Abstract
“He had been eight years upon a project of extracting sunbeams out of cucumbers...” (Swift 1726). At one time it may have seemed equally ludicrous to look for heat shock proteins in the absence of heat. Nonetheless the pursuit of developmentally or metabolically regulated Hsps has begun and there is now a solid foundation for future research in this area. The wealth of this information has been generated in nonplant systems and thus we have divided this Chapter into two sections. The first section summarizes reports of the developmental expression of heat shock genes. This is not an exhaustive documentation, but a synopsis of reports that have implications for plants. Generalities drawn from yeast and Drosophila research have been applicable to many systems that utilize this highly conserved network of proteins. More detail on Hsp functions from yeast, Drosophila,and mammalian systems can be gleaned from other Chapters in this Volume, or the current review by Lindquist and Craig (1988). A useful review for a comparison of sequences between plant and animal heat stress proteins, as well as a comprehensive review of heat shock in plants, is that of Neumann et al. (1989). The last section of this Chapter will focus on the expression of plant Hsps when development and heat shock coincide. In some organs, specific developmental programs preclude a normal heat-shock response. A tally of such events and a review of heat shock protein levels in nonstressed tissues will hopefully give the reader some clues as to how plants utilize heat shock genes and their cognates during growth and development.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abernethy RH, Thiel DS, Petersen NS, Helm K (1989) Thermotolerance is developmentally dependent in germinating wheat seed. Plant Physiol 89: 569–576
Arrigo AP, Darlix JL, Khandijan EW, Simon M, Sphar PF (1985) Characterization of the prosome from Drosophila and its similarity to the cytoplasmic structures formed by the low molecular weight heat-shock proteins. EMBO J 4: 399–406
Arrigo AP, Welch WJ (1987) Characterization and purification of small 28 000-dalton mammalian heat shock protein. J Biol Chem 262: 15359–15369
Ashburner M, Richards G (1976) The role of ecdysone in the control of gene activity in the polytene chromosomes of Drosophila. In: Lawrence PA (ed) Insect development. Wiley, New York, pp 203–225
Ashbumer J, Bonner J (1979) The induction of gene activity in Drosophila by heat shock. Cell 17: 241–254
Ayme A. Tissieres A (1985) Locus 67B of Drosophila melanogaster contains seven, not four, closely related heat shock genes. EMBO J 4: 2949–2954
Bamett T, Altschuler M, McDaniel CN, Mascarenhas JP (1980) Heat shock induced proteins in plant cells. Dev Genet 1: 331–340
Barrier JV, Bensaude O, Morange O, Babinet C (1987) Mouse 89 kD heat shock protein. Two polypep-tides with distinct developmental expression regulation. Exp Cell Res 170: 186–194
Baszczynski CL, Walden DB, Atkinson BG (1982) Regulation of gene expression in corn (Zea mays L.) by heat shock, Can J Biochem 60: 569–579
Baszczynski CL, Walden DB, Atkinson BG (1983) Regulation of gene expression in corn (Zea mays L.) by heat shock. II. In vitro analysis of RNAs from heat shocked seedlings. Can J Biochem 61: 395–403
Bensaude O, Morange M (1983) Spontaneous high expression of heat shock protein in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. EMBO J 2: 173–177
Berendes HD, Holt Th KH (1964) The induction of chromosomal activities by temperature shocks. Genen Phaenen 9: 1–7
Berger EM, Woodward MP (1983) Small heat shock proteins in Drosophila may confer thermal tolerance. Exp Cell Res 147: 437–442
Bienz M, Gurdon JB (1982) The heat-shock response inXenopus oocytes is controlled at the translational level. Cell 29: 811–819
