Skip to main content
SpringerLink
Log in

Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In plants small heat shock proteins (sHsp) are abundantly expressed upon heat stress in vegetative tissue, however, sHsp expression is also developmentally induced in pollen. The developmental induction of sHsp has been related to the potential for stress-induced microspore embryogenesis. We investigated the polymorphism among sHsp and their expression during pollen development and after heat stress in tobacco. Real-time RT-PCR was used for quantification of mRNA of two known and nine newly isolated cDNAs representing cytosolic sHsp. At normal temperature most of these genes are not transcribed in vegetative tissues, however, all genes were expressed during pollen development. Low levels of mRNAs were found for sHsp-1A and -1B in early-unicellular stage, increasing four to sevenfold in mature pollen. Nine other genes are up-regulated in unicellular and down-regulated in bicellular pollen; three these genes show stage-specific expression. Western analysis revealed that cytosolic class I and II sHsp are developmentally expressed during all stages of pollen development. Different subsets of cytosolic sHsp genes are expressed in a stage-specific fashion suggesting that certain sHsp genes may play specific roles in early, others during later stages of pollen development. Heat stress results in a relatively weak and incomplete response in pollen: (i) the heat-induced levels of mRNA (excepting sHsp-2B, −3Cand -6) are much lower than in leaves, (ii) several sHsp are not detected after heat stress in pollen, although, they are heat-inducibly expressed in leaves. Application of heat stress, cold, and starvation, which induce microspore embryogenesis, modify mRNA levels and the patterns of 2-D-separated sHsp, but only heat stress enhances the expression of sHsp in microspores. There is no correlation of the expression of specific sHsp with the potential for microspore embryogenesis.

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

References

  • D. Albani LS. Robert PA. Donaldson I. Altosaar P. Arnison S. Fabijanski (1990) ArticleTitleCharacterization of a pollen-specific gene family from Brassica napus which is activated during early microspore development Plant Mol Biol 15 605–622 Occurrence Handle10.1007/BF00017835 Occurrence Handle1:CAS:528:DyaK3MXhtlOju7c%3D Occurrence Handle2102378

    Article  CAS  PubMed  Google Scholar 

  • D. Albani R. Sardana LS. Robert I. Altosaar P. Arnison S. Fabijanski (1992) ArticleTitleA Brassica napus gene family which shows sequence similarity to ascorbate oxidase is expressed in developing pollen. Molecular characterization and analysis of promoter activity in transgenic tobacco plants Plant J 2 331–342 Occurrence Handle1:CAS:528:DyaK3sXkt1Wlt7o%3D Occurrence Handle1303799

    CAS  PubMed  Google Scholar 

  • R.L.. Allen D.M.. Lonsdale (1993) ArticleTitleMolecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development Plant J 3 261–271 Occurrence Handle10.1046/j.1365-313X.1993.t01-14-00999.x Occurrence Handle1:CAS:528:DyaK3sXkt1Wrurs%3D Occurrence Handle8106080

    Article  CAS  PubMed  Google Scholar 

  • C.. Almoguera J. Jordano (1992) ArticleTitleDevelopmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs Plant Mol Biol 19 781–792 Occurrence Handle10.1007/BF00027074 Occurrence Handle1:CAS:528:DyaK3sXkt1Cktbc%3D Occurrence Handle1386536

    Article  CAS  PubMed  Google Scholar 

  • C. Almoguera P. Prieto-Dapena J. Jordano (1998) ArticleTitleDual regulation of a heat shock promoter during embryogenesis: stage-dependent role of heat shock elements Plant J 13 437–446 Occurrence Handle10.1046/j.1365-313X.1998.00044.x Occurrence Handle1:CAS:528:DyaK1cXitFyrsrs%3D Occurrence Handle9680992

    Article  CAS  PubMed  Google Scholar 

  • S.F. Altschul TL. Madden AA. Schäffer J. Zhang Z. Zhang W. Miller D. Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694

    Article  CAS  PubMed  Google Scholar 

  • N. Apuya J. Zimmerman (1992) ArticleTitleHeat shock gene expression is controlled primarily at the translational level in carrot cells and somatic embryos Plant Cell 4 657–665 Occurrence Handle10.1105/tpc.4.6.657 Occurrence Handle1:CAS:528:DyaK38XltVygsLc%3D Occurrence Handle12297657

