Skip to main content
Log in

Genome-wide identification of salinity responsive HSP70s in common bean

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

Abstract

The present study is aimed to identify and characterize HSP70 (PvHSP70) genes in two different common bean cultivars under salt stress. For this purpose various in silico methods such as RNAseq data and qRT-PCR analysis were used. A total of 24 candidate PvHSP70 gene were identified. Except for chromosome 4 and 7, these candidate PvHSP70 genes were distributed on the remaining chromosomes. While the lowest number of PvHSP70 genes was determined on chromosomes 1, 3, 5, 7, 9, 10 and 11 (one HSP70 gene), the highest number of PvHSP70s was on chromosomes 6 and 8 (seven HSP70 genes each). Three genes; PvHSP70-5, -9, and -10 were found to have no-introns. In addition, four tandemly and six segmentally duplicated gene couples were detected. A total of 13 PvHSP70 genes were targeted by miRNAs of 44 plant species and the most targeted genes were PvHSP70-5 and -23. The expression profile of PvHSP70 genes based on publicly available RNA-seq data was identified and salt treated leaf tissue was found to have more gene expression levels compared to the root. qRT-PCR analysis showed that the transcript concentrations of upregulated PvHSP70 genes in leaves of Zulbiye (sensitive) were mostly higher than those of Yakutiye (resistant). The present study revealed that PvHSP70 genes might play an important role in salt stress response for common bean cultivars and variability between cultivars also suggests that these genes could be used as functional markers for salt tolerance in common bean.

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
Fig. 7

Similar content being viewed by others

References

  1. Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J proteom 71(4):391–411. doi:10.1016/j.jprot.2008.07.005

    Article  CAS  Google Scholar 

  2. Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15(12):664–674. doi:10.1016/j.tplants.2010.08.002

    Article  CAS  PubMed  Google Scholar 

  3. Li Z, Srivastava P (2004) Heat-shock proteins. Current protocols in immunology/edited by John E Coligan [et al] Appendix 1:Appendix 1T.10.1002/0471142735.ima01ts58

  4. Cashikar AG, Duennwald M, Lindquist SL (2005) A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280(25):23869–23875. doi:10.1074/jbc.M502854200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genom 10:393. doi:10.1186/1471-2164-10-393

    Article  Google Scholar 

  6. 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. doi:10.1016/j.tplants.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  7. Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272(5268):1606–1614

    Article  CAS  PubMed  Google Scholar 

  8. Masand S, Yadav SK (2016) Overexpression of MuHSP70 gene from Macrotyloma uniflorum confers multiple abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 43(2):53–64. doi:10.1007/s11033-015-3938-y

    Article  CAS  PubMed  Google Scholar 

  9. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40(2):253–266. doi:10.1016/j.molcel.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  10. Masand S, Yadav SK (2016) Overexpression of MuHSP70 gene from Macrotyloma uniflorum confers multiple abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 43(2):53–64

    Article  CAS  PubMed  Google Scholar 

  11. Sung DY, Kaplan F, Guy CL (2001) Plant Hsp70 molecular chaperones: protein structure, gene family, expression and function. Physiol Plant 113(4):443–451. doi:10.1034/j.1399-3054.2001.1130402.x

    Article  CAS  Google Scholar 

  12. Guy CL, Li QB (1998) The organization and evolution of the spinach stress 70 molecular chaperone gene family. Plant Cell 10(4):539–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhou SJ, Jing Z, Shi JL (2013) Genome-wide identification, characterization, and expression analysis of the MLO gene family in Cucumis sativus. Genet mol res 12(4):6565–6578. doi:10.4238/2013.December.11.8

    Article  CAS  PubMed  Google Scholar 

  14. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647. doi:10.1146/annurev.biochem.70.1.603

    Article  CAS  PubMed  Google Scholar 

  15. Daugaard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581(19):3702–3710. doi:10.1016/j.febslet.2007.05.039

    Article  CAS  PubMed  Google Scholar 

  16. Jego G, Hazoume A, Seigneuric R, Garrido C (2013) Targeting heat shock proteins in cancer. Cancer Lett 332(2):275–285. doi:10.1016/j.canlet.2010.10.014

    Article  CAS  PubMed  Google Scholar 

  17. Alvim FC, Carolino SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126(3):1042–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cho EK, Hong CB (2006) Over-expression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep 25(4):349–358. doi:10.1007/s00299-005-0093-2

    Article  CAS  PubMed  Google Scholar 

  19. Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146(3):1231–1241. doi:10.1104/pp.107.114496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jungkunz I, Link K, Vogel F, Voll LM, Sonnewald S, Sonnewald U (2011) AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. Plant J 66(6):983–995. doi:10.1111/j.1365-313X.2011.04558.x

    Article  CAS  PubMed  Google Scholar 

  21. Augustine SM, Cherian AV, Syamaladevi DP, Subramonian N (2015) Erianthus arundinaceus HSP70 (EaHSP70) acts as a key regulator in the formation of anisotropic interdigitation in sugarcane (saccharum spp. hybrid) in response to drought stress. Plant Cell Physiol 56(12):2368–2380

