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

Photosynthesis Research

Volumn 82, Issue 3, 2004, Pages 221-240

  Schroda, Michael ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

chaperone; Chlamydomonas; chloroplast; Hsp100 Clp; Hsp60; Hsp70; Hsp90; sHsp

Indexed keywords

ALGAE; ARABIDOPSIS; CHLAMYDOMONAS; EUKARYOTA;

EID: 11144314848     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-004-2216-y     Document Type: Review

References (107)

1. Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell A, Zheng B, Vallon O, Rodermel SR, Shinozaki K and Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol 125: 1912-1918
2. Agarwal M, Katiyar-Agarwal S, Sahi C, Gallie DR and Grover A (2001) Arabidopsis thaliana Hsp100 proteins: kith and kin. Cell Stress Chaperones 6: 219-224
3. Amir-Shapira D, Leustek T, Dalie B, Weissbach H and Brot N (1990) Hsp70 proteins, similar to Escherichia coli DnaK, in chloroplasts and mitochondria of Euglena gracilis. Proc Natl Acad Sci USA 87: 1749-1752
4. 2 adapted cells of Chlamydomonas reinhardtii. DNA Res 7: 305-307
5. Asamizu E, Nakamura Y, Sato S, Fukuzawa H and Tabata S (1999) A 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
6. Bertsch U, Soll J, Seetharam R and Viitanen PV (1992) Identification, characterization, and DNA sequence of a functional 'double' groES-like chaperonin from chloroplasts of higher plants. Proc Natl Acad Sci USA 89: 8696-8700
7. Bonk M, Tadros M, Vandekerckhove J, Al-Babili S and Beyer P (1996) Purification and characterization of chaperonin 60 and heat-shock protein 70 from chromoplasts of Narcissus pseudonarcissus. Plant Physiol 111: 931-939
8. Boston RS, Viitanen PV and Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32: 191-222
9. Brutnell TP, Sawers RJH, Mant A and Langdale JA (1999) BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11: 849-864
10. Brychzy A, Rein T, Winklhofer KF, Hartl FU, Young JC and Obermann WMJ (2003) Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. EMBO J 22: 3613-3623
11. Bukau B and Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366
12. Cao D, Lin Y and Cheng C-L (2000) Genetic interactions between the chlorate-resistant mutant cr88 and the photomorphogenic mutants cop1 and hy5. Plant Cell 12: 199-210
13. Cao D, Froehlich JE, Zhang H and Cheng C-L (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33: 107-118
14. 1 core. Proc Natl Acad Sci USA 91: 11497-11501
15. Chen Q, Osteryoung K and Vierling E (1994) A 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vivo and in organelle. J Biol Chem 269: 13216-13223
16. DeRocher AE, Helm KW, Lauzon LM and Vierling E (1991) Expression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery. Plant Physiol 96: 1038-1047
17. Dickson R, Weiss C, Howard RJ, Alldrick SP, Ellis RJ, Lorimer G, Azem A and Viitanen PV (2000) Reconstitution of higher plant chloroplast chaperonin 60 tetradecamers active in protein folding. J Biol Chem 275: 11829-11835
18. Drzymalla C, Schroda M and Beck CF (1996) Light inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol Biol 31: 1185-1194
19. 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
20. Emanuelsson O, Nielsen H, Brunak S and von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016
21. Emelyanov VV (2002) Phylogenetic relationship of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution. Gene 299: 125-133
22. Fischer N and Rochaix JD (2001 ) The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii. Mol Genet Genomics 265: 888-894
23. Flaherty KM, DeLuca-Flaherty C and McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346: 623-628
24. Franzén L-G, Rochaix J-D and von Heijne G (1990) Chloroplast transit peptides from green alga Chlamydomonas share features with both mitochondrial and higher plant chloroplast presequences. FEBS Lett 280: 165-168
25. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70: 603-649
26. Fuhrmann M, Oertel W and Hegemann P (1999) A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J 19: 353-361
27. Fuhrmann M, Stahlberg A, Govorunova E, Rank S and Hegemann P (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J Cell Sci 114: 3857-3863
28. Gallie DR, Fortner D, Peng J and Puthoff D (2002) ATP-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
29. Glover JR and Lindquist S (1998) Hsp104, Hsp70 and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82
30. Goloubinoff P, Mogk A, Ben Zvi AP, Tomoyasu T and Bukau B (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA 96: 13732-13737
31. Grimm B, Ish-Shalom D, Even D, Glaczinski H, Ottersbach P, Ohad I and Kloppstech K (1989) The 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
32. Halperin T, Zheng B, Itzhaki H, Clarke AK and Adam Z (2001) Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol Biol 45: 461-468
33. Härndahl U, Kokke BPA, Gustavsson N, Linse S, Berggren K, Tjerneld F, Boelens W and Sundby C (2001) The 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
34. Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F-U and Kuriyan J (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276: 431-435