    Article  CAS  PubMed  Google Scholar 

  • T. Ariizumi M. Amagai D. Shibata K. Hatakeyama M. Watanabe K. Toriyama (2002) ArticleTitleComparative study of promoter activity of three anther-specific genes encoding lipid transfer protein, xyloglucan endotransglucosylase/hydrolase and polygalacturonase in transgenic Arabidopsis thaliana Plant Cell Reports 21 90–96 Occurrence Handle10.1007/s00299-002-0487-3 Occurrence Handle1:CAS:528:DC%2BD38XlsVeqtbw%3D

    Article  CAS  Google Scholar 

  • I. Atanassov E. Russinova L. Antonov A. Atanassov (1998) ArticleTitleExpression of an anther-specific chalcone synthase-like gene is correlated with uninucleate microspore development in Nicotiana sylvestris Plant Mol Biol 38 1169–1178 Occurrence Handle10.1023/A:1006074508779 Occurrence Handle1:CAS:528:DyaK1MXksVGltQ%3D%3D Occurrence Handle9869422

    Article  CAS  PubMed  Google Scholar 

  • BG. Atkinson M. Raizada RA. Bouchard J. Frappier D. Walden (1993) ArticleTitleThe independent stage-specific expression of the 18-kDa heat shock protein genes during microsporogenesis in Zea mays L Dev Genet 14 15–26 Occurrence Handle10.1002/dvg.1020140104 Occurrence Handle1:CAS:528:DyaK3sXlvF2lt7c%3D

    Article  CAS  Google Scholar 

  • N. Banzet C. Richaud Y. Deveaux M. Kazmaier J. Gagnon C. Triantaphlides (1998) ArticleTitleAccumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells Plant J 13 519–527 Occurrence Handle10.1046/j.1365-313X.1998.00056.x Occurrence Handle1:CAS:528:DyaK1cXitFyrs7w%3D Occurrence Handle9680997

    Article  CAS  PubMed  Google Scholar 

  • E. Basha GJ. Lee B. Demeler E. Vierling (2004) ArticleTitleChaperone activity of cytosolic small heat shock proteins from wheat European J Biochem 271 1426–1436 Occurrence Handle10.1111/j.1432-1033.2004.04033.x Occurrence Handle1:CAS:528:DC%2BD2cXjsFeksb8%3D

    Article  CAS  Google Scholar 

  • RM. Benito Moreno F. Macke M-T. Hauser A. Alwen E. Heberle-Bors (1988) Sporophytes and male gametophytes from in vitrocultured, immature tobacco pollen M. Cresti P. Gori E. Pacini (Eds) Sexual Reproduction in Higher Plants. Springer Berlin 137–142

    Google Scholar 

  • T. Berkelman T. Stenstedt (1998) 2-D Electrophoresis using Immobilized pH Gradients: Principles and Methods Amersham Pharmacia Biotech Piscataway

    Google Scholar 

  • R. Bouchard (1990) ArticleTitleCharacterization 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 Occurrence Handle1:CAS:528:DyaK3cXltFShs7o%3D Occurrence Handle2332163

    CAS  PubMed  Google Scholar 

  • K. Brander C. Kuhlemeier (1995) ArticleTitleA pollen-specific DEAD-box protein related to translation initiation factor eIF-4A from tobacco Plant Mol Biol 27 637–649 Occurrence Handle10.1007/BF00020219 Occurrence Handle1:CAS:528:DyaK2MXlt1Wnurg%3D Occurrence Handle7727743

    Article  CAS  PubMed  Google Scholar 

  • R. Carranco C. Almoguera J. Jordano (1997) ArticleTitleA plant small heat shock protein gene expressed during zygotic embryogenesis but noninductible by heat stress J Biol Chem 272 27470–27475 Occurrence Handle10.1074/jbc.272.43.27470 Occurrence Handle1:CAS:528:DyaK2sXmvFyru7w%3D Occurrence Handle9341201

    Article  CAS  PubMed  Google Scholar 

  • R. Carranco C. Almoguera J. Jordano (1999) ArticleTitleAn imperfect heat shock element and different upstream sequences are required for the seed-specific expression of a small heat shock protein gene Plant Physiol 121 723–730 Occurrence Handle10.1104/pp.121.3.723 Occurrence Handle1:CAS:528:DyaK1MXns12nt74%3D Occurrence Handle10557220

