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Molecular and Cellular Biology, February 1999, p. 1144-1158, Vol. 19, No. 2
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Seven Novel Methylation Guide Small Nucleolar RNAs Are Processed from a Common Polycistronic Transcript by Rat1p and RNase III in Yeast

Liang-Hu Qu,1 Anthony Henras,2 Yong-Jun Lu,1 Hui Zhou,1 Wei-xin Zhou,1 Yuan-Qi Zhu,1 Jin Zhao,1 Yves Henry,2 Michèle Caizergues-Ferrer,2 and Jean-Pierre Bachellerie2,*

Biotechnology Research Center, Zhongshan University, Guangzhou 510 275, People's Republic of China,1 and Laboratoire de Biologie Moléculaire Eucaryote du CNRS, Université Paul Sabatier, Toulouse, France2

Received 21 September 1998/Returned for modification 28 October 1998/Accepted 9 November 1998

Through a computer search of the genome of the yeast Saccharomyces cerevisiae, the coding sequences of seven different box C/D antisense small nucleolar RNAs (snoRNAs) with the structural hallmarks of guides for rRNA ribose methylation have been detected clustered over a 1.4-kb tract in an inter-open reading frame region of chromosome XIII. The corresponding snoRNAs have been positively identified in yeast cells. Disruption of the nonessential snoRNA gene cluster specifically suppressed the seven cognate rRNA ribose methylations but did not result in any growth delay under the conditions of yeast culture tested. The seven snoRNAs are processed from a common polycistronic transcript synthesized from an independent promoter, similar to some plant snoRNAs but in marked contrast with their vertebrate functional homologues processed from pre-mRNA introns containing a single snoRNA. Processing of the polycistronic precursor requires nucleases also involved in rRNA processing, i.e., Rnt1p and Rat1p. After disruption of the RNT1 gene, the yeast ortholog of bacterial RNase III, production of the seven mature snoRNAs was abolished, while the polycistronic snoRNA precursor accumulated. In cells lacking functional Rat1p, an exonuclease involved in the processing of both pre-rRNA and intron-encoded snoRNAs, several processing intermediates of the polycistronic precursor accumulated. This allowed for the mapping in the precursor of the presumptive Rnt1p endonucleolytic cuts which provide entry sites for subsequent exonucleolytic trimming of the pre-snoRNAs. In line with known properties of double-stranded RNA-specific RNase III, pairs of Rnt1p cuts map next to each other on opposite strands of long double-helical stems in the secondary structure predicted for the polycistronic snoRNA precursor.

* Corresponding author. Mailing address: Laboratoire de Biologie Moléculaire Eucaryote du CNRS, Université Paul Sabatier, 118 Route de Narbonne, 31062 Toulouse Cédex 04, France. Phone: (33) 5 61 33 59 34. Fax: (33) 5 61 33 58 86. E-mail: bachel{at}ibcg.biotoul.fr.

Molecular and Cellular Biology, February 1999, p. 1144-1158, Vol. 19, No. 2
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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