35. Hartl F-U and Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858
36. Hill JE and Hemmingsen SM (2001) Arabidopsis thaliana type I and II chaperonins. Cell Stress Chap 6: 190-200
37. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC and Burrows FJ (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425: 407-410
38. Kim KK, Kim R and Kim S-H (1998) Crystal structure of a small heat-shock protein. Nature 394: 595-599
39. Ko K, Bornemisza O, Kourtz L, Ko ZW, Plaxton WC and Cashmore AR (1992) Isolation and characterization of a cDNA clone encoding a cognate 70 kDa heat shock protein of the chloroplast envelope. J Biol Chem 267: 2986-2993
40. Koumoto Y, Shimada T, Kondo M, Takao T, Shimonishi Y, Hara-Nishimura I and Nishimura M (1999) Chloroplast Cpn20 forms a tetrameric structure. Plant J 17: 467-477
41. Koumoto Y, Shimada T, Kondo M, Hara-Nishimura I and Nishimura M (2001) Chloroplasts have a novel Cpn10 in addition to Cpn20 as co-chaperonins in Arabidopsis thaliana. J Biol Chem 276: 29688-29694
42. Kourtz L and Ko K (1997) The early stage of chloroplast protein import involves Com70. J Biol Chem 272: 2808-2813
43. Krishna P and Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chap 6: 238-246
44. Lee B-H, Won S-H, Lee H-S, Miyao M, Chung W-I, Kim I-Jand Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245: 283-290
45. Lee GJ, Roseman AM, Saibil HR and Vierling E (1997) A 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
46. Lee S, Owen HA, Prochaska DJ and Barnum SR (2000) HSP16.6 bis involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Curr Microbiol 40: 283-287
47. Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M and Tsai FT (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115: 229-240
48. Liberek K, Marszalek J, Ang D, Georgopoulos C and Zylicz M (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88: 2874-2878
49. Lin B-L, Wang J-S, Liu H-C, Chen R-W, Meyer Y, Barakat A and Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chap 6: 201-208
50. Lin Y and Cheng CL (1997) A chlorate-resistant mutant defective in the regulation of nitrate reductase gene expression in Arabidopsis defines a new HY locus. Plant Cell 9: 21-35
51. 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)
52. Lumbreras V, Stevens DR and Purton S (1998) Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron. Plant J 14: 441-447
53. Madueño F, Napier JA and Gray JC (1993) Newly imported iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5: 1865-1876
54. Marshall JS, DeRocher AE, Keegstra K and Vierling E (1990) Identification of heat shock protein hsp70 homologues in chloroplasts. Proc Natl Acad Sci USA 87: 374-378
55. Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH and Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14: 2659-2679
56. Meyer P, Prodromou C, Hu B, Vaughan C, Roe SM, Panaretou B, Piper PW and Pearl LH (2003) Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol Cell 11: 647-658
57. Miernyk JA (1999) Protein folding in the plant cell. Plant Phys 121: 695-703
58. Miernyk JA (2001) The J-domain proteins of Arabidopsis thaliana: an unexpectedly large and diverse family of chaperones. Cell Stress Chap 6: 209-218
59. Mogk A, Schlieker C, Friedrich KL, Schönfeld H-J, Vierling E and Bukau B (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most effeciently by ClpB/DnaK. J Biol Chem 278: 31033-31042
60. Müller FW. Igloi GL and Beck CF (1992) Structure of a gene encoding heat-shock protein HSP70 from the unicellular alga Chlamydomonas reinhardtii. Gene 111: 165-173
61. Narberhaus F (2002) α-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66: 64-93
62. Nielsen E, Akita M, Davila-Aponte J and Keegstra K (1997) Stable 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
63. Orme W, Walker AR, Gupta R and Gray JC (2001) A novel plastid-targeted J-domain protein in Arabidopsis thaliana. Plant Mol Biol 46: 615-626
64. Peltier J-B, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I and van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12: 319-342
65. Peltier J-B, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepsdorff P, von Heijne G and van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14: 211-236
66. Prodromou C, Roe SM, O'Brien O, Ladbury JE, Piper PW and Pearl LH (1997) Identification and structural charactarization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90: 65-75
67. Queitsch C, Sangster TA and Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624
68. Richter K and Buchner J (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188: 281-290
69. Rochaix J-D (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29: 209-230
70. Rüdiger S, Germeroth L, Schneider-Mergener J and Bukau B (1997) Substrate specificity of the DnaK chaperone determined by screening of cellulose-bound peptide libraries. EMBO J 16: 1501-1507
71. Rutherford SL and Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342
72. Scharf K-D, Siddique M and Vierling E (2001) The 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
