Chloroplast-targeted Hsp90 plays essential roles in plastid development and embryogenesis in Arabidopsis possibly linking with VIPP1

Physiologia Plantarum

Volumn 150, Issue 2, 2014, Pages 292-307

  Feng, Juanjuan ^a   Fan, Pengxiang ^a   Jiang, Ping ^a   Lv, Sulian ^a   Chen, Xianyang ^a   Li, Yinxin ^a  

^a INSTITUTE OF BOTANY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; BACTERIAL DNA; HEAT SHOCK PROTEIN 90; HSP90 5 PROTEIN, ARABIDOPSIS; HSP90-5 PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; T DNA; T-DNA; VIPP1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CELL FRACTIONATION; CHLOROPLAST; CHROMOSOME SEGREGATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC COMPLEMENTATION; GENETIC TRANSFORMATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PRENATAL DEVELOPMENT; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOPLAST; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; CHROMOSOME SEGREGATION; DNA, BACTERIAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; HSP90 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MUTAGENESIS, INSERTIONAL; PHOTOSYNTHESIS; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOPLASTS; SEEDLING; SUBCELLULAR FRACTIONS; SUPPRESSION, GENETIC; TRANSFORMATION, GENETIC;

EID: 84892482896     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12083     Document Type: Article

References (74)

