Advertisement

Molecular Biology Reports

, Volume 46, Issue 6, pp 5745–5757 | Cite as

Overexpression of Ks-type dehydrins gene OeSRC1 from Olea europaea increases salt and drought tolerance in tobacco plants

  • Samuel Aduse Poku
  • Zafer Seçgin
  • Musa KavasEmail author
Original Article

Abstract

Agricultural production is greatly affected by environmental stresses, such as cold, drought and high-salinity. It is possible to produce tolerant genotypes by transferring genes encoding protective proteins or enzymes from other organisms. In this regard, the current study was aimed to clone a novel OeSRC1 gene identified during the transcriptome profiling of olives (Olea europaea L.) and to investigate the function of this gene in tobacco plants. Functional evaluation of OeSRC1 gene in putative transgenic tobacco plants were carried out under drought, cold and salt stress conditions by using molecular and biochemical tools. It was observed that the transgenic tobacco plants exhibited higher seed germination and survival rates, better root and shoot growth under cold, salt and drought stress treatments compared to wild type plants. Our results also demonstrated that, under stress conditions, transgenic plants accumulated more free proline while no significant changes were observed regarding electrolyte leakage. Ascorbate peroxidase activity of OeSRC1-overexpressing plants was higher than those of the WT plants under different stress conditions. The overall results demonstrate the explicit role of OeSRC1 gene in conferring multiple abiotic stress tolerance at the whole-plant level. The multifunctional role of olive OeSRC1 gene looks good to enhance environmental stress tolerance in diverse plants.

Keywords

Abiotic stress tolerance KS-type dehydrin OeSRC1 gene Olive 

Notes

Acknowledgements

This research was supported by Research Fund of Ondokuz Mayıs University PYO.ZRT.1904.15.006.

Author contributions

SAP: Carried out the experiment, analyzed the data. ZS: helped in performing the experiment. MK: conceived the idea, planned the experiments, supervised the experiments, wrote the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

11033_2019_5008_MOESM1_ESM.jpg (249 kb)
Supplementary material 1 (JPEG 248 kb) Fig. S1. Average root length (cm) of WT and Line 4 plantlets. Plantlets germinated and incubated on MS medium containing 200 mM NaCl and 400 mM Mannitol for 8 weeks
11033_2019_5008_MOESM2_ESM.docx (11 kb)
Supplementary material 2 (DOCX 10 kb)

