The organization and evolution of the spinach stress 70 molecular chaperone gene family

Plant Cell

Volumn 10, Issue 4, 1998, Pages 539-556

  Guy, Charles L ^a   Li, Qin Bao ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0032051742     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.10.4.539     Document Type: Article

References (81)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Andersen, J.A., Li, Q.-B., Haskell, D.W., and Guy, C.L. (1994). Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock gene during cold acclimation. Plant Physiol. 104, 1359-1370.
3. Ausubel, P.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K., eds (1989). Current Protocols in Molecular Biology. (New York: Wiley Interscience).
4. Bardwell, J.C., and Craig, E.A. (1984). Major heat shock gene of Drosophila and Escherichia coli heat-inducible dnaK gene are homologous. Proc. Natl. Acad. Sci. USA 81, 848-852.
5. Bates, E.E., Vergne, P., and Dumas, C. (1994). Analysis of the cytosolic hsp70 gene family in Zea mays. Plant Mol. Biol. 25, 909-916.
6. Boorstein, W.R., Ziegelhoffer, T., and Craig, E.A. (1994). Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 38, 1-17.
7. Bui, E.T., Bradley, P.J., and Johnson, P.J. (1996). A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. USA 93, 9651-9656.
8. Casey, R., Creissen, G., Domoney, C., Forster, C., and Matta, N. (1994). An intron-containing nuclear stress-70 gene from Pisum sativum. Mol. Biol. Evol. 11, 325-326.
9. Corpas, F.J., and Trelease, R.N. (1997). The plant 73-kDa peroxisomal membrane protein (PMP73) is immunorelated to molecular chaperones. Eur. J. Cell Biol. 73, 49-57.
10. Craig, E.A., and Jacobsen, K. (1985). Mutations in cognate genes of Saccharomyces cerevisiae hsp70 result in reduced growth rates at low temperature. Mol. Cell. Biol. 5, 3517-3524.
11. Craig, E.A., Ingolia, T.D., and Manseau, L.J. (1983). Expression of Drosophila heat-shock cognate genes during heat shock and development. Dev. Biol. 99, 418-426.
12. Curtis, S.E., and Clegg, M.T. (1984). Molecular evolution of chloroplast DNA sequences. Mol. Biol. Evol. 1, 291-301.
13. Denecke, J., Goldman, M.H.S., Demolder, J., Seurinck, J., and Botterman, J. (1991). The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3, 1025-1035.
14. DeRocher, A., and Vierling, E. (1995). Cytoplasmic HSP70 homologues of pea: Differential expression in vegetative and embryonic organs. Plant Mol. Biol. 27, 441-456.
15. Dhankher, O.P., Drew, J.E., and Gatehouse, J.A. (1997). Characterization of a pea hsp70 gene which is both developmentally and stress-regulated. Plant Mol. Biol. 34, 345-352.
16. Drzymalla, C., Schroda, M., and Beck, C.F. (1996). Light-inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol. Biol. 31, 1185-1194.
17. Duck, N., McCormick, S., and Winter, J. (1989). Heat shock protein hsp70 cognate gene expression in vegetative and reproductive organs of Lycopersicon esculentum. Proc. Natl. Acad. Sci. USA 86, 3674-3678.
18. Ellis, R.J. (1993). The general concept of molecular chaperones. Philos. Trans. R. Soc. Lond. B Biol. Sci. 339, 257-261.
19. Flaherty, K.M., DeLuca-Flaherty, C., and McKay, D.B. (1990). Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346, 623-628.
20. Flynn, G.C., Chappell, T.G., and Rothman, J.E. (1989). Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245, 385-390.
21. Gaut, B.S., Morton, B.R., McCaig, B.C., and Clegg, M.T. (1996). Substitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene/Adh parallel rate differences at the plastid gene rbcL. Proc. Natl. Acad. Sci. USA 93, 10274-10279.
22. Gavel, Y., and von Heijne, G. (1990). Cleavage-site motifs in mitochondrial targeting peptides. Protein Eng. 4, 33-37.
23. Günther, E., and Walter, L. (1994). Genetic aspects of the hsp70 multigene family in vertebrates. Experimentia 30, 987-1001.
24. Gupta, R.S., and Golding, G.B. (1993). Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria and eukaryotes. J. Mol. Evol. 37, 573-582.
25. Gupta, R.S., Aitken, K., Falah, M., and Singh, B. (1994). Cloning of Giardia lamblia heat shock protein HSP70 homologs: Implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91, 2895-2899.
26. Guy, C.L., and Haskell, D. (1987). Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation-induced proteins. Plant Physiol. 84, 872-878.
27. Heschl, M.F., and Baillie, D.L. (1990). The HSP70 multigene family of Caenorhabditis elegans. Comp. Biochem. Physiol. 96, 633-637.
28. Hightower, L.E., Sadis, S.E., and Takenaka, I.M. (1994). Interactions of vertebrate hsc70 and hsp70 with unfolded proteins and peptides. In The Biology of Heat Shock Proteins and Molecular Chaperones, R.I. Morimoto, A. Tissières, and C. Georgopoulos, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 179-207.
