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Current Genetics

, Volume 48, Issue 4, pp 235–246 | Cite as

The YJR127C/ZMS1 gene product is involved in glycerol-based respiratory growth of the yeast Saccharomyces cerevisiae

  • Lin Lu
  • George G. Roberts
  • Cynthia Oszust
  • Alan P. HudsonEmail author
Research Article

Abstract

A putative yeast mitochondrial upstream activating sequence (UAS) was used in a one-hybrid screening procedure that identified the YJR127C ORF on chromosome X. This gene was previously designated ZMS1 and is listed as a transcription factor on the SGD website. Real time RT-PCR assays showed that expression of YJR127C/ZMS1 was glucose-repressible, and a deletion mutant for the gene showed a growth defect on glycerol-based but not on glucose- or ethanol-based medium. Real time RT-PCR analyses identified severely attenuated transcript levels from GUT1 and GUT2 to be the source of that growth defect, the products of GUT1 and GUT2 are required for glycerol utilization. mRNA levels from a large group of mitochondria- and respiration-related nuclear genes also were shown to be attenuated in the deletion mutant. Importantly, transcript levels from the mitochondrial OLI1 gene, which has an associated organellar UAS, were attenuated in the ΔYJR127C mutant during glycerol-based growth, but those from COX3 (OXI2), which lacks an associated mitochondrial UAS, were not. Transcriptome analysis of the glycerol-grown deletion mutant showed that genes in several metabolic and other categories are affected by loss of this gene product, including protein transport, signal transduction, and others. Thus, the product of YJR127C/ZMS1 is involved in transcriptional control for genes in both cellular genetic compartments, many of which specify products required for glycerol-based growth, respiration, and other functions.

Keywords

Respiration Mitochondria Transcriptional control Mitochondrial DNA 

Notes

Acknowledgments

This work was supported by a Merit Review to A.P.H. from the Dept. Veterans Affairs Medical Research Service, and by a REAP Award from the same source to A.P.H. and other investigators at the Detroit D.V.A. Medical Center. We are grateful to Dr. P. James for supplying the pGAD library used in the original one-hybrid screening procedure, and to Drs. N. Davis and J. Hegemann for supplying plasmids used in experiments described here. We thank Dr. J.A. Whittum-Hudson for use of her Nikon E-600 microscope.