Binelli G, Mascarenhas JP (1990) Arabidopsis: sensitivity of growth to high temperature. Dev Genet (in press)
Bond U, Schlesinger MJ (1986) The chicken ubiquitin gene contains a heat shock promoter and expresses an unstable mRNA in heat shocked cells. Mol Cell Biol 6: 4601–4610
Bond U, Agnell N, Hass AL, Redman K, Schlesinger MJ (1988) Ubiquitin in stressed chicken embryo fibroblasts. J Biol Chem 263: 2384–2388
Borkovich KA, Farrelly FW, Finkelstein DB, Tavlien J, Lindquist S (1989) Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9: 3919–3930
Bouchard RA (1990) Characterization of expressed meiotic prophase repeat transcript clones of Lilium: meiosis-specific expression, relatedness, and affinities to small heat shock protein genes. Genome 33: 68–79
Bouchard RA, Walden DB (1990) Stage-specific expression of a small heat shock gene in anthers. Maize Gene Coop News Lett 64: 122
Burke JJ, Orzech KA (1988) The heat shock response in higher plants: a biochemical model. Plant Cell Envir 11: 441–444
Burke TJ, Callis J, Viertstra RD (1988) Characterization of a polyubiquitin gene from Arabidopsis thaliana. Mol Gen Genet 213: 435–443
Cannon C, Wood S, Kalish F, Brunke K (1987) Sequence of a genomic clone for an hsp81 gene from Brassica oleracea. J Cell Biol 105: 246a
Chappell TG, Welch WJ, Schlossman DM, Palter KB, Schlesinger MJ, Rothman JE (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45: 3–13
Cheny C, Shearn MA (1983) Developmental regulation of Drosophila disc proteins; synthesis of a heat shock protein under non-heat shock conditions. Dev Biol 95: 325–330
Christensen AH, Quail PH (1989) Sequence analysis and transcriptional regulation by heat shock of polyubiquitin transcripts from maize. Plant Mol Biol 12: 619–632
Cohen RS, Meselson M (1985) Separate regulatory elements for the heat-inducible and ovarian expression of the Drosophila hsp26 gene. Cell 43: 737–746
Coldiron-Raichlin P, Dietrich PS, Sinibaldi RM (1986) The heat shock response of Arabidopsis thaliana. J Cell Biol 103: 176a
Cooper P, Ho TD, Hauptmann RM (1984) Tissue specificity of the heat-shock response in maize. Plant Physiol 75: 431–441
Craig EA, Ingolia TD, Manseau LJ (1983) Expression of heat shock cognates during heat shock and development. Dev Biol 99: 418–426
Czamecka E, Nagao RT, Key JL, Gurley WB (1988) Characterization of Gmhsp26-A, a stress gene encoding a divergent heat shock protein of soybean: heavy metal induced inhibition of intron processing. Mol Cell Biol 8: 1113–1122
Czarnecka E, Key JL. Gurley WB (1989) Regulatory domains of the Gmhsp 17.5-E heat shock promoter of soybean. Mol Cell Biol 9:3457–3463
De Nettencourt D (1977) In: Frankel R, Gall GAE, Linskens HF, (eds) Monographs on theoretical and applied genetics. Springer, Berlin Heidelberg New York, pp 106–107
Deshaies RJ, Koch BD, Werner-Washbume M, Craig EA, Schekman R (1988) A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332: 800–805
Dietrich PS, Sinibaldi RM (1983) Sequence homology between Zea mays DNA and Drosphila heat shock genes. J Cell Biol 97: 150a
Dietrich PS, Sinibaldi RM (1984) Expression of Zea mays DNA sequences homologous to Drosophila heat shock genes, J Cell Biol 99: 451a
Dietrich PS, Bouchard RA, Sinibaldi RM (1986) Isolation of Maize 83, 70 and 18 Kd heat shock genes. J Cell Biol 103: 311a
Dietrich Ps, Bouchard RA, Silva EM, Sinibaldi RM (1987) The complete sequence of a maize 18 Kd heat shock gene. J Cell Biol 105: 245a
Duck J, McCormick S, 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
El Ahmadi AB, Stevens MA (1979) Reproductive responses of heat-tolerant tomatoes to high temperatures. J Am Soc Hort Sci 104: 686–691
Finley D, Ozkaynak E., Varshaysky A (1987) The yeast polyubiquitin gene is essential for resistance at high temperatures, starvations and other stresses. Cell 48: 1035–1046
