Plant Molecular Biology

, Volume 56, Issue 6, pp 947–957 | Cite as

Gamma carbonic anhydrase like complex interact with plant mitochondrial complex I

  • Mariano Perales
  • Gustavo Parisi
  • María Silvina Fornasari
  • Alejandro Colaneri
  • Fernando Villarreal
  • Nahuel González-Schain
  • Julián Echave
  • Diego Gómez-Casati
  • Hans-Peter Braun
  • Alejandro Araya
  • Eduardo Zabaleta
Article

Abstract

We report the identification by two hybrid screens of two novel similar proteins, called Arabidopsis thaliana gamma carbonic anhydrase like1 and 2 (AtγCAL1 and AtγCAL2), that interact specifically with putative Arabidopsis thaliana gamma Carbonic Anhydrase (AtγCA) proteins in plant mitochondria. The interaction region that was located in the N-terminal 150 amino acids of mature AtγCA and AtγCA like proteins represents a new interaction domain. In vitro experiments indicate that these proteins are imported into mitochondria and are associated with mitochondrial complex I as AtγCAs. All plant species analyzed contain both AtγCA and AtγCAL sequences indicating that these genes were conserved throughout plant evolution. Structural modeling of AtγCAL sequences show a deviation of functionally important active site residues with respect to γCAs but could form active interfaces in the interaction with AtγCAs. We postulate a CA complex tightly associated to plant mitochondrial complex.

Keywords

Complex I Gamma carbonic anhydrase plant mitochondria respiratory chain 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alber, B.E., Ferry, J.G. 1994A carbonic anhydrase from the archaeon Methanosarcina thermophilaProc. Natl. Acad. Sci. USA9169096913Google Scholar
  2. Badger, M.R., Price, G.D. 2003CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolutionJ. Exp. Bot.54609622Google Scholar
  3. Busi, M.V., Bustamante, C., D’Angelo, M.C., Hidalgo-Cuevas, M., Boggio, M., Valle, E., Zabaleta, E. 2003MADS box expressed during tomato seed and fruit developmentPlant Mol. Biol.54801815Google Scholar
  4. Combet, C., Blanchet, C., Geourjon, C., Deleage, G. 2000NPS@: network protein sequence analysisTrends Biochem. Sci.25147150Google Scholar
  5. Cuff, J.A., Birney, E., Clamp, M., Barton, G. 2000ProtEST: protein multiple sequence alignments from expressed sequence tagsBioinformatics16111116Google Scholar
  6. Eubel, H., Jänsch, L., Braun, H.-P. 2003New Insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex IIPlant Physiol.133274286Google Scholar
  7. Eubel, H., Heinemeyer, J., Braun, H.-P. 2004Identification and characterization of respirosome in potato mitochondriaPlant Physiol.13414501459Google Scholar
  8. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, Univ. of Washington, SeatleGoogle Scholar
  9. Ferraroni, M., Tilli, S., Briganti, F., Chegwidden, W., Supuran, C., Wiebauer, K., Tashian, R., Scozzafava, A. 2002Crystal structure of a zinc-activated variant of human carbonic anhydrase I, CA I Michigan 1: evidence for a second zinc binding site involving arginine coordinationBiochemistry4162376244Google Scholar
  10. Gietz, D., St Jean, A., Woods, A., Schiesti, R. 1992Improved method for high efficiency transformation of intact yeast cellsNucl. Acids Res.201425Google Scholar
  11. Heazlewood, J.L., Howell, K., Millar, A.H. 2003Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plantspecific subunitsBiochim. Biophys. Acta1604159169Google Scholar
  12. Herz, U., Schroder, W., Liddell, A., Leaver, C.J., Brennicke, A., Grohmann, L. 1994Purification of the NADH:ubiquinone oxidoreductase (complex I) of the respiratory chain from the inner mitochondrial membrane of Solanum tuberosumJ. Biol. Chem.26922632269Google Scholar
  13. Hewett-Emmett, D., Tashian, R.E. 1996Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene familiesMol. Phylogenet. Evol.55077Google Scholar
  14. Hewett-Emmett, D. 2000

