10 2TH, UK.

³ To whom correspondence should be addressed: Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA, UK. Tel.: 44-1603-255356; Fax: 44-1603-255288; E-mail: tony.michael{at}bbsrc.ac.uk.

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