Frova C, Taramino G, Binelli G (1989) Heat shock proteins during pollen development in maize. Dev Genet 10: 324–332
Gausing K, Barkardottin R (1986) Structure and expression of ubiquitin in higher plants. Eur J Biochem 158: 57–62
Glaser RL, Lis JT (1990) Multiple, compensatory regulatory elements specify spermatocyte-specific expression of the Drosophila melanogaster hsp26 gene. Mol Cell Biol 10: 131–137
Glaser RL, Wolfner MF, Lis JT (1986) Spatial and temporal pattern of HSP26 expression during normal development. EMBO J 5: 747–754
Hagen G, Uhrhammer N, Guilfoyle TJ (1988) Regulation of expression of an auxin-induced soybean sequence by cadmium. J Biol Chem 263: 6442–6443
Hamner KC, Bonner J (1983) Photoperiodism in relation to hormones as factors in floral initiation and development. Bot Gaz 115: 361–364
Helm KW, Abernethy RH (1990) Heat shock protein and their mRNAs in dry and early inbibing embryos of wheat. Plant Physiol 93: 1626–1633
Hemmingsen SM, Woolford C, Van Der Vies SM,Tilly K, Dennis DT, Georgopoulos CP, Hendrix RW, Ellis RJ (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333: 330–335
Heuss-LaRosa K, Mayer RR, Chery JH (1987) Synthesis of only two heat shock proteins is required for thermoadaptation in cultured cowpea cells. Plant Physiol 85: 4–7
Hightower LE, White FD (1982) Preferential synthesis of rat heat-shock and glucose-regulated proteins in stressed cardiovascular cells. In: Schlesinger MJ, Ashburner M, Tissiere A (eds) Heat shock from bacteria to man. Cold Spring Harbor Lab, New York, pp 369–378
Hunter KW, Cook CL, Hayunga EG (1984) Leishmanial differentiation in vitro: induction of heat shock proteins. Biochem Biophys Res Commun 125: 755–760
Imamura A (1953) Photoperiodic initiation of flower primordia in Japanese morning glory Pharbitis nil chois. Proc Jpn Acad 29: 368–373
Ingolia TD,Craig EA (1982a) Drosophila gene related to the major heat shock induced gene is transcribed at normal temperatures and not induced by heat. Proc Natl Acad Sci USA 79:525–529
Ingolia TD, Craig EA (1982b) Four small Drosophila heat shock proteins are related to each other and to mammalian a—crystallin. Proc Natl Acad Sci USA 71: 2360–2364
Ireland RC, Berger EM (1982) Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. Proc Natl Acad Sci USA 79: 855–859
Kalish F, Cannon C, Brunke K (1986) Characterization of a putative Hsp81 gene in Brassica oleracea which is both constitutive and inducible. J Cell Biol 103: 176a
Kasambalides EJ. Lanks KW (1985) Anatagonistic effects of insulin and dexamethasone on glucose—regulated and heat shock protein synthesis. J Cell Physiol 123: 283–287
Kassenbrock CK, Garcia PD, Walter P, Kelly R (1988) Heavy—chain binding protein recognizes aberrant polypeptides translocated in vitro. Nature 333: 90–93
Kim Y—J, Shuman J, Sette M, Przybyla A)1984) Nuclear localization and phosphorylation of three 25kilodalton rat stress proteins. Mol Cell Biol 4: 468–474
Kloetzel P, Bautz EKF (1983) Heat shock proteins are associate with hnRNP in Drosophila melanogaster tissue culture cells. EMBO J 2: 705–710
Kulomaa MS, Weigel NL, Klein-Sek DA, Beattie SA, Connelly OM (1986) Amino acid sequence of a chicken heat shock protein derived from the complementary DNA nucleotide sequence. Biochemistry 25: 6244–6251
Kurtz S, Rossi J, Petko L, Lindquist S (1986) An ancient development induction: heat-shock proteins induced in sporulation and oogenesis. Science 231: 1154–1157
Lawrence F, Robert—Gero M (1985) Induction of heat shock stress proteins in promastigotes of three Leishmania species. Proc Natl Acad Sci USA 82: 4414–4417
Lee S (1990) Expression of hsp86 in mail germ cells. Mol Cell Biol 10: 3239–3242
Lin JJC, Welch WJ, Garrels JI, Feramisco J (1982) The association of the 100 Kd heat shock protein with the Golgi apparatus. In:Schlesinger MJ, Ashburner M, Tissieres A (eds) Heat shock from bacteria to man. Cold Spring Harbor Lab, New York, pp 267–273
Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22: 631–677
Lotan T, Ori N, Fluhr R (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1: 881–867
Mansfield MA, Key JL (1987) Synthesis of the low molecular weight heat shock proteins in plants. Plant Physiol 84: 1007–1017
Mazzarella RA, Green M (1987) Grp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homogous to the 90-KD heat shock protein (hsp90) and the 94-Kd glucose regulated protein (Grp94). J Biol Chem 262: 8875–8883
McElwain EF, Spiker S (1989) A wheat cDNA clone which is homologous to the 17 Kd heat shock protein gene family of soybean. Nuel Acids Res 17: 1764
Meyer J, Chartier Y (1983) Long lived and short lived heat shock protein in tobacco mesophyll protoplasts. Plant Physiol 72: 26–32
Moore SK, Kozak C, Robinson EA, Ulrich SJ, Appella E (1987) Cloning and nucleotide sequence of the murine hsp84 cDNA and chromosome assignment of related sequences. Gene 56: 29–40
Moore SK, Kozak C, Robinson EA, Ulrich SJ, Appella E (1989) Murine 86 and 84 Kd heat shock proteins, cDNA sequences, chromosome assignments and evolutionary origins. J Biol Chem 264: 5343–5351
Morimoto RI, Milarski KL (1990) Expression and function of vertebrate hsp70 genes. In Georgopoulos C, Tissieres A, Morimoto RI (eds). Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, New York, pp 323–359
Munro S, Pelham HRB (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899–907
Nakayama S (1958) Studies on the dark process in the photoperiodic response of Pharbitis seedlings. Sci Rep Tohok Univ S4 Biol 24: 137
Necchi A, Pogna NE, Mapelli S (1987) Early and late heat shock proteins in wheats and other cereal species. Plant Physiol 84: 1378–1384
Nene V, Dunne DW, Johnson KW, Taylor DW, Cordingley JS (1986) Sequence and expression of a major egg antigen from Schistosoma mansoni. Homologies to heat shock proteins and alpha - crystallins. Mol Biochem Parasitol 21: 179–188
Neumann D, Nover L, Parthier B, Rieger R, Scharf K-D, Wollgiehn R, Nieden U (1989) Heat shock and other response systems of plants. Biol Zentralbl, pp 1–156
Nieto-Sotelo J, Vierling E, Ho T-HD (1990) Cloning, sequence analysis and expression of a cDNA encoding a plastid localized heat shock protein in maize Plant Physiol (in press)
Nover L, Scharf KD, Neumann D (1983) Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Mol Cell Biol 3: 1648–1655
Nover L, Scharf KD (1984) Synthesis, modification and structural binding of heat shock proteins in tomato cell cultures. Eur J Biochem 139: 303–313
Nover L, Munsche F, Neumann D, Ohme K, Scharf KD (1986) Control of ribosome biosynthesis in plant cell cultures under heat shock conditions ribosomal RNA. Eur J Biochem 160: 297–304
Nover L, Scharf KD, Neumann D (1989) Cytoplasmic heat shock granules are formed from precursor particles and contain a set of mRNAs. Mol Cell Biol 9: 1298–1308
O’Conner D, Lis J (1981) Two closely linked transcription units within 63B heat shock puff locus of D. melanogaster display strikingly different regulation. Nucl Acids Res 9: 5075–5092
Ougham Hi, Stoddart JL (1986) Synthesis of heat shock protein and acquisition of thermotolerance in high-temperature tolerant and high-temperature susceptible lines of sorghum. Plant Sci 44: 163–167
Palter KB. Watanabe M, Stinson L, Mahowald AP, Craig EA (1986) Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol Cell Biol 6:1187–1203
Parag HA, Raboy B, Kulka RG (1987) Effect of heat shock on protein degradation in mammalian cells: involvement of the ubiquitin system. EMBO J 6: 55–61
Pauli D, Tonka C-H, Ayme-Southgate A (1988) An unusual split Drosophila heat shock gene expressed during embryogenesis, pupation and in testis. J Mol Biol 200: 47–53
