biologia plantarum

International journal on Plant Life established by Bohumil N�mec in 1959

Biologia plantarum 63:268-277, 2019 | DOI: 10.32615/bp.2019.031

Heterologous expression of the AtDREB1A gene in tomato confers tolerance to chilling stress

S.G. Karkute1, R. Krishna1, W.A. Ansari1, B. Singh1, P.M. Singh1, M. Singh2, A.K. Singh1,*
1 ICAR-Indian Institute of Vegetable Research, Varanasi - 221305, Uttar Pradesh, India
2 ICAR-Directorate of Onion and Garlic Research, Pune - 410505, Maharashtra, India

Tomato is highly sensitive to chilling stress (0 - 12 �C) which severely affects plant growth and development. Transgenic tomato plants expressing the AtDREB1A gene under the control of the rd29A promoter were evaluated for its tolerance to chilling stress by exposing them to 4 �C for 5 d. The cold stress caused an increase in production of reactive oxygen species, however, transgenic plants had an effective antioxidant system due to an enhanced synthesis of catalase (CAT), superoxide dismutase (SOD), and ascorbate and so the reduced content of hydrogen peroxide and superoxide anions. Transgenic plants showed a slightly less reduction of chlorophyll and carotenoid content compared to wild-type plants. Similarly, a higher relative water content and a less electrolyte leakage were observed in transgenic plants. Accumulation of osmoprotectants, like proline and soluble sugars, helped transgenic plants to maintain a proper osmotic balance under the cold stress. Stress-responsive genes pyrroline-5-carboxylate synthase, CAT, SOD, and lipid peroxidase showed enhanced expressions under the cold stress in transgenic plants compared to wild-type plants. A recurrent exposure to the cold stress at the reproductive stage showed even higher expressions of these genes as compared to plants exposed to the cold stress for the first time. Thus, transgenic plants showed a better adaptation to the cold stress than non-transgenic plants by acquiring the stress memory of the stress experienced at the seedling stage.

Keywords: catalase, proline, Solanum lycopersicum, stress memory, stress-responsive genes, superoxide dismutase, transgenic plants

Accepted: December 8, 2018; Prepublished online: December 8, 2018; Published online: January 19, 2019  Show citation

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Karkute, S.G., Krishna, R., Ansari, W.A., Singh, B., Singh, P.M., Singh, M., & Singh, A.K. (2019). Heterologous expression of the AtDREB1A gene in tomato confers tolerance to chilling stress. Biologia plantarum,�63,�Article 268-277. https://doi.org/10.32615/bp.2019.031
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    References

