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J. Biol. Chem., Vol. 279, Issue 24, 25066-25074, June 11, 2004

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A Repeated GGA Motif Is Critical for the Activity and Stability of the Riboregulator RsmY of Pseudomonas fluorescens^*

Claudio Valverde, Magnus Lindell¶||, E. Gerhart H. Wagner¶||, and Dieter Haas

From the Département de Microbiologie Fondamentale, Bâtiment de Biologie, Université de Lausanne, CH-1015 Lausanne (Dorigny), Switzerland and the ^¶Institute of Cell & Molecular Biology, Biomedical Center, Uppsala University, Box 596, SE-751 24, Uppsala, Sweden

The riboregulator RsmY of Pseudomonas fluorescens strain CHA0 is an example of small regulatory RNAs belonging to the global Rsm/Csr regulatory systems controlling diverse cellular processes such as glycogen accumulation, motility, or formation of extracellular products in various bacteria. By binding multiple molecules of the small regulatory protein RsmA, RsmY relieves the negative effect of RsmA on the translation of several target genes involved in the biocontrol properties of strain CHA0. RsmY and functionally related riboregulators have repeated GGA motifs predicted to be exposed in single-stranded regions, notably in the loops of hairpins. The secondary structure of RsmY was corroborated by in vivo cleavage with lead acetate. RsmY mutants lacking three or five (out of six) of the GGA motifs showed reduced ability to derepress the expression of target genes in vivo and failed to bind the RsmA protein efficiently in vitro. The absence of GGA motifs in RsmY mutants resulted in reduced abundance of these transcripts and in a shorter half-life (6 min as compared with 27 min for wild type RsmY). These results suggest that both the interaction of RsmY with RsmA and the stability of RsmY strongly depend on the GGA repeats and that the ability of RsmY to interact with small regulatory proteins such as RsmA may protect this RNA from degradation.

Received for publication, February 20, 2004

^* This work was supported in part by grants from the Swiss National Foundation for Scientific Research (project 3100A0-100180), the Roche Research Foundation, and the European project ECO-SAFE (QLK2-2000-01759). 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.

^|| Supported by grants from The Swedish Research Council and the Swedish Foundation for Strategic Research.

To whom correspondence should be addressed: Tel.: 54-11-4365-7100; Fax: 54-11-4365-7182; E-mail: cvalver{at}unq.edu.ar.

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