Pelham H, Bienz M (1982) DNA sequences required for transcriptional regulation of the Drosophila hsp70 heat-shock gene in monkey cells and Xenopus oocytes. In: Schlesinger MI, Ashburner M, Tissieres A (eds) Heat shock from bacteria to man. Cold Spring Harbor Lab, New York, pp 43–48
Petko L, Lindquist S (1986) Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell 45: 885–8
Riley GJ (1984) Effects of high temperature on RNA-synthesis during germination of maize (Zea mays L.) Plant Sci Lett 35: 201–206
Rimland J, Akhayat O, Infante D, Infante AA (1988) Developmental regulation and biochemical analysis of 21 Kd heat shock protein in sea urchins. J Cell Biochem (Suppl) 12D: 271
Ritossa FM (1962) A new puffing pattern induced by heat shock and DNP in Drosophila.Experientia 18: 571–573
Ritossa FM (1964) Experimental activation of specific loci in polytene chromosomes of Drosophila. Exp Cell Res 36: 515–523
Rollet E. Best-Belpomme H (1986) HSP26 and 27 are phosphorylated in response to heat shock and ecdysterone in Drosophila melanogaster cells. Biochem Biophys Res Commun 14: 426–433
Rose MD, Misraond L, Vogel J (1989) KAR2, a karyogamy gene, is the yeast homologue of mammalian BIP/GRP78. Cell 57: 1211–1216
Russnack RH, Candido PM (1985) Locus encoding a family small heat shock genes in Caenorhabditis elegans: two genes duplicated to form a 34.8 kilobase inverted repeat. Mol Cell Biol 5: 1268–1278
Sanchez Y, Lindquist SL (1990) HSP104 required for induced thermotolerance. Science 248: 1112–1115
Schöffl F, Key JL (1982) An analysis of mRNAs for a group of heat shock proteins of soybean using cloned cDNAs. J Appl Genet 1: 301–314
Schöffl F, Key JL (1983) Indentification of a multigene family for small heat shock proteins in soybean and physical characterization of one individual gene coding region. Plant Mol Biol 2: 269–278
Schöffl F, Baumann G, Raschke E, Beavan M (1986) The expression of heat-shock genes in higher plants Philos Trans R Soc Lond 314: 453–468
Schöffl F, Rieping M, Baumann G, Bevan M, Angermueller S (1989) The function of plant heat shock promoter elements in the regulated expression of chimaeric genes in transgenic tobacco. Mol Gen Genet 217: 246–253
Schoper JB, Lambert RJ, Vasilas BL, Westgate ME (1987) Plant factors controlling seed set in maize. Plant Physiol 83: 121–125
Schrauwen JAM,Reijnen WH, De Leeuw HCGM, van Herpen MMA (1986) Response of pollen to heat stress. Acta Bot Neerl 35: 312–327
Schuldt C, Kloetzel BM (1985) Analysis of cytoplasmic 19S ring-type particles in Drosophila which contain hsp23 at normal growth temperature. Dev Biol 11: 65–74
Schwabe WW (1969) Morphogenic responses to climate. In: Evans LT (ed) The induction of flowering. Cornell University Press, Ithaca, New York, pp 318–333
Sciandra JJ, Subjeck JR (1983) The effects of glucose on protein synthesis and thermosensitivity in Chinese hamster ovary cell. J Biol Chem 258: 12091–12093
Sciandra JJ, Subject J, Hughes CS (1984) Induction of glucose-regulated proteins during anaerobic exposure and of heat-shock proteins after reoxygenation. Proc Natl Acad Sci USA 81: 4843–4847
Sirotkin K, Davidson N (1982) Developmentally regulated transcription from Drosophila melangaster chromosomal site 67B. Dey Biol 89: 196–210
Sorger PK, Pelham HRB (1987) The glucose-regulated protein grp94 is related to heat shock protein hsp90. J Mol Biol 194: 341–344
Southgate R, Ayme A, Voelmy R (1983) Nucleotide sequence analysis of the Drosophila small heat shock gene cluster ât locus 67B, J Mol Biol 165: 35–37
Spear I, Thimann KV (1954) The interrelation between CO, metabolism and photoperiodism in Kalanchoe. 11. Effect of prolonged darkness and high temperature. Plant Physiol 29: 414–417
Subjeck J, Shyy TT, Shen J, Johnson J (1983) Association between the mammalian 110 000 dalton heatshock protein and nucleoli. J Cell Biol 97: 139–1395
Swift J (1726) Voyage to la Puta. In: Gulliver’s travels. Benjamin Motte Chapter 5,.