Supplementary material

294_2005_23_MOESM1_ESM.pdf (194 kb)
Supplementary material

References

  1. Adrian GS, McCammon MT, Montgomery DL, Douglas MG (1986) Sequences required for delivery and localization of the ADP/ATP translocator to the mitochondrial inner membrane. Mol Cell Biol 6(2):626–634PubMedGoogle Scholar
  2. Clayton DA (2000) Transcription and replication of mitochondrial DNA. Hum Reprod 15(suppl 2):11–17CrossRefPubMedGoogle Scholar
  3. Coppee JU, Rieger KJ, Kaniak A, di Rago JP, Groundinsky O, Slonimski P (1996) PetCR46, a gene which is essential for respiration and integrity of the mitochondrial genome. Yeast 12:577–582CrossRefPubMedGoogle Scholar
  4. Fromont-Racine M, Rain JC, Legrain P (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 16:277–282CrossRefPubMedGoogle Scholar
  5. Gérard HC, Freise J, Rudy D, Krauß-Opatz B, Köhler L, Zeidler H, Schumacher HR, Whittum-Hudson JA, Hudson AP (2002) Chlamydia trachomatis genes whose products are related to energy metabolism are expressed differentially in active vs. persistent infection. Microb Infect 4:13–22CrossRefGoogle Scholar
  6. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391CrossRefPubMedGoogle Scholar
  7. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Hohnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:546–567CrossRefPubMedGoogle Scholar
  8. Gonzalez E, Fernandez MR, Larroy C, Sola L, Pericas MA, Pares X, Biosca JA (2000) Characterization of a (2R,3R)-2,3-butanediol dehydrogenase as the Saccharomyces cerevisiae YAL060W gene product. Disruption and induction of the gene. J Biol Chem 275:35876–35885Google Scholar
  9. Grabowska D, Chelstowska A (2003) The ALD6 gene product is indispensable for providing NADPH in yeast cells lacking glucose-6-phosphate dehydrogenase activity. J Biol Chem 278:13984–13988CrossRefPubMedGoogle Scholar
  10. Grauslund M, Lopes JM, Rønnow B (1999) Expression of GUT1, which encodes glycerol kinase in Saccharomyces cerevisiae, is controlled by the positive regulators Adf1p, Ino2p and Ino4p and the negative regulator Opi1; in a carbon source-dependent fashion. Nucl Acids Res 27:4391–4398CrossRefPubMedGoogle Scholar
  11. Gurvitz A, Hartig A, Ruis H, Hamilton B, de Couet HG (2002) Preliminary characterisation of DML1, an essential Saccharomyces cerevisiae gene related to misato of Drosophila melanogaster. FEMS Yeast Res 2:123–35CrossRefPubMedGoogle Scholar
  12. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne J-B, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104CrossRefPubMedGoogle Scholar
  13. Heinisch JJ, Muller S, Schluter E, Jacoby J, Rodicio R (1998) Investigation of two yeast genes encoding putative isoenzymes of phosphoglycerate mutase. Yeast 14:203–213CrossRefPubMedGoogle Scholar
  14. van Helden J, Andre B, Collado-Vides J (1998) Extracting regulatory sites from the upstream region of yeast genes by computational analysis of oligonucleotide frequencies. J Mol Biol 281:827–841CrossRefPubMedGoogle Scholar
  15. Hiratsuka M, Agatsuma Y, Mizugaki M (1999) Rapid detection of CYP2C9*3 alleles by real time fluorescence PCR based on SYBR green. Mol Genet Metabol 68:357–362CrossRefGoogle Scholar
  16. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, Yang L, Wolting C, Donaldson I, Schandorff S, Shewnarane J, Vo M, Taggart J, Goudreault M, Muskat B, Alfarano C, Dewar D, Lin Z, Michalickova K, Willems AR, Sassi H, Nielsen PA, Rasmussen KJ, Andersen JR, Johansen LE, Hansen LH, Jespersen H, Podtelejnikov A, Nielsen E, Crawford J, Poulsen V, Sorensen BD, Matthiesen J, Hendrickson RC, Gleeson F, Pawson T, Moran MF, Durocher D, Mann M, Hogue CW, Figeys D, Tyers M (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectroscopy. Nature 415:180–183CrossRefPubMedGoogle Scholar
  17. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O’Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425:686–691CrossRefPubMedGoogle Scholar
  18. Iqbal J, Rahman MU, Gérard HC, Yu J, Nevel CA, Hudson AP (1996) A probable cis-regulatory element on yeast mitochondrial DNA responsible for cAMP-dependent transcription. Curr Genet 30:493–501CrossRefPubMedGoogle Scholar
  19. Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168PubMedGoogle Scholar
  20. Kumar A, Agarwal S, Heyman JA, Matson S, Heidtman M, Piccirillo S, Umansky L, Drawid A, Jansen R, Liu Y, Cheung KH, Miller P, Gerstein M, Roeder GS, Snyder M (2002) Subcellular localization of the yeast proteome. Gen Dev 16:707–719CrossRefGoogle Scholar
  21. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, Gerber GK, Hannet NM, Harbison CT, Thompson CM, Simon I, Zeitlinger J, Jennings EG, Murray HL, Gordon DB, Ren B, Wyrick JJ, Tagne J-B, Volkert TL, Fraenkel E, Gifford DK, Young RA (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298:799–804CrossRefPubMedGoogle Scholar
  22. Lu L, Roberts G, Simon KW, Yu J, Hudson AP (2003). Rsf1p, a nuclear gene product required for respiratory growth of Saccharomyces cerevisiae. Curr Genet 43:263–272CrossRefPubMedGoogle Scholar
  23. McEntee CM, Hudson AP (1989) Preparation of RNA from unspheroplasted yeast cells (Saccharomyces cerevisiae). Anal Biochem 176:303–306CrossRefPubMedGoogle Scholar
  24. McEntee CM, Cantwell R, Rahman MU, Hudson AP (1993) Transcription of the yeast mitochondrial genome requires cAMP. Mol Gen Genet 241:213–224CrossRefPubMedGoogle Scholar
  25. Muhlenhoff U, Stadler JA, Richhardt N, Seubert A, Eickhorst T, Schweyen RJ, Lill R, Wiesenberger G (2003) A specific role of the yeast mitochondrial carriers MRS3/4p in mitochondrial iron acquisition under iron-limiting conditions. J Biol Chem 278(42):40612–40620CrossRefPubMedGoogle Scholar
  26. Pavlik P, Simon M, Schuster T, Ruis H (1993) The glycerol kinase (GUT1) gene of Saccharomyces cerevisiae: cloning and characterization. Curr Genet 24:21–25CrossRefPubMedGoogle Scholar
  27. Ptashne M, Gann A (2001) Transcription initiation: imposing specificity by localization. Essays Biochem 37:1–15PubMedGoogle Scholar
  28. Rahman MU, Hudson AP (1995a) Nature and transcriptional role of catalytic subunits of yeast mitochondrial cAMP-dependent protein kinase (Saccharomyces cerevisiae). Biochem Biophys Res Commun 206:756–763CrossRefPubMedGoogle Scholar
  29. Rahman MU, Hudson AP (1995b) Substrates for yeast mitochondrial cAMP-dependent protein kinase activity. Biochem Biophys Res Commun 214:188–194CrossRefPubMedGoogle Scholar
  30. Rahman MU, Kleyman TR, McEntee CM, Hudson AP (1994) Regulation of mitochondrial cAMP-dependent protein kinase activity in yeast. Biochem Mol Biol Int 34:745–753PubMedGoogle Scholar
  31. Rønnow B, Kielland-Brandt MC (1993) GUT2, a gene for mitochondrial glycerol-3-phosphate dehydrogenase of Saccharomyces cerevisiae. Yeast 9:1121–1130CrossRefPubMedGoogle Scholar
  32. Sherman F (1991) Getting started with yeast. Guthrie C, Fink GR (eds) In: Guide to yeast genetics and molecular biology. Meth Enzymol 194:3–21Google Scholar
  33. Srinivasan S, Seaman M, Nemoto Y, Daniell L, Suchy SF, Emr S, DeCa D, Nussbaum R (1997) Disruption of three phosphatidylinositol-polyphosphate 5-phosphatase genes in Saccharomyces cerevisiae results in pleiotropic abnormalities of vacuole morphology, cell shape, and osmohomeostasis. Eur J Cell Biol 74:350–360PubMedGoogle Scholar
  34. Uetz, P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwin B, Conover D, Kalbfleisch T, Vihayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623–627CrossRefPubMedGoogle Scholar
  35. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Veronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen P, Johnston M, Davis RW (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901–906CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Lin Lu
    • 1
  • George G. Roberts
    • 1
  • Cynthia Oszust
    • 1
  • Alan P. Hudson
    • 1
    • 2
    Email author
  1. 1.Department of Immunology and MicrobiologyWayne State University School of MedicineDetroitUSA
  2. 2.Department of Veterans Affairs Medical CenterMedical Research ServiceDetroitUSA

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