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Ashu Singh Manoj Kumar Sharma R. S. Sengar

Abstract

Proline accumulation occurs in a large range of plant species in retaliation to the numerous abiotic stresses. An exclusive research pattern suggests there is a pragmatic relation between proline accumulation and plant stress tolerance. In this review, we will discuss the metabolism of proline accumulation and its role in stress tolerance in plants. Pertaining to the literature cited clearly indicates that not only does it acts as an osmolyte, it also plays important roles during stress as a metal chelator and an antioxidative defence molecule. Moreover, when applied exogenously at low concentrations, proline enhanced stress tolerance in plants. However, some reports point out adverse effects of proline when applied at higher doses. Role of proline gene in seed germination, flowering and other developmental programmes; thus creation of transgene overexpressing this gene would provide better and robust plants. In this context this review gives a detailed account of different proline gene over-expressed in all the trans-genic crops so far.

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Keywords

Abiotic stress, Osmoprotectant, Proline, ROS, Transgenic

References
Anoop, N. and Gupta, A.K. (2003). Transgenic indica rice cv IR-50 over-expressing Vigna aconitifolia ?1-pyrroline-5-carboxylate synthetase cDNA shows tolerance to high salt. Journal of Plant Biochemistry and Biotechnology, 12: 109-116.
Armengaud, P., Thiery, L.R., Buhot, N.O., Grenier, D., March, G. and Savoure, A.D. (2004). Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiologia Plantarum, 120: 442-450.
Ashraf, M. and Foolad, M.R. (2005). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59: 206-16.
Ayliffe, M.A., Mitchell, H.J., Deuschle, K. and Pryor, A. J. (2005). Comparative analysis in cereals of a key proline catabolism gene. Molecular Genetics and Genomics, 274: 494-505.
Bajaj, S. and Mohanty, A. (2005). Recent advances in rice biotechnology towards genetically superior transgenic rice. Plant Biotechnology Journal, 3: 275-307.
Barnett, N.M. and Naylor, A.W. (1966). Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiology, 41: 1222-1230.
Bassi, R. and Sharma, S.S. (1993a). Changes in proline content accompanying the uptake of zinc and copper by Lemna minor. Annals of Botany, 72: 151-154.
Bassi, R. and Sharma, S.S. (1993b). Proline accumulation in wheat seedlings exposed to zinc and copper. Phytochemistry, 33: 1339-1342.
Behelgardy, M.F., Motamed, N. and Jazii F.R. (2012). Expression of the P5CS gene in transgenic versus non-transgenic olive (Olea europaea) under salinity stress. World Applied Sciences Journal, 18: 580-583.
Ben Hassine, A., Ghanem, M.E., Bouzid, S., and Lutts, S. (2008). An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. Journal of Experimental Botany, 59: 1315-1326.
Bernstein, L. (1961). Osmotic adjustment of plants to saline media. I. Steady state. American Journal of Botany, 48: 909-918.
Boggess, S.F., Aspinall, D. and Paleg, L.G. (1976). Stress metabolism. IX. The significance of end-product inhibition of proline biosynthesis and of compartmentation in relation to stress-induced proline accumulation. Australian Journal of Plant Physiology, 3: 513-525.
Boggess, S.F., Paleg, L.G. and Aspinall, D. (1975). ?1-pyrroline-5-carboxylic acid dehydrogenase in barley, a proline-accumulating species. Plant Physiology, 56: 259-262.
Bohnert HJ, Jensen RG. (1996). Strategies for engineering water-stress tolerance in plants. Trends in Biotechnology, 14: 89-97.
Bohnert, H.J. and Shen, B. (1999). Transformation and compatible solutes. Scientia Horticulturae, 78: 237-260.