    1. Aebi, H.: Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
    2. Akhtar, M., Jaiswal, A., Taj, G., Jaiswal, J.P., Qureshi, M.I., Singh, N.K.: DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. - J. Genet. 91: 385-395, 2012. Go to original source...
    3. Amini, S., Ghobadi, C., Yamchi, A.: Proline accumulation and osmotic stress: an overview of P5CS gene in plants. - Mol. Breed. 3: 44-55, 2015.
    4. Baek, K.H., Skinner, D.Z.: Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. - Plant Sci. 165: 1221-1227, 2003. Go to original source...
    5. Bates, L.S., Walden, R.P., Teare, I.D.: Rapid determination of free proline for water stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
    6. Chaitanya, K.S.K., Naithani, S.C.: Role of superoxide lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f. - New Phytol. 126: 623-627, 1994. Go to original source...
    7. Chinnusamy, V., Zhu, J., Zhu, J.K.: Gene regulation during cold acclimation in plants. - Physiol. Plant. 126: 52-61, 2006. Go to original source...
    8. Crisp, P.A., Ganguly, D., Eichte,n S.R., Borevitz, J.O., Pogson, B.J.: Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. - Sci. Adv. 2: 1501340, 2016. Go to original source...
    9. Dibax, R., Deschamps, C., Bespalhok-Filho, J.C., Vieira, L.G.E., Molinari, H.B.C., De Campos, M.K.F., Quoirin, M.: Organogenesis and Agrobacterium tumifaciens-mediated transformation of Eucalyptus saligna with P5CS gene. - Biol. Plant. 54: 6-12, 2010. Go to original source...
    10. DuBois, M., Gilles, K.A., Hamilton J.K., Rebers, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. - Anal. Chem. 28: 350-356, 1956. Go to original source...
    11. Fedoroff, N.V., Battisti, D.S., Beachy, R.N. , Cooper, P.J., Fischhoff, D.A., Hodges, C.N., Knauf, V.C., Lobell, D., Mazur, B.J., Molden, D., Reynolds, M.P., Ronald, P.C., Rosegrant, M.W., Sanchez, P.A., Vonshak, A., Zhu, J.K.: Radically rethinking agriculture for the 21st century. - Science 327: 833-834, 2010. Go to original source...
    12. Fleta-Soriano, E., Munn�-Bosch, S.: Stress memory and the inevitable effects of drought: a physiological perspective. - Front. Plant. Sci. 7: 143, 2016. Go to original source...
    13. Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., Thomashow, M.F.: Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. - Plant J. 16: 433-442, 1998. Go to original source...
    14. Goulas, E., Schubert, M., Kieselbach, T., Kleczkowski, L.A., Gardestrom, P., Schroder, W., Hurry, V.: The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. - Plant J. 47: 720-734, 2006. Go to original source...
    15. Heath, J.J., Cipollini, D.F., Stireman, J.O.: The role of carotenoids and their derivatives in mediating interactions between insects and their environment. - Arthropod Plant Interact. 7: 1-20, 2013. Go to original source...
    16. Heath, R.L., Packer, L.:Photoperoxidation in isolated chloroplasts: I. Kinetics and stechiometry of fatty acid peroxidation. - Arch. Biochem. Biophys. 125: 189-198, 1968. Go to original source...
    17. Hoekstra, F.A., Golovina, E.A., Buitink, J.: Mechanism of plant desiccation tolerance. - Trends Plant Sci.6: 1360-1385, 2001. Go to original source...
    18. Hsieh, T.H., Lee, J.T., Yang, P.T., Chiu, L.H., Charng, Y.Y., Wang, Y.C., Chan, M.T.: Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. - Plant Physiol. 129: 1086-1094, 2002. Go to original source...
    19. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F.: Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. -Science 280: 104-106, 1998. Go to original source...
    20. Jana, S., Choudhury, M.A.:Glycolate metabolism of three submerged aquatic angiosperm during aging. - Aquat. Bot. 12: 345-354, 1981. Go to original source...
    21. Janska, A., Aprile, A., Zamecn�k, J., Cattivelli, L., Ovesna, J.: Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. - Funct. integr.Genomics 11: 307-325, 2011. Go to original source...
    22. Khare, N., Goyary, D., Singh, N.K., Shah, P., Rathore, M., Anandhan, S., Sharma, D., Arif, M., Ahmed, Z.: Transgenic tomato cv. PusaUphar expressing a bacterial mannitol-1-phosphate dehydrogenase gene confers abiotic stress tolerance. - Plant Cell Tissue Organ Cult. 103: 267-277, 2010. Go to original source...