    Evolution and distribution of the carbonic anhydrase gene families

    Chegwidden, W.R.Carter, N.D.Edwards, Y.H. eds. The Carbonic Anhdyrases. New HorizonsBirkhäuser VerlagBasel2976
    Google Scholar
  15. Iverson, T.M., Alber, B.E., Kisker, C., Ferry, J.G., Rees, D.C. 2000A closer look at the active site of gamma-class carbonic anhydrases: high-resolution crystallographic studies of the carbonic anhydrase from methanosarcina thermophilaBiochemistry3992229231Google Scholar
  16. Kelley, L.A., MacCallum, R.M., Sternberg, M.J. 2000Enhanced genome annotation using structural profiles in the program 3D-PSSMJ. Mol. Biol.299499520Google Scholar
  17. Kisker, C., Schindelin, H., Alber, B.E., Ferry, J.G., Rees, D.C. 1996A left-hand beta-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophilaEMBO J.1523232330Google Scholar
  18. Kruft, V., Eubel, H., Jänsch, L., Werhahn, W., Braun, H-P. 2001Proteomic approach to identify novel mitochondrial proteins in ArabidopsisPlant Physiol12716941710CrossRefPubMedGoogle Scholar
  19. Lesburg, C.A., Huang, C.C., Christianson, D., Fierke, C.A. 1997Histidine carboxamide ligand substitutions in the zinc binding site of carbonic anhydrase Ii alter metal coordination geometry but retain catalytic activityBiochemistry361578015791Google Scholar
  20. Leterme, S., Boutry, M. 1993Purification and preliminary characterization of mitochondrial complex I (NADH: ubiquinone reductase) from broad bean (Vicia faba L.)Plant Physiol102435443Google Scholar
  21. Maeda, S., Badger, M.R., Price, G.D. 2002Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942Mol. Microbiol.43425435Google Scholar
  22. Merlin, C., Masters, M., McAteer, S., Coulson, A. 2003Why is carbonic anhydrase essential to Escherichia coli?J. Bacteriol.18564156424Google Scholar
  23. Millar, A.H., Eubel, H., Jansch, L., Kruft, V., Heazlewood, J.L. and Braun, H.P. 2004. Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. (in press)Google Scholar
  24. McCall, K., Fierke, C. 2004Probing determinants of the metal ion selectivity in carbonic anhydrase using mutagenesisBiochemistry4339793986Google Scholar
  25. McGuffin, L.J., Bryson, K., Jones, D.T. 2000The PSIPRED protein structure prediction serverBioinformatics16404405CrossRefPubMedGoogle Scholar
  26. Parisi, G., Fornasari, M., Echave, J. 2000Evolutionary analysis of gamma-carbonic anhydrase structurally related proteinsMol. Phylogene. Evol.14323334Google Scholar
  27. Parisi, G., Perales, M., Fornasari, M.S., Colaneri, A., González-Shain, N., Gómez-Casati, D., Zimmermann, S., Brennicke, A., Araya, A., Ferry, J.G., Echave, J. and Zabaleta, E. 2004a. Gamma Carbonic Anhydrases in Plant Mitochondria. Plant Mol. Biol. (In press)Google Scholar
  28. Parisi, G. Fornasari, M.S. and Echave, J. 2004b. Dynactins p25 and p27 are predicted to adopt the LβH fold FEBS lett. (In press)Google Scholar
  29. Price, G.D., Hewit, S.M., Harrison, K., Badger, M.R. 1993Analysis of genomic DNA region from the cyanobacteria Synechococcus sp strain PCC7942 involved in carboxysome assembly and functionJ. Bacteriol.17528712879Google Scholar
  30. Raetz, C.R., Roderick, S.L. 1995A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferaseScience2709971000Google Scholar
  31. Sali, A., Blundell, T.L. 1993Comparative protein modeling by satisfaction of spatial restraintsJ. Mol. Biol.234779815Google Scholar
  32. Sambrook, J., Russell, D. 2001Molecular Cloning, a Laboratory Manual. 3rd ednCold Spring Harbor Laboratory PressNew YorkGoogle Scholar
  33. Schägger, H. 2001Blue-native gels to isolate protein complexes from mitochondriaMeth. Cell Biol.65231244Google Scholar
  34. Schägger, H., Pfeiffer, K. 2000The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexesEMBO J.1917771783Google Scholar
  35. Smith, K., Jakubzick, S.C., Whittam, T.S., Ferry, J.G. 1999Carbonic anhydrase is an ancient enzyme widespread in prokaryotesProc. Natl. Acad. Sci. USA961518415189Google Scholar
  36. Thompson, J.D., Gibson, T.D., Plewniak, F., Jeanmougin, F., Higgins, D.G. 1997The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucl. Acids Res.2548764882Google Scholar
  37. Tripp, B.C., Ferry, J.G. 2000A Structure-Function Study of a proton transport pathway in the gamma-class carbonic anhydrase from methanosarcina thermophilaBiochemistry3992329240Google Scholar
  38. Tripp, B., Bell, C., Cruz, F., Krebs, C., Ferry, J.G. 2004A role for iron in an ancient carbonic anhydraseJ. Biol. Chem.27966836687Google Scholar
  39. Tu, C.K., Rowlett, R., Tripp, B.C., Ferry, J.G., Silverman, D.N. 2002Chemical rescue of proton transfer in catalysis by carbonic anhydrases in the beta- and gamma-classBiochemistry411542915435Google Scholar
  40. Vaara, M. 1992Eight bacterial proteins, including UDP-N-acetylglucosamine acyltransferase (LpxA) and three other transferases of Escherichia coli, consist of a six-residue periodicity themeFEMS Microbiol. Lett.76249254Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Mariano Perales
    • 1
  • Gustavo Parisi
    • 2
  • María Silvina Fornasari
    • 2
  • Alejandro Colaneri
    • 1
  • Fernando Villarreal
    • 1
  • Nahuel González-Schain
    • 1
  • Julián Echave
    • 2
  • Diego Gómez-Casati
    • 1
  • Hans-Peter Braun
    • 3
  • Alejandro Araya
    • 4
  • Eduardo Zabaleta
    • 1
    • 5
  1. 1.Instituto de Investigaciones BiotecnológicasIIB-INTECH (CONICET/UNSAM)ChascomúsArgentina
  2. 2.Centro de Estudios de InvestigacionesUniversidad Nacional de QuilmesBernal.Argentina
  3. 3.Institut für Angewandte GenetikUniversität HannoverHannoverGermany
  4. 4.UMR 5097 R.E.G.E.R.CNRS and Université Victor Segalen Bordeaux 2BordeauxFrance
  5. 5.Instituto de Investigaciones BiológicasUniversidad Nacional de Mar del PlataMar del PlataArgentina

Personalised recommendations