Skip to main content
SpringerLink
Log in

The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The first draft of the Chlamydomonas nuclear genome was searched for genes potentially encoding members of the five major chaperone families, Hsp100/Clp, Hsp90, Hsp70, Hsp60, the small heat shock proteins, and the Hsp70 and Cpn60 co-chaperones GrpE and Cpn10/20, respectively. This search yielded 34 potential (co-)chaperone genes, among them those 8 that have been reported earlier inChlamydomonas. These 34 genes encode all the (co-)chaperones that have been expected for the different compartments and organelles from genome searches in Arabidopsis, where 74 genes have been described to encode basically the same set of (co-)chaperones. Genome data from Arabidopsis and Chlamydomonas on the five major chaperone families are compared and discussed, with particular emphasis on chloroplast chaperones.

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

Similar content being viewed by others

Abbreviations

Cpn:

chaperonin

EST:

expressed sequence tag

HSP:

heat shock protein

ORF:

open reading frame

NBD:

nucleotide binding domain

References

  • Z Adam I Adamska K Nakabayashi O Ostersetzer K Haussuhl A Manuell B Zheng O Vallon SR Rodermel K Shinozaki AK Clarke (2001) ArticleTitleChloroplast and mitochondrial proteases in Arabidopsis A proposed nomenclature Plant Physiol 125 1912–1918 Occurrence Handle10.1104/pp.125.4.1912 Occurrence Handle11299370

    Article  PubMed  Google Scholar 

  • M Agarwal S Katiyar-Agarwal C Sahi DR Gallie A Grover (2001) ArticleTitle Arabidopsis thaliana Hsp100 proteins: kith and kin Cell Stress Chaperones 6 219–224 Occurrence Handle11599563

    PubMed  Google Scholar 

  • D Amir-Shapira T Leustek B Dalie H Weissbach N Brot (1990) ArticleTitleHsp70 proteins, similar to Escherichia coli DnaK, in chloroplasts and mitochondria of Euglena gracilis Proc Natl Acad Sci USA 87 1749–1752 Occurrence Handle2106681

    PubMed  Google Scholar 

  • E Asamizu K Miura K Kucho Y Inoue H Fukuzawa K Ohyama Y Nakamura S Tabata (2000) ArticleTitleGeneration of expressed sequence tags from low-CO2 and high-CO2 adapted cells of Chlamydomonas reinhardtii DNA Res 7 305–307 Occurrence Handle11089912

    PubMed  Google Scholar 

  • E Asamizu Y Nakamura S Sato H Fukuzawa S Tabata (1999) ArticleTitleA large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii Generation of 3433 non-redundant expressed sequence tags. DNA Res 6 369–373

    Google Scholar 

  • U Bertsch J Soll R Seetharam PV Viitanen (1992) ArticleTitleIdentification, characterization, and DNA sequence of a functional ‘double’ groES-like chaperonin from chloroplasts of higher plants Proc Natl Acad Sci USA 89 8696–8700 Occurrence Handle1356267

    PubMed  Google Scholar 

  • M Bonk M Tadros J Vandekerckhove S Al-Babili P Beyer (1996) ArticleTitlePurification and characterization of chaperonin 60 and heat-shock protein 70 from chromoplasts of Narcissus pseudonarcissus Plant Physiol 111 931–939 Occurrence Handle10.1104/pp.111.3.931 Occurrence Handle8754688

    Article  PubMed  Google Scholar 

  • RS Boston PV Viitanen E Vierling (1996) ArticleTitleMolecular chaperones and protein folding in plants Plant Mol Biol 32 191–222 Occurrence Handle10.1007/BF00039383 Occurrence Handle8980480

    Article  PubMed  Google Scholar 

  • TP Brutnell RJH Sawers A Mant JA Langdale (1999) ArticleTitleBUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize Plant Cell 11 849–864 Occurrence Handle10.1105/tpc.11.5.849 Occurrence Handle10330470

    Article  PubMed  Google Scholar 

  • A Brychzy T Rein KF Winklhofer FU Hartl JC Young WMJ Obermann (2003) ArticleTitleCofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system EMBO J 22 3613–3623 Occurrence Handle10.1093/emboj/cdg362 Occurrence Handle12853476

