Transcriptional collision between convergent genes in budding yeast

Transcriptional interference between genes and the regulatory elements of simple eukaryotes such as Saccharomyces cerevisiae is an unavoidable consequence of their compressed genetic arrangement. We have shown previously that with the tandem arranged genes GAL10 and GAL7, inefficient transcriptional termination of the upstream gene inhibits initiation of transcription on the downstream gene. We now show that transcriptional interference can occur also with S. cerevisiae RNA polymerase II genes arranged convergently. We demonstrate that when the GAL10 and GAL7 genes are rearranged in a convergent orientation, transcriptional initiation occurs at full levels. However, as soon as the two transcripts begin to overlap, elongation is restricted, resulting in a severe reduction in steady-state mRNA accumulation. This effect is observed only in cis arrangement, arguing against RNA-interference effects acting on the potential generation of antisense transcripts. These data reinforce the necessity of separating adjacent RNA polymerase II transcription units by efficient termination signals.

[1]  N. Proudfoot,et al.  Balancing transcriptional interference and initiation on the GAL7 promoter of Saccharomyces cerevisiae. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[2]  S. Kruglyak,et al.  Regulation of adjacent yeast genes. , 2000, Trends in genetics : TIG.

[3]  J. Pérez-Ortín,et al.  Transcriptional and Structural Study of a Region of Two Convergent Overlapping Yeast Genes , 1999, Current Microbiology.

[4]  Grant J. Jensen,et al.  Yeast RNA Polymerase II at 5 Å Resolution , 1999, Cell.

[5]  G. Jensen,et al.  Electron Crystal Structure of an RNA Polymerase II Transcription Elongation Complex , 1999, Cell.

[6]  Jing Zhao,et al.  Formation of mRNA 3′ Ends in Eukaryotes: Mechanism, Regulation, and Interrelationships with Other Steps in mRNA Synthesis , 1999, Microbiology and Molecular Biology Reviews.

[7]  J. Pérez-Ortín,et al.  The yeast FBP1 poly(A) signal functions in both orientations and overlaps with a gene promoter. , 1998, Nucleic acids research.

[8]  N. Proudfoot,et al.  Poly(A) signals control both transcriptional termination and initiation between the tandem GAL10 and GAL7 genes of Saccharomyces cerevisiae , 1998, The EMBO journal.

[9]  N. Proudfoot,et al.  Nascent transcription from the nmt1 and nmt2 genes of Schizosaccharomyces pombe overlaps neighbouring genes , 1998, The EMBO journal.

[10]  L. Minvielle-Sebastia,et al.  Coupling termination of transcription to messenger RNA maturation in yeast. , 1998, Science.

[11]  M. D. Del Olmo,et al.  Transcription termination downstream of the Saccharomyces cerevisiae FBP1 [changed from FPB1] poly(A) site does not depend on efficient 3'end processing. , 1998, RNA.

[12]  C. Springer,et al.  The Adjacent Yeast Genes ARO4 and HIS7Carry No Intergenic Region* , 1997, The Journal of Biological Chemistry.

[13]  N. Proudfoot,et al.  Transcriptional termination signals for RNA polymerase II in fission yeast , 1997, The EMBO journal.

[14]  B. Dujon.  The yeast genome project: what did we learn? , 1996, Trends in genetics : TIG.

[15]  M. Aigle,et al.  Complete DNA sequence of yeast chromosome II. , 1994, The EMBO journal.

[16]  D. Atkins,et al.  Antisense gene expression in yeast. , 1994, Biological chemistry Hoppe-Seyler.

[17]  F. Thoma,et al.  Transcription through the yeast origin of replication ARS1 ends at the ABFI binding site and affects extrachromosomal maintenance of minichromosomes. , 1994, Nucleic acids research.

[18]  A. Myers,et al.  Functional analysis of mRNA 3' end formation signals in the convergent and overlapping transcription units of the S. cerevisiae genes RHO1 and MRP2. , 1993, Nucleic acids research.

[19]  Elaine A. Ostrander,et al.  Local domains of supercoiling activate a eukaryotic promoter in vivo , 1993, Nature.

[20]  A. Nicolas,et al.  The Saccharomyces cerevisiae ARG4 initiator of meiotic gene conversion and its associated double-strand DNA breaks can be inhibited by transcriptional interference. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Elder,et al.  Complementary transcripts from two genes necessary for normal meiosis in the yeast Saccharomyces cerevisiae , 1990, Molecular and cellular biology.

[22]  A. Varshavsky,et al.  The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein , 1989, Nature.

[23]  L. Guarente,et al.  Mutational analysis of a yeast transcriptional terminator , 1989 .

[24]  Y. Tsao,et al.  Transcription-driven supercoiling of DNA: Direct biochemical evidence from in vitro studies , 1989, Cell.

[25]  G. Giaever,et al.  Supercoiling of intracellular DNA can occur in eukaryotic cells , 1988, Cell.

[26]  R. W. Davis,et al.  Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae , 1988, Molecular and cellular biology.

[27]  J. Wang,et al.  Supercoiling of the DNA template during transcription. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[28]  K. Bloom,et al.  Genetic manipulation of centromere function , 1987, Molecular and cellular biology.

[29]  L. Johnston,et al.  Molecular characterisation of the DNA ligase gene, CDC17, from the fission yeast Schizosaccharomyces pombe. , 1987, European journal of biochemistry.