Skip to main content
Log in

ATP synthase subunit c/III/9 gene sequences as a tool for interkingdom and metaphytes molecular phylogenies

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

The 38 sequences of the ATPase c/III/9 gene determined in bacteria, fungi, mammals, and higher plants have been used to construct phylogenetic trees by distance matrix and parsimony methods (checked by bootstrapping); alignments have been performed on the deduced amino-acid sequences and then transferred back to the nucleotide sequences. Three lineages stand out: (1) eubacteria (except cyanobacteria and a purple bacteria), (2) chloroplasts, together with cyanobacteria, and (3) mitochondria together with nuclei and α purple bacteria. The clear monophyly of the mitochondrial/nuclear lineage, taken all together, strongly suggests that the nuclear copies of the gene now residing in the eukaryotic nucleus originate from a mitochondrial transfer. Within this lineage, metaphytes emerge late and as a cohesive group, after fungi (as a dispersed group) and metazoa, yielding an order that markedly differs from that obtained through typical RNA nuclear molecules. The possible biphyletic origin of mitochondria based on mitochondrial rRNA sequences is not evidenced by these sequences. Internal branches within both the chloroplastic and the mitochondrial lineages are consistent with botanical evolutionary schemes based on morphological characters. In spite of its relatively small size, the ATPase c/III/9 gene therefore displays remarkable properties as a phylogenetic index and adds a new tool for molecular evolutionary reconstructions, especially within the metaphytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baroin A, Perasso R, Qu L-H, Brugerolle G, Bachellerie J-P, Adoutte A (1988) Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S rRNA. Proc Acad Sci USA 85:3474–3478

    Google Scholar 

  • Bland MM, Levings CS III, Matzinger DF (1986) The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet 204:8–16

    Google Scholar 

  • Bonhomme S, Bird S, Bonen L (1989) Comparison of the wheat mitochondrial ATP9 gene sequence with mitochondrial and chloroplast homologues from other plants. Plant Mol Biol 13: 395–397

    Google Scholar 

  • Brown TA, Ray JA, Waring RB, Scazzocchio C, Davies RW (1984) A mitochondrial reading frame which may code for a second form of ATPase 9 in Aspergillus nidulans. Curr Genet 8:489–492

    Google Scholar 

  • Brusilow WSA, Scarpetta MA, Hawthorne CA, Clark WP (1989) Organization and sequence of the genes coding for the proton-translocating ATPase of Bacillus megaterium. J Biol Chem 264:1528–1533

    Google Scholar 

  • Cedergren R, Gray MW, Abel Y, Sankoff D (1988) The evolutionary relationships among known life forms. J Mol Evol 28:98–112

    Google Scholar 

  • Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666

    Google Scholar 

  • Cozens AL, Walker JE (1987) The organization and sequence of the genes for ATP synthase subunits in thecyanobacterium Synechococcus 6301. Support for an endosymbiotic origin of chloroplasts. J Mol Biol 194:359–383

    Google Scholar 

  • Cummings DJ, McNally KL, Domenico JM, Matsuura ET (1990) The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr Genet 17(5):375–402

    Google Scholar 

  • Denda K, Konishi J, Oshima T, Date T, Yoshida M (1989) A gene encoding the proteolipid subunit of Sulfolobus acidocaldarius ATPase complex. J Biol Chem 264:7119–7121

    Google Scholar 

  • Dewey RE, Schuster AM, Leving CS III Timothy DH (1985) Nucleotide sequence of Fo ATPase proteolipid (subunit 9) gene of maize mitochondria. Proc Natl Acad Sci USA 82: 1015–1019

    Google Scholar 

  • Falk G, Walker JE (1988) DNA sequence of a gene cluster coding for subunits of the 170 membrane sector of ATP synthase in Rhodospirillum rubrum. Biochem J 254:109–122

    Google Scholar 

  • Farrell LB, Nagley P (1987) Human liver cDNA clones encoding proteolipid subunit 9 of the mitochondrial ATPase complex. Biochem Biophys Res Commun 144:1257–1264

    Google Scholar 

  • Futai M, Kanazawa H (1983) Structure and function of protontranslocating adenosine triphosphatase (F0F1). Biochemical and molecular biological approaches. Microbiol Rev 47(3): 285–312

    Google Scholar 

  • Gay NJ, Walker JE (1981) The atp operon. Nucleotide sequence of the promoter and the gene for the membrane protein and the d subunit of Escherichia coli. Nucleic Acids Res 9:3919–3926

    Google Scholar 

  • Gay NJ, Walker JE (1985) Two genes encoding the bovine mitochondrial ATP synthase proteolipid specify precursors with different import sequences and are expressed in a tissuespecific manner. EMBO J 4:3519–3524