    Article  CAS  PubMed  Google Scholar 

  22. Yer EN, Baloglu MC, Ziplar UT, Ayan S, Unver T (2015) Drought-responsive Hsp70 gene analysis in populus at genome-wide level. Plant Molecular Biology Reporter.1–18

  23. Goodstein DM, Shu SQ, 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(D1):D1178–D1186. doi:10.1093/nar/gkr944

    Article  CAS  PubMed  Google Scholar 

  24. Guo AY, Zhu QH, Chen X, Luo JC (2007) [GSDS: a gene structure display server]. Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji 29 (8):1023–1026

  25. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J hered 93(1):77–78

    Article  CAS  PubMed  Google Scholar 

  26. Yang ZF, Gu SL, Wang XF, Li WJ, Tang ZX, Xu CW (2008) Molecular evolution of the CPP-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 67(3):266–277. doi:10.1007/s00239-008-9143-z

    Article  CAS  PubMed  Google Scholar 

  27. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic acids research 34 (Web Server issue):W369–373. 10.1093/nar/gkl198

  28. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic acids research 33 (Web Server issue):W116–120. 10.1093/nar/gki442

  29. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. doi:10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Letunic I, Bork P (2011) Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478. doi:10.1093/nar/gkr201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35 (Web Server issue):W585–587. 10.1093/nar/gkm259

  33. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP SignalP and related tools. Nat Protoc 2(4):953–971

    Article  CAS  PubMed  Google Scholar 

  34. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. doi:10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  35. Zhang YJ (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704. doi:10.1093/nar/gki383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28(1):235–242. doi:10.1093/Nar/28.1.235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4(3):363–371. doi:10.1038/nprot.2009.2

    Article  CAS  PubMed  Google Scholar 

  38. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34 (Web Server issue):W609-612.10.1093/nar/gkl315

  39. Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genom 3(1–4):35–44

    Article  CAS  Google Scholar 

  40. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17(1):32–43

    Article  CAS  PubMed  Google Scholar 

  41. Hiz MC, Canher B, Niron H, Turet M (2014) Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PLoS One 9(3):e92598. doi:10.1371/journal.pone.0092598

    Article  PubMed  PubMed Central  Google Scholar 

  42. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628. doi:10.1038/nmeth.1226

    Article  CAS  PubMed  Google Scholar 

  43. Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21(7):1280–1281. doi:10.1093/bioinformatics/bti141

    Article  CAS  PubMed  Google Scholar 

  44. Guler NS, Saglam A, Demiralay M, Kadioglu A (2012) Apoplastic and symplastic solute concentrations contribute to osmotic adjustment in bean genotypes during drought stress. Turk J Biol 36(2):151–160. doi:10.3906/biy-1101-177

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  46. Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6(3):201–208. doi:10.1379/1466-1268(2001)006<0201:Gaoths>2.0.Co;2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhou SJ, Jing Z, Shi JL (2013) Genome-wide identification, characterization, and expression analysis of the MLO gene family in Cucumis sativus. Genet Mol Res 12(4):6565–6578. doi:10.4238/2013.December.11.8

    Article  CAS  PubMed  Google Scholar 

  48. Wang Y, Lin S, Song Q, Li K, Tao H, Huang J, Chen X, Que S, He H (2014) Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: hsp70s as a case study. BMC Genom 15:344. doi:10.1186/1471-2164-15-344

    Article  Google Scholar 

  49. 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/Zhongguo yi chuan xue hui bian ji 36 (9):921–933

  50. Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48(4):535–547. doi:10.1111/j.1365-313X.2006.02889.x

    Article  CAS  PubMed  Google Scholar 

  51. 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(8):1046–1059. doi:10.1111/j.1365-3040.2009.01987.x

    Article  CAS  PubMed  Google Scholar 

  52. 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 14:532. doi:10.1186/1471-2164-14-532

    Article  CAS  Google Scholar 

  53. Yang JY, Sun Y, Sun AQ, Yi SY, Qin J, Li MH, Liu J (2006) The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant Mol Biol 62(3):385–395. doi:10.1007/s11103-006-9027-9

    Article  CAS  PubMed  Google Scholar 

  54. Sarkar NK, Kundnani P, Grover A (2013) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18(4):427–437. doi:10.1007/s12192-012-0395-6

    Article  CAS  PubMed  Google Scholar 

  55. Zhang J, Li JB, Liu BB, Zhang L, Chen J, Lu MZ (2013) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genom 14:532. doi:10.1186/1471-2164-14-532

    Article  CAS  Google Scholar 

  56. Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New phytol 183(3):557–564. doi:10.1111/j.1469-8137.2009.02923.x

    Article  PubMed  Google Scholar 

  57. Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92(1):155–161

    Article  PubMed  Google Scholar 

  58. Wang YP, Wang XY, Tang HB, Tan X, Ficklin SP, Feltus FA, Paterson AH (2011) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 6(12):e28150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhang L, Zhao HK, Dong QL, Zhang YY, Wang YM, Li HY, Xing GJ, Li QY, Dong YS (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. doi:10.3389/fpls.2015.00773