29. Hughes, A.L. (1993). Nonlinear relationships among evolutionary rates identify regions of functional divergence in heat-shock protein 70 genes. Mol. Biol. Evol. 10, 243-255.
30. Ingolia, T.D., and Craig, E.A. (1982). Drosophila gene related to the major heat shock-induced gene is transcribed at normal temperatures and not induced by heat shock. Proc. Natl. Acad. Sci. USA 79, 525-529.
31. James, P., Pfund, C., and Craig, E.A. (1997). Functional specificity among Hsp70 molecular chaperones. Science 275, 387-389.
32. Joshi, C.P., Kumar, S., and Nguyen, H.T. (1996). Application of modified differential display technique for cloning and sequencing of the 3′ region from three putative members of the wheat HSP70 gene family. Plant Mol. Biol. 30, 641-646.
33. Kalinski, A., Rowley, D.L., Loer, D.S., Foley, C., Buta, G., and Herman, E.M. (1995). Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs. Planta 195, 611-621.
34. Kawula, T.H., and Lelivelt, M.J. (1994). Mutations in a gene encoding a new Hsp70 suppress rapid DMA inversion and bgl activation, but not proU derepression in hns-1 mutant Escherichia coli. J. Bacteriol. 176, 610-619.
35. Ko, K., Bornemisza, O., Kourtz, L., Ko, Z.W., Plaxton, W.C., and Cashmore, A.R. (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.
36. Koes, R.E., Spelt, C.E., Mol, J.N.M., and Gerats, A.G.M. (1987). The chalcone synthase multigene family of Petunia hybrida (V30): Sequence homology, chromosomal localization and evolutionary aspects. Plant Mol. Biol. 10, 375-385.
37. Koizumi, N., and Sano, H. (1997). Isolation of two genes encoding luminal binding protein from Arabidopsis thaliana. Plant Physiol. 113, 664.
38. Kourtz, L., and Ko, K. (1997). The early stage of chloroplast protein import involves Com70. J. Biol. Chem. 272, 2808-2813.
39. Lee, J.H., and Schoffl, F. (1996). An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol. Gen. Genet. 252, 11-19.
40. Lelivelt, M.J., and Kawula, T.H. (1995). Hsc66, an Hsp70 homolog of Escherichia coli, is induced by cold shock but not by heat shock. J. Bacteriol. 177, 4900-4907.
41. Li, Q.-B., and Guy, C.L. (1996). Prolonged final extension time increases cloning efficiency of PCR products. BioTechniques 21, 192, 196.
42. Li, Q.-B., Anderson, J.V., and Guy, C.L. (1994). A cDNA clone encoding a spinach 70-kilodalton heat-shock cognate. Plant Physiol. 105, 457-458.
43. Liberek, K., Skowyra, D., Zylicz, M., Johnson, C., and Georgopoulos, C. (1991). The Escherichia coli DnaK chaperone, the 70-kDa heat shock protein eukaryotic equivalent, changes conformation upon ATP hydrolysis, thus triggering its dissociation from a bound target protein. J. Biol. Chem. 266, 14491-14496.
44. Lin, T.Y., Duck, N.B., Winter, J., and Folk, W.R. (1991). Sequences of two hsc 70 cDNAs from Lycopersicon esculentum. Plant Mol. Biol. 16, 475-478.
45. Marshall, J.S., and Keegstra, K. (1992). Isolation and characterization of a cDNA clone encoding the major Hsp70 of the pea chloroplast stroma. Plant Physiol. 100, 1048-1054.
46. Marshall, J.S., DeRocher, A.E., Keegstra, K., and Vierling, E. (1990). Identification of heat shock protein hsp70 homologues in chloroplasts. Proc. Natl. Acad. Sci. USA 87, 374-378.
47. McKay, D.B., Wilbanks, S.M., Flaherty, K.M., Ha, J.-H., O'Brien, M.C., and Shirvanee, L.L. (1994). Stress-70 proteins and their interaction with nucleotides. In The Biology of Heat Shock Proteins and Molecular Chaperones, R.I. Morimoto, A. Tissières, and C. Georgopoulos, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 153-177.
48. Minton, K.W., Karmin, P., Hahn, G.M., and Minton, A.P. (1982). Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: A model for the biological role of heat shock proteins. Proc. Natl. Acad. Sci. USA 79, 7107-7111.
49. Moniz de Sa, M., and Drouin, G. (1996). Phylogeny and substitution rates of angiosperm actin genes. Mol. Biol. Evol. 13, 1198-1212.
50. Mooney, B., and Harmey, M.A. (1996). The occurrence of hsp70 in the outer membrane of plant mitochondria. Biochem. Biophys. Res. Commun. 218, 309-313.
51. Morimoto, R.I., Tissières, A., and Georgopoulos, C., eds (1994). The Biology of Heat Shock Proteins and Molecular Chaperones. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
52. Mues, G.I., Munn, T.Z., and Raese, J.D. (1986). A human gene family with sequence homology to Drosophila melanogaster Hsp70 heat shock genes. J. Biol. Chem. 261, 874-877.
