Skip to main content
Log in

Small heat shock protein LimHSP16.45 protects pollen mother cells and tapetal cells against extreme temperatures during late zygotene to pachytene stages of meiotic prophase I in David Lily

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Plant meiotic prophase I is a complicated process involving the late zygotene and pachytene stages, both crucial for completing synapsis and recombination. Using David Lily (Lilium davidii var. Willmottiae) as our research material, we performed suppression subtractive hybridization to construct EST library of anthers at various stages of development by the pollen mother cells. From this library, we identified small heat shock protein LimHSP16.45 was highly expressed during the late zygotene to pachytene stages. Our results also showed that LimHSP16.45 was almost specifically expressed in the anther compared with the root, stem, or leaf, and in situ expression of LimHSP16.45 mRNAs showed strong signals in the pollen mother cells and tapetal cells. LimHSP16.45 could be induced by heat and cold in lily anthers, and its ectopic expression enhanced the viability of E. coli cells under both high and low temperatures. In vitro, it acted as molecular chaperone and could help luciferase refolding after heat shock stress. All of these data suggest that LimHSP16.45, working as molecular chaperone, possibly protects pollen mother cells and tapetal cells against extreme temperatures during late zygotene to pachytene stages of meiotic prophase I in David Lily.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Atkinson BG, Raizada M, Bouchard RA, Frappier JRH, Walden DB (1993) The independent stage-specific expression of the 18 kDa heat shock protein genes during microsporogenesis in Zea mays L. Dev Genet 14:15–26

    Article  PubMed  CAS  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    Article  PubMed  CAS  Google Scholar 

  • Cabane M, Calvet P, Vincens P, Boudet AM (1993) Characterization of chilling-acclimation-related proteins in soybean and identification of one as a member of the heat shock protein (HSP70) family. Planta 190:346–353

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Romero JM, Doyle S, Elliot R, Murphy G, Carpenter R (1990) Floricaula a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322

    Article  PubMed  CAS  Google Scholar 

  • Dietrich PS, Bouchard RA, Casey ES, Sinibaldi RM (1991) Isolation and characterization of a small heat shock protein gene from maize. Plant Physiol 96:1268–1276

    Article  PubMed  CAS  Google Scholar 

  • Hamant O, Ma H, Cande WZ (2006) Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57:267–302

    Article  PubMed  CAS  Google Scholar 

  • Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266–1274

    Article  PubMed  CAS  Google Scholar 

  • Hopf N, Plesofsky-Vig N, Brambl R (1992) The heat shock response of pollen and other tissues of maize. Plant Mol Biol 19:623–630

    Article  PubMed  CAS  Google Scholar 

  • Horwitz J (1992) a-Crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    Article  PubMed  CAS  Google Scholar 

  • Huijser P, Klien J, Lonnig WE, Meijer H, Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly is caused by the loss of function of the MADS-box gene SQUAMOSA in Antirrhinum majus. EMBO J 11:1239–1249

    PubMed  CAS  Google Scholar 

  • Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    PubMed  CAS  Google Scholar 

  • Keeler SJ, Boettger CM, Haynes JG, Kuches KA, Johnson MM, Thureen DL, Keeler CL, Kitto SL (2000) Acquired thermotolerance and expression of the HSP100/ClpB genes of Lima Bean. Plant Physiol 123:1121–1132

    Article  PubMed  CAS  Google Scholar 

  • Krishna P, Sacco M, Cherutti JF, Hill S (1995) Cold-induced accumulation of hsp90 transcripts in Brassica napus. Plant Physiol 107:915–923

    PubMed  CAS  Google Scholar 

  • Kobayashi T, Kobayashi E, Sato S, Hotta Y, Miyajima N, Tanaka A, Tabata S (1994) Characterization of cDNAs induced in meiotic prophase in lily microsporocytes. DNA Res 1:15–26

    Article  PubMed  CAS  Google Scholar 

  • Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38:233–271

    Article  PubMed  CAS  Google Scholar 

  • Lam WS, Yang X, Makaroff CA (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci 118:3037–3048