    Google Scholar 

  60. Hou JJ, Jiang PP, Qi SM, Zhang K, He QX, Xu CZ, Ding ZH, Zhang KW, Li KP (2016) Isolation and functional validation of salinity and osmotic stress inducible promoter from the maize type-ii h + -pyrophosphatase gene by deletion analysis in transgenic tobacco plants. PLoS One 11(4):e0154041

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 31(4):597–606. doi:10.1007/s10529-008-9880-5

    Article  CAS  PubMed  Google Scholar 

  63. Kose S, Furuta M, Imamoto N (2012) Hikeshi, a nuclear import carrier for Hsp70 s, protects cells from heat shock-induced nuclear damage. Cell 149(3):578–589. doi:10.1016/j.cell.2012.02.058

    Article  CAS  PubMed  Google Scholar 

  64. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20(8):2238–2251. doi:10.1105/tpc.108.059444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Chi X, Yang Q, Chen X, Wang J, Pan L, Chen M, Yang Z, He Y, Liang X, Yu S (2011) Identification and characterization of microRNAs from peanut (Arachis hypogaea L.) by high-throughput sequencing. PLoS One 6(11):e27530. doi:10.1371/journal.pone.0027530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Debernardi JM, Rodriguez RE, Mecchia MA, Palatnik JF (2012) Functional specialization of the plant mir396 regulatory network through distinct microrna-target interactions. PLoS Genet. doi:10.1371/journal.pgen.1002419

    PubMed  PubMed Central  Google Scholar 

  67. Rodriguez RE, Ercoli MF, Debernardi JM, Breakfield NW, Mecchia MA, Sabatini M, Cools T, De Veylder L, Benfey PN, Palatnik JF (2015) MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in arabidopsis roots. Plant Cell 27(12):3354–3366

    Article  CAS  PubMed  Google Scholar 

  68. Liu DM, Yu DQ (2009) MicroRNA (miR396) negatively regulates expression of ceramidase-like genes in Arabidopsis. Prog Nat Sci 19(6):781–785. doi:10.1016/j.pnsc.2008.09.006

    Article  CAS  Google Scholar 

  69. Dong CH, Pei HX (2014) Over-expression of miR397 improves plant tolerance to cold stress in Arabidopsis thaliana. J Plant Biol 57(4):209–217. doi:10.1007/s12374-013-0490-y

    Article  CAS  Google Scholar 

  70. Guleria P, Yadav SK (2011) Identification of miR414 and expression analysis of conserved miRNAs from Stevia rebaudiana. Genom proteom bioinform 9(6):211–217. doi:10.1016/S1672-0229(11)60024-7

    Article  CAS  Google Scholar 

  71. Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146(2):333–350. doi:10.1104/pp.107.112821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17(6):369–381. doi:10.1016/j.tplants.2012.02.004

    Article  CAS  PubMed  Google Scholar 

  73. Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21(7):951–960. doi:10.1093/bioinformatics/bti125

    Article  PubMed  Google Scholar 

  74. Mulaudzi-Masuku T, Mutepe RD, Mukhoro OC, Faro A, Ndimba B (2015) Identification and characterization of a heat-inducible Hsp70 gene from Sorghum bicolor which confers tolerance to thermal stress. Cell Stress Chaperones 20(5):793–804. doi:10.1007/s12192-015-0591-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Guo HM, Li ZC, Zhou ML, Cheng HM (2014) cDNA-AFLP analysis reveals heat shock proteins play important roles in mediating cold, heat, and drought tolerance in Ammopiptanthus mongolicus. Funct Integr Genomics 14(1):127–133. doi:10.1007/s10142-013-0347-y

    Article  CAS  PubMed  Google Scholar 

  76. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutierrez S, Nicolas C, Monte E (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol 167(8):659–665. doi:10.1016/j.jplph.2009.11.012

    Article  CAS  PubMed  Google Scholar 

  77. Hiz MC, Canher B, Niron H, Turet M (2014) Transcriptome Analysis of Salt Tolerant Common Bean (Phaseolus vulgaris L.) under Saline Conditions. PLoS One. doi:10.1371/journal.pone.0092598

    PubMed  PubMed Central  Google Scholar 

  78. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci. doi:10.3389/Fpls.2014.00151

    PubMed  PubMed Central  Google Scholar 

  80. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24(1):23–58

    Article  CAS  Google Scholar 

  81. Sun WN, 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(5):407–415

    Article  CAS  PubMed  Google Scholar 

  82. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front plant sci 5:151. doi:10.3389/fpls.2014.00151

    Article  PubMed  PubMed Central  Google Scholar 

  83. Garg DSS, Dalal S, Tiwari R, Singh R (2012) Heat shock protein based SNP marker for terminal heat stress in wheat (Triticum aestivum L.). Aust J Crop Sci 6(11):1516–1521

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to İlker Büyük.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Büyük, İ., Inal, B., Ilhan, E. et al. Genome-wide identification of salinity responsive HSP70s in common bean. Mol Biol Rep 43, 1251–1266 (2016). https://doi.org/10.1007/s11033-016-4057-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-016-4057-0

Keywords

Navigation