Abstract
ATP1-111, a suppressor of the slow-growth phenotype of yme1Δ lacking mitochondrial DNA is due to the substitution of phenylalanine for valine at position 111 of the alpha-subunit of mitochondrial ATP synthase (Atp1p in yeast). The suppressing activity of ATP1-111 requires intact beta (Atp2p) and gamma (Atp3p) subunits of mitochondrial ATP synthase, but not the stator stalk subunits b (Atp4p) and OSCP (Atp5p). ATP1-111 and other similarly suppressing mutations in ATP1 and ATP3 increase the growth rate of wild-type strains lacking mitochondrial DNA. These suppressing mutations decrease the growth rate of yeast containing an intact mitochondrial chromosome on media requiring oxidative phosphorylation, but not when grown on fermentable media. Measurement of chronological aging of yeast in culture reveals that ATP1 and ATP3 suppressor alleles in strains that contain mitochondrial DNA are longer lived than the isogenic wild-type strain. In contrast, the chronological life span of yeast cells lacking mitochondrial DNA and containing these mutations is shorter than that of the isogenic wild-type strain. Spore viability of strains bearing ATP1-111 is reduced compared to wild type, although ATP1-111 enhances the survival of spores that lacked mitochondrial DNA.
Similar content being viewed by others
References
Abrahams JP, Leslie AGW, Lutter R, Walker J (1994) Nature (London) 370:621–628
Barros MH, Bandy B, Tahara EB, Kowaltowski AJ (2004) J Biol Chem 279:49883–49888
Brengues M, Pintard L, Lapeyre B (2002) J Biol Chem 277:40505–40512
Buchet K, Godinot C (1998) J Biol Chem 273:22983–22989
Cabezon E, Montgomery MG, Leslie AG, Walker JE (2003) Nat Struct Biol 10:744–750
Camougrand N, Pelissier P, Velours G, Guerin M (1995) J Mol Biol 247:588–596
Campbell CL, Tanaka N, White KH, Thorsness PE (1994) Mol Biol Cell 5:899–905.
Caviston TL, Ketchum CJ, Sorgen PL, Nakamoto RK, Cain BD (1998) FEBS Lett 429:201–206
Chen XJ, Clark-Walker GD (1999) Mol Gen Genet 262:898–908
Chen XJ, Clark-Walker GD (2000) Int Rev Cytol 194:197–238
Choih SJ, Ferro AJ, Shapiro SK (1977) J Bacteriol 131:63–68
Clark-Walker GD, Chen XJ (1996) Mol Gen Genet 252:746–750
Clark-Walker GD, Hansbro PM, Gibson F, Chen XJ (2000) Biochim Biophys Acta 1478:125–137
Croes AF (1967) Planta 76:227–237
Duncan TM, Bulygin VV, Zhou Y, Hutcheon ML, Cross RL (1995) Proc Natl Acad Sci USA 92:10964–10968
Eisler H, Frohlich KU, Heidenreich E (2004) Exp Cell Res 300:345–353
Enns R, Criddle RS (1977) Arch Biochem Biophys 183:742–752
Faye G, Fukuhara H, Grandchamp C, Lazowska J, Michel F, Casey J, Getz G, Locker J, Rabinowitz M, Bolotin-Fukuhara M, Coen D, Deutsch J, Dujon B, Netter P, Slonimski P (1973) Biochimie 55:779–792
Fleury C, Mignotte B, Vayssiere JL (2002) Biochimie 84:131–141
Fox TD, Folley LS, Mulero JJ, McMullin TW, Thorsness PE, Hedin LO, Costanzo MC (1991) Methods Enzymol 194:149–165
Fraga D, Hermolin J, Oldenburg M, Miller MJ, Fillingame RH (1994) J Biol Chem 269:7532–7537
Gaballo A, Zanotti F, Raho G, Papa S (1999) FEBS Lett 463:7–11
Giraud MF, Velours J (1997) Eur J Biochem 245:813–818
Goldring ES, Grossman LI, Krupnick D, Cryer DR, Marmur J (1970) J Mol Biol 52:323–335
Gorsich SW, Shaw JM (2004) Mol Biol Cell 15:4369–4381
Hanekamp T, Thorsness PE (1996) Mol Cell Biol 16:2764–2771
Hartig A, Breitenbach M (1980) Current Genetics 1:97–102
Hartig A, Schroeder R, Mucke E, Breitenbach M (1981) Current Genetics 4:29–36
Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich KU, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004) J Cell Biol 164:501–507
Herman PK, Rine J (1997) Embo J 16:6171–6181
Heslot H, Goffeau A, Louis C (1970) J Bacteriol 104:473–481
Jakubowski W, Bartosz G (1997) Int J Biochem Cell Biol 29:1297–1301
Kominsky DJ, Thorsness PE (2000) Genetics 154:147–154
Kominsky DJ, Brownson MP, Updike D, Thorsness PE (2002) Genetics Society of America