    Article  PubMed  Google Scholar 

  • B Bukau AL Horwich (1998) ArticleTitleThe Hsp70 and Hsp60 chaperone machines Cell 92 351–366 Occurrence Handle10.1016/S0092-8674(00)80928-9 Occurrence Handle9476895

    Article  PubMed  Google Scholar 

  • D Cao Y Lin C-L Cheng (2000) ArticleTitleGenetic interactions between the chlorate-resistant mutant cr88 and the photomorphogenic mutants cop1 and hy5 Plant Cell 12 199–210 Occurrence Handle10.1105/tpc.12.2.199 Occurrence Handle10662857

    Article  PubMed  Google Scholar 

  • D Cao JE Froehlich H Zhang C-L Cheng (2003) ArticleTitleThe chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90 Plant J 33 107–118 Occurrence Handle10.1046/j.1365-313X.2003.016011.x Occurrence Handle12943545

    Article  PubMed  Google Scholar 

  • GG Chen AT Jagendorf (1994) ArticleTitleChloroplast molecular chaperone-assisted refolding and reconstitution of an active multisubunit coupling factor CF1 core Proc Natl Acad Sci USA 91 11497–11501 Occurrence Handle7972091

    PubMed  Google Scholar 

  • Q Chen K Osteryoung E Vierling (1994) ArticleTitleA 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vivo and in organelle J Biol Chem 269 13216–13223 Occurrence Handle8175751

    PubMed  Google Scholar 

  • AE Rocher ParticleDe KW Helm LM Lauzon E Vierling (1991) ArticleTitleExpression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery Plant Physiol 96 1038–1047

    Google Scholar 

  • R Dickson C Weiss RJ Howard SP Alldrick RJ Ellis G Lorimer A Azem PV Viitanen (2000) ArticleTitleReconstitution of higher plant chloroplast chaperonin 60 tetradecamers active in protein folding J Biol Chem 275 11829–11835 Occurrence Handle10.1074/jbc.275.16.11829 Occurrence Handle10766808

    Article  PubMed  Google Scholar 

  • C Drzymalla M Schroda CF Beck (1996) ArticleTitleLight inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii Plant Mol Biol 31 1185–1194 Occurrence Handle10.1007/BF00040835 Occurrence Handle8914534

    Article  PubMed  Google Scholar 

  • Eisenberg-Domovich Y, Kloppstech K and Ohad I (1994) Reversible membrane association of heat-shock protein 22 in Chlamydomonas reinhardtii during heat shock and recovery. Eur J Biochem 1041–1046.

  • O Emanuelsson H Nielsen S Brunak Heijne G von (2000) ArticleTitlePredicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 1005–1016 Occurrence Handle10.1006/jmbi.2000.3903 Occurrence Handle10891285

    Article  PubMed  Google Scholar 

  • VV Emelyanov (2002) ArticleTitlePhylogenetic relationship of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution Gene 299 125–133 Occurrence Handle10.1016/S0378-1119(02)01021-1 Occurrence Handle12459260

    Article  PubMed  Google Scholar 

  • N Fischer JD Rochaix (2001) ArticleTitleThe flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii Mol Genet Genomics 265 888–894 Occurrence Handle10.1007/s004380100485 Occurrence Handle11523806

    Article  PubMed  Google Scholar 

  • KM Flaherty C DeLuca-Flaherty DB McKay (1990) ArticleTitleThree-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein Nature 346 623–628 Occurrence Handle10.1038/346623a0 Occurrence Handle2143562

    Article  PubMed  Google Scholar 

  • L-G Franzén J-D Rochaix Heijne G von (1990) ArticleTitleChloroplast transit peptides from green alga Chlamydomonas share features with both mitochondrial and higher plant chloroplast presequences FEBS Lett 280 165–168

    Google Scholar 

  • J Frydman (2001) ArticleTitleFolding of newly translated proteins in vivo the role of molecular chaperones Annu Rev Biochem 70 603–649 Occurrence Handle10.1146/annurev.biochem.70.1.603 Occurrence Handle11395418

