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Comparative physiological responses of the yeast halotolerance genes expressed in transgenic lines of tomato cv Rio Grande under saline conditions

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Abstract

We previously analyzed the transgenic lines of tomato cv Rio Grande over-expressing the yeast HAL I and HAL II genes for their response to salt stress under in vitro conditions. In this study, six homozygous tomato lines harbouring the yeast HAL I or HAL II genes with highest expression level were selected for exploring their physiological responses against different salt stresses in the field. These transgenic plants showed significant growth and improved water content in comparison with control under 100 and 150 mM salt stress conditions. The HAL I and HAL II lines showed better Ca2+ content than their control counterparts. Furthermore, the transgenic lines exhibited lower values of relative electrical conductivity and improved resistance against the fungal pathogens Fusarium oxysporum and Alternaria solani when tested by detached leaf and agar tube dilution assays. Physiological analyses carried out in this study suggest an involvement of multiple mechanisms in transgenic tomato plants harbouring yeast genes to confer biotic and abiotic tolerance under stress conditions.

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References

  • Ahmed I, Islam M, Arshad W, Mannan A, Ahmad W, Mirza B (2009) High quality plant DNA extraction for PCR: an easy approach. J Appl Genet 50:105–107

    Article  PubMed  CAS  Google Scholar 

  • Arrillaga I, Gil-Mascarell R, Gisbert C, Sales E, Montesinos C, Serrano R, Moreno V (1998) Expression of the yeast HAL 2 gene in tomato increases the in vitro salt tolerance of transgenic progenies. Plant Sci 136:219–226

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Improving plant abiotic-stress resistance by exogenous application of osmoprotectants glycine betaine and proline. Env Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Aswath CR, Kim SH, Mo SY, Kim DH (2005) Transgenic plants of creeping bent grass harbouring the stress inducible gene, 9-cis-epoxycarotenoid dioxygenase, are highly tolerant to drought and NaCl stress. J Plant Growth Regul 47:129–139

    Article  CAS  Google Scholar 

  • Cervera M, Ortega C, Navarro A, Navarro L, Pena L (2000) Generation of transgenic citrus plants with the tolerance-to-salinity gene HAL 2 from yeast. J Hort Sci Biotechnol 75:26–30

    CAS  Google Scholar 

  • Chatzidimitriadou K, Nianiou-Obeidat I, Madesis P, Perl-Treves R, Tsaftaris A (2009) Expressions of SOD transgene in pepper confer stress tolerance and improve shoot regeneration. Electronic J Biotechnol 12(4):1–9

    Google Scholar 

  • Choi JY, Seo YS, Kim SJ, Kim WT, Shin JS (2011) Constitutive expression of CaXTH3, a hot pepper xyloglucan endotransglucosylase/hydrolase, enhanced tolerance to salt and drought stresses without phenotypic defects in tomato plants (Solanum lycopersicum cv. Dotaerang). Plant Cell Rep 30:867–877

    Article  PubMed  CAS  Google Scholar 

  • Ellul P, Rios G, Atares A, Roig LA, Serrano R, Moreno V (2003) The expression of Saccharomyces cerevisiae HAL I gene increases salt tolerance in transgenic water melon. Theor Appl Genet 107:462–469

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Ren Z, Zhao Y, Zhang H (2003) Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133:1873–1881

    Article  PubMed  CAS  Google Scholar 

  • Gisbert C, Rus AM, Bolarin MC, Lopez-Coronado JM, Arrillaga I, Montesinos C, Caro M, Serrano R, Moreno V (2000) The yeast HAL 1 gene improves salt tolerance of transgenic tomato. Plant Physiol 123:393–402

    Article  PubMed  CAS  Google Scholar 

  • Glase HU, Thomas D, Gaxiola R, Montrichard F, Surdin-Kerjan Y, Serrano R (1993) Salt tolerant and methionine biosynthesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J 12:3105–3110

    Google Scholar 

  • Hanif M, Hussain M, Ali S, Bhatti MH, Ahmed MS, Mirza B, Evans HS (2007) Synthesis, spectroscopic investigation, crystal structure and biological screening, including antitumor activity of organotin IV derivatives of piperonylic acid. Turk J Chem 31:349–361