Theodorakis NG, Zand DJ, Kotzbauer PT, Williams GT, Morimoto RI (1989) Hemin-induced transcriptional activation of the HSP70 gene during erythroid maturation in K562 cells is due to a heat shock factor mediated stress response. Mol Cell Biol 9: 3166–3173
Thomas SR, Lengyel JA (1986) Ecdysteroid-regulated heat shock gene expression during Drosophila melanogaster development. J Cell Physiol 127: 451–456
Van der Ploeg LH, Giannini SH, Cantor CR (1985) Heat shock genes: regulatory role for differentiation in parasitic protozoa. Science 228: 1443–1436
Van Herpen MMA, Reijnen WH, Schrauwen JAM, De Groot, PFM, Jager JWJ, Wullems GJ (1989) Heat shock proteins and survival of germinating pollen of Gillum longiflorum and Nicotiana tabacum. J Plant Physiol 134: 345–351
Vierling E, Key JL (1985) Ribulose 1.5-bisphosphate carboxylase synthesis during heat shock. Plant Physiol 78: 155–162
Vierling E, Sun A (1987) Developmental expression of heat shock protein. In: Cherry J (ed) Environmental stress in plants: biochemical and biophysical mechanisms. Springer, Berlin Heidelberg New York Tokyo, pp 343–354
Vierling E, Nagao RT, DeRocher AE, Harris LM (1988) A heat shock protein localized to chloroplasts is a member of a eukaryotic superfamily of heat shock proteins. EMBO 7: 575–581
Vierling E, Nagao RT, DeRocher AE, Harris LM (1989) The major low molecular weight heat shock protein in chloroplasts shows antigenic conservation among diverse higher plant species. Mol Cell Biol 9: 461–468
Vierstra RD, Langon SM, Schaller GE (1989) Complete amino acid sequence of ubiquitin from the higher plant Avena sativa. Biochemistry 25: 3105–3108
Welch WJ, Garrels Jl, Thomas GP, Lin JJC, Feramisco J (1983) Biochemical characterization of the mammalian stress proteins and idenity of 2 stress proteins as glucose and Ca+2-inonophore regulated proteins. J Biol Chem 258: 7102–7111
Whelan SA, Hightower LE (1985) Differential induction of glucose-regulated and heat shock proteins. J Cell Physiol 125: 251–258
Wu BJ, Morimoto RI (1985) Transcription of the human hsp70 gene is induced by serum stimulation. Proc Natl Acad Sci 82: 6070–6074
Xiao C-M, Mascarenhas JP (1985) High temperature-induced thermotolerance in pollen tubes of Tradescantia and heat shock proteins. Plant Physiol 78: 887–890
Xiao H, Lis JT (1989) Heat shock and developmental regulation of the Drosophila melanogaster hsp83 gene. Mol Cell Biol 9: 1746–1753
Xiao H, Lis JT (1990) Closely related DNA sequences specify distinct patterns of developmental expression in Drosophila melanogaster. Mol Cell Biol 10: 3272–3276
Yoshida S, Satake T, Mackill DS (1981) High temperature stress in rice. Int Rice Res Inst 67: 1–15
Zakeri Z, Wolgemuth DJ (1987) Developmental-stage-specific expression of the HSP70 gene family during differentiation of the mammalian male germ line. Mol Cell Biol 7: 1791–1796
Zakeri Z, Wolgemuth DJ, Hunt CR (1988) Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line. Mol Cell Biol 8: 2925–2932
Zimmerman JL, Petri WL, Meselson M (1983) Accumulation of specific subsets of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32: 1161–1170
Zimmerman JL, Apuya N, Darwish K, O’Carroll C (1989) Novel regulation of heat shock genes during carrot somatic embryo development. Plant Cell 1: 1137–1146
Zivy M (1987) Genetic variability for heat shock proteins in common wheat. Theor Appl Genet 74: 209–213
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1991 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Winter, J., Sinibaldi, R. (1991). The Expression of Heat Shock Protein and Cognate Genes During Plant Development. In: Hightower, L., Nover, L. (eds) Heat Shock and Development. Results and Problems in Cell Differentiation, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-46712-0_7
Download citation
DOI: https://doi.org/10.1007/978-3-540-46712-0_7
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-21993-5
Online ISBN: 978-3-540-46712-0
eBook Packages: Springer Book Archive