Skip to main content
SpringerLink
Log in

Conservation of dual-targeted proteins in Arabidopsis and rice points to a similar pattern of gene-family evolution

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Gene duplication followed by acquisition of specific targeting information and dual targeting were evolutionary strategies enabling organelles to cope with overlapping functions. We examined the evolutionary trend of dual-targeted single-gene products in Arabidopsis and rice genomes. The number of paralogous proteins encoded by gene families and the dual-targeted orthologous proteins were analysed. The number of dual-targeted proteins and the corresponding gene-family sizes were similar in Arabidopsis and rice irrespective of genome sizes. We show that dual targeting of methionine aminopeptidase, monodehydroascorbate reductase, glutamyl-tRNA synthetase, and tyrosyl-tRNA synthetase was maintained despite occurrence of whole-genome duplications in Arabidopsis and rice as well as a polyploidization followed by a diploidization event (gene loss) in the latter.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Babiychuk E, Muller F, Eubel H, Braun HP, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33:899–909

    Article  PubMed  CAS  Google Scholar 

  • Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298–305

    Article  PubMed  CAS  Google Scholar 

  • Bhushan S, Stahl A, Nilsson S, Lefebvre B, Seki M, Roth C, McWilliam D, Wright SJ, Liberles DA, Shinozaki K, Bruce BD, Boutry M, Glaser E (2005) Catalysis, subcellular localization, expression and evolution of the targeting peptides degrading protease, AtPreP2. Plant Cell Physiol 46:985–996

    Article  PubMed  CAS  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    Article  PubMed  CAS  Google Scholar 

  • Carneiro VT, Pelletier G, Small I (1993) Transfer RNA-mediated suppression of stop codons in protoplasts and transgenic plants. Plant Mol Biol 22:681–690

    Article  PubMed  CAS  Google Scholar 

  • Carrie C, Murcha MW, Kuehn K, Duncan O, Barthet M, Smith PM, Eubel H, Meyer E, Day DA, Millar AH, Whelan J (2008) Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett 582:3073–3079

    Article  PubMed  CAS  Google Scholar 

  • Castillo-Davis CI, Hartl DL (2002) Genome evolution and developmental constraint in Caenorhabditis elegans. Mol Biol Evol 19:728–735

    PubMed  CAS  Google Scholar 

  • Chabregas SM, Luche DD, Van Sluys MA, Menck CFM, Silva-Filho MC (2003) Differential usage of two in-frame translational start codons regulates subcellular localization of Arabidopsis thaliana THI1. J Cell Sci 116:285–291

    Article  PubMed  CAS  Google Scholar 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    Article  PubMed  CAS  Google Scholar 

  • Cho HS, Lee SS, Kim KD, Hwang I, Lim JS, Park YI, Pai HS (2004) DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell 16:2665–2682

    Article  PubMed  CAS  Google Scholar 

  • Christensen AC, Lyznik A, Mohammed S, Elowsky CG, Elo A, Yule R, Mackenzie SA (2005) Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 17:2805–2816

    Article  PubMed  CAS  Google Scholar 

  • Cleary SP, Tan FC, Nakrieko KA, Thompson SJ, Mullineaux PM, Creissen GP, von Stedingk E, Glaser E, Smith AG, Robinson C (2002) Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J Biol Chem 277:562–1569

    Article  Google Scholar 

  • Creissen G, Reynolds H, Xue Y, Mullineaux P (1995) Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J 8:167–175

    Article  PubMed  CAS  Google Scholar 

  • Davies JC, Petrov DA (2004) Preferential duplication of conserved proteins in eukaryotic genomes. PloS Biol 2:318–326

    Article  Google Scholar 

  • Dinkins RD, Conn HM, Dirk LMA, Williams MA, Houtz RL (2003) The Arabidopsis thaliana peptide deformylase 1 protein is localized to both mitochondria and chloroplasts. Plant Sci 165:751–758

    Article  CAS  Google Scholar 

  • Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Marechal-Drouard L, Small ID (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:16484–16489

    Article  PubMed  Google Scholar 

  • Dyal SD, Brown MT, Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304:253–257

    Article  Google Scholar 

  • Elo A, Lyznik A, Gonzalez DO, Kachman SD, Mackenzie S (2003) Nuclear genes encoding mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Plant Cell 15:1619–1631

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Giegé P, Heazlewood JL, Roessner-Tunali U, Millar AH, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15:2140–2151

    Article  PubMed  Google Scholar 

  • Giglione C, Serero A, Pierre M, Boisson B, Meinnel T (2000) Identification of eukaryotic peptide deformylases reveals universality of N-terminal protein processing mechanisms. EMBO J 19:5916–5929

    Article  PubMed  CAS  Google Scholar 

  • Heazlewood JL, Tonti-Filippini J, Verboom RE, Millar AH (2005) Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis. Plant Physiol 139:598–609

    Article  PubMed  CAS  Google Scholar 

  • Hedtke B, Meixner M, Gillandt S, Richter E, Borner T, Weihe A (1999) Green fluorescent protein as a marker to investigate targeting of organellar RNA polymerases of higher plants in vivo. Plant J 17:557–561

