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. 1995 Jul;140(3):945–956. doi: 10.1093/genetics/140.3.945

Rtm1: A Member of a New Family of Telomeric Repeated Genes in Yeast

F Ness 1, M Aigle 1
PMCID: PMC1206678  PMID: 7672593

Abstract

We have isolated a new yeast gene called RTM1 whose overexpression confers resistance to the toxicity of molasses. The RTM1 gene encodes a hydrophobic 34-kD protein that contains seven potential transmembrane-spanning segments. Analysis of a series of industrial strains shows that the sequence is present in multiple copies and in variable locations in the genome. RTM loci are always physically associated with SUC telomeric loci. The SUC-RTM sequences are located between X and Y' subtelomeric sequences at chromosome ends. Surprisingly RTM sequences are not detected in the laboratory strain X2180. The lack of this sequence is associated with the absence of any SUC telomeric gene previously described. This observation raises the question of the origin of this nonessential gene. The particular subtelomeric position might explain the SUC-RTM sequence amplification observed in the genome of yeasts used in industrial biomass or ethanol production with molasses as substrate. This SUC-RTM sequence dispersion seems to be a good example of genomic rearrangement playing a role in evolution and environmental adaptation in these industrial yeasts.

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Selected References

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  1. Adams J., Puskas-Rozsa S., Simlar J., Wilke C. M. Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae. Curr Genet. 1992 Jul;22(1):13–19. doi: 10.1007/BF00351736. [DOI] [PubMed] [Google Scholar]
  2. Bennetzen J. L., Hall B. D. The primary structure of the Saccharomyces cerevisiae gene for alcohol dehydrogenase. J Biol Chem. 1982 Mar 25;257(6):3018–3025. [PubMed] [Google Scholar]
  3. Bonneaud N., Ozier-Kalogeropoulos O., Li G. Y., Labouesse M., Minvielle-Sebastia L., Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast. 1991 Aug-Sep;7(6):609–615. doi: 10.1002/yea.320070609. [DOI] [PubMed] [Google Scholar]
  4. Burkholder A. C., Hartwell L. H. The yeast alpha-factor receptor: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res. 1985 Dec 9;13(23):8463–8475. doi: 10.1093/nar/13.23.8463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Button L. L., Astell C. R. The Saccharomyces cerevisiae chromosome III left telomere has a type X, but not a type Y', ARS region. Mol Cell Biol. 1986 Apr;6(4):1352–1356. doi: 10.1128/mcb.6.4.1352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carle G. F., Olson M. V. An electrophoretic karyotype for yeast. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3756–3760. doi: 10.1073/pnas.82.11.3756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlson M., Botstein D. Organization of the SUC gene family in Saccharomyces. Mol Cell Biol. 1983 Mar;3(3):351–359. doi: 10.1128/mcb.3.3.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  9. Carlson M., Celenza J. L., Eng F. J. Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol. 1985 Nov;5(11):2894–2902. doi: 10.1128/mcb.5.11.2894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carlson M., Osmond B. C., Botstein D. Genetic evidence for a silent SUC gene in yeast. Genetics. 1981 May;98(1):41–54. doi: 10.1093/genetics/98.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chan C. S., Tye B. K. Organization of DNA sequences and replication origins at yeast telomeres. Cell. 1983 Jun;33(2):563–573. doi: 10.1016/0092-8674(83)90437-3. [DOI] [PubMed] [Google Scholar]
  12. Charron M. J., Read E., Haut S. R., Michels C. A. Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Genetics. 1989 Jun;122(2):307–316. doi: 10.1093/genetics/122.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Crouzet M., Urdaci M., Dulau L., Aigle M. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene. Yeast. 1991 Oct;7(7):727–743. doi: 10.1002/yea.320070708. [DOI] [PubMed] [Google Scholar]
  14. Dohlman H. G., Thorner J., Caron M. G., Lefkowitz R. J. Model systems for the study of seven-transmembrane-segment receptors. Annu Rev Biochem. 1991;60:653–688. doi: 10.1146/annurev.bi.60.070191.003253. [DOI] [PubMed] [Google Scholar]
  15. Doignon F., Aigle M., Ribereau-Gayon P. Resistance to imidazoles and triazoles in Saccharomyces cerevisiae as a new dominant marker. Plasmid. 1993 Nov;30(3):224–233. doi: 10.1006/plas.1993.1054. [DOI] [PubMed] [Google Scholar]
  16. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
  17. Gottesman M. M., Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem. 1993;62:385–427. doi: 10.1146/annurev.bi.62.070193.002125. [DOI] [PubMed] [Google Scholar]
  18. Gottschling D. E., Aparicio O. M., Billington B. L., Zakian V. A. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990 Nov 16;63(4):751–762. doi: 10.1016/0092-8674(90)90141-z. [DOI] [PubMed] [Google Scholar]
  19. Gömpel-Klein P., Brendel M. Allelism of SNQ1 and ATR1, genes of the yeast Saccharomyces cerevisiae required for controlling sensitivity to 4-nitroquinoline-N-oxide and aminotriazole. Curr Genet. 1990 Jul;18(1):93–96. doi: 10.1007/BF00321122. [DOI] [PubMed] [Google Scholar]