    CAS  Google Scholar 

  • Hasthanasombut S, Ntui V, Supaibulwatana K, Mii M, Nakamura I (2010) Expression of Indica rice OsBADH1 gene under salinity stress in transgenic tobacco. Plant Biotech Rep 4:74–83

    Article  Google Scholar 

  • Hepler PK (2005) Calcium, a central regulator of plant growth and development. Plant Cell 17:2142–2155

    Article  PubMed  CAS  Google Scholar 

  • Hu L, Lu H, Liu Q, Chen X, Jiang X (2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol 25(10):1273–1281

    Article  PubMed  CAS  Google Scholar 

  • Hussaiani AM, Abdin MZ (2008) Development of transgenic strawberry (Fragaria X ananassa Duch.) plants tolerant to salt stress. Plant Sci 174:446–455

    Article  Google Scholar 

  • Khare N, Goyary D, Singh NK, Shah P, Rathore M, Anandhan S, Sharma D, Arif M, Ahmed Z (2010) Transgenic tomato cv. Pusa Uphar expressing a bacterial mannitol-1-phosphate dehydrogenase gene confers abiotic stress tolerance. Plant Cell Tiss Organ Cult 103:267–277

    Article  CAS  Google Scholar 

  • Khoudi H, Nouri-Khemakhem A, Gouiaa S, Masmoudi K (2009) Optimization of regeneration and transformation parameters in tomato for the improvement of its salinity and drought tolerance. African J Biotechnol 8(22):6068–6076

    CAS  Google Scholar 

  • Kim YH, Lim S, Yang KS, Kim CY, Kwon SY, Lee HS, Wang X, Zhou Z, Yun DJ, Kwak SS (2009) Expression of Arabidopsis NDPK2 increases antioxidant enzyme activities and enhances tolerance to multiple environmental stresses in transgenic sweet potato plants. Mol Breeding 24:233–244

    Article  CAS  Google Scholar 

  • Lu Z, Liu D, Liu S (2007) Two rice cytosolic ascorbate peroxidases differentially improves salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917

    Article  PubMed  CAS  Google Scholar 

  • Moriwaki T, Yamamoto Y, Aida T, Funahashi T, Shishido MA, Prodhan SH, Komamine A, Motohashi T (2008) Overexpression of the Escherichia coli catalase gene, kat E enhances tolerance to salinity in the transgenic indica rice cultivar, BR5. Plant Biotechnol Rep 2:41–46

    Article  Google Scholar 

  • Park EJ, Jeknić Z, Pino MT, Murata N, Chen TH (2007) Glycine betaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 308:994–1005

    Article  Google Scholar 

  • Prabhavathi V, Rajam MV (2007) Mannitol-accumulating transgenic eggplants exhibit enhanced resistance to fungal wilts. Plant Sci 173:50–54

    Article  CAS  Google Scholar 

  • Rajam MV, Chandola N, Goud PS, Singh D, Kashyap V, Chaudhry ML, Sihachakr D (2007) Thaumatin gene confers resistance to fungal pathogens as well as to abiotic stresses in transgenic tobacco plants. Biol Plant 51(1):135–141

    Article  CAS  Google Scholar 

  • Roy R, Purty RS, Agrawal V, Gupta SC (2006) Transforamtion of tomato cultivar “Pusa Ruby” with bsp A gene from Populus tremula for drought tolerance. Plant Cell Tiss Organ Cult 84:55–67

    Article  CAS  Google Scholar 

  • Rus AM, Estan MT, Gisbert C, Garcia Sogo B, Serrano R, Caro M, Moreno V, Bolarin MC (2001) Expressing the yeast HAL I gene in tomato increases fruit yield and enhances K+/Na+ selectivity under salt stress. Plant Cell Environ 24:875–880

    Article  CAS  Google Scholar 

  • Saad BR, Zouari N, Randhan WB, Azaza J, Meynard D, Guiderdoni E, Hassairi A (2010) Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger “AlSAP” gene isolated from the halophyte grass Aeluropus littoralis. Plant Mol Biol 72:171–190

