Biologia plantarum 64:271-279, 2020 | DOI: 10.32615/bp.2019.080
Salt tolerance of potato genetically engineered with the Atriplex canescens BADH gene
- 1 Four Brothers Group Pakistan,77-D/1, 1st Floor Lahore Centre, Main Boulevard Gulberg, Lahore, Punjab 54000, Pakistan
- 2 Department of Plant Pathology, China Agricultural University, Beijing 100093, P.R. China
- 3 Centre of Excellence in Molecular Biology, University of Punjab, Lahore, Punjab 53700, Pakistan
- 4 Institute of Molecular Biology and Biotechnology, University of Lahore, Lahore, Punjab 54000, Pakistan
Potato (Solanum tuberosum L.) is among the top staple foods in the world, and salinity adversely affects its yield and quality. To improve salt tolerance in potato, the present study is focused on the Agrobacterium-mediated transformation of potato by the Atriplex canescens betaine aldehyde dehydrogenase (BADH) gene driven by single, double, and triple CaMV 35S promoters. The study led first to the detection of seven lines containing the BADH gene followed by the identification of T-DNA insertions via DNA hybridization and enzyme-linked immunosorbent assays. The salt tolerance was found to be promoter dependent, as the lines with triple promoters showed a higher resistance than those tranformed with single and double promoters. The transgenic lines showed lower content of H2O2 and malondialdehyde and a lower relative electrical conductivity than wild-type plants. Furthermore, these lines also showed higher proline and chlorophyll content. In silico analysis confirmed that the A. canescens BADH protein had a remarkable tendency to interact with sodium ions and water molecules like other BADH proteins. Taken together, the overexpression of BADH under triple CaMV 35S promoters enhanced salt tolerance of potato.
Keywords: Atriplex canescens, CaMV 35S promoter, chlorophyll, malondialdehyde, proline, Solanum tuberosum.
Received: December 17, 2018; Revised: June 9, 2019; Accepted: June 11, 2019; Published online: March 27, 2020 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Supplementary files
| Download file | Ali6044 Suppl.pdf File size: 543.35 kB |
References
- Ali, Q., Ali, A., Ahsan, M., Ali, S., Khan, N.H., Muhammad, S., Abbas, H.G., Nasir, I.A., Husnain, T.: Line × tester analysis for morpho-physiological traits of Zea mays L. seedlings. - Adv. Life Sci. 1: 242-253, 2014.
- Ali, Q., Ahsan, M., Ali, F., Aslam, M., Khan, N.H., Munzoor, M., Mustafa, H.S.B., Muhammad, S.: Heritability, heterosis and heterobeltiosis studies for morphological traits of maize (Zea mays L.) seedlings. - Adv.. Life Sci. 1: 52-63, 2013.
- Ali, Q., Ahsan, M., Kanwal, N., Ali, F., Ali, A., Ahmed, W., Ishfaq, M., Saleem, M.: Screening for drought tolerance: comparison of maize hybrids under water deficit condition. - Adv. Life Sci. 3: 51-58, 2016.
- Axel, C., Zannini, E., Coffey, A., Guo, J., Waters, D.M., Arendt, E.K.: Ecofriendly control of potato late blight causative agent and the potential role of lactic acid bacteria: a review. - Appl. Microbiol. Biotechnol. 96: 37-48, 2012.
Go to original source... - Babakhani, B., Khavari-Nejad, R., Fahimi, H., Saadatmand, S.: Biochemical responses of alfalfa (Medicago sativa L.) cultivars subjected to NaCl salinity stress. - Afr. J Biotechnol. 10: 11433-11441, 2013.
- Bates, L., Waldren, R., Teare, I.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973.
Go to original source... - Boyer, J.: Differential Scanning Calorimetry in the Analysis of Foods. - Marcel Dekker, New York, 2004.
- Chou, K.C., Shen, H.B.: Euk-mPLoc: a fusion classifier for large-scale eukaryotic protein subcellular location prediction by incorporating multiple sites. - J. Proteome Res. 6: 1728-1734, 2007.
Go to original source... - Cookson, S.J., Moreno, M.J.C., Hevin, C., Mendome, L.Z.N., Delrot, S., Trossat-Magnin, C., Ollat, N.: Graft union formation in grapevine induces transcriptional changes related to cell wall modification, wounding, hormone signalling, and secondary metabolism. - J. exp. Bot. 64:, 2013.