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Won SH, Lee HS, Miyao M, Chung WI, Kim IJ, Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245:283–290

    Article  PubMed  CAS  Google Scholar 

  • Lee GJ, Roseman AM, Saibil HR, 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(3):659–671

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2DDCT method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  • Low D, Brandle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211:575–582

    Article  PubMed  CAS  Google Scholar 

  • Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, hsp17.7, results in increased or decreased thermotolerance double danger. Plant J 20:89–99

    Article  PubMed  CAS  Google Scholar 

  • Masson JY, West SC (2001) The Rad51 and Dmc1 recombinases: a non-identical twin relationship. Trends Biochem Sci 26:131–136

    Article  PubMed  CAS  Google Scholar 

  • Merck KB, Groenen PJ, Voorter CE, de Haard-Hoekman WA, Horwitz J, Bloemendal H, de Jong WW (1993) Structural and functional similarities of bovine-crystallin and mouse small heat-shock protein. J Biol Chem 268:1046–1052

    PubMed  CAS  Google Scholar 

  • Nakai A (1999) New aspects in the vertebrate heat stress factor system: HsfA3 and HsfA4. Cell Stress Chaperones 4:86–93

    Article  PubMed  CAS  Google Scholar 

  • Nover L (1991) Heat shock response. CRC Press, Boca Raton

    Google Scholar 

  • Nover L, Scharf KD (1997) Heat stress proteins and transcription factors. Cell MOI Life Sci 53:80–103

    Article  CAS  Google Scholar 

  • Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Schart KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6(3):177–189

    Article  PubMed  CAS  Google Scholar 

  • Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190(3):523–544

    Article  PubMed  CAS  Google Scholar 

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of proteins. Annu Rev Genet 27:437–496

    Article  PubMed  CAS  Google Scholar 

  • Prandl R, Kloske E, SchOffl F (1995) Developmental regulation and tissue-specific differences of heat shock gene expression in transgenic tobacco and Arabidopsis plants. Plant Mol Biol 28:73–82

    Article  PubMed  CAS  Google Scholar 

  • Puizina J, Siroky J, Mokros P, Schweizer D, Riha K (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–1978

    Article  PubMed  CAS  Google Scholar 

  • Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069–1080

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein smHSPs17.7. Plant Cell Rep 27:329–334

    Article  PubMed  CAS  Google Scholar 

  • Siaud N, Dray E, Gy I, Gerard E, Takvorian N, Doutriaux MP (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J 23:1392–1401

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Bernard C, van de Cotte B, van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415

    Article  PubMed  CAS  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Schoffl F (2005) Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco. Plant Mol Biol 57(4):487–502

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338

    Article  CAS  Google Scholar 

  • Wei LQ, Wen YX, Zhu YD, Su Z, Xue YB, Wang T (2010) Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11:338

    Article  PubMed  Google Scholar 

  • Yang JF, Stewart GR (1991) Response of higher plants to heat shock. Acta Botanica Sinica 33:292–296

    Google Scholar 

  • Yoon HJ, Kim KP, Park SM, Hong CB (2005) Functional Mode of NtHSP1 7.6, a cytosolic small heat-shock protein from Nicotiana tabacum. J Plant Biol 48(1):120–127

    Article  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Liu AL, Chen XB, Zhou XY, Gao GF, Wang WF, Zhang XW (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166(8):851–861

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by grants from the National Natural Science Foundation of China (No. 30970234), the Chunhui Program of Chinese Ministry of Education (2009), and Fundamental Research Funds for the Central Universities (No. lzujbky-2010-58).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heng Liu.

Additional information

Communicated by F. Brandizzi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mu, C., Wang, S., Zhang, S. et al. Small heat shock protein LimHSP16.45 protects pollen mother cells and tapetal cells against extreme temperatures during late zygotene to pachytene stages of meiotic prophase I in David Lily . Plant Cell Rep 30, 1981–1989 (2011). https://doi.org/10.1007/s00299-011-1106-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1106-y

Keywords

Navigation