    Article  CAS  PubMed  Google Scholar 

  • JL. Carpenter SE. Ploense D. Snustad C. Silflow (1992) ArticleTitlePreferential expression of an α-tubulin gene of Arabidopsis in pollen Plant Cell 4 557–571 Occurrence Handle10.1105/tpc.4.5.557 Occurrence Handle1:CAS:528:DyaK3sXltlCgsQ%3D%3D Occurrence Handle1498610

    Article  CAS  PubMed  Google Scholar 

  • HEM. Christensen S. Ramachandran CT. Tan U. Surana C. Dong N. Chua (1996) ArticleTitleArabidopsis profilins are functionally similar to yeast profilins: identification of a vascular bundle-specific profilin and a pollen-specific profilin Plant J 10 269–279 Occurrence Handle10.1046/j.1365-313X.1996.10020269.x Occurrence Handle1:CAS:528:DyaK28XlvFags7w%3D Occurrence Handle8771785

    Article  CAS  PubMed  Google Scholar 

  • MA. Coca C. Almoguera T. Thomas J. Jordano (1996) ArticleTitleDifferential regulation of small heat-shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter Plant Mol Biol 31 863–876 Occurrence Handle10.1007/BF00019473 Occurrence Handle1:CAS:528:DyaK28XlslCku7o%3D Occurrence Handle8806416

    Article  CAS  PubMed  Google Scholar 

  • A. Coleman L. Goff (1985) ArticleTitleApplication of fluorochromes to pollen biology I Mithramycin and 4′ 6-diamidino-2-phenylindole (DAPI) as vital stains and for quantification of nuclear DNA Stain Technol 60 145–154 Occurrence Handle1:CAS:528:DyaL2MXltVWgurg%3D Occurrence Handle2411019

    CAS  PubMed  Google Scholar 

  • JHG. Cordewener JBM. Custers HM. Dons M. VanLookeren Campagne (1996) Molecular and biochemical events during the induction of microspore embryogenesis SM. Mohanjain S. Sopory RE. Veilleux (Eds) In vitro Haploid Production in Higher Plants Kluwer Academic Publishers Dordrecht 111–124

    Google Scholar 

  • JHG. Cordewener G. Hause E. Gorgen R. Busink B. Hause HJM. Dons AAM. Van Lammeren M. VanLookeren Campagne P. Pechan (1995) ArticleTitleChanges in synthesis and localization of members of the 70-kDa class of heat shock proteins accompany the induction of embryogenesis in Brassica napus L microspores Planta 196 747–755 Occurrence Handle10.1007/BF01106770 Occurrence Handle1:CAS:528:DyaK2MXnt1aqu74%3D

    Article  CAS  Google Scholar 

  • JBM. Custers MT. Oldenhof JAM. Schrauwen JHG. Cordewener GJ. Wullems M. VanLookeren Campagne (1997) ArticleTitleAnalysis of microspore-specific promoters in transgenic tobacco Plant Mol Biol 35 689–699 Occurrence Handle10.1023/A:1005846527674 Occurrence Handle1:CAS:528:DyaK1cXis1Cqtw%3D%3D Occurrence Handle9426591

    Article  CAS  PubMed  Google Scholar 

  • E. Czarnecka WB. Gurley RT. Nagao L. Mosquera J. Key (1985) ArticleTitleDNA sequence and transcript mapping of a soybean gene encoding a small heart shock protein Proc Natl Acad Sci USA 82 3726–3730 Occurrence Handle1:CAS:528:DyaL2MXks1ygtb4%3D

    CAS  Google Scholar 

  • VA. Dzelzkàlns MK. Thorsness KG. Dwyer JS. Baxter MA. Balent M. Nasrallah J. Nasrallah (1993) ArticleTitleDistinct cis-acting elements direct pistil-specific and pollen-specific activity of the Brassica S locus glycoprotein gene promoter Plant Cell 5 855–863 Occurrence Handle10.1105/tpc.5.8.855 Occurrence Handle8400868

    Article  PubMed  Google Scholar 

  • J. Engel (1997) Signifikante Schule der schlichten Statistik Filander Verlag Fürth

    Google Scholar 

  • J. Gao SR. Kim YY. Chung J. Lee G. An (1994) ArticleTitleDevelopmental and environmental regulation of two ribosomal protein genes in tobacco Plant Mol Biol 25 761–770 Occurrence Handle10.1007/BF00028872 Occurrence Handle1:CAS:528:DyaK2cXmsVOksrc%3D Occurrence Handle8075394