    Article  PubMed  Google Scholar 

  • M Fuhrmann W Oertel P Hegemann (1999) ArticleTitleA synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii Plant J 19 353–361 Occurrence Handle10.1046/j.1365-313X.1999.00526.x Occurrence Handle10476082

    Article  PubMed  Google Scholar 

  • M Fuhrmann A Stahlberg E Govorunova S Rank P Hegemann (2001) ArticleTitleThe abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses J Cell Sci 114 3857–3863 Occurrence Handle11719552

    PubMed  Google Scholar 

  • DR Gallie D Fortner J Peng D Puthoff (2002) ArticleTitleATP-dependent hexameric assembly of the heat shock protein Hsp101 involves multiple interaction domains and a functional C-proximal nucleotide-binding domain J Biol Chem 277 39617–39626 Occurrence Handle12151400

    PubMed  Google Scholar 

  • JR Glover S Lindquist (1998) ArticleTitleHsp104, Hsp70 and Hsp40: a novel chaperone system that rescues previously aggregated proteins Cell 94 73–82 Occurrence Handle10.1016/S0092-8674(00)81223-4 Occurrence Handle9674429

    Article  PubMed  Google Scholar 

  • P Goloubinoff A Mogk A Ben Zvi T Tomoyasu B Bukau (1999) ArticleTitleSequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network Proc Natl Acad Sci USA 96 13732–13737 Occurrence Handle10.1073/pnas.96.24.13732 Occurrence Handle10570141

    Article  PubMed  Google Scholar 

  • B Grimm D Ish-Shalom D Even H Glaczinski P Ottersbach I Ohad K Kloppstech (1989) ArticleTitleThe nuclear-coded chloroplast 22 kDa heat shock protein of Chlamydomonas Evidence for translocation into the organell without a processing step Eur J Biochem 182 539–546 Occurrence Handle10.1111/j.1432-1033.1989.tb14861.x Occurrence Handle2473899

    Article  PubMed  Google Scholar 

  • T Halperin B Zheng H Itzhaki AK Clarke Z Adam (2001) ArticleTitlePlant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease Plant Mol Biol 45 461–468 Occurrence Handle10.1023/A:1010677220323 Occurrence Handle11352464

    Article  PubMed  Google Scholar 

  • U Härndahl BPA Kokke N Gustavsson S Linse K Berggren F Tjerneld W Boelens C Sundby (2001) ArticleTitleThe chaperone-like activity of a small heat shock protein is lost after sulfoxidation of conserved methionines in a surface-exposed amphipathic α-helix Biochim Biophys Acta 1545 227–237 Occurrence Handle11342048

    PubMed  Google Scholar 

  • CJ Harrison M Hayer-Hartl M Di Liberto F-U Hartl J Kuriyan (1997) ArticleTitleCrystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK Science 276 431–435 Occurrence Handle10.1126/science.276.5311.431 Occurrence Handle9103205

    Article  PubMed  Google Scholar 

  • F-U Hartl M Hayer-Hartl (2002) ArticleTitleMolecular chaperones in the cytosol: from nascent chain to folded protein Science 295 1852–1858 Occurrence Handle10.1126/science.1068408 Occurrence Handle11884745

    Article  PubMed  Google Scholar 

  • JE Hill SM Hemmingsen (2001) ArticleTitle Arabidopsis thaliana type I and II chaperonins Cell Stress Chap 6 190–200

    Google Scholar 

  • A Kamal L Thao J Sensintaffar L Zhang MF Boehm LC Fritz FJ Burrows (2003) ArticleTitleA high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors Nature 425 407–410 Occurrence Handle10.1038/nature01913 Occurrence Handle14508491

    Article  PubMed  Google Scholar 

  • KK Kim R Kim S-H Kim (1998) ArticleTitleCrystal structure of a small heat-shock protein Nature 394 595–599

