Skip to main content
SpringerLink
Log in

Genome wide and evolutionary analysis of heat shock protein 70 proteins in tomato and their role in response to heat and drought stress

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Heat shock protein 70 (HSP70) proteins play a crucial role in mitigating the detrimental effects of abiotic stresses in plants. In the present study, 21 full length non-redundant SlHSP70 genes were detected and characterized in tomato (Solanum lycopersicum L.). The SlHSP70 genes were classified into four groups based on phylogenetic analysis. Similarities were observed in gene features and motif structures of SlHSP70s belonging to the same group. SlHSP70 genes were unevenly and unequally mapped on 11 chromosomes. Segmental and tandem duplication are the main events that have contributed to the expansion of the SlHSP70 genes. A large number of groups and sub-groups were generated during comparative analysis of HSP70 genes in multiple plant species including tomato. These findings indicated a common ancestor which created diverse sub-groups prior to a mono-dicot split. The selection pressure on specific codons was identified through a maximum-likelihood approach and we found some important coding sites in the coding region of all groups. Diversifying positive selection was indirectly associated with evolutionary changes in SlHSP70 proteins and suggests that gene evolution modulated the tomato domestication event. In addition, expression analysis using RNA-seq revealed that 21 SlHSP70 genes were differentially expressed in response to drought and heat stress. SlHSP70-5 was down-regulated by heat treatment and up-regulated by drought stress. Furthermore, the expression of some of the duplicate genes was partially redundant, while others showed functional diversity. Our results indicate the diverse role of HSP70 gene family in S. lycopersicum under drought and heat stress conditions and open the gate for further investigation of HSP70 gene family functions, especially under drought and heat stress.

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

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

Similar content being viewed by others

References

  1. 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(5):244–252. https://doi.org/10.1016/j.tplants.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  2. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10(3):310–316. https://doi.org/10.1016/j.pbi.2007.04.011

    Article  CAS  PubMed  Google Scholar 

  3. Lata C, Yadav A, Prasad M (2011) Role of plant transcription factors in abiotic stress tolerance. Abiotic stress response in plants, vol 10. INTECH Open Access Publishers, London, pp 269–296

    Google Scholar 

  4. Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64(2):391–403. https://doi.org/10.1093/jxb/ers355

    Article  CAS  PubMed  Google Scholar 

  5. Datta K, Rahalkar K, Dinesh D (2017) Heat shock proteins (Hsp): classifications and its involvement in health and disease. J Pharma Care Health Syst 4(2):1–3

    Google Scholar 

  6. Renner T, Waters ER (2007) Comparative genomic analysis of the Hsp70s from five diverse photosynthetic eukaryotes. Cell Stress Chaperones 12(2):172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1(2):97–98. https://doi.org/10.1379/1466-1268(1996)001%3c0097:dothsr%3e2.3.co;2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sung DY, Kaplan F, Guy CL (2001) Plant Hsp70 molecular chaperones: protein structure, gene family, expression and function. Physiol Plant 113(4):443–451

    Article  CAS  Google Scholar 

  9. Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11(8):579–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684. https://doi.org/10.1007/s00018-004-4464-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tomiczek B, Delewski W, Nierzwicki L, Stolarska M, Grochowina I, Schilke B, Dutkiewicz R, Uzarska MA, Ciesielski SJ, Czub J, Craig EA, Marszalek J (2020) Two-step mechanism of J-domain action in driving Hsp70 function. PLoS Comput Biol 16(6):e1007913. https://doi.org/10.1371/journal.pcbi.1007913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim JY, Barua S, Huang MY, Park J, Yenari MA, Lee JE (2020) Heat shock protein 70 (HSP70) induction: chaperonotherapy for neuroprotection after brain injury. Cells 9(9):2020. https://doi.org/10.3390/cells9092020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zuiderweg ER, Hightower LE, Gestwicki JE (2017) The remarkable multivalency of the Hsp70 chaperones. Cell Stress Chaperones 22(2):173–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Collins EJ, Bowyer C, Tsouza A, Chopra M (2022) Tomatoes: an extensive review of the associated health impacts of tomatoes and factors that can affect their cultivation. Biology (Basel) 11(2):239

