Skip to main content
Log in

The Populus trichocarpa PtHSP17.8 involved in heat and salt stress tolerances

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

Abstract

Key message

PtHSP17.8 was regulated by various abiotic stresses. Overexpression of PtHSP17.8 enhanced the tolerance to heat and salt stresses through maintain ROS homeostasis and cooperate with stress-related genes in Arabidopsis.

Abstract

Small heat shock proteins (sHSPs) play important roles in response to diverse biotic and abiotic stresses, especially in heat tolerance. However, limited information is available on the stress tolerance roles of sHSPs in woody species. To explore the function of sHSPs in poplar, we isolated and characterized PtHSP17.8 from Populus trichocarpa. Phylogenetic analysis and subcellular localization revealed that PtHSP17.8 was a cytosolic class I sHSP. The gene expression profile of PtHSP17.8 in various tissues showed that it was significantly accumulated in stem and root, which was consistent with the GUS expression pattern driven by promoter of PtHSP17.8. The expression of PtHSP17.8 could be induced by various abiotic stresses and significantly activated by heat stress. Overexpression of PtHSP17.8 enhanced the tolerance to heat and salt stresses in Arabidopsis. The seedling survival rate, root length, relative water content, antioxidative enzyme activities, proline, and soluble sugar content were increased in transgenic Arabidopsis under heat and salt stresses, but not in normal condition. The co-expression network of PtHSP17.8 were constructed and demonstrated many stress responsive genes included. The stress-related genes in the co-expression network were up-regulated in the PtHSP17.8 overexpression seedlings. These results suggest that PtHSP17.8 confers heat and salt tolerances in plants.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  CAS  PubMed  Google Scholar 

  • Al-Whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ Sci 23:139–150

    Article  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  • Bradshaw H, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313

    Article  CAS  Google Scholar 

  • Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35:1912–1931

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung HS, Koo AJ, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146:952–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ, Wang X, Qiu AL, Zhang TX, Lin J (2013) CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 36:757–774

    Article  CAS  PubMed  Google Scholar 

  • De Jong W, Leunissen J, Voorter C (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126

    PubMed  Google Scholar 

  • del Carmen Martinez-Ballesta M, Carvajal M (2014) New challenges in plant aquaporin biotechnology. Plant Sci 217:71–77

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    Article  CAS  PubMed  Google Scholar 

  • Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Article  CAS  PubMed  Google Scholar 

  • Hubberten H-M, Watanabe M, Bielecka M, Heyneke E, Aarabi F, Hoefgen R (2015) More than a substrate: the O-acetylserine responsive transcriptome. In: Molecular physiology and ecophysiology of sulfur. Springer, Berlin, pp 133–143

  • Jiang C, Xu J, Zhang H, Zhang X, Shi J, Li M, Ming F (2009) A cytosolic class I small heat shock protein, RcHSP17. 8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ 32:1046–1059

    Article  CAS  PubMed  Google Scholar 

  • Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenol oxidase activities during rice leaf senescence. Plant Physiol 57:315–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DH, Xu Z-Y, Hwang I (2013) AtHSP17.8 overexpression in transgenic lettuce gives rise to dehydration and salt stress resistance phenotypes through modulation of ABA-mediated signaling. Plant Cell Rep 32:1953–1963

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Wang L, Zhang J, Li J, Zheng H, Chen J, Lu M (2014) WUSCHEL-related Homeobox genes in Populus tomentosa: diversified expression patterns and a functional similarity in adventitious root formation. BMC Genom 15:296

    Article  Google Scholar 

  • Ma C, Haslbeck M, Babujee L, Jahn O, Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141:47–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami T, Matsuba S, Funatsuki H, Kawaguchi K, Saruyama H, Tanida M, Sato Y (2004) Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol Breed 13:165–175

    Article  CAS  Google Scholar 

  • Pirkkala L, Nykänen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15:1118–1131

    Article  CAS  PubMed  Google Scholar 

  • Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotox Environ Safe 104:202–208