    23. Law, M.Y., Charles, S.A., Halliwell, B.: Glutathione and ascorbic acid in spinach (Spinaceaoleracea) chloroplast: the effect of hydrogen peroxide and paraquat. - Biochem. J. 210: 899-903, 1983. Go to original source...
    24. Lichtenthaler, H.K., Buschmann, B.C.: Current Protocols in Food Analytical Chemistry. - John Wiley and Sons, New York 2001.
    25. Liu, X.Q., Liu, C.Y., Guo, Q., Zhang, M., Cao, B.N., Xiang, Z.H., Zhao, A.C.: Mulberry transcription factor MnDREB4A confers tolerance to multiple abiotic stresses in transgenic tobacco. - PLoS ONE 22: 0145619, 2015. Go to original source...
    26. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real time quantitative PCR and the 2-∆∆CT method. - Methods 25: 402-408, 2001. Go to original source...
    27. Mishra, H.P., Fridovich, I.: The role of superoxide anion in the auto-oxidation of epinephrine and a simple assay for superoxide dismutase. - J. biol. Chem. 247: 3170-3175, 1972. Go to original source...
    28. Pino, M.T., Skinner, J.S., Jeknic, Z., Hayes, P.M., Soeldner, A.H., Thomashow, M.F., Chen, T.H.H.: Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. - Plant Cell Environ. 31: 393-406, 2008. Go to original source...
    29. Prasad, T.K., Anderson, M.D., Martin, B.A., Stewart, C.R.: Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. -Plant Cell 6: 65-74, 1994. Go to original source...
    30. Rai, G.K., Rai, N.P., Kumar, S., Yadav, A., Rathaur, S., Singh, M.: Effects of explant age, germination medium, pre-culture parameters, inoculation medium, pH, washing medium, and selection regime on Agrobacterium-mediated trans-formation of tomato. - In Vitro cell. dev. Biol. Plant. 48:565-78, 2012. Go to original source...
    31. Rai, G.K., Rai, N.P., Rathaur, S., Kumar, S., Singh, M.: Expression of rd29A::AtDREB1A/CBF3 in tomato alleviates drought-induced oxidative stress by regulating key enzymatic and non-enzymatic antioxidants. - Plant Physiol. Biochem. 69: 90-100, 2013. Go to original source...
    32. Rozen, S., Skaletsky, H.J.: Primer3, http://www-genome.wi.mit.edu/genome_software/other/primer3.html, 1998.
    33. Shao, H.B., Chen, X.Y., Chu, L.Y., Zhao, X.N., Wu, G., Yuan, Y.B., Zhao, C.X., Hu, Z.M.: Investigation on the relationship of proline with wheat anti-drought under soil water deficits. - Colloids Surf. B. Biointerfaces 53: 113-119, 2006. Go to original source...
    34. Singh, S., Rathore, M., Goyary, D., Singh, R.K., Anandhan, S., Sharma, D.K., Ahmed, Z.: Induced ectopic expression of At-CBF1 in marker-free transgenic tomatoes confers enhanced chilling tolerance. - Plant Cell Rep. 30: 1019-1028, 2011. Go to original source...
    35. Song, S.Y., Chen, Y., Chen, J., Dai, X.Y., Zhan, W.H.: Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. - Planta 234: 331-345, 2011. Go to original source...
    36. Weiss, J., Egea-Cortines, M. (only two authors): Transcriptomic analysis of cold response in tomato fruits identifies dehydrin as a marker of cold stress. - J. appl. Genet. 50: 311-319, 2009. Go to original source...
    37. Wibowo, A., Becker, C., Marconi, G., Durr, J., Price, J., Hagmann, J., Papareddy, R., Putra, H., Kageyama, J., Becker, J., Weigel, D.: Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. - Elife 5: e13546, 2016. Go to original source...
    38. Yamaguchi-Shinozak,i K., Shinozaki, K.: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. - Annu. Rev. Plant Biol. 57: 781-803, 2006. Go to original source...
    39. Zhang, C.J., Liu, J.X., Zhang, Y.Y., Cai, X.F., Gong, P.J., Zhang, J.H., Wang, T.T., Li, H.X., Ye, Z.B.: Over-expression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. - Plant Cell Rep. 30: 389-398, 2011. Go to original source...
    40. Zhu, J.K.:Cell signalling under salt, water and cold stresses. - Curr. Opin. Plant. Biol. 4: 401-406, 2011. Go to original source...
    41. Zong, J.M., Li, X.W., Zhou, Y.H., Wang, F.W., Wang, N., Dong, Y.Y., Yuan, Y.X., Chen, H., Liu, X.M., Yao, N., Li, H.Y.: The AaDREB1transcription factor from the cold-tolerant plant Adonis amurensis enhances abiotic stress tolerance in transgenic plant. - Int. J. mol. Sci. 17: 611-626, 2016. Go to original source...

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