References

  1. 1.
    Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S et al (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763PubMedGoogle Scholar
  2. 2.
    Holmberg N, Bulow L (1998) Improving stress tolerance in plants by gene transfer. Trends Plant Sci 3:61–66Google Scholar
  3. 3.
    Sahoo DP, Kumar S, Mishra S, Kobayashi Y, Panda SK, Sahoo L (2016) Enhanced salinity tolerance in transgenic mungbean overexpressing Arabidopsis antiporter (NHX1) gene. Mol Breed 36(10):144Google Scholar
  4. 4.
    Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer, New York, p 513Google Scholar
  5. 5.
    Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1249Google Scholar
  6. 6.
    Harris D, Tripathi R, Joshi A (2002) On-farm seed priming to improve crop establishment and yield in dry direct-seeded rice. In: Mortimer M, Pandey S, Wade L, Tuong TP, Lopes K, Hardy B (eds) Direct seeding: research strategies and opportunities. International Research Institute, Manila, pp 231–240Google Scholar
  7. 7.
    Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates Inc, Sunderland, p 782Google Scholar
  8. 8.
    Yadav RS, Hash CT, Bidinger FR, Devos KM, Howarth CJ (2004) Genomic regions associated with grain yield and aspects of post-flowering drought tolerance in pearl millet across stress environments and tester background. Euphytica 136:265–277Google Scholar
  9. 9.
    Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3(2):30Google Scholar
  10. 10.
    Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Phys 51:463–499Google Scholar
  11. 11.
    Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedGoogle Scholar
  12. 12.
    Zhu XY, Li XP, Zou Y, Chen WX, Lu WJ (2012) Cloning, characterization and expression analysis of ∆1-pyrroline-5-carboxylate synthetase (P5CS) gene in harvested papaya (Carica papaya) fruit under temperature stress. Food Res Int 49:272–279Google Scholar
  13. 13.
    Guerzoni JTS, Belintani NG, Moreira RMP, Hoshino AA, Domingues DS, Bespalhok Filho JC et al (2014) Stress-induced Delta 1-pyrroline-5-carboxylate synthetase (P5CS) gene confers tolerance to salt stress in transgenic sugarcane. Acta Physiol Plant 36:2309–2319Google Scholar
  14. 14.
    Ghanti SKK, Sujata KG, Kumar BMV, Karba NN, Reddy KJ, Rao MS et al (2011) Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biol Plant 55:634–640Google Scholar
  15. 15.
    Cong LL, Zhang XQ, Yang FY, Liu SJ, Zhang YW (2014) Isolation of the P5CS gene from reed canary grass and its expression under salt stress. Genet Mol Res 13:9122–9133PubMedGoogle Scholar
  16. 16.
    Li J, Phan T-T, Li Y-R, Xing Y-X, Yang L-T (2018) Isolation, transformation and overexpression of sugarcane SoP5CS gene for drought tolerance improvement. Sugar Tech 20:464–473Google Scholar
  17. 17.
    Zhu M, Meng X, Cai J, Li G, Dong T, Li Z (2018) Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biol 18:83PubMedPubMedCentralGoogle Scholar
  18. 18.
    Jin X, Xue Y, Wang R, Xu R, Bian L, Zhu B et al (2013) Transcription factor OsAP21 gene increases salt/drought tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 40:1743–1752PubMedGoogle Scholar
  19. 19.
    Wang N-N, Xu S-W, Sun Y-L, Liu D, Zhou L, Li Y et al (2019) The cotton WRKY transcription factor (GhWRKY33) reduces transgenic Arabidopsis resistance to drought stress. Sci Rep 9:724PubMedPubMedCentralGoogle Scholar
  20. 20.
    Thirumalaikumar VP, Devkar V, Mehterov N, Ali S, Ozgur R, Turkan I et al (2018) NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnol J 16:354–366PubMedGoogle Scholar
  21. 21.
    Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9:591–596PubMedGoogle Scholar
  22. 22.
    Magwanga RO, Lu P, Kirungu JN, Lu HJ, Wang XX, Cai XY et al (2018) Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet 19(1):6PubMedPubMedCentralGoogle Scholar
  23. 23.
    Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Phys Plant 100:291–296Google Scholar
  24. 24.
    Hara M, Monna S, Murata T, Nakano T, Amano S, Nachbar M et al (2016) The Arabidopsis KS-type dehydrin recovers lactate dehydrogenase activity inhibited by copper with the contribution of His residues. Plant Sci 245:135–142PubMedGoogle Scholar
  25. 25.
    Amara I, Capellades M, Ludevid MD, Pagès M, Goday A (2013) Enhanced water stress tolerance of transgenic maize plants over-expressing LEA Rab28 gene. J Plant Physiol 170:864–873PubMedGoogle Scholar
  26. 26.
    RoyChoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859PubMedGoogle Scholar
  27. 27.
    Cheng Z, Targolli J, Huang X, Wu R (2002) Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.). Mol Breed 10:71–82Google Scholar
  28. 28.
    Liu Y, Song QP, Li DX, Yang XH, Li DQ (2017) Multifunctional roles of plant dehydrins in response to environmental stresses. Front Plant Sci 8:1018PubMedPubMedCentralGoogle Scholar
  29. 29.
    Svensson J, Ismail AM, Tapio Palva E, Close TJ (2002) Dehydrins. In: Storey KB, Storey JM (eds) Cell and molecular response to stress. Elsevier, Amsterdam, pp 155–171Google Scholar
  30. 30.
    Koag M-C, Wilkens S, Fenton RD, Resnik J, Vo E, Close TJ (2009) The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol 150:1503–1514PubMedPubMedCentralGoogle Scholar
  31. 31.
    Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance. Plant Signal Behav 6:1503–1509PubMedPubMedCentralGoogle Scholar