Go to original source... - Diaz-Sanchez, Á.G., González-Segura, L., Mújica-Jiménez, C., Rudiño-Piñera, E., Montiel, C., Martínez-Castilla, L.P., Muñoz-Clares, R.A.: Amino acid residues critical for the specificity for betaine aldehyde of the plant ALDH10 isoenzyme involved in the synthesis of glycine betaine. - Plant Physiol. 158: 1570-1582, 2012.
Go to original source... - Farace, G., Visconti, S., Marchive, C., Aducci, P., Marra, M., Trossat-Magnin, C.: Characterization, functional validation and gene expression patterns of two 14-3-3 isoforms from Vitis vinifera. -Vitis 54: 33-40, 2015.
- Foolad, M.: Comparison of salt tolerance during seed germination and vegetative growth in tomato by QTL mapping. -Genome 42: 727-734, 1999.
Go to original source... - Fujiwara, T., Hori, K., Ozaki, K., Yokota, Y., Mitsuya, S., Ichiyanagi, T., Hattori, T. and Takabe, T.: Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenases in barley. - Physiol. Plant. 134: 22-30, 2008.
Go to original source... - Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D., Bairoch, A.: ExPASy: the proteomics server for in-depth protein knowledge and analysis. -Nucl. Acids Res. 31: 3784-3788, 2003.
Go to original source... - Ghosh, P., Rathinasabapathi, B., Teplitski, M., Ma, L.Q.: Bacterial ability in AsIII oxidation and AsV reduction: relation to arsenic tolerance, P uptake, and siderophore production. - Chemosphere. 30: 995-1000, 2015.
Go to original source... - Giri, J.: Glycinebetaine and abiotic stress tolerance in plants. - Plant Signal. Behav. 6: 1746-1751, 2011.
Go to original source... - Guo, Y., Zhang, L., Xiao, G., Cao, S., Gu, D., Tian, W., Chen, S.: Expression of betaine aldehyde dehydrogenase gene and salinity tolerance in rice transgenic plants. - Sci. China Series C: Life Sci. 40: 496-501, 1997.
Go to original source... - Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., Bohnert, H.J.: Plant cellular and molecular responses to high salinity. - Annu. Rev. Plant Biol. 51: 463-499, 2000.
Go to original source... - Hemraj, V., Diksha, S. and Avneet, G.: A review on commonly used biochemical test for bacteria. Innovare J Life Sci, 1: 1-7, 2013.
- Hou, Q., Bartels, D.: Comparative study of the aldehyde dehydrogenase (ALDH) gene superfamily in the glycophyte Arabidopsis thaliana and Eutrema halophytes. - Ann. Bot. 115: 465-479, 2014
Go to original source... - Ishitani, M., Arakawa, K., Mizuno, K., Kishitani, S., Takabe, T.: Betaine aldehyde dehydrogenase in the Gramineae: levels in leaves of both betaine-accumulating and nonaccumulating cereal plants. - Plant Cell Physiol. 34: 493-495, 1993.
- Jbir-Koubaa, R., Charfeddine, S., Ellouz, W., Saidi, M. N., Drira, N., Gargouri-Bouzid, R., Nouri-Ellouz, O.: Investigation of the response to salinity and to oxidative stress of interspecific potato somatic hybrids grown in a greenhouse. - Plant Cell Tissue Organ Cult. ??: 1-15, 2014.
Go to original source... - Jia, G.-X., Zhu, Z.-Q., Chang, F.-Q., Li, Y.-X.: Transformation of tomato with the BADH gene from Atriplex improves salt tolerance. - Plant Cell Rep. 21: 141-146, 2002.
Go to original source... - Kiani, S., Ali, A., Bajwa, K. S., Muzaffar, A., Ashraf, M.A., Samiullah, T.R., Shahid, A., Husnain, T.: Cloning and chloroplast-targeted expression studies of insect-resistant gene with ricin fusion-gene under chloroplast transit peptide in cotton. - Electron. J. Biotechnol. 16: 1-14, 2013.
Go to original source... - Krivosheeva, A., Varlamova, T., Yurieva, N., Sobol'kova, G., Kholodova, V., Belyaev, D.: Potato transformation with the HvNHX3 gene and the improvement of transformant salt tolerance. - Russ. J. Plant Physiol. 61: 792-800, 2014.
Go to original source... - Levy, D., Tai, G.: Differential response of potatoes (Solanum tuberosum L.) to salinity in an arid environment and field performance of the seed tubers grown with fresh water in the following season. - Agr. Water Manage. 116: 122-127, 2013.