1. Apuya NR, Yadegari R, Fischer RL, Harada JJ, Zimmerman JL, Goldberg RB (2001) The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60α gene. Plant Physiol 126: 717-730
2. Aseeva E, Ossenbuhl F, Eichacker LA, Wanner G, Soll J, Vothknecht UC (2004) Complex formation of VIPP1 depends on its alpha-helical PspA-like domain. J Biol Chem 279: 35535-35541
3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113
4. Baumbusch LO, Hughes DW, Galau GA, Jakobsen KS (2004) LEC1, FUS3, ABI3 and Em expression reveals no correlation with dormancy in Arabidopsis. J Exp Bot 55: 77-87
5. Bihmidine S, Bryan NM, Payne KR, Parde MR, Okalebo JA, Cooperstein SE, Awada T (2009) Photosynthetic performance of invasive Pinus ponderosa and Juniperus virginiana seedlings under gradual soil water depletion. Plant Biol (Stuttg) 12: 668-675
6. Brehelin C, Kessler F (2008) The plastoglobule: a bag full of lipid biochemistry tricks. Photochem Photobiol 84: 1388-1394
7. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D (2010) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol 155: 1678-1689
8. Cao D, Froehlich JE, Zhang H, Cheng CL (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33: 107-118
9. Constan D, Froehlich JE, Rangarajan S, Keegstra K (2004) A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 136: 3605-3615
10. Fan P, Wang X, Kuang T, Li Y (2009) An efficient method for the extraction of chloroplast proteins compatible for 2-DE and MS analysis. Electrophoresis 30: 3024-3033
11. 2 in vivo. Plant J 48: 427-439
12. Heide H, Nordhues A, Drepper F, Nick S, Schulz-Raffelt M, Haehnel W, Schroda M (2009) Application of quantitative immunoprecipitation combined with knockdown and cross-linking to Chlamydomonas reveals the presence of vesicle-inducing protein in plastids 1 in a common complex with chloroplast HSP90C. Proteomics 9: 3079-3089
13. Hsu SC, Belmonte MF, Harada JJ, Inoue K (2010) Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr Genomics 11: 338-349
14. Inaba T, Ito-Inaba Y (2010) Versatile roles of plastids in plant growth and development. Plant Cell Physiol 51: 1847-1853
15. Inoue H, Li M, Schnell DJ (2013) An essential role for chloroplast heat shock protein 90 (Hsp90C) in protein import into chloroplasts. Proc Natl Acad Sci USA 110: 3173-3178
16. Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H, Okada K (2002) SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J 21: 898-908
17. Kadota Y, Shirasu K (2011) The HSP90 complex of plants. Biochim Biophys Acta 1823: 689-697
18. Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 365: 729-748
19. Kessler F, Blobel G (1996) Interaction of the protein import and folding machineries of the chloroplast. Proc Natl Acad Sci USA 93: 7684-7689
20. Kovacheva S, Bédard J, Wardle A, Patel R, Jarvis P (2007) Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 50: 364-379
21. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6: 238-246
22. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98: 4238-4242
23. Latijnhouwers M, Xu XM, Moller SG (2010) Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232: 567-578
24. Li Z, Thomas TL (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10: 383-398
25. Lin Y, 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
26. T method. Methods 25: 402-408
27. Liu C, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M, Schroda M (2005) J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids 1. Mol Biol Cell 16: 1165-1177
28. Liu C, Willmund F, Golecki JR, Cacace S, Hess B, Markert C, Schroda M (2007) The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J 50: 265-277
29. Liu J, Yang H, Lu Q, Wen X, Chen F, Peng L, Zhang L, Lu C (2012) PsbP-domain protein1, a nuclear-encoded thylakoid lumenal protein, is essential for photosystem I assembly in Arabidopsis. Plant Cell 24: 4992-5006
30. Lo SM, Theg SM (2012) Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoid. Plant J 71: 656-668
31. Ma J, Peng L, Guo J, Lu Q, Lu C, Zhang L (2007) LPA2 is required for efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 19: 1980-1993
32. Manfre AJ, Lanni LM, Marcotte WR Jr (2006) The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development. Plant Physiol 140: 140-149
33. Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana II: the developing embryo. Can J Bot 69: 461-476
34. Mayer MP, Bukau B (1999) Molecular chaperones: the busy life of Hsp90. Curr Biol 9: R322-R325
35. Meinke D, Muralla R, Sweeney C, Dickerman A (2008) Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci 13: 483-491
36. Milioni D, Hatzopoulos P (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol Biol 35: 955-961
37. Myouga F, Akiyama K, Motohashi R, Kuromori T, Ito T, Iizumi H, Ryusui R, Sakurai T, Shinozaki K (2010) The Chloroplast Function Database: a large-scale collection of Arabidopsis Ds/Spm- or T-DNA-tagged homozygous lines for nuclear-encoded chloroplast proteins, and their systematic phenotype analysis. Plant J 61: 529-542
38. Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94: 12949-12956
39. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2: 279-289
40. Nielsen E, Akita M, Davila-Aponte J, 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
41. Nordhues A, Schöttler MA, Unger AK, Geimer S, Schönfelder S, Schmollinger S, Rütgers M, Finazzi G, Soppa B, Sommer F, Mühlhaus T, Roach T, Krieger-Liszkay A, Lokstein H, Crespo JL, Schroda M. (2012) Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24: 637-659
42. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739-759
43. Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271-294
44. Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12: 319-341
45. Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155: 1545-1551
46. Porra RJ, Schafer W, Gad'on N, Katheder I, Drews G, Scheer H (1996) Origin of the two carbonyl oxygens of bacteriochlorophyll a. Demonstration of two different pathways for the formation of ring E in Rhodobacter sphaeroides and Roseobacter denitrificans, and a common hydratase mechanism for 3-acetyl group formation. Eur J Biochem 239: 85-92
47. Prassinos C, Haralampidis K, Milioni D, Samakovli D, Krambis K, Hatzopoulos P (2008) Complexity of Hsp90 in organelle targeting. Plant Mol Biol 67: 323-334
48. Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228: 111-133
49. Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329: 11-16
50. Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188: 281-290
51. Ruppel NJ, Hangarter RP (2007) Mutations in a plastid-localized elongation factor G alter early stages of plastid development in Arabidopsis thaliana. BMC Plant Biol 7: 37
52. Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol 136: 2700-2709
53. Schmitz G, Schmidt M, 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
54. Schroda M (2004) The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast. Photosynth Res 82: 221-240
55. Schroda M, Mühlhaus T (2009) A 'foldosome' in the chloroplast. Plant Signal Behav 4: 301-303
56. Shi LX, Theg SM (2010) A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22: 205-220
57. Shi LX, Theg SM (2011) The motors of protein import into chloroplasts. Plant Signal Behav 6: 1397-1401
58. Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146: 1231-1241
59. Su PH, Li HM (2010) Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22: 1516-1531
60. Song H, Zhao R, Fan P, Wang X, Chen X, Li Y (2009a) Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229: 955-964
61. Song H, Fan P, Li Y (2009b) Overexpression of organellar and cytosolic AtHsp90 in Arabidopsis thaliana impaires plant tolerance to oxidative stress. Plant Mol Biol Rep 27: 342-349
62. Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19: 1347-1361
63. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135: 1206-1220
64. Vaucheret H, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Mourrain P, Palauqui JC, Vernhettes S (1998) Transgene-induced gene silencing in plants. Plant J 16: 651-659
65. Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541: 91-101
66. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438
67. Wang L, Ouyang M, Li Q, Zou M, Guo J, Ma J, Lu C, Zhang L (2010) The Arabidopsis chloroplast ribosome recycling factor is essential for embryogenesis and chloroplast biogenesis. Plant Mol Biol 74: 47-59
68. West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6: 1731-1745
69. Willmund F, Schroda M (2005) HEAT SHOCK PROTEIN 90C is a bona fide Hsp90 that interacts with plastidic HSP70B in Chlamydomonas reinhardtii. Plant Physiol 138: 2310-2322
70. Willmund F, Dorn KV, Schulz-Raffelt M, Schroda M (2008) The chloroplast DnaJ homolog CDJ1 of Chlamydomonas reinhardtii is part of a multichaperone complex containing HSP70B, CGE1, and HSP90C. Plant Physiol 148: 2070-2082
71. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
72. Zhang L, Sakamoto W (2013) Possible function of VIPP1 in thylakoids: protection but not formation? Plant Signal Behav 8: e22860
73. Zhang Y, Ding S, Lu Q, Yang Z, Wen X, Zhang L, Lu C (2011) Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase. Biochim Biophys Acta 1807: 391-403
74. Zhang L, Kato Y, Otters S, Vothknecht UC, Sakamoto W (2012) Essential role of VIPP1 in chloroplast envelope maintenance in Arabidopsis. Plant Cell 24: 3695-3707