    Google Scholar 

  • K Ko O Bornemisza L Kourtz ZW Ko WC Plaxton AR Cashmore (1992) ArticleTitleIsolation and characterization of a cDNA clone encoding a cognate 70 kDa heat shock protein of the chloroplast envelope J Biol Chem 267 2986–2993 Occurrence Handle1371110

    PubMed  Google Scholar 

  • Y Koumoto T Shimada M Kondo T Takao Y Shimonishi I Hara-Nishimura M Nishimura (1999) ArticleTitleChloroplast Cpn20 forms a tetrameric structure Plant J 17 467–477 Occurrence Handle10.1046/j.1365-313X.1999.00388.x Occurrence Handle10205903

    Article  PubMed  Google Scholar 

  • Y Koumoto T Shimada M Kondo I Hara-Nishimura M Nishimura (2001) ArticleTitleChloroplasts have a novel Cpn10 in addition to Cpn20 as co-chaperonins in Arabidopsis thaliana J Biol Chem 276 29688–29694 Occurrence Handle10.1074/jbc.M102330200 Occurrence Handle11402030

    Article  PubMed  Google Scholar 

  • L Kourtz K Ko (1997) ArticleTitleThe early stage of chloroplast protein import involves Com70 J Biol Chem 272 2808–2813 Occurrence Handle10.1074/jbc.272.5.2808 Occurrence Handle9006921

    Article  PubMed  Google Scholar 

  • P Krishna G Gloor (2001) ArticleTitleThe Hsp90 family of proteins in Arabidopsis thaliana Cell Stress Chap 6 238–246

    Google Scholar 

  • B-H Lee S-H Won H-S Lee M Miyao W-I Chung I-J Kim J Jo (2000) ArticleTitleExpression of the chloroplast-localized small heat shock protein by oxidative stress in rice Gene 245 283–290 Occurrence Handle10.1016/S0378-1119(00)00043-3 Occurrence Handle10717479

    Article  PubMed  Google Scholar 

  • GJ Lee AM Roseman HR Saibil E Vierling (1997) ArticleTitleA small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state EMBO J 16 659–671 Occurrence Handle10.1093/emboj/16.3.659 Occurrence Handle9034347

    Article  PubMed  Google Scholar 

  • S Lee HA Owen DJ Prochaska SR Barnum (2000) ArticleTitleHSP16.6 bis involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium Synechocystis sp PCC 6803. Curr Microbiol 40 283–287

    Google Scholar 

  • S Lee ME Sowa YH Watanabe PB Sigler W Chiu M Yoshida FT Tsai (2003) ArticleTitleThe structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state Cell 115 229–240 Occurrence Handle10.1016/S0092-8674(03)00807-9 Occurrence Handle14567920

    Article  PubMed  Google Scholar 

  • K Liberek J Marszalek D Ang C Georgopoulos M Zylicz (1991) ArticleTitle Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK Proc Natl Acad Sci USA 88 2874–2878 Occurrence Handle1826368

    PubMed  Google Scholar 

  • B-L Lin J-S Wang H-C Liu R-W Chen Y Meyer A Barakat M Delseny (2001) ArticleTitleGenomic analysis of the Hsp70 superfamily in Arabidopsis thaliana Cell Stress Chap 6 201–208

    Google Scholar 

  • Y Lin CL Cheng (1997) ArticleTitleA chlorate-resistant mutant defective in the regulation of nitrate reductase gene expression in Arabidopsis defines a new HY locus Plant Cell 9 21–35 Occurrence Handle10.1105/tpc.9.1.21 Occurrence Handle9014362

    Article  PubMed  Google Scholar 

  • Liu C, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M and Schroda M (2004) Vesicle-inducing protein in plastids 1 (VIPP1) interacts with chloroplast HSP70 via CDJ2, a new type of J-domain protein (submitted).

