Transcriptional Collision Between Convergent Genes in Budding Yeast

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Jun 22

PMID 12077310

Citations 148

Authors

Elizabeth M Prescott

Nick J Proudfoot

Affiliations

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Abstract

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.

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References

McGrath J, Varshavsky A . The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature. 1989; 340(6232):400-4. DOI: 10.1038/340400a0. View

Osborne B, Guarente L . Mutational analysis of a yeast transcriptional terminator. Proc Natl Acad Sci U S A. 1989; 86(11):4097-101. PMC: 287396. DOI: 10.1073/pnas.86.11.4097. View

Rocco V, de Massy B, Nicolas A . The Saccharomyces cerevisiae ARG4 initiator of meiotic gene conversion and its associated double-strand DNA breaks can be inhibited by transcriptional interference. Proc Natl Acad Sci U S A. 1992; 89(24):12068-72. PMC: 50699. DOI: 10.1073/pnas.89.24.12068. View

Dunaway M, Ostrander E . Local domains of supercoiling activate a eukaryotic promoter in vivo. Nature. 1993; 361(6414):746-8. DOI: 10.1038/361746a0. View

Peterson J, Myers A . Functional analysis of mRNA 3' end formation signals in the convergent and overlapping transcription units of the S. cerevisiae genes RHO1 and MRP2. Nucleic Acids Res. 1993; 21(23):5500-8. PMC: 310593. DOI: 10.1093/nar/21.23.5500. View

Tanaka S, Halter D, Reszel B, Thoma F . Transcription through the yeast origin of replication ARS1 ends at the ABFI binding site and affects extrachromosomal maintenance of minichromosomes. Nucleic Acids Res. 1994; 22(19):3904-10. PMC: 308387. DOI: 10.1093/nar/22.19.3904. View

Feldmann H, Aigle M, ALJINOVIC G, Andre B, Baclet M, Barthe C . Complete DNA sequence of yeast chromosome II. EMBO J. 1994; 13(24):5795-809. PMC: 395553. DOI: 10.1002/j.1460-2075.1994.tb06923.x. View

Atkins D, Arndt G, Izant J . Antisense gene expression in yeast. Biol Chem Hoppe Seyler. 1994; 375(11):721-9. DOI: 10.1515/bchm3.1994.375.11.721. View

Dujon B . The yeast genome project: what did we learn?. Trends Genet. 1996; 12(7):263-70. DOI: 10.1016/0168-9525(96)10027-5. View

10.

Birse C, Lee B, Hansen K, Proudfoot N . Transcriptional termination signals for RNA polymerase II in fission yeast. EMBO J. 1997; 16(12):3633-43. PMC: 1169987. DOI: 10.1093/emboj/16.12.3633. View

11.

Springer C, Valerius O, Strittmatter A, Braus G . The adjacent yeast genes ARO4 and HIS7 carry no intergenic region. J Biol Chem. 1997; 272(42):26318-24. DOI: 10.1074/jbc.272.42.26318. View

12.

Aranda A, Perez-Ortin J, Moore C, del Olmo M . Transcription termination downstream of the Saccharomyces cerevisiae FBP1 [changed from FPB1] poly(A) site does not depend on efficient 3'end processing. RNA. 1998; 4(3):303-18. PMC: 1369619. View

13.

Birse C, Lee B, Keller W, Proudfoot N . Coupling termination of transcription to messenger RNA maturation in yeast. Science. 1998; 280(5361):298-301. DOI: 10.1126/science.280.5361.298. View

14.

Hansen K, Birse C, Proudfoot N . Nascent transcription from the nmt1 and nmt2 genes of Schizosaccharomyces pombe overlaps neighbouring genes. EMBO J. 1998; 17(11):3066-77. PMC: 1170646. DOI: 10.1093/emboj/17.11.3066. View

15.

Greger I, Proudfoot N . Poly(A) signals control both transcriptional termination and initiation between the tandem GAL10 and GAL7 genes of Saccharomyces cerevisiae. EMBO J. 1998; 17(16):4771-9. PMC: 1170806. DOI: 10.1093/emboj/17.16.4771. View

16.

Aranda A, Perez-Ortin J, Moore C, Del Olmo M . The yeast FBP1 poly(A) signal functions in both orientations and overlaps with a gene promoter. Nucleic Acids Res. 1998; 26(20):4588-96. PMC: 147910. DOI: 10.1093/nar/26.20.4588. View

17.

Zhao J, Hyman L, Moore C . Formation of mRNA 3' ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev. 1999; 63(2):405-45. PMC: 98971. DOI: 10.1128/MMBR.63.2.405-445.1999. View

18.

Poglitsch C, Meredith G, Gnatt A, Jensen G, Chang W, Fu J . Electron crystal structure of an RNA polymerase II transcription elongation complex. Cell. 1999; 98(6):791-8. DOI: 10.1016/s0092-8674(00)81513-5. View

19.

Fu J, Gnatt A, Bushnell D, Jensen G, Thompson N, Burgess R . Yeast RNA polymerase II at 5 A resolution. Cell. 1999; 98(6):799-810. DOI: 10.1016/s0092-8674(00)81514-7. View

20.

Puig S, Perez-Ortin J, Matallana E . Transcriptional and structural study of a region of two convergent overlapping yeast genes. Curr Microbiol. 1999; 39(6):369-0373. DOI: 10.1007/s002849900474. View