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Song B, Liu K, Gao Y, Zhao L, Fang H, Li Y, Pei L, Xu Y (2017) Lycopene and risk of cardiovascular diseases: a meta-analysis of observational studies. Mol Nutr Food Res 61(9):1601009

    Article  Google Scholar 

  16. Niinemets Ü, Valladares F (2004) Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biol 6(03):254–268

    Article  CAS  PubMed  Google Scholar 

  17. El Sappah A, Abbas M, Elrys AS, Yadav V, El-Sappah HH, Zhu Y, Huang Q, Yu W, Soaud SA, Xianming Z (2021) The Hsp70 gene family in Solanum lycopersicum; genome-wide identification and expression analysis under heavy metals stresses.

  18. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944

    Article  CAS  PubMed  Google Scholar 

  19. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31(13):3784–3788. https://doi.org/10.1093/nar/gkg563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chen C, Chen H, He Y, Xia R (2018) TBtools, a toolkit for biologists integrating various biological data handling tools with a user-friendly interface. BioRxiv. https://doi.org/10.1101/289660

    Article  Google Scholar 

  21. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Simpson MG (2010) Plant systematics. Phylogenetic systematics, 2nd edn. Academic Press, Cambridge

    Google Scholar 

  23. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373. https://doi.org/10.1093/nar/gkl198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301. https://doi.org/10.1093/nar/gkr1065

    Article  CAS  PubMed  Google Scholar 

  25. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):10

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lee TH, Kim J, Robertson JS, Paterson AH (2017) Plant genome duplication database. Methods Mol Biol (Clifton, NJ) 1533:267–277. https://doi.org/10.1007/978-1-4939-6658-5_16

    Article  CAS  Google Scholar 

  27. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kosakovsky Pond S, Delport W, Muse SV, Scheffler K (2010) Correcting the bias of empirical frequency parameter estimators in codon models. PLoS ONE 5(7):e11230

    Article  PubMed  PubMed Central  Google Scholar 

  29. Stanfel LE (1996) A new approach to clustering the amino acid. J Theor Biol 183(2):195–205

    Article  CAS  PubMed  Google Scholar 

  30. Delport W, Scheffler K, Botha G, Gravenor MB, Muse SV, Pond SLK (2010) CodonTest: modeling amino acid substitution preferences in coding sequences. PLoS Comput Biol 6(8):e1000885

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kosiol C, Holmes I, Goldman N (2007) An empirical codon model for protein sequence evolution. Mol Biol Evol 24(7):1464–1479

    Article  CAS  PubMed  Google Scholar 

  32. Davoudi M, Chen J, Lou Q (2022) Genome-wide identification and expression analysis of heat shock protein 70 (HSP70) gene family in pumpkin (Cucurbita moschata) rootstock under drought stress suggested the potential role of these chaperones in stress tolerance. Int J Mol Sci 23(3):1918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang L, Zhao H-K, Dong Q-l, Zhang Y-Y, Wang Y-M, Li H-Y, Xing G-J, Li Q-Y, Dong Y-S (2015) Genome-wide analysis and expression profiling under heat and drought treatments of HSP70 gene family in soybean (Glycine max L.). Front Plant Sci 6:773

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zhang Y, Wang M, Chen J, Rong J, Ding M (2014) Genome-wide analysis of HSP70 superfamily in Gossypium raimondii and the expression of orthologs in Gossypium hirsutum. Yi Chuan = Hereditas 36(9):921–933

    CAS  PubMed  Google Scholar 

  35. Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 31(4):597–606

    Article  CAS  PubMed  Google Scholar 

  36. Kose S, Furuta M, Imamoto N (2012) Hikeshi, a nuclear import carrier for Hsp70s, protects cells from heat shock-induced nuclear damage. Cell 149(3):578–589