    Article  CAS  PubMed  Google Scholar 

  • R. Gupta JTL. Ting LN. Sokolov S. Johnson S. Luan (2002) ArticleTitleA tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis Plant Cell 14 2495–2507 Occurrence Handle10.1105/tpc.005702 Occurrence Handle1:CAS:528:DC%2BD38XotFelsL0%3D Occurrence Handle12368500

    Article  CAS  PubMed  Google Scholar 

  • N. Gustavsson BP. Kokke U. Harndahl M. Silow U. Bechtold Z. Poghosyan D. Murphy W. Boelens C. Sundby (2002) ArticleTitleA peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein Plant J 29 545–553 Occurrence Handle10.1046/j.1365-313X.2002.029005545.x Occurrence Handle1:CAS:528:DC%2BD38XislOhsbw%3D Occurrence Handle11874568

    Article  CAS  PubMed  Google Scholar 

  • H. Harada M. Kyo J. Imamura (1988) The induction of embryogenesis in Nicotiana immature pollen culture G. Bock J. Marsh (Eds) Application of Plant Cell and Tissue Culture. Wiley Chichester 59–74

    Google Scholar 

  • E. Harlow D. Lane (1988) Antibodies: A Laboratory Manual Cold Spring Harbor Laboratory New York

    Google Scholar 

  • J. Hartwell GI. Jenkins M. Wilkins H. Nimmo (1999) ArticleTitleThe light induction of maize phosphoenolpyruvate carboxylase kinase translatable mRNA requires transcription but not translation Plant Cell Environ 22 883–889 Occurrence Handle10.1046/j.1365-3040.1999.00455.x Occurrence Handle1:CAS:528:DyaK1MXlsFGnsrk%3D

    Article  CAS  Google Scholar 

  • Hoch B, Lutsch G, Schlegel WP, Stahl J, Wallukat G, Bartel S, Krause EG, Benndorf R, Karczewski P (1996) HSP25 in isolated perfused rat hearts: localization and response to hyperthermia. Mol Cell Biochem 160–161:231–239

    Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R851–13

    Google Scholar 

  • S. Huang YQ. An JM. McDowell E. McKinney R. Meagher (1996) ArticleTitleThe Arabidopsis thaliana ACT4/ACT12 actin gene subclass is strongly expressed throughout pollen development Plant J 10 189–202 Occurrence Handle10.1046/j.1365-313X.1996.10020189.x Occurrence Handle1:CAS:528:DyaK28XlvFagsro%3D Occurrence Handle8771777

    Article  CAS  PubMed  Google Scholar 

  • Y. Jia RF. Ransom M. Shibanuma C. Liu M. Welsh W. Smoyer (2001) ArticleTitleIdentification and characterization of hic-5/ARA55 as an hsp27 binding protein J Biol Chem 276 39911–39918 Occurrence Handle10.1074/jbc.M103510200 Occurrence Handle1:CAS:528:DC%2BD3MXotFGiur0%3D Occurrence Handle11546764

    Article  CAS  PubMed  Google Scholar 

  • MK. Kandasamy EC. McKinney R. Meagher (1999) ArticleTitleThe late pollen-specific actins in angiosperms Plant J 18 681–691 Occurrence Handle10.1046/j.1365-313x.1999.00487.x Occurrence Handle1:CAS:528:DyaK1MXlsFGhtr0%3D Occurrence Handle10417720

    Article  CAS  PubMed  Google Scholar 

  • JL. Key C. Lin Y. Chen (1981) ArticleTitleHeat shock proteins of higher plants Proc Natl Acad Sci USA 78 3526–3530 Occurrence Handle1:CAS:528:DyaL3MXksFyitb0%3D

    CAS  Google Scholar 

  • SY. Kim C. Hong I. Lee (2001) ArticleTitleHeat shock stress causes stage-specific male sterility in Arabidopsis thaliana J Plant Res 114 301–307

    Google Scholar 

  • T. Kobayashi E. Kobayashi S. Sato Y. Hotta N. Miyajima A. Tanaka S. Tabata (1994) ArticleTitleCharacterization of cDNAs induced in meiotic prophase in Lily microsporocytes DNA Res 1 15–26 Occurrence Handle1:CAS:528:DyaK2MXmtVCjuw%3D%3D Occurrence Handle7584025

    CAS  PubMed  Google Scholar 

  • M. Kyo H. Harada (1986) ArticleTitleControl of the developmental pathway of tobacco pollen in vitro Planta 168 427–432 Occurrence Handle10.1007/BF00392260 Occurrence Handle1:CAS:528:DyaL28XlvVOksb4%3D