Go to original source... - Liu, X., Cheng, S., Liu, J., Ou, Y., Song, B., Zhang, C., Lin, Y., Li, X.-Q., Xie, C.: The potato protease inhibitor gene, plays roles in the cold-induced sweetening of potato tubers by modulating invertase activity. - Postharvest Biol. Technol. 86: 265-271, 2013.
Go to original source... - Liu, X., Zhang, C., Ou, Y., Lin, Y., Song, B., Xie, C., Liu, J., Li, X.Q.: Systematic analysis of potato acid invertase genes reveals that a cold-responsive member, StvacINV1, regulates cold-induced sweetening of tubers. - Mol. Genet. Genomics 286: 109-118, 2011.
Go to original source... - Luo, D., Niu, X., Yu, J., Yan, J., Gou, X., Lu, B.-R., Liu, Y.: Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). - Plant Cell Rep. 31: 1625-1635, 2012.
Go to original source... - Ma, L.Q., Rathinasabapathi, B., Wang, X., Mathews, S., Ghosh, P.: Arsenic biotransformation and transfer from rhizosphere to plant. - In: Ng, J.C., Noller, N., Naidu, R., Bundschuh, J., Bhattacharya, P. (ed.): Proceedings of the 4th International Congress on Arsenic in the Environment. P. 101. CRC Press, Cairns, 2012.
- Mitsuya, S., Kuwahara, J., Ozaki, K., Saeki, E., Fujiwara, T., Takabe, T.: Isolation and characterization of a novel peroxisomal choline monooxygenase in barley. - Planta 234: 1215-1226, 2011.
Go to original source... - Murashige, T., Skoog, F.: A revised medium for rapid growth and bio assays with tobacco tissue cultures. - Physiol. Plant. 15: 473-497, 1962.
Go to original source... - Muzaffar, A., Kiani, S., Khan, M.A.U., Rao, A.Q., Ali, A., Awan, M.F., Iqbal, A., Nasir, I.A., Shahid, A.A., Husnain, T.: Chloroplast localization of Cry1Ac and Cry2A protein - an alternative way of insect control in cotton. - Biol. Res. 48: 1-11, 2015.
Go to original source... - Nakamura, T., Nomura, M., Mori, H., Jagendorf, A.T., Ueda, A., Takabe, T.: An isozyme of betaine aldehyde dehydrogenase in barley. - Plant Cell Physiol. 42: 1088-1092, 2015.
Go to original source... - Pieper, U., Eswar, N., Davis, F. P., Braberg, H., Madhusudhan, M S., Rossi, A., Marti-Renom, M., Karchin, R., Webb, B.M., Eramian, D.: MODBASE: a database of annotated comparative protein structure models and associated resources. - Nucl. Acids Res. 34: D291-D295, 2006.
Go to original source... - Puniran-Hartley, N., Hartley, J., Shabala, L., Shabala, S.: Salinity-induced accumulation of organic osmolytes in barley and wheat leaves correlates with increased oxidative stress tolerance: in planta evidence for cross-tolerance. - Plant Physiol. Biochem. 83: 32-39, 2014.
Go to original source... - Rajaeian, S., Ehsanpour, A.A., Javadi, M., Shojaee, B.: Ethanolamine induced modification in glycine betaine and proline metabolism in Nicotiana rustica under salt stress. - Biol. Plant. 61: 797-800, 2017.
Go to original source... - Rao, A.Q., Bajwa, K.S., Puspito, A.N., Khan, M., Abbas, M.A., Bakhsh, A., Shahid, A.A., Nasir, I.A., Husnain, T.: Variation in expression of phytochrome B gene in cotton (Gossypium hirsutum L.). - J. agr. Sci. Technol. 15: 1033-1042, 2013.
- Rathinasabapathi, B.: Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. - Ann. Bot. 86: 709-716, 2000.
Go to original source... - Rathinasabapathi, B., Burnet, M., Russell, B.L., Gage, D.A., Liao, P.-C., Nye, G.J., Scott, P., Golbeck, J.H., Hanson, A.D.: Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. - Proc. nat. Acad. Sci. USA 94: 3454-3458, 1997.
Go to original source... - Rhodes, D., Hanson, A.: Quaternary ammonium and tertiary sulfonium compounds in higher plants. - Annu. Rev. Plant Biol. 44: 357-384, 1993.