    Article  PubMed  CAS  Google Scholar 

  • Hedtke B, Borner T, Weihe A (2000) One RNA polymerase serving two genomes. EMBO Rep 1:435–440

    Article  PubMed  CAS  Google Scholar 

  • Hedtke B, Legen J, Weihe A, Herrmann RG, Börner T (2002) Six active phage-type RNA polymerase genes in Nicotiana tabacum. Plant J 30:625–637

    Article  PubMed  CAS  Google Scholar 

  • Herman PL, Ramberg H, Baack RD, Markwell J, Osterman JC (2002) Formate dehydrogenase in Arabidopsis thaliana: overexpression and subcellular localization in leaves. Plant Sci 163:1137–1145

    Article  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Jorgensen R (2004) Sequencing maize: just sample the salsa or go for the whole enchilada. Plant Cell 16:787–788

    Article  PubMed  Google Scholar 

  • Kleine T, Lockhart P, Batschauer A (2003) An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J 35:93–103

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Dokiya Y, Sugita M (2001) Dual targeting of phage-type RNA polymerase to both mitochondria and plastids is due to alternative translation initiation in single transcripts. Biochem Biophys Res Commun 289:1106–1113

    Article  PubMed  CAS  Google Scholar 

  • Kusumi K, Yara A, Mitsui N, Tozawa Y, Iba K (2004) Characterization of a rice nuclear-encoded plastid RNA polymerase gene OsRpoTp. Plant Cell Physiol 45:1194–1201

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie SA (2005) Plant organellar protein targeting: a traffic plan still under construction. Trends Cell Biol 15:548–554

    Article  PubMed  CAS  Google Scholar 

  • Menand B, Maréchal-Drouard L, Sakamoto W, Dietrich A, Wintz H (1998) A single gene of chloroplast origin codes for mitochondrial and chloroplastic methionyl-tRNA synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 95:11014–11019

    Article  PubMed  CAS  Google Scholar 

  • Millar AH, Whelan J, Small I (2006) Recent surprises in protein targeting to mitochondria and plastids. Curr Opin Plant Biol 9:610–615

    Article  PubMed  CAS  Google Scholar 

  • Mireau H, Lancelin D, Small ID (1996) The same Arabidopsis gene encodes both cytosolic and mitochondrial alanyl-tRNA synthetase. Plant Cell 8:1027–1039

    Article  PubMed  CAS  Google Scholar 

  • Moon S, Giglione C, Lee D-Y, An S, Jeong D-H, Meinnel T, An G (2008) Rice peptide deformylase PDF1B is crucial for development of chloroplasts. Plant Cell Physiol 49:1536–1546

    Article  PubMed  CAS  Google Scholar 

  • Murcha MW, Elhafez D, Lister R, Tonti-Filippini J, Baumgartner M, Philippar K, Carrie C, Mokranjac D, Soll J, Whelan J (2007) Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol 143:199–212

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Yamaguchi Y, Sano H (2000) Plant mercaptopyruvate sulfurtransferases: molecular cloning, subcellular localization and enzymatic activities. Eur J Biochem 267:5621–5630

    Article  PubMed  CAS  Google Scholar 

  • Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43:697–705

    Article  PubMed  CAS  Google Scholar 

  • Ono Y, Sakai A, Takechi K, Takio S, Takusagawa M, Takano H (2007) NtPolIlike1and NtPolI-like2, bacterial DNA polymerase I homologues isolated from BY-2 cultured tobacco cells, encode DNA polymerases engaged in DNA replication in both plastids and mitochondria. Plant Cell Physiol 48:1679–1692

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA, Peterson DG, Rong J, Wicker TM (2004) Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity. Curr Opin Biotechnol 15:120–125

    Article  PubMed  CAS  Google Scholar 

  • Peeters N, Small I (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541:54–63

    Article  PubMed  CAS  Google Scholar 

  • Pujol C, Bailly M, Kern D, Maréchal-Drouard L, Becker H, Duchêne AM (2008) Dual-targeted tRNA-dependent amidotransferase ensures both mitochondrial and chloroplastic Gln-tRNAGln synthesis in plants. Proc Natl Acad Sci USA 105:6481–6485

    Article  PubMed  CAS  Google Scholar 

  • Puyaubert J, Denis L, Alban C (2008) Dual targeting of Arabidopsis holocarboxylase synthetase1: a small upstream open reading frame regulates translation initiation and protein targeting. Plant Physiol 146:478–491

    Article  PubMed  CAS  Google Scholar 

  • Raynaud C, Sozzani R, Glab N, Domenichini S, Perennes C, Cella R, Kondorosi E, Bergounioux C (2006) Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J 47:395–407

    Article  PubMed  CAS  Google Scholar 

  • Richter U, Kiessling J, Hedtke B, Decker E, Reski R, Börner T, Weihe A (2002) Two RpoT genes of Physcomitrella patens encode phage-type RNA polymerases with dual targeting to mitochondria and plastids. Gene 290:95–105