    Article  CAS  Google Scholar 

  • JH. Lee A. Hübel F. Schöffl (1995) ArticleTitleDepression of the activity of genetically enginered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermal tolerance in transgenic Arabidopsis Plant J 8 603–612 Occurrence Handle10.1046/j.1365-313X.1995.8040603.x Occurrence Handle1:CAS:528:DyaK2MXpslSnu7s%3D Occurrence Handle7496404

    Article  CAS  PubMed  Google Scholar 

  • GJ. Lee AM. Roseman H. 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 Handle1:CAS:528:DyaK2sXisV2it7c%3D Occurrence Handle9034347

    CAS  PubMed  Google Scholar 

  • G. Lee E. Vierling (2000) ArticleTitleA small heat shock protein cooperates with heat shock protein 70 system to reactivate a heat-denatured protein Plant Physiol 122 189–197 Occurrence Handle10.1104/pp.122.1.189 Occurrence Handle1:CAS:528:DC%2BD3cXmvFamtQ%3D%3D Occurrence Handle10631262

    Article  CAS  PubMed  Google Scholar 

  • D. Löw K. Brandle L. Nover C. Forreiter (2000) ArticleTitleCytosolic heat-stress proteins Hsp177 class I and Hsp173 class II of tomato act as molecular chaperones in vivo Planta 211 575–582 Occurrence Handle10.1007/s004250000315 Occurrence Handle11030557

    Article  PubMed  Google Scholar 

  • S. Marchetti G. Zaina C. Chiabà C. Pappalardo A. Pitotti (2001) ArticleTitleIsolation and characterization of an endonuclease synthesized by barley (Hordeum vulgare L) uninucleate microspores Planta 213 199–206 Occurrence Handle10.1007/s004250000507 Occurrence Handle1:CAS:528:DC%2BD3MXkt1aku7w%3D Occurrence Handle11469584

    Article  CAS  PubMed  Google Scholar 

  • J. Mascarenhas (1990) ArticleTitleGene activity during pollen development Ann Rev Plant Physiol Plant Mol Biol 41 317–338 Occurrence Handle10.1146/annurev.pp.41.060190.001533

    Article  Google Scholar 

  • J. Mascarenhas D. Crone (1996) ArticleTitlePollen and heat-shock response Sex Plant Reprod 9 370–374 Occurrence Handle10.1007/s004970050059

    Article  Google Scholar 

  • I. Mittermann I. Swoboda E. Pierson N. Eller D. Kraft R. Valenta E. Heberle-Bors (1995) ArticleTitleMolecular cloning and characterization of profilin from tobacco (Nicotiana tabacum): increased profilin expression during pollen maturation Plant Mol Biol 27 137–146 Occurrence Handle10.1007/BF00019185 Occurrence Handle1:CAS:528:DyaK2MXktFWlsb0%3D Occurrence Handle7865783

    Article  CAS  PubMed  Google Scholar 

  • JH. Mu H. Lee T. Kao (1994) ArticleTitleCharacterization of a pollen-expressed receptor-like kinase gene of Petunia inflata and the activity of its encoded kinase Plant Cell 6 709–721 Occurrence Handle10.1105/tpc.6.5.709 Occurrence Handle1:CAS:528:DyaK2cXmsVOmtrs%3D Occurrence Handle8038606

    Article  CAS  PubMed  Google Scholar 

  • T. Murashige F. Skoog (1962) ArticleTitleA revised medium for rapid growth and bioassays with tobacco tissue cultures Physiol Plant 15 437–497

    Google Scholar 

  • RT. Nagao E. Czarnecka WB. Gurley F. Schoeffl JL. Key (1985) ArticleTitleGenes for low-molecular-weight heat shock proteins of soybeans: sequence analysis of a multigene family Mol Cell Biol 5 3417–3428 Occurrence Handle1:CAS:528:DyaL28XmtlWrtg%3D%3D Occurrence Handle3939317

    CAS  PubMed  Google Scholar 

  • TC. Newman M. Ohme-Takagi C. Taylor P. Green (1993) ArticleTitleDST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco Plant Cell 5 701–714 Occurrence Handle10.1105/tpc.5.6.701 Occurrence Handle1:CAS:528:DyaK2cXhtVais74%3D Occurrence Handle8329900