Kono K, Matsunaga R, Hirata A, Suzuki G, Abe M, Ohya Y (2005) Yeast 22:129–139
Kuenzi MT, Tingle MA, Halvorson HO (1974) J Bacteriol 117:80–88
Lai-Zhang J, Mueller DM (2000) Eur J Biochem 267:2409–2418
Langer T, Kaser M, Klanner C, Leonhard K (2001) Biochem Soc Trans 29:431–436
Longo VD, Ellerby LM, Bredesen DE, Valentine JS, Gralla EB (1997) J Cell Biol 137:1581–1588
Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Yeast 14:953–961
Ludovico P, Rodrigues F, Almeida A, Silva MT, Barrientos A, Corte-Real M (2002) Mol Biol Cell 13:2598–2606
Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich KU (1999) J Cell Biol 145:757–767
Mazzoni C, Herker E, Palermo V, Jungwirth H, Eisenberg T, Madeo F, Falcone C (2005) EMBO Rep 6:1076–1081
Miyakawa I, Hiroyuki A, Sando N (1984) J Cell Sci 66:21–38
Mosher ME, White LK, Hermolin J, Fillingame RH (1985) J Biol Chem 260:4807–4814
Muller M, Gumbiowski K, Cherepanov DA, Winkler S, Junge W, Engelbrecht S, Panke O (2004) Eur J Biochem 271:3914–3922
Nagley P, Linnane AW (1970) Biochem Biophys Res Commun 39:989–996
Newlon MC, Hall BD (1978) Mol Gen Genet 165:113–114
Noji H, Yasuda R, Yoshida M, Kinosita K, Jr. (1997) Nature 386:299–302
Olempska-Beer Z (1987) Anal Biochem 164:278–286
Omote H, Sambonmatsu N, Saito K, Sambongi Y, Iwamoto-Kihara A, Yanagida T, Wada Y, Futai M (1999) Proc Natl Acad Sci USA 96:7780–7784
Palleroni NJ (1961) Phyton 16:117–128
Paul M, Velours J, Arselin de Chateaubodeau G, Aigle M, Guerin B (1989) Eur J Biochem 185:163–171
Prescott M, Bush NC, Nagley P, Devenish RJ (1994) Biochem Mol Biol Int 34:789–799
Puglisi PP, Zennaro E (1971) Experientia 27:963–964
Rodgers AJ, Capaldi RA (1998) J Biol Chem 273:29406–29410
Rousseau P, Halvorson HO (1973) Can J Microbiol 19:1311–1318
Sabbert D, Engelbrecht S, Junge W (1996) Nature 381:623–625
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory
Saverese JJ (1974) Canadian Jounal of Microbiology 20:1517–1522
Schulenberg B, Aggeler R, Murray J, Capaldi RA (1999) J Biol Chem 274:34233–34237
Seigel JL, Miller JJ (1971) Can J Microbiol 17:837–845
Seufert W, McGrath JP, Jentsch S (1990) Embo J 9:4535–4541
Shafer KS, Hanekamp T, White KH, Thorsness PE (1999) Curr Genet 36:183–194
Sherman F, Fink GR, Hicks JB (1986) Methods in yeast genetics. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press
Smith CP, Thorsness PE (2005) Eukaryot Cell 4:2078–2086
Soubannier V, Rusconi F, Vaillier J, Arselin G, Chaignepain S, Graves PV, Schmitter JM, Zhang JL, Mueller D, Velours J (1999) Biochemistry 38:15017–15024
Steele DF, Butler CA, Fox TD (1996) Proc Natl Acad Sci USA 93:5253–5257
Temple MD, Perrone GG, Dawes IW (2005) Trends Cell Biol 15:319–326
Thorsness PE, Fox TD (1993) Genetics 134:21–28
Thorsness PE, White KH, Fox TD (1993) Mol Cell Biol 13:5418–5426.
Tingle MA, Kuenzi MT, Halvorson HO (1974) J Bacteriol 117:89–93
Todd RD, Douglas MG (1981) J Biol Chem 256:6984–6989
Treinin M, Simchen G (1993) Curr Genet 23:223–227
Tzagoloff A (1979) Methods Enzymol 55:351–358
Uh M, Jones D, Mueller DM (1990) J Biol Chem 265:19047–19052
Valiyaveetil FI, Fillingame RH (1998) J Biol Chem 273:16241–16247
Van Dyck L, Langer T (1999) Cell Mol Life Sci 56:825–842
Velours J, Arselin de Chateaubodeau G, Galante M, Guerin B (1987) Eur J Biochem 164:579–584
Weber ER, Rooks RS, Shafer KS, Chase JW, Thorsness PE (1995) Genetics 140:435–442
Xiao Y, Metzl M, Mueller DM (2000) J Biol Chem 275:6963–6968
Xu G, West TP (1992) Experientia 48:786–788
Xu T, Zanotti F, Gaballo A, Raho G, Papa S (2000) Eur J Biochem 267:4445–4455
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Francis, B.R., White, K.H. & Thorsness, P.E. Mutations in the Atp1p and Atp3p subunits of yeast ATP synthase differentially affect respiration and fermentation in Saccharomyces cerevisiae . J Bioenerg Biomembr 39, 127–144 (2007). https://doi.org/10.1007/s10863-007-9071-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10863-007-9071-4