Go to original source... - Sakamoto, A., Murata, N.: Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. - J. exp. Bot. 51: 81-88, 2000.
Go to original source... - Saneoka, H., Ishiguro, S., Moghaieb, R.E.: Effect of salinity and abscisic acid on accumulation of glycinebetaine and betaine aldehyde dehydrogenase mRNA in Sorghum leaves (Sorghum bicolor). - J. Plant Physiol. 158: 853-859, 2001.
Go to original source... - Si, H., Zhang, N., Wang, D.: Drought and salinity tolerance in transgenic potato. - In: He Z., Larkin R., Honeycutt W. (ed.): Sustainable Potato Production: Global Case Studies. Pp. 373-387. Springer, Dordrecht 2012.
Go to original source... - Sudhersan, C., Manuel, S.J., Ashkanani, J., Al-Ajeel, A.: In vitro screening of potato cultivars for salinity tolerance. -Amer. Eurasian J. Sustain. Agr. 6: 344-348, 2012.
- Tang, W., Sun, J., Liu, J., Liu, F., Yan, J., Gou, X., Lu, B.R., Liu, Y.: RNAi-directed downregulation of betaine aldehyde dehydrogenase 1 (OsBADH1) results in decreased stress tolerance and increased oxidative markers without affecting glycine betaine biosynthesis in rice (Oryza sativa). - Plant mol. Biol. 86: 443-454, 2014.
Go to original source... - Tylichová, M., Kopeèný, D., Moréra, S., Briozzo, P., Lenobel, R., Snégaroff, J., ©ebela, M.: Structural and functional characterization of plant aminoaldehyde dehydrogenase from Pisum sativum with a broad specificity for natural and synthetic aminoaldehydes. - J. mol. Biol. 396: 870-882, 2010.
Go to original source... - Van Leeuwen, J., Lehtinen, T., Lair, G., Bloem, J., Hemerik, L., Ragnarsdóttir, K., Gísladóttir, G., Newton, J., De Ruiter, P.: An ecosystem approach to assess soil quality in organically and conventionally managed farms in Iceland and Austria, 2014. Soil Discuss. 1: 201-237, 2014.
Go to original source... - Weretilnyk, E.A., Hanson, A.D.: Betaine aldehyde dehydrogenase from spinach leaves: purification, in vitro translation of the mRNA, and regulation by salinity. - Arch. Biochem. Biophys. 271: 56-63, 1989.
Go to original source... - Wood, D., Lenne, J.M.: The conservation of agrobiodiversity on-farm: questioning the emerging paradigm. - Biodiversity Conserv. 6: 109-129, 1997.
Go to original source... - Wood, E.M., Miles, T.D., Wharton, P.S.: The use of natural plant volatile compounds for the control of the potato postharvest diseases, black dot, silver scurf and soft rot. - Biol. Control 64: 152-159, 2013.
Go to original source... - Xiao, G., Zheng, F., Qiu, Z., Yao, Y.: Impact of climate change on water use efficiency by wheat, potato and corn in semiarid areas of China. - Agr. Ecosyst. Environ. 181: 108-114, 2013.
Go to original source... - Xing, W., Rajashekar, C.: Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. - Environ. exp. Bot. 46: 21-28, 2001.
Go to original source... - Yu, C.S., Chen, Y.C., Lu, C.H., Hwang, J.K.: Prediction of protein subcellular localization. - Proteins: Struct. Funct. Bioinform. 64: 643-651, 2006.
Go to original source... - Yu, H.Q., Zhou, X.Y., Wang, Y.G., Zhou, S.F., Fu, F.L., Li, W.C.: A betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus enhances tolerance of Arabidopsis to high salt and drought stresses. - Plant Growth Regul. 83: 265-276, 2017.
Go to original source... - Zhang, H., Lu, L., Chen, L., Tao, Z., Chen, F., Zhong, S., Liu, Y., Tian, Y., Yan, P.: Molecular cloning, expression, and regulation of the ovalbumin gene in pigeon oviduct epithelial cells. - Genet. mol. Res. 13: 117-126, 2014.
Go to original source... - Zhang, J.-L., Shi, H.: Physiological and molecular mechanisms of plant salt tolerance. - Photosynth. Res. 115: 1-22, 2013.
Go to original source... - Zhu, L.J., Guan, D.X., Luo, J., Rathinasabapathi, B., Ma, L.Q.: Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. - Chemosphere 113: 9-16, 2014.
Go to original source...