  20. Hagen D. C., McCaffrey G., Sprague G. F., Jr Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1418–1422. doi: 10.1073/pnas.83.5.1418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Higgins C. F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. doi: 10.1146/annurev.cb.08.110192.000435. [DOI] [PubMed] [Google Scholar]
  22. Jäger D., Philippsen P. Many yeast chromosomes lack the telomere-specific Y' sequence. Mol Cell Biol. 1989 Dec;9(12):5754–5757. doi: 10.1128/mcb.9.12.5754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kanazawa S., Driscoll M., Struhl K. ATR1, a Saccharomyces cerevisiae gene encoding a transmembrane protein required for aminotriazole resistance. Mol Cell Biol. 1988 Feb;8(2):664–673. doi: 10.1128/mcb.8.2.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Karin M., Najarian R., Haslinger A., Valenzuela P., Welch J., Fogel S. Primary structure and transcription of an amplified genetic locus: the CUP1 locus of yeast. Proc Natl Acad Sci U S A. 1984 Jan;81(2):337–341. doi: 10.1073/pnas.81.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kuchler K., Sterne R. E., Thorner J. Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells. EMBO J. 1989 Dec 20;8(13):3973–3984. doi: 10.1002/j.1460-2075.1989.tb08580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leppert G., McDevitt R., Falco S. C., Van Dyk T. K., Ficke M. B., Golin J. Cloning by gene amplification of two loci conferring multiple drug resistance in Saccharomyces. Genetics. 1990 May;125(1):13–20. doi: 10.1093/genetics/125.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Louis E. J., Haber J. E. Mitotic recombination among subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1990 Mar;124(3):547–559. doi: 10.1093/genetics/124.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Louis E. J., Haber J. E. The structure and evolution of subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1992 Jul;131(3):559–574. doi: 10.1093/genetics/131.3.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Louis E. J., Haber J. E. The subtelomeric Y' repeat family in Saccharomyces cerevisiae: an experimental system for repeated sequence evolution. Genetics. 1990 Mar;124(3):533–545. doi: 10.1093/genetics/124.3.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Louis E. J., Naumova E. S., Lee A., Naumov G., Haber J. E. The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. Genetics. 1994 Mar;136(3):789–802. doi: 10.1093/genetics/136.3.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Marger M. D., Saier M. H., Jr A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 1993 Jan;18(1):13–20. doi: 10.1016/0968-0004(93)90081-w. [DOI] [PubMed] [Google Scholar]
  32. McGrath J. P., Varshavsky A. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature. 1989 Aug 3;340(6232):400–404. doi: 10.1038/340400a0. [DOI] [PubMed] [Google Scholar]
  33. Michels C. A., Read E., Nat K., Charron M. J. The telomere-associated MAL3 locus of Saccharomyces is a tandem array of repeated genes. Yeast. 1992 Aug;8(8):655–665. doi: 10.1002/yea.320080809. [DOI] [PubMed] [Google Scholar]
  34. Naumov G. I., Naumova E. S., Lantto R. A., Louis E. J., Korhola M. Genetic homology between Saccharomyces cerevisiae and its sibling species S. paradoxus and S. bayanus: electrophoretic karyotypes. Yeast. 1992 Aug;8(8):599–612. doi: 10.1002/yea.320080804. [DOI] [PubMed] [Google Scholar]
  35. Naumov G., Naumova E., Turakainen H., Suominen P., Korhola M. Polymeric genes MEL8, MEL9 and MEL10--new members of alpha-galactosidase gene family in Saccharomyces cerevisiae. Curr Genet. 1991 Sep;20(4):269–276. doi: 10.1007/BF00318514. [DOI] [PubMed] [Google Scholar]
  36. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  37. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sharp P. M., Cowe E. Synonymous codon usage in Saccharomyces cerevisiae. Yeast. 1991 Oct;7(7):657–678. doi: 10.1002/yea.320070702. [DOI] [PubMed] [Google Scholar]
  39. Szostak J. W., Blackburn E. H. Cloning yeast telomeres on linear plasmid vectors. Cell. 1982 May;29(1):245–255. doi: 10.1016/0092-8674(82)90109-x. [DOI] [PubMed] [Google Scholar]
  40. Turakainen H., Kristo P., Korhola M. Consideration of the evolution of the Saccharomyces cerevisiae MEL gene family on the basis of the nucleotide sequences of the genes and their flanking regions. Yeast. 1994 Dec;10(12):1559–1568. doi: 10.1002/yea.320101205. [DOI] [PubMed] [Google Scholar]
  41. Turakainen H., Naumov G., Naumova E., Korhola M. Physical mapping of the MEL gene family in Saccharomyces cerevisiae. Curr Genet. 1993 Dec;24(6):461–464. doi: 10.1007/BF00351706. [DOI] [PubMed] [Google Scholar]
  42. Walmsley R. W., Chan C. S., Tye B. K., Petes T. D. Unusual DNA sequences associated with the ends of yeast chromosomes. Nature. 1984 Jul 12;310(5973):157–160. doi: 10.1038/310157a0. [DOI] [PubMed] [Google Scholar]
  43. Welch J. W., Fogel S., Cathala G., Karin M. Industrial yeasts display tandem gene iteration at the CUP1 region. Mol Cell Biol. 1983 Aug;3(8):1353–1361. doi: 10.1128/mcb.3.8.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zaret K. S., Sherman F. DNA sequence required for efficient transcription termination in yeast. Cell. 1982 Mar;28(3):563–573. doi: 10.1016/0092-8674(82)90211-2. [DOI] [PubMed] [Google Scholar]

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