    Google Scholar 

  • Gibbs SP (1978) The chloroplasts ofEuglena may have evolved from symbiotic green algae. Can J Bot 56:2883–2889

    Google Scholar 

  • Giovannoni SJ, Turner S, Olsen GL, Barns S, Lane DJ, Pace N (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592

    Google Scholar 

  • Grabau EA, Asleson CM, Hegenbach BG (1990) Nucleotide sequence and transcription of the soybean mitochondrial ATPase subunit 9 gene. Plant Mol Biol 15:183–186

    Google Scholar 

  • Gray MW (1989) The evolutionary origin of organelles. Trends Genet 9(5):294–299

    Google Scholar 

  • Gray MW, Sankoff D, Cedergren RJ (1984) On the evolutionary descent of organisms and organelle: a global phylogeny based on a highly conserved structural core in small subunit rRNA. Nucleic Acids Res 12:5837–5852

    Google Scholar 

  • Gray MW, Cedergren RJ, Abel Y, Sankoff D (1989) On the evolutionary origin of the plant mitochondrion and its genome. Proc Natl Acad Sci USA 86:2267–2271

    Google Scholar 

  • Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662

    Google Scholar 

  • Heywood VH (1978) The flowering plants of the world. Oxford University Press, Oxford

    Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo Y, Honji Y, Sun C, Meng B, Li Y, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194

    Google Scholar 

  • Howe CJ, Auffret AD, Doherty A, Boman CM, Dyer CM, Gray JC (1982) Location and nucleotide sequence of the gene for the proton-translocating subunit of wheat chloroplast ATP synthase. Proc Natl Acad Sci USA 82:6903–6907

    Google Scholar 

  • Hudson GS, Mason JG, Holton TA, Koller B, Cox GB, Whitfeld PR, Bottomley W (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF(1) and three CF(0) subunits of the H(+)-ATP synthase complex and the ribosomal protein S2. J Mol Biol 196:283–298

    Google Scholar 

  • John P (1987) Paracoccus as a free living mitochondrion. Ann NY Acad Sci 503:140–150

    Google Scholar 

  • Kaleikau EK, Andre CP, Walbot V (1990) Sequence of the F0-ATPase proteolipid (atp9) gene from rice mitochondria. Nucleic Acids Res 18:370

    Google Scholar 

  • Kazama S, Suzuki T, Akihama T (1990) Nucleotide sequence of the F0-ATPase subunit 9 gene from tomato mitochondria. Nucleic Acids Res 18:5879

    Google Scholar 

  • Krumbolz LR, Esser U, Simoni RD (1989) Nucleotide sequence of the unc operon of Vibrio alginolyticus. Nucleic Acids Res 17:7993–7994

    Google Scholar 

  • Lambertus AM, Hensgen LA, Grivell LA, Borst P, Bos JL (1979) Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc Natl Acad Sci USA 76:1663–1667

    Google Scholar 

  • Mc-Carn DF, Whitaker RA, Alam J, Vrba JM, Curtis SE (1988) Genes encoding the alpha, gamma, delta, and four F-0 subunits of ATP synthase constitute an operon in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 170:3448–3458

    Google Scholar 

  • Morikami A, Nakamura K (1987) The pea ATPase subunit 9 gene is located upstream of the ATPase a-subunit gene. Nucleic Acids Res 12:4692

    Google Scholar 

  • Nagley P (1988) Eukaryotic membrane genetics: the F0 sector of mitochondrial ATP synthase. Trends Genet 1:46–52

    Google Scholar 

  • Nielsen N, Hansen F, Hoppe J, Friedl P, Meyenburg K (1981) The nucleotide sequences of the atp genes coding for 170 subunit a, b, c and the F1 subunit d of the membrane bound ATPase of Escherichia coli. Mol Gen Genet 184:33–39

    Google Scholar 

  • Nowak C, Kuck U (1990) RNA editing of the mitochondrial atp9 transcript from wheat. Nucleic Acids Res 18:7164

    Google Scholar 

  • Ohta S, Yodha M, Ishizuka M, Hirata H, Hamamoto T, Otawara-Hamamoto Y, Matsuda K, Kagawa Y (1988) Sequence and over expression of subunits of adenosine triphosphate synthase in thermophilic bacterium PS3. Biochem Biophys Acta 933:141–155

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kodchit T, Shirai H, Sano T, Sano S, Umesomo K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inukuchi H, Ozeki H (1986) Chloroplast gene organization deduced from sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574

    Google Scholar 

  • Passavant CW, Hallick RB (1985) Location, nucleotide sequence and expression of the proton-translocating subunit gene of the E. gracilis chloroplast ATP synthase. Plant Mol Biol 4:347–354