    Article  CAS  PubMed  Google Scholar 

  • MT. Oldenhof PFM. Groot Particlede JH. Visser JM. Schrauwen G. Wullems (1996) ArticleTitleIsolation and characterization of a microspore-specific gene from tobacco Plant Mol Biol 31 213–225 Occurrence Handle10.1007/BF00021785 Occurrence Handle1:CAS:528:DyaK28XltFGltbw%3D Occurrence Handle8756588

    Article  CAS  PubMed  Google Scholar 

  • S. Park C. Hong (1998) ArticleTitleComparison of the structure and expression pattern for a low molecular weight heat-shock protein cDNA clone from Nicotiana tabacum Mol Cells 8 594–599 Occurrence Handle1:CAS:528:DyaK1cXotVeju7g%3D Occurrence Handle9856347

    CAS  PubMed  Google Scholar 

  • R. Prändl E. Kloske F. Schöffl (1995) ArticleTitleDevelopmental regulation and tissue specific differences of heat shock gene expression in transgenic tobacco and Arabidopsis plants Plant Mol Biol 28 73–82 Occurrence Handle10.1007/BF00042039 Occurrence Handle7787189

    Article  PubMed  Google Scholar 

  • V. Raghavan (1986) Emryogenesis in Angiosperms: A Developmental and Experimental Study Cambridge University Press New York

    Google Scholar 

  • W. Ramakrishna ZP. Deng CK. Ding A. Handa R. Ozminkowski (2003) ArticleTitleA novel small heat shock protein gene, vis1, contributes to pectin depolymerization and juice viscosity in tomato fruit Plant Physiol 131 725–735 Occurrence Handle10.1104/pp.012401 Occurrence Handle1:CAS:528:DC%2BD3sXhtlyjs7Y%3D Occurrence Handle12586896

    Article  CAS  PubMed  Google Scholar 

  • E. Raschke G. Baumann F. Schöffl (1988) ArticleTitleNucleotide sequence analysis of soybean small heat shock protein genes belonging to two different multigene families J Mol Biol 199 549–557 Occurrence Handle10.1016/0022-2836(88)90300-2 Occurrence Handle1:CAS:528:DyaL1cXls1CmtLg%3D Occurrence Handle3351943

    Article  CAS  PubMed  Google Scholar 

  • T. Reynolds (1997) ArticleTitlePollen embryogenesis Plant Mol Biol 33 1–10 Occurrence Handle10.1023/A:1005748614261 Occurrence Handle1:CAS:528:DyaK2sXhsVegs74%3D Occurrence Handle9037154

    Article  CAS  PubMed  Google Scholar 

  • MR. Roberts GD. Foster RP. Blundell SW. Robinson A. Kumar J. Draper R. Scott (1993) ArticleTitleGametophytic and sporophytic expression of an anther-specific Arabidopsis thaliana gene Plant J 3 111–120 Occurrence Handle10.1046/j.1365-313X.1993.t01-5-00999.x Occurrence Handle1:CAS:528:DyaK3sXisVyqsrg%3D Occurrence Handle8401599

    Article  CAS  PubMed  Google Scholar 

  • A. Sabehat S. Lurie D. Weiss (1998) ArticleTitleExpression of small heat-shock proteins at low temperatures Plant Physiol 117 651–658 Occurrence Handle10.1104/pp.117.2.651 Occurrence Handle1:CAS:528:DyaK1cXjvFGksb0%3D Occurrence Handle9625718

    Article  CAS  PubMed  Google Scholar 

  • J. Sambrook E. Fritsch T. Maniatis (1989) Molecular cloning Cold Spring Harbor Laboratory Press New York

    Google Scholar 

  • KD. Scharf M. Siddique E. Vierling (2001) ArticleTitleThe expending family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains Cell Stress Chaperones 6 225–238 Occurrence Handle1:CAS:528:DC%2BD3MXnslKhtb8%3D Occurrence Handle11599564

    CAS  PubMed  Google Scholar 

  • F. Schöffl J. Key (1982) ArticleTitleAn analysis of mRNAs for a group of heat shock proteins of soybean using cloned cDNAs J Mol Appl Genet 1 301–314 Occurrence Handle6896722

    PubMed  Google Scholar 

  • F. Schöffl R. Prändl A. Reindl (1998) ArticleTitleRegulation of the heat shock response Plant Physiol 117 1135–1141 Occurrence Handle10.1104/pp.117.4.1135 Occurrence Handle9701569