    Article  PubMed  Google Scholar 

  • Safdar N, Yasmeen A, Mirza B (2011) An insight into functional genomics of transgenic lines of tomato cv Rio Grande harbouring yeast halotolerance genes. Plant Biol 13(4):620–631

    Article  PubMed  CAS  Google Scholar 

  • Sergeeva E, Shah S, Glick BR (2006) Growth of transgenic canola (Brassica napus cv. Westar) expressing a bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene on high concentrations of salt. World J Micro Biotechnol 22:277–282

    Article  CAS  Google Scholar 

  • Serrano R (1996) Salt tolerance in plants microorganisms-toxicity targets and defense responses. Int Rev Cytol 4:281–287

    Google Scholar 

  • Teixeira J, Pereira S (2007) High salinity and drought act on an organ-dependent manner on potato glutamine synthetase expression and accumulation. Environ Exp Bot 60:121–126

    Article  CAS  Google Scholar 

  • Vijayan K (2009) Approaches for enhancing salt tolerance in mulberry Morus L.—a review. Plant Omics J 2:41–59

    CAS  Google Scholar 

  • Wang Y, Jiang J, Zhao X, Liu G, Yang C, Zhan L (2006) A novel LEA gene from Tamarix androssowii confers drought tolerance in transgenic tobacco. Plant Sci 171:655–662

    Article  CAS  Google Scholar 

  • Yang SX, Zhao YX, Zhang Q, He YK, Zhang H, Luo (2001) HAL 1 mediate salt adaptation in Arabidopsis thaliana. Cell Res 11:142–148

    Article  PubMed  CAS  Google Scholar 

  • Xue Y, Pena R, Xiong A, Li X, Zha D, Yao Q (2009) Yeast heat-shock protein gene HSP26 enhances freezing tolerance in Arabidopsis. J Plant Physiol 166:844–850

    Article  PubMed  CAS  Google Scholar 

  • Zhao F, Guo S, Zhang H, Zhao Y (2006) Expression of yeast SOD2 in transgenic rice results in increased salt tolerance. Plant Sci 170:216–224

    Article  CAS  Google Scholar 

  • Zhao J, Gou S, Chen S, Zhang H, Zhao Y (2009) Expression of yeast YAP1 in transgenic Arabidopsis results in increased salt tolerance. J Plant Biol 52:56–64

    Google Scholar 

  • Zhou SF, Chen XY, Xue XN, Zhang XG, Li YX (2007) Physiological and growth responses of tomato progenies harboring the betaine aldehyde dehydrogenase gene to salt stress. J Integrative Plant Biol 49:628–637

    Article  CAS  Google Scholar 

  • Zhou W, Li Y, Zhao BC, Ge RC, Shen YZ, Wang G, Huang ZJ (2009) Overexpression of TaSTRG gene improves salt and drought tolerance in rice. J Plant Physiol 166:1660–1671

    Article  PubMed  CAS  Google Scholar 

  • Zhu B, Chen THH, Li PH (1995) Activation of two osmotin-like protein genes by abiotic stimuli and fungal pathogens in transgenic potato plants. Plant Physiol 108:929–939

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors sincerely thank Dr. Ramon Serrano (Instituto de Biologia Molecular y Celular de plantas, Valencia, Spain) for the kind provision of HAL I and HAL II constructs. We are also thankful to the Higher Education Commission of Pakistan for the financial support of this research project.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biochemistry, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Naila Safdar, Bushra Mirza & Nazif Ullah

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  1. Naila Safdar
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  2. Bushra Mirza
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  3. Nazif Ullah
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Corresponding author

Correspondence to Bushra Mirza.

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Communicated by S. Abe.

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Safdar, N., Mirza, B. & Ullah, N. Comparative physiological responses of the yeast halotolerance genes expressed in transgenic lines of tomato cv Rio Grande under saline conditions. Acta Physiol Plant 35, 919–929 (2013). https://doi.org/10.1007/s11738-012-1135-3

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  • DOI: https://doi.org/10.1007/s11738-012-1135-3

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