53. Munro, S., and Pelham, H.R. (1987). A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907.
54. Neumann, D., Emmermann, M., Thierfelder, J.-M., zur Nieden, U., Clericus, M., Braun, H.-P., Nover, L., and Schmitz, U.K. (1993). HSP68-A DnaK-like heat-stress protein of plant mitochondria. Planta 190, 32-43.
55. Neven, L.G., Haskell, D.W., Hofig, A., Li, Q.-B., and Guy, C.L. (1993). Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol. Biol. 21, 291-305.
56. Nover, L., and Scharf, K.-D. (1997). Heat stress proteins and transcription factors. Cell. Mol. Life Sci. 53, 80-103.
57. Ohta, T. (1994). Further examples of evolution by gene duplication revealed through DNA sequence comparisons. Genetics 138, 1331-1337.
58. Pierpaoli, E.V., Sandmeier, E., Baici, A., Schonfeld, H.J., Gisler, S., and Christen, P. (1997). The power stroke of the DnaK/DnaJ/GrpE molecular chaperone system. J. Mol. Biol. 269, 757-768.
59. Rassow, J., von Ahsen, O., Borner, U., and Pfanner, N. (1997). Molecular Chaperones: Towards a characterization of the heat-shock protein family. Trends Cell Biol. 7, 129-133.
60. Rensing, S.A., and Maier, U.-G. (1994). Phylogenetic analysis of the stress-70 protein family. J. Mol. Evol. 30, 80-86.
61. Roberts, J.K., and Key, J.L. (1991). Isolation and characterization of a soybean hsp70 gene. Plant Mol. Biol. 16, 671-683.
62. Rochester, D.E., Winer, J.A., and Shah, D.M. (1986). The structure and expression of maize genes encoding the major heat shock protein, hsp70. EMBO J. 5, 451-458.
63. Rubin, D.M., Mehta, A.D., Zhu, J., Shoham, S., Chen, X., Wells, Q.R., and Palter, K.B. (1993). Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes. Gene 128, 155-163.
64. Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
65. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
66. Schilke, B., Forster, J., Davis, J., James, P., Walter, W., Laloraya, S., Johnson, J., Miao, B., and Craig, E. (1996). The cold sensitivity of a mutant Saccharomyces cerevisiae lacking a mitochondrial heat shock protein 70 is suppressed by loss of mitochondrial DMA. J. Cell Biol. 134, 603-613.
67. Schnell, D.J., Kessler, F., and Blobel, G. (1994). Isolation of components of the chloroplast protein import machinery. Science 266, 1007-1012.
68. Seaton, B.L., and Vickery, L.E. (1994). A gene encoding a DnaK/hsp70 homolog in Escherichia coli. Proc. Natl. Acad. Sci. USA 91, 2066-2070.
69. Storozhenko, S., De Pauw, P., Kushnir, S., Van Montagu, M., and Inze, D. (1996). Identification of an Arabidopsis thaliana cDNA encoding a HSP70-related protein belonging to the HSP110/SSE1 subfamily. FEBS Lett. 390, 113-118.
70. Swofford, D.L. (1993). Phylogenetic Analysis Using Parsimony. (Champaign, IL: Illinois Natural History Survey).
71. Tatusov, R.L., Koonin, E.V., and Lipman, D.J. (1997). A genomic perspective on protein families. Science 278, 631-637.
72. Walker, E.L., Weeden, N.F., Taylor, C.B., Green, P., and Coruzzi, G.M. (1995). Molecular evolution of duplicate copies of genes encoding cytosolic glutamine synthetase in Pisum sativum. Plant Mol. Biol. 29, 1111-1125.
73. 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.
74. Waters, E.R. (1995). The molecular evolution of the small heat-shock proteins in plants. Genetics 141, 785-795.
75. Waters, E.R., Lee, G.J., and Vierling, E. (1996). Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47, 325-338.
76. Watts, F.Z., Walters, A.J., and Moore, A.L. (1992). Characterization of PHSP1, a cDNA encoding a mitochondrial HSP70 from Pisum sativum. Plant Mol. Biol. 18, 23-32.
77. Wimmer, B., Lottspeich, F., Van der Klei, I., Veenhuis, M., and Gietl, C. (1997). The glyoxysomal and plastid molecular chaperone (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. Proc. Natl. Acad. Sci. USA 94, 13624-13629.
78. Wrobel, R.L., O'Brian, G.R., and Boston, R.S. (1997). Comparative analysis of BiP gene expression in maize endosperm. Gene 204, 105-113.
79. Wu, C.H., Caspar, T., Browse, J.A., Lindquist, S., and Somerville, C. (1988). Characterization of an HSP70 cognate gene family in Arabidopsis. Plant Physiol. 88, 731-740.
80. Wu, S.H., Wang, C., Chen, J., and Lin, B.L. (1994). Isolation of a cDNA encoding a 70-kDa heat-shock cognate protein expressed in vegetative tissues of Arabidopsis thaliana. Plant Mol. Biol. 25, 577-583.
81. Zhou, J., and Kleinhofs, A. (1996). Molecular evolution of nitrate reductase genes. J. Mol. Evol. 42, 432-442.