    Article  PubMed  Google Scholar 

  • F. Schöffl R. Prändl A. Reindl (1998) Molecular responses to heat stress K. Shinozaki K. Yamaguchi-Shinozaki (Eds) Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants. RG Landes Company Austin TX 81–98

    Google Scholar 

  • JM. Segui-Simarro P. Testillano MC. Risueno (2003) ArticleTitleHsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus L J Struct Biol 142 379–391 Occurrence Handle10.1016/S1047-8477(03)00067-4 Occurrence Handle12781665

    Article  PubMed  Google Scholar 

  • M. Singh PL. Blialla H. Xu M. Singh (2003) ArticleTitleIsolation and characterization of a flowering plant male gametic cell-specific promoter FEBS Lett 542 47–52 Occurrence Handle10.1016/S0014-5793(03)00335-1 Occurrence Handle1:CAS:528:DC%2BD3sXjt1OhtL4%3D Occurrence Handle12729896

    Article  CAS  PubMed  Google Scholar 

  • P. Smykal J. Masin I. Hrdy I. Konopasek V. Zarsky (2000) ArticleTitleChaperone activity of tobacco HSP18, a small heat-shock protein, is inhibited by ATP Plant J 23 703–713 Occurrence Handle10.1046/j.1365-313x.2000.00837.x Occurrence Handle1:CAS:528:DC%2BD3cXnslWgtrk%3D Occurrence Handle10998182

    Article  CAS  PubMed  Google Scholar 

  • W. Sun C. Bernard B. Vande Cotte M. Van Montagu N. Verbruggen (2001) ArticleTitleAt-HSP176A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression Plant J 27 407–415 Occurrence Handle10.1046/j.1365-313X.2001.01107.x Occurrence Handle1:CAS:528:DC%2BD3MXnvVansr0%3D Occurrence Handle11576425

    Article  CAS  PubMed  Google Scholar 

  • N. Sunderland F. Wicks (1973) ArticleTitleEmbryoid formation in pollen grains of Nicotiana tabacum J Exp Bot 22 213–226

    Google Scholar 

  • I. Tanaka (1997) ArticleTitleDifferentiation of generative and vegetative cells in angiosperm pollen Sex Plant Reprod 10 1–7 Occurrence Handle10.1007/s004970050060

    Article  Google Scholar 

  • SJ. Tebbutt H. Rogers D. Lonsdale (1994) ArticleTitleCharacterization of a tobacco gene encoding a pollen-specific polygalacturonase Plant Mol Biol 25 283–297 Occurrence Handle10.1007/BF00023244 Occurrence Handle1:CAS:528:DyaK2cXlsFSgtbg%3D Occurrence Handle8018876

    Article  CAS  PubMed  Google Scholar 

  • M. Thangavelu D. Belostotsky MW. Bevan RB. Flavell H. Rogers D. Lonsdale (1993) ArticleTitlePartial characterization of the Nicotiana tabacum actin gene family: evidence for pollen-specific expression of one of the gene family members Mol Gen Genet 240 290–295 Occurrence Handle1:CAS:528:DyaK2cXisVKjsg%3D%3D Occurrence Handle8355661

    CAS  PubMed  Google Scholar 

  • A. Touraev E. Heberle-Bors (1999) ArticleTitleMicrospore embryogenesis and In vitro pollen maturation in tobacco Methods Mol Biol 111 281–292 Occurrence Handle1:STN:280:DyaK1M7otVygtA%3D%3D Occurrence Handle10080995

    CAS  PubMed  Google Scholar 

  • RA. Volkov I. Panchuk F. Schöffl (2003) ArticleTitleHeat-stress dependent and developmental modulation of gene expression: the potential of house-keeping genes as internal standards in mRNA expression profiling using real-time RT-PCR J Exp Bot 54 2343–2349 Occurrence Handle10.1093/jxb/erg244 Occurrence Handle1:CAS:528:DC%2BD3sXns1CnsL0%3D Occurrence Handle14504302

    Article  CAS  PubMed  Google Scholar 

  • E. Waters (1995) ArticleTitleThe molecular evolution of the small heat-shock proteins in plants Genetics 141 785–795 Occurrence Handle1:CAS:528:DyaK28Xht1CgtLY%3D Occurrence Handle8647410

    CAS  PubMed  Google Scholar 

  • E. Waters E. Vierling (1999) ArticleTitleThe diversification of plant cytosolic small heart shock proteins preceded the divergence of mosses Mol Biol Evol 16 127–139 Occurrence Handle1:CAS:528:DyaK1MXjvVGksQ%3D%3D Occurrence Handle10331257