  • V Lumbreras DR Stevens S Purton (1998) ArticleTitleEfficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron Plant J 14 441–447 Occurrence Handle10.1046/j.1365-313X.1998.00145.x

    Article  Google Scholar 

  • F Madueño JA Napier JC Gray (1993) ArticleTitleNewly imported iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma Plant Cell 5 1865–1876 Occurrence Handle10.1105/tpc.5.12.1865 Occurrence Handle12271059

    Article  PubMed  Google Scholar 

  • JS Marshall AE Rocher ParticleDe K Keegstra E Vierling (1990) ArticleTitleIdentification of heat shock protein hsp70 homologues in chloroplasts Proc Natl Acad Sci USA 87 374–378 Occurrence Handle2296591

    PubMed  Google Scholar 

  • JE Maul JW Lilly L Cui CW Pamphilis Particlede W Miller EH Harris DB Stern (2002) ArticleTitleThe Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats Plant Cell 14 2659–2679 Occurrence Handle10.1105/tpc.006155 Occurrence Handle12417694

    Article  PubMed  Google Scholar 

  • P Meyer C Prodromou B Hu C Vaughan SM Roe B Panaretou PW Piper LH Pearl (2003) ArticleTitleStructural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions Mol Cell 11 647–658 Occurrence Handle10.1016/S1097-2765(03)00065-0 Occurrence Handle12667448

    Article  PubMed  Google Scholar 

  • JA Miernyk (1999) ArticleTitleProtein folding in the plant cell Plant Phys 121 695–703 Occurrence Handle10.1104/pp.121.3.695

    Article  Google Scholar 

  • JA Miernyk (2001) ArticleTitleThe J-domain proteins of Arabidopsis thaliana: an unexpectedly large and diverse family of chaperones Cell Stress Chap 6 209–218

    Google Scholar 

  • A Mogk C Schlieker KL Friedrich H-J Schönfeld E Vierling B Bukau (2003) ArticleTitleRefolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most effeciently by ClpB/DnaK J Biol Chem 278 31033–31042 Occurrence Handle10.1074/jbc.M303587200 Occurrence Handle12788951

    Article  PubMed  Google Scholar 

  • FW Müller GL Igloi CF Beck (1992) ArticleTitleStructure of a gene encoding heat-shock protein HSP70 from the unicellular alga Chlamydomonas reinhardtii Gene 111 165–173

    Google Scholar 

  • F Narberhaus (2002) ArticleTitleα-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network Microbiol Mol Biol Rev 66 64–93 Occurrence Handle10.1128/MMBR.66.1.64-93.2002 Occurrence Handle11875128

    Article  PubMed  Google Scholar 

  • E Nielsen M Akita J Davila-Aponte K Keegstra (1997) ArticleTitleStable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone EMBO J 16 935–946 Occurrence Handle10.1093/emboj/16.5.935 Occurrence Handle9118955

    Article  PubMed  Google Scholar 

  • W Orme AR Walker R Gupta JC Gray (2001) ArticleTitleA novel plastid-targeted J-domain protein in Arabidopsis thaliana Plant Mol Biol 46 615–626 Occurrence Handle10.1023/A:1010665702621 Occurrence Handle11516154

    Article  PubMed  Google Scholar 

  • J-B Peltier G Friso DE Kalume P Roepstorff F Nilsson I Adamska Wijk KJ van (2000) ArticleTitleProteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins Plant Cell 12 319–342 Occurrence Handle10.1105/tpc.12.3.319 Occurrence Handle10715320

    Article  PubMed  Google Scholar 

  • J-B Peltier O Emanuelsson DE Kalume J Ytterberg G Friso A Rudella DA Liberles L Söderberg P Roepsdorff G Heijne Particlevon KJ Wijk Particlevan (2002) ArticleTitleCentral functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction Plant Cell 14 211–236 Occurrence Handle10.1105/tpc.010304 Occurrence Handle11826309

    Article  PubMed  Google Scholar 

  • C Prodromou SM Roe O O’Brien JE Ladbury PW Piper LH Pearl (1997) ArticleTitleIdentification and structural charactarization of the ATP/ADP-binding site in the Hsp90 molecular chaperone Cell 90 65–75 Occurrence Handle10.1016/S0092-8674(00)80314-1 Occurrence Handle9230303

    Article  PubMed  Google Scholar 

  • C Queitsch TA Sangster S Lindquist (2002) ArticleTitleHsp90 as a capacitor of phenotypic variation Nature 417 618–624