    Article  CAS  Google Scholar 

  • Ruibal C, Castro A, Carballo V, Szabados L, Vidal S (2013) Recovery from heat, salt and osmotic stress in Physcomitrella patens requires a functional small heat shock protein PpHsp16.4. BMC Plant Biol 13:174

    Article  PubMed  PubMed Central  Google Scholar 

  • Sabehat A, Lurie S, Weiss D (1998) Expression of small heat-shock proteins at low temperatures a possible role in protecting against chilling injuries. Plant Physiol 117:651–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song H, Fan P, Li Y (2009) Overexpression of organellar and cytosolic AtHSP90 in Arabidopsis thaliana impairs plant tolerance to oxidative stress. Plant Mol Biol Rep 27:342–349

    Article  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  CAS  PubMed  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. BBA Gene Struct Expr 1577:1–9

    Article  CAS  Google Scholar 

  • Sun L, Liu Y, Kong X, Zhang D, Pan J, Zhou Y, Wang L, Li D, Yang X (2012) ZmHSP16. 9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. Plant Cell Rep 31:1473–1484

    Article  CAS  PubMed  Google Scholar 

  • Topp SD (2008) Regulation of defense responses mediated by Bon1 and Bap2 in Arabidopsis thaliana. Cornell University, Ithaca

    Google Scholar 

  • Wang F, Dong Q, Jiang H, Zhu S, Chen B, Xiang Y (2012) Genome-wide analysis of the heat shock transcription factors in Populus trichocarpa and Medicago truncatula. Mol Biol Rep 39:1877–1886

    Article  PubMed  Google Scholar 

  • Wang A, Yu X, Mao Y, Liu Y, Liu G, Liu Y, Niu X (2015) Overexpression of a small heat-shock-protein gene enhances tolerance to abiotic stresses in rice. Plant Breed 134:384–393

    Article  CAS  Google Scholar 

  • Yan Y, Stolz S, Chételat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19:2470–2483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Yang S, Li Y, Hua J (2007) The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiol 145:135–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Liu S, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol Biol 68:131–143

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genom 14(1):532

    Article  CAS  Google Scholar 

  • Zhang L, Zhang Q, Gao Y, Pan H, Shi S, Wang Y (2014) Overexpression of heat shock protein gene PfHSP21.4 in Arabidopsis thaliana enhances heat tolerance. Acta Physiol Plant 36:1555–1564

    Article  CAS  Google Scholar 

  • Zhang J, Liu B, Li J, Zhang L, Wang Y, Zheng H, Lu M, Chen J (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genom 16(1):1

    Article  Google Scholar 

  • Zhang J, Chen H, Wang H, Li B, Yi Y, Kong F, Liu J, Zhang H (2016) Constitutive expression of a tomato small heat shock protein gene LeHSP21 improves tolerance to high-temperature stress by enhancing antioxidation capacity in tobacco. Plant Mol Biol Rep 34:399–409

    Article  CAS  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu D, Li R, Liu X, Sun M, Wu J, Zhang N, Zhu Y (2014) The positive regulatory roles of the TIFY10 proteins in plant responses to alkaline stress. PLoS One 9:e111984

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the China Postdoctoral Science Foundation [2014 M550104] to J.Z. and the National Key Basic Research Program of China [2012CB114500] and a Collaborative Innovation Plan of Jiangsu Higher Education to M.L.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jin Zhang or Mengzhu Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by K Chong.

J. Li and J. Zhang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2016_1973_MOESM1_ESM.tif

Fig. S1 The cis- acting elements in promoter of PtHSP17.8 gene were searched in PlantCARE database. The promoter region (1.5 kb upstream to 0.5 kb downstream of the transcription starting site) of PtHSP17.8 was analyzed in PlantCARE database (a). The description and statistics of cis-acting elements were shown in (b). (TIFF 1107 kb)

Table S1. Primer sequences used in this study (XLSX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, J., Zhang, J., Jia, H. et al. The Populus trichocarpa PtHSP17.8 involved in heat and salt stress tolerances. Plant Cell Rep 35, 1587–1599 (2016). https://doi.org/10.1007/s00299-016-1973-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1973-3

Keywords

Navigation