  32. 32.
    Kavas M, Baloglu MC, Yucel AM, Oktem HA (2016) Enhanced salt tolerance of transgenic tobacco expressing a wheat salt tolerance gene. Turk J Biol 40:727–735Google Scholar
  33. 33.
    Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z et al (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol Lett 30:1275–1280PubMedGoogle Scholar
  34. 34.
    Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher-plants. Proc Natl Acad Sci USA 87:8526–8530PubMedGoogle Scholar
  35. 35.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT) method. Methods 25:402–408PubMedPubMedCentralGoogle Scholar
  36. 36.
    Hodges DM, DeLong JM, Forney CF, Prange RKJP (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611Google Scholar
  37. 37.
    Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207Google Scholar
  38. 38.
    Akcay UC, Ercan O, Kavas M, Yildiz L, Yilmaz C, Oktem HA et al (2010) Drought-induced oxidative damage and antioxidant responses in peanut (Arachis hypogaea L.) seedlings. Plant Growth Regul 61:21–28Google Scholar
  39. 39.
    Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753PubMedGoogle Scholar
  40. 40.
    Halder T, Upadhyaya G, Basak C, Das A, Chakraborty C, Ray S (2018) Dehydrins impart protection against oxidative stress in transgenic tobacco plants. Front Plant Sci 9:136PubMedPubMedCentralGoogle Scholar
  41. 41.
    Tiwari P, Indoliya Y, Singh PK, Singh PC, Chauhan PS, Pande V et al (2019) Role of dehydrin-FK506-binding protein complex in enhancing drought tolerance through the ABA-mediated signaling pathway. Environ Exp Bot 158:136–149Google Scholar
  42. 42.
    Halder T, Upadhyaya G, Ray S (2017) YSK2 type dehydrin (SbDhn1) from sorghum bicolor showed improved protection under high temperature and osmotic stress condition. Front Plant Sci 8:918PubMedPubMedCentralGoogle Scholar
  43. 43.
    Li ZG, Zhao LX, Kai GY, Yu SW, Cao YF, Pang YZ et al (2004) Cloning and expression analysis of a water stress-induced gene from Brassica oleracea. Plant Physiol Biochem 42:789–794PubMedGoogle Scholar
  44. 44.
    Takahashi R, Joshee N, Kitagawa Y (1994) Induction of chilling resistance by water-stress, and Cdna sequence-analysis and expression of water stress-regulated genes in rice. Plant Mol Biol 26:339–352PubMedGoogle Scholar
  45. 45.
    Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16Google Scholar
  46. 46.
    Day CD, Lee E, Kobayashi T, Holappa LD, Albert H, Ow DW (2000) Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. Gene Dev 14:2869–2880PubMedGoogle Scholar
  47. 47.
    Kooter JM, Matzke MA, Meyer P (1999) Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci 4:340–347PubMedGoogle Scholar
  48. 48.
    Neumann PM (2008) Coping mechanisms for crop plants in drought-prone environments. Ann Bot-London 101:901–907Google Scholar
  49. 49.
    Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396Google Scholar
  50. 50.
    Wu D, Sun Y, Wang H, Shi H, Su M, Shan H et al (2018) The SlNAC8 gene of the halophyte Suaeda liaotungensis enhances drought and salt stress tolerance in transgenic Arabidopsis thaliana. Gene 662:10–20PubMedGoogle Scholar
  51. 51.
    Hara M, Kondo M, Kato T (2013) A KS-type dehydrin and its related domains reduce Cu-promoted radical generation and the histidine residues contribute to the radical-reducing activities. J Exp Bot 64:1615–1624PubMedPubMedCentralGoogle Scholar
  52. 52.
    Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466PubMedPubMedCentralGoogle Scholar
  53. 53.
    Zhu X, Gong H, Chen G, Wang S, Zhang C (2005) Different solute levels in two spring wheat cultivars induced by progressive field water stress at different developmental stages. J Arid Environ 62:1–14Google Scholar
  54. 54.
    Liu GZ, Li XL, Jin SX, Liu XY, Zhu LF, Nie YC et al (2014) Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS ONE 9:e86895PubMedPubMedCentralGoogle Scholar
  55. 55.
    Liu H, Yu CY, Li HX, Ouyang B, Wang TT, Zhang JH et al (2015) Overexpression of ShDHN, a dehydrin gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses in tomato. Plant Sci 231:198–211PubMedGoogle Scholar
  56. 56.
    Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A et al (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026PubMedGoogle Scholar
  57. 57.
    Rubio MC, Gonzalez EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J et al (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531–540PubMedGoogle Scholar
  58. 58.
    Bao F, Du D, An Y, Yang W, Wang J, Cheng T et al (2017) Overexpression of Prunus mume dehydrin genes in tobacco enhances tolerance to cold and drought. Front Plant Sci 8:151PubMedPubMedCentralGoogle Scholar
  59. 59.
    Roychoudhury A, Nayek S (2014) Structural aspects and functional regulation of late embryogenesis abundant (LEA) genes and proteins conferring abiotic stress tolerance in plants. In: Ferro A (ed) Abiotic stress: role in sustainable agriculture, detrimental effects and management strategies. Nova Science Publishers, New York, pp 43–109Google Scholar
  60. 60.
    Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratory of Plant Cell Technology, Graduate School of Horticulture, Faculty of HorticultureChiba UniversityChibaJapan
  2. 2.Department of Agricultural Biotechnology, Faculty of AgricultureOndokuz Mayıs UniversitySamsunTurkey

Personalised recommendations