73. Schiene-Fischer C, Habazettl J, Schmid FX and Fischer G (2002) The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isonierase. Nat Struct Biol 9: 419-424
74. Schirmer EC, Lindquist S and Vierling E (1994) An Arabidopsis heat stress protein complements a thermotolerance defect in yeast. Plant Cell 6: 1899-1909
75. Schirmer EC, Glover JR, Singer MA and Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21: 289-296
76. Schlicher T and Soll J (1996) Molecular chaperones are present in the thylakoid lumen of pea chloroplasts. FEBS Lett 379: 302-304
77. Schmitz G, Schmidt M and Feierabend J (1996) Characterization 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
78. Schnell DJ (1995) Shedding light on the chloroplast protein import machinery. Cell 83: 521-524
79. Schnell DJ, Kessler F and Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266: 1007-1012
80. Schroda M, Vallon O, Wollman F-A and Beck CF (1999) A 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
81. Schroda M, Blöcker D and Beck CF (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J 21: 121-131
82. Schroda M, Kropat J, Oster U, Rüdiger W, Vallon O, Wollman F-A and Beck CF (2001a) A role for molecular chaperones in assembly and repair of Photosystem II. Biochem Soc Trans 29: 413-418
83. Schroda M, Vallon O, Whitelegge JP, Beck CF and Wollman F-A (2001b) The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. Plant Cell 13: 2823-2839
84. Schroda M, Beck CF and Vallon O (2002) Sequence elements within an HSP70 promoter counteract transcriptional transgene silencing in Chlamydomonas. Plant J 31: 445-455
85. Schuster G, Even D, Kloppstech K and Ohad I (1988) Evidence for protection by heat-shock proteins against photoinhibition during heat-shock. EMBO J 7: 1-6
86. Shrager J, Hauser C, Chang CW, Harris EH. Davies J, McDermott J, Tamse R, Zhang Z and Grossman AR (2003) The Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information. Plant Physiol 131: 401-408
87. Sizova I, Fuhrmann M and Hegemann P (2001) A Streptomyces rimosus aph VIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 277: 221-229
88. Soellick T, Uhrig JF, Bucher GL, Kellmann JW and Schreier PH (2000) The 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
89. Sung DY, Vierling E and Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126: 789-800
90. Takahashi A, Casais C, Ichimura K and Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100: 11777-11782
91. Thompson MD, Paavola CD, Lenvik TR and Gantt JS (1995) Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible. Plant Mol Biol 27: 1031-1035
92. Tsugeki R and Nishimura M (1993) Interaction of homologues of Hsp70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts. FEBS Lett 320: 198-202
93. Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH and Vigh L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci USA 99: 13504-13509
94. van Montfort RLM, Basha E, Friedrich KL, Slingsby C and Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8: 1025-1030
95. Viitanen PV, Schmidt M, Buchner J, Suzuki T, Vierling E, Dickson R, Lorimer G, Gatenby A and Soil J (1995) Functional characterization of the higher plant chloroplast chaperonins. J Biol Chem 270: 18158-18164
96. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H and Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendent of the cyanobacterial cell division protein Ftn2. Plant Cell 15: 1918-1933
97. von Gromoff ED, Treier U and Beck CF (1989) Three light-inducible heat shock genes of Chlamydomonas reinhardtii. Mol Cell Biol 9: 3911-3918
98. Wang H, Goffreda M and Leustek T (1993) Characteristics of an Hsp70 homolog localized in higher plant chloroplasts that is similar to DnaK, the Hsp70 of prokaryotes. Plant Physiol 102: 843-850
99. Waters E and Vierling E (1999) Chloroplast small heat shock proteins: evidence for atypical evolution of an organelle-localized protein. Proc Natl Acad Sci USA 96: 14394-14399
100. Waters ER, Lee GJ and Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 296: 325-338
101. Wu C, Seibert FS and Ko K (1994) Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein. J Biol Chem 269: 32264-32271
102. 7 chaperonin complex. Nature 388: 741-750
103. Yokthongwattana K, Chrost B, Behrman S, Casper-Lindley C and Melis A (2001) Photosystem II damage and repair cycle in the green alga Dunaliella salina: involvement of a chloroplast-localized HSP70. Plant Cell Phys 42: 1389-1397
104. Young JC, Moarefi I and Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154: 267-273
105. Young JC, Barral JM and Hartl F-U (2003) More than folding: localized functions of cytosolic chaperones. Trends Biochem Sci 28: 541-547
106. Zheng B, Halperin T, Hruskova-Heidingsfeldova O, Adam Z and Clarke AK (2002) Characterization of chloroplast Clp proteins in Arabidopsis: Localization, tissue specificity and stress responses. Physiol Plant 114: 92-101
107. Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman M and Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272: 1606-1614