    Article  PubMed  CAS  Google Scholar 

  • Rojo E, Zouhar J, Kovaleva V, Hong S, Raikhel NV (2003) The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in Arabidopsis. Mol Biol Cell 14:361–369

    Article  PubMed  CAS  Google Scholar 

  • Rokov-Plavec J, Dulic M, Duchêne AM, Weygand-Durasevic I (2008) Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep 27:1157–1168

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schatz G, Dobberstein B (1996) Common principles of protein translocation across membranes. Science 271:1519–1526

    Article  PubMed  CAS  Google Scholar 

  • Schwacke R, Fischer K, Ketelsen B, Krupinska K, Krause K (2007) Comparative survey of plastid and mitochondrial targeting properties of transcription factors in Arabidopsis and rice. Mol Genet Genomics 277:631–646

    Article  PubMed  CAS  Google Scholar 

  • Silva-Filho MC (2003) One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Curr Opin Plant Biol 6:589–595

    Article  PubMed  CAS  Google Scholar 

  • Silva-Filho MC, Wieers M-C, Chaumont F, Flugge U-I, Boutry M (1997) Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane protein. J Biol Chem 272:15264–15269

    Article  PubMed  CAS  Google Scholar 

  • Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590

    Article  PubMed  CAS  Google Scholar 

  • Su Z, Wang J, Yu J, Huang X, Gu X (2006) Evolution of alternative splicing after gene duplication. Genome Res 16:182–189

    Article  PubMed  CAS  Google Scholar 

  • Sunderland PA, West CE, Waterworth WM, Bray CM (2006) An evolutionarily conserved translation initiation mechanism regulates nuclear or mitochondrial targeting of DNA ligase 1 in Arabidopsis thaliana. Plant J 47:356–367

    Article  PubMed  CAS  Google Scholar 

  • Taira M, Valtersson U, Burkhardt B, Ludwig RA (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16:2048–2058

    Article  PubMed  CAS  Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 6:1–15

    Google Scholar 

  • Thatcher LF, Carrie C, Andersson CR, Sivasithamparam K, Whelan J, Singh KB (2007) Differential gene expression and subcellular targeting of Arabidopsis glutathione S-transferase F8 is achieved through alternative transcription start sites. J Biol Chem 282:28915–28928

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Nishikawa T, Fujimoto M, Takanashi H, Arimura S, Tsutsumi N, Kadowaki K (2008) Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol Biol Evol 25:1566–1575

    Article  PubMed  CAS  Google Scholar 

  • van Engelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res 4:288–290

    Article  PubMed  Google Scholar 

  • Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15:2192–2202

    Article  PubMed  CAS  Google Scholar 

  • von Braun SS, Sabetti A, Hanic-Joyce PJ, Gu J, Schleiff E, Joyce PB (2007) Dual targeting of the tRNA nucleotidyltransferase in plants: not just the signal. J Exp Bot 58:4083–4093

    Article  Google Scholar 

  • Wall MK, Mitchenall LA, Maxwell A (2004) Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc Natl Acad Sci USA 101:7821–7826

    Article  PubMed  CAS  Google Scholar 

  • Xu XM, Moller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25:900–909

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Li WH (2004) Developmental constraint on gene duplicability in fruit flies and nematodes. Gene 340:237–240

    Article  PubMed  CAS  Google Scholar 

  • Zaegel V, Guermann B, Le Ret M, Andrés C, Meyer D, Erhardt M, Canaday J, Gualberto JM, Imbault P (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18:3548–3563

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by FAPESP and CNPq, Brazil. C.V.M. was supported by a fellowship from CNPq. R.A.O.R., P.A.S.M. and C.M.B. were supported by fellowships from FAPESP. M.C·S.F. is a research fellow of CNPq. The authors thank Carlos Menck and Christine Stock for helpful suggestions and critical read of the manuscript.

Author information

Authors and Affiliations

  1. Departamento de Genética, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, Av. Pádua Dias, 11, C.P. 83, Piracicaba, SP, 13400-970, Brazil

    Carolina V. Morgante, Ricardo A. O. Rodrigues, Phellippe A. S. Marbach, Camila M. Borgonovi, Daniel S. Moura & Marcio C. Silva-Filho

Authors
  1. Carolina V. Morgante
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ricardo A. O. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Phellippe A. S. Marbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Camila M. Borgonovi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel S. Moura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marcio C. Silva-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcio C. Silva-Filho.

Additional information

Communicated by S. Hohmann.

C. V. Morgante and R. A. O. Rodrigues contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (PDF 157 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgante, C.V., Rodrigues, R.A.O., Marbach, P.A.S. et al. Conservation of dual-targeted proteins in Arabidopsis and rice points to a similar pattern of gene-family evolution. Mol Genet Genomics 281, 525–538 (2009). https://doi.org/10.1007/s00438-009-0429-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-009-0429-7

Keywords

Search

Navigation