    Article  CAS  PubMed  Google Scholar 

  37. Jung K-H, Gho H-J, Nguyen MX, Kim S-R, An G (2013) Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress. Funct Integr Genomics 13(3):391–402

    Article  CAS  PubMed  Google Scholar 

  38. Lin B-L, Wang J-S, Liu H-C, Chen R-W, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6(3):201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sarkar NK, Kundnani P, Grover A (2013) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18(4):427–437

    Article  CAS  PubMed  Google Scholar 

  40. Lespinet O, Wolf YI, Koonin EV, Aravind L (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12(7):1048–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17(6):505–512

    Article  PubMed  Google Scholar 

  42. Ahmad MZ, Sana A, Jamil A, Nasir JA, Ahmed S, HameedAbdullah MU (2019) A genome-wide approach to the comprehensive analysis of GASA gene family in Glycine max. Plant Mol Biol 100(6):607–620

    Article  CAS  PubMed  Google Scholar 

  43. Blanc G, Wolfe K (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell Online 16(7):1667–1678

    Article  CAS  Google Scholar 

  44. Ha M, Kim E-D, Chen ZJ (2009) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc Natl Acad Sci USA 106(7):2295–2300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Force A, Lynch M, Pickett FB, Amores A, Yan Y-l, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Fetterman CD, Rannala B, Walter MA (2008) Identification and analysis of evolutionary selection pressures acting at the molecular level in five forkhead subfamilies. BMC Evol Biol 8(1):261

    Article  PubMed  PubMed Central  Google Scholar 

  47. Marini NJ, Thomas PD, Rine J (2010) The use of orthologous sequences to predict the impact of amino acid substitutions on protein function. PLoS Genet 6(5):e1000968

    Article  PubMed  PubMed Central  Google Scholar 

  48. Czarnecka E, Key J, Gurley WB (1989) Regulatory domains of the Gmhsp17.5-E heat shock promoter of soybean. Mol Cell Biol 9(8):3457–3463

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6(2):251–264

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Kurepa J, Wang S, Li Y, Smalle J (2009) Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav 4(10):924–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thanks the whole team participated in this research work and present it in front of scientific community.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Author notes

  1. Muhammad Zulfiqar Ahmad and Zamarud Shah have contributed equally.

Authors and Affiliations

  1. Department of Plant Breeding and Genetics, Faculty of Agriculture, University of Agriculture, D.I. Khan, Pakistan

    Muhammad Zulfiqar Ahmad

  2. Department of Biotechnology, University of Science and Technology, Bannu, Pakistan

    Zamarud Shah, Arif Ullah & Afrasyab Khan

  3. Institute de Farmacia, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, 5090000, Valdivia, Chile

    Shakeel Ahmed

  4. Department of Biochemistry, Shaheed Benazir Bhutto Women University, Peshawar, Pakistan

    Bushra Ahmad

Authors
  1. Muhammad Zulfiqar Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zamarud Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arif Ullah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shakeel Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bushra Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Afrasyab Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MZA and ZS designed the research. MZA, ZS, AU, AK extracted the data. MZA, ZS and AU analysed and wrote the manuscript. MZA, BA and SA arranged and revised the manuscript. All the contributors read and approved for submission.

Corresponding author

Correspondence to Muhammad Zulfiqar Ahmad.

Ethics declarations

Conflict of interest

All authors did not have any conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PPT 1297 KB)

Supplementary file2 (XLS 137 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmad, M.Z., Shah, Z., Ullah, A. et al. Genome wide and evolutionary analysis of heat shock protein 70 proteins in tomato and their role in response to heat and drought stress. Mol Biol Rep 49, 11229–11241 (2022). https://doi.org/10.1007/s11033-022-07734-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-022-07734-1

Keywords

Search

Navigation