    Google Scholar 

  • Perasso R, Baroin A, Adoutte A (1990) The emergence of eukaryotic algae within the protists: a molecular phylogeny based on ribosomal RNA sequencing. Exp Phycol 1:1–19

    Google Scholar 

  • Perasso R, Baroin A, Qu L-H, Bachellerie J-P, Adoutte A (1989) Origin of algae. Nature 339:142–144

    Google Scholar 

  • Pritchard AE, Seilhamer JJ, Mahalingam R, Sable CL, Venuti SE, Cummings DJ (1990) Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Res 18: 178–180

    Google Scholar 

  • Qu LH, Nicholoso M, Bachellerie JP (1988) Phylogenetic calibration of 5′ terminal domain of large rRNA achieved by determining twenty eukaryote sequences. J Mol Evol 28:113–124

    Google Scholar 

  • Recipon H (1990) The sequence of the sunflower mitochondrial ATPase subunit 9 gene. Nucleic Acids Res 18(6):1644

    Google Scholar 

  • Rodermel SR, Bogorad L (1987) Molecular evolution and nucleotide sequences of the maize plastid genes for the alpha subunit of CF1 (atpA) and the proteolipid subunit of CF0 (atpH). Genetics 116(1):127–139

    Google Scholar 

  • Schulte E, Staubach S, Laser B, Kück U (1989) Wheat mitochondrial DNA: organization and sequences of the atpA and atp9 genes. Nucleic Acids Res 17:7531

    Google Scholar 

  • Schuster W, Brennicke A (1989) Conserved sequence elements at putative processing sites in plant mitochondria. Curr Genet 15:187–192

    Google Scholar 

  • Schuster W, Brennicke A (1990) RNA editing of ATPase subunit 9 transcript in Oenothera mitochondria. FEBS Lett 268: 252–256

    Google Scholar 

  • Shavit N (1980) Energy transduction in chloroplasts. Structure and function of the ATPase complex. Annu Rev Biochem 49: 111–138

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuada J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of tobacco chloroplast genome. Its gene organization and expression. EMBO J 5:2043–2049

    Google Scholar 

  • Sogin ML, Elwood H, Gunderson JH (1986) Evolutionary diversity of eukaryotic small subunit rRNA genes. Proc Natl Sci USA 83:1383–1387

    Google Scholar 

  • Sourdis J, Nei M (1988) Relative efficiencies of the maximum parsimony and the distance-matrix methods in obtaining the correct phylogenetic tree. Mol Biol Evol 5:298–311

    Google Scholar 

  • Stewart KD, Mattox KR (1984) The case for a polyphyletic origin of mitochondria: morphological and molecular comparisons. J Mol Evol 21:54–57

    Google Scholar 

  • Strotman H, Bicke L, Sandkötter S (1984) Structure, functions and regulation of chloroplast ATPase. Annu Rev Plant Physiol 35:97–120

    Google Scholar 

  • Thorsness PE, Fox TD (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346:376–379

    Google Scholar 

  • Van der Boogaart P, Samallo J, Agsterible E (1982) Similar gene for a mitochondrial ATPase subunit in the nuclear and mitochondrial genome of Neurospora crassa. Nature 298:187–189

    Google Scholar 

  • Viebrok A, Perz A, Sebald W (1982) The imported preprotein of the proteolipid subunit of the mitochondrial ATP synthase from Neurospora crassa. Molecular cloning and sequencing of the mRNA. EMBO J 1(5):565–571

    Google Scholar 

  • Wahleitner JA, Wolstenholme DR (1988) Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res 16:6897–6913

    Google Scholar 

  • Ward M, Turner G (1986) The ATP synthase subunit 9 gene of Aspergillus nidulans. Sequence and transcription. Mol Gen Genet 205:331–338

    Google Scholar 

  • Wintz H, Skunca M, Pillay DTN (1987) Nucleotide sequence and transcription analysis of the gene coding for subunit III of soybean chloroplast proton-translocating ATPase. Gene 59:47–53

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

  • Xue Y, Thomas CM, Davies DR (1989) Nucleotide sequence and transcription of the sugar beet mitochondrial F0F1-ATPase subunit 9 gene. Nucleic Acids Res 17:8857

    Google Scholar 

  • Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR(1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447

    Google Scholar 

  • Young EG, Hanson MR, Dierks PM (1986) Sequence and transcription analysis of the petunia mitochondrial gene for the ATP synthase proteolipid subunit. Nucleic Acids Res 14:7995–8006

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Recipon, H., Perasso, R., Adoutte, A. et al. ATP synthase subunit c/III/9 gene sequences as a tool for interkingdom and metaphytes molecular phylogenies. J Mol Evol 34, 292–303 (1992). https://doi.org/10.1007/BF00160236

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160236

Key words

Navigation