    Google Scholar 

  • K Richter J Buchner (2001) ArticleTitleHsp90: chaperoning signal transduction J Cell Physiol 188 281–290 Occurrence Handle10.1002/jcp.1131 Occurrence Handle11473354

    Article  PubMed  Google Scholar 

  • J-D Rochaix (1995) ArticleTitle Chlamydomonas reinhardtii as the photosynthetic yeast Annu Rev Genet 29 209–230 Occurrence Handle10.1146/annurev.ge.29.120195.001233 Occurrence Handle8825474

    Article  PubMed  Google Scholar 

  • S Rüdiger L Germeroth J Schneider-Mergener B Bukau (1997) ArticleTitleSubstrate specificity of the DnaK chaperone determined by screening of cellulose-bound peptide libraries EMBO J 16 1501–1507 Occurrence Handle10.1093/emboj/16.7.1501 Occurrence Handle9130695

    Article  PubMed  Google Scholar 

  • SL Rutherford S Lindquist (1998) ArticleTitleHsp90 as a capacitor for morphological evolution Nature 396 336–342

    Google Scholar 

  • K-D Scharf M Siddique E Vierling (2001) ArticleTitleThe expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins) Cell Stress Chaperones 6 225–237 Occurrence Handle11599564

    PubMed  Google Scholar 

  • C Schiene-Fischer J Habazettl FX Schmid G Fischer (2002) ArticleTitleThe hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase Nat Struct Biol 9 419–424 Occurrence Handle10.1038/nsb804 Occurrence Handle12021775

    Article  PubMed  Google Scholar 

  • EC Schirmer S Lindquist E Vierling (1994) ArticleTitleAn Arabidopsis heat stress protein complements a thermotolerance defect in yeast Plant Cell 6 1899–1909 Occurrence Handle10.1105/tpc.6.12.1899 Occurrence Handle7866032

    Article  PubMed  Google Scholar 

  • EC Schirmer JR Glover MA Singer S Lindquist (1996) ArticleTitleHSP100/Clp proteins: a common mechanism explains diverse functions Trends Biochem Sci 21 289–296 Occurrence Handle10.1016/0968-0004(96)10038-4 Occurrence Handle8772382

    Article  PubMed  Google Scholar 

  • T Schlicher J Soll (1996) ArticleTitleMolecular chaperones are present in the thylakoid lumen of pea chloroplasts FEBS Lett 379 302–304 Occurrence Handle10.1016/0014-5793(95)01534-5 Occurrence Handle8603711

    Article  PubMed  Google Scholar 

  • G Schmitz M Schmidt J Feierabend (1996) ArticleTitleCharacterization of a plastid-specific HSP90 homologue: identification of a cDNA sequence, phylogenetic descendence and analysis of its mRNA and protein expression Plant Mol Biol 30 479–492 Occurrence Handle10.1007/BF00049326 Occurrence Handle8605300

    Article  PubMed  Google Scholar 

  • DJ Schnell (1995) ArticleTitleShedding light on the chloroplast protein import machinery Cell 83 521–524 Occurrence Handle10.1016/0092-8674(95)90090-X Occurrence Handle7585953

    Article  PubMed  Google Scholar 

  • DJ Schnell F Kessler G Blobel (1994) ArticleTitleIsolation of components of the chloroplast protein import machinery Science 266 1007–1012 Occurrence Handle7973649

    PubMed  Google Scholar 

  • M Schroda O Vallon F-A Wollman CF Beck (1999) ArticleTitleA chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition Plant Cell 11 1165–1178 Occurrence Handle10.1105/tpc.11.6.1165 Occurrence Handle10368186

    Article  PubMed  Google Scholar 

  • M Schroda D Blöcker CF Beck (2000) ArticleTitleThe HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas Plant J 21 121–131 Occurrence Handle10.1046/j.1365-313x.2000.00652.x Occurrence Handle10743653

    Article  PubMed  Google Scholar 

  • M Schroda J Kropat U Oster W Rüdiger O Vallon F-A Wollman CF Beck (2001a) ArticleTitleA role for molecular chaperones in assembly and repair of Photosystem II Biochem Soc Trans 29 413–418 Occurrence Handle10.1042/BST0290413