    CAS  PubMed  Google Scholar 

  • N. Wehmeyer LD. Hernandez R. Finkelstein E. Vierling (1996) ArticleTitleSynthesis of small heat-shock proteins is part of the developmental program of late seed maturation Plant Physiol 112 747–757 Occurrence Handle10.1104/pp.112.2.747 Occurrence Handle1:CAS:528:DyaK28XmsFKksb0%3D Occurrence Handle8883386

    Article  CAS  PubMed  Google Scholar 

  • N. Wehmeyer E. Vierling (2000) ArticleTitleThe expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance Plant Physiol 122 1099–1108 Occurrence Handle10.1104/pp.122.4.1099 Occurrence Handle1:CAS:528:DC%2BD3cXktFSqtbk%3D Occurrence Handle10759505

    Article  CAS  PubMed  Google Scholar 

  • H. Xu I. Swoboda PL. Bhalla AM. Sijbers C. Zhao EK. Ong J. Hoeijmakers M. Singh (1998) ArticleTitlePlant homologue of human excision repair gene ERCC1 points to conservation of DNA repair mechanisms Plant J 13 823–829 Occurrence Handle10.1046/j.1365-313X.1998.00081.x Occurrence Handle1:CAS:528:DyaK1cXislejsLs%3D Occurrence Handle9681020

    Article  CAS  PubMed  Google Scholar 

  • HL. Xu I. Swoboda P. Bhalla M. Singh (1999) ArticleTitleMale gametic cell-specific expression of H2A and H3 histone genes Plant Mol Biol 39 607–614 Occurrence Handle10.1023/A:1006162120037 Occurrence Handle1:CAS:528:DyaK1MXitFClu78%3D Occurrence Handle10092186

    Article  CAS  PubMed  Google Scholar 

  • HL. Xu I. Swoboda P. Bhalla M. Singh (1999) ArticleTitleMale gametic cell-specific gene expression in flowering plants Proc Natl Acad Sci USA 96 2554–2558 Occurrence Handle10.1073/pnas.96.5.2554 Occurrence Handle1:CAS:528:DyaK1MXhvVWjsr4%3D Occurrence Handle10051681

    Article  CAS  PubMed  Google Scholar 

  • B. Ylstra S. McCormick (1999) ArticleTitleAnalysis of mRNA stabilities during pollen development and in BY2 cells Plant J 20 101–108 Occurrence Handle10.1046/j.1365-313X.1999.00580.x Occurrence Handle1:CAS:528:DyaK1MXnsVGqsr4%3D Occurrence Handle10571869

    Article  CAS  PubMed  Google Scholar 

  • L. Young R. Wilen P. Bonham-Smith (2004) ArticleTitleHigh temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production J Exp Bot 55 485–495 Occurrence Handle10.1093/jxb/erh038 Occurrence Handle1:CAS:528:DC%2BD2cXms1entg%3D%3D Occurrence Handle14739270

    Article  CAS  PubMed  Google Scholar 

  • V. Zarsky D. Garrido N. Eller J. Tupy O. Vicente F. Schöffl E. Heberle-Bors (1995) ArticleTitleThe expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation Plant Cell Environ 18 139–147 Occurrence Handle1:CAS:528:DyaK2MXltlGiu7g%3D

    CAS  Google Scholar 

  • JP. Zhao W. Newcomb D. Simmonds (2003) ArticleTitleHeat-shock proteins 70 kDa and 19 kDa are not requiredfor induction of embryogenesis of Brassica napus L cv topas microspores Plant Cell Physiol 44 1417–1421 Occurrence Handle10.1093/pcp/pcg162 Occurrence Handle1:CAS:528:DC%2BD2cXhsFOjtQ%3D%3D Occurrence Handle14701938

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zentrum für Molekularbiologie der Pflanzen–Allgemeine Genetik, Universität Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany

    Roman A. Volkov, Irina I. Panchuk & Fritz Schöffl

Authors
  1. Roman A. Volkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irina I. Panchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fritz Schöffl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fritz Schöffl.

Electronic supplementary material

Electronic supplementary material

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volkov, R.A., Panchuk, I.I. & Schöffl, F. Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco. Plant Mol Biol 57, 487–502 (2005). https://doi.org/10.1007/s11103-005-0339-y

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-0339-y

Keywords

Search

Navigation