    Article  Google Scholar 

  • M Schroda O Vallon JP Whitelegge CF Beck F-A Wollman (2001b) ArticleTitleThe chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing Plant Cell 13 2823–2839 Occurrence Handle10.1105/tpc.13.12.2823

    Article  Google Scholar 

  • M Schroda CF Beck O Vallon (2002) ArticleTitleSequence elements within an HSP70 promoter counteract transcriptional transgene silencing in Chlamydomonas Plant J 31 445–455 Occurrence Handle10.1046/j.1365-313X.2002.01371.x Occurrence Handle12182703

    Article  PubMed  Google Scholar 

  • G Schuster D Even K Kloppstech I Ohad (1988) ArticleTitleEvidence for protection by heat-shock proteins against photoinhibition during heat-shock EMBO J 7 1–6

    Google Scholar 

  • J Shrager C Hauser CW Chang EH Harris J Davies J McDermott R Tamse Z Zhang AR Grossman (2003) ArticleTitleThe Chlamydomonas reinhardtii genome project A guide to the generation and use of the cDNA information Plant Physiol 131 401–408 Occurrence Handle10.1104/pp.016899 Occurrence Handle12586865

    Article  PubMed  Google Scholar 

  • I Sizova M Fuhrmann P Hegemann (2001) ArticleTitleA Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii Gene 277 221–229 Occurrence Handle10.1016/S0378-1119(01)00616-3 Occurrence Handle11602359

    Article  PubMed  Google Scholar 

  • T Soellick JF Uhrig GL Bucher JW Kellmann PH Schreier (2000) ArticleTitleThe movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins Proc Natl Acad Sci USA 97 2373–2378 Occurrence Handle10.1073/pnas.030548397 Occurrence Handle10688879

    Article  PubMed  Google Scholar 

  • DY Sung E Vierling CL Guy (2001) ArticleTitleComprehensive expression profile analysis of the Arabidopsis Hsp70 gene family Plant Physiol 126 789–800 Occurrence Handle10.1104/pp.126.2.789 Occurrence Handle11402207

    Article  PubMed  Google Scholar 

  • A Takahashi C Casais K Ichimura K Shirasu (2003) ArticleTitleHSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis Proc Natl Acad Sci USA 100 11777–11782 Occurrence Handle10.1073/pnas.2033934100 Occurrence Handle14504384

    Article  PubMed  Google Scholar 

  • MD Thompson CD Paavola TR Lenvik JS Gantt (1995) ArticleTitle Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible Plant Mol Biol 27 1031–1035 Occurrence Handle10.1007/BF00037029 Occurrence Handle7766872

    Article  PubMed  Google Scholar 

  • R Tsugeki M Nishimura (1993) ArticleTitleInteraction of homologues of Hsp70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts FEBS Lett 320 198–202 Occurrence Handle10.1016/0014-5793(93)80585-I Occurrence Handle8096466

    Article  PubMed  Google Scholar 

  • NM Tsvetkova I Horváth Z Török WF Wolkers Z Balogi N Shigapova LM Crowe F Tablin E Vierling JH Crowe L Vigh (2002) ArticleTitleSmall heat-shock proteins regulate membrane lipid polymorphism Proc Natl Acad Sci USA 99 13504–13509 Occurrence Handle10.1073/pnas.192468399 Occurrence Handle12368478

    Article  PubMed  Google Scholar 

  • RLM Montfort Particlevan E Basha KL Friedrich C Slingsby E Vierling (2001) ArticleTitleCrystal structure and assembly of a eukaryotic small heat shock protein Nat Struct Biol 8 1025–1030 Occurrence Handle10.1038/nsb722 Occurrence Handle11702068

    Article  PubMed  Google Scholar 

  • PV Viitanen M Schmidt J Buchner T Suzuki E Vierling R Dickson G Lorimer A Gatenby J Soll (1995) ArticleTitleFunctional characterization of the higher plant chloroplast chaperonins J Biol Chem 270 18158–18164 Occurrence Handle10.1074/jbc.270.30.18158 Occurrence Handle7629128

    Article  PubMed  Google Scholar 

  • S Vitha JE Froehlich O Koksharova KA Pyke H Erp Particlevan KW Osteryoung (2003) ArticleTitleARC6 is a J-domain plastid division protein and an evolutionary descendent of the cyanobacterial cell division protein Ftn2 Plant Cell 15 1918–1933 Occurrence Handle10.1105/tpc.013292 Occurrence Handle12897262

    Article  PubMed  Google Scholar 

  • ED Gromoff Particlevon U Treier CF Beck (1989) ArticleTitleThree light-inducible heat shock genes of Chlamydomonas reinhardtii Mol Cell Biol 9 3911–3918 Occurrence Handle2779571

    PubMed  Google Scholar 

  • H Wang M Goffreda T Leustek (1993) ArticleTitleCharacteristics of an Hsp70 homolog localized in higher plant chloroplasts that is similar to DnaK, the Hsp70 of prokaryotes Plant Physiol 102 843–850 Occurrence Handle10.1104/pp.102.3.843 Occurrence Handle8278536

    Article  PubMed  Google Scholar 

  • E Waters E Vierling (1999) ArticleTitleChloroplast small heat shock proteins: evidence for atypical evolution of an organelle-localized protein Proc Natl Acad Sci USA 96 14394–14399 Occurrence Handle10.1073/pnas.96.25.14394 Occurrence Handle10588716

    Article  PubMed  Google Scholar 

  • ER Waters GJ Lee E Vierling (1996) ArticleTitleEvolution, structure and function of the small heat shock proteins in plants J Exp Bot 296 325–338

    Google Scholar 

  • C Wu FS Seibert K Ko (1994) ArticleTitleIdentification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein J Biol Chem 269 32264–32271 Occurrence Handle7798226

    PubMed  Google Scholar 

  • Z Xu AL Horwich PB Sigler (1997) ArticleTitleThe crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex Nature 388 741–750 Occurrence Handle10.1038/41944 Occurrence Handle9285585

    Article  PubMed  Google Scholar 

  • K Yokthongwattana B Chrost S Behrman C Casper-Lindley A Melis (2001) ArticleTitlePhotosystem II damage and repair cycle in the green alga Dunaliella salina: involvement of a chloroplast-localized HSP70 Plant Cell Phys 42 1389–1397 Occurrence Handle10.1093/pcp/pce179

    Article  Google Scholar 

  • JC Young I Moarefi FU Hartl (2001) ArticleTitleHsp90: a specialized but essential protein-folding tool J Cell Biol 154 267–273 Occurrence Handle10.1083/jcb.200104079 Occurrence Handle11470816

    Article  PubMed  Google Scholar 

  • JC Young JM Barral F-U Hartl (2003) ArticleTitleMore than folding: localized functions of cytosolic chaperones Trends Biochem Sci 28 541–547 Occurrence Handle10.1016/j.tibs.2003.08.009 Occurrence Handle14559183

    Article  PubMed  Google Scholar 

  • B Zheng T Halperin O Hruskova-Heidingsfeldova Z Adam AK Clarke (2002) ArticleTitleCharacterization of chloroplast Clp proteins in Arabidopsis: Localization, tissue specificity and stress responses Physiol Plant 114 92–101 Occurrence Handle10.1034/j.1399-3054.2002.1140113.x Occurrence Handle11982939

    Article  PubMed  Google Scholar 

  • X Zhu X Zhao WF Burkholder A Gragerov CM Ogata M Gottesman WA Hendrickson (1996) ArticleTitleStructural analysis of substrate binding by the molecular chaperone DnaK Science 272 1606–1614 Occurrence Handle8658133

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Biologie II/Biochemie, Universität Freiburg, Schänzlestr. 1, 79104, Freiburg, Germany

    Michael Schroda

Authors
  1. Michael Schroda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Schroda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schroda, M. The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast. Photosynth Res 82, 221–240 (2004). https://doi.org/10.1007/s11120-004-2216-y

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-004-2216-y

Keywords

Search

Navigation