Boyer, J.S. (1982). Plant productivity and environment.Science, 218: 443-448
Boyer, J.S. (2010). Drought decision-making. Journal of Experimental Botany, 61: 3493-3497.
Briens, M. and Larher, F. (1982). Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell and Environment, 5: 287-292.
Chen, M., Wei H., Cao J., Liu, R., Wang, Y. and Zheng C. (2007). Expression of Bacillus subtilis proBA genes and reduction of feedback inhibition of proline synthesis increases proline production and confers osmotolerance in transgenic Arabidopsis. Journal of Biochemistry and Molecular Biology, 40: 396-403.
Chen, J.B., Zhao, L.Y. and Mao, X.G. (2010). Response of PvP5CS1 transgenic Arabidopsis plants to drought and salt-stress. Acta Agronomica Sinica, 36: 147-153.
Chen, J.B., Yang, J.W., Zhang Z.Y., Feng X.F., Wang, S.M. (2013). Two P5CS genes from common bean exhibiting different tolerance to salt stress in transgenic Arabidopsis. Journal of Genetics, 92: 461-469.
Choudhary, N.L., Sairam, R.K. and Tyagi, A. (2005).Expression of delta1-pyrroline-5- carboxylate synthetase gene during drought in rice (Oryza sativa L.). Indian Journal of Biochemistry and Biophysics, 42: 366-370.
Csonka, L. (1989). Physiological and genetic responses of bacteria to osmotic stress. Microbiology Reviews, 53: 121-147.
De Campos, M.K.F., De Carvalho, K., De Souzaa, F.S., Marura, C.J., Pereira, L.F.P., Filhoc, J.C.B. and Vieira, L.G.E. (2011). Drought tolerance and antioxidant enzymatic activity in transgenic ‘Swingle’ citrumelo plants over-accumulating proline. Environmental and Experimental Botany, 72: 242-250.
De Ronde, J.A., Spreeth, M.H. and Cress, W.A. (2000). Effect of antisense-?1-pyrroline-5-carboxylate reductase
transgenic soybean plants subjected to osmotic and drought stress. Plant Growth Regulation, 32: 13-26.
De Ronde, J.A., Cress, W.A., Kruger, G.H.J., Strasser, R.J. and Van Staden, J. (2004). Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5VR gene, during heat and drought stress. Journal of Plant Physiology, 161: 1211-1224.
Delauney, A.J. and Verma, D.P.S. (1993). Proline biosynthesis and osmo-regulation in plants. Plant Journal, 4: 215-223.
Deng, G., Liang, J., Xu, D., Long, H., Pan, Z. and Yu, M. (2013). The relationship between proline content, the expression level of P5CS (?1-Pyrroline-5-Carboxylate Synthetase), and drought tolerance in Tibetan hulless barley (Hordeum vulgare var. nudum). Russian Journal of Plant Physiology, 60(5): 693-700.
Deuschle, K., Funck, D., Hellmann, H., Diischner, K., Binder, S. and Frommer, W.B. (2001). A nuclear gene encoding mitochondrial ?1-pyrroline-5-carboxylic acid dehydrogenase and its potential role in protection from proline toxicity. Plant Journal, 27: 345-355.
Dobra, J., Motyka, V., Dobrev, P., Malbeck, J., Prasil, I.T., Haisel, D., Gaudinova, A., Havlova, M., Gubis, J. and Vankova, R. (2010). Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology, 167: 1360-1370.
Dobra, J., Vankov, R.S., Havlov, M., Burman, A.J., Libus, J. and Storchov, H. (2011). Tobacco leaves and roots differ in the expression of proline metabolism-related genes in the course of drought stress and subsequent recovery. Journal of Plant Physiology, 168: 1588-1597.
Elthon, T.E. and Stewart, C.R. (1981). Sub mitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiology, 67: 780-784
Elthon, T.E. and Stewart, C.R. (1982). Proline oxidation in corn mitochondria: involvement of NAD, relationship to ornithine metabolism, and sidedness on the inner membrane. Plant Physiology, 70: 567-572.
Evers, D., Lefevre, I., Legay, S., Lamoureux, D., Hausman, J.-F., Gutierrez Rosales, R.O., Tincopa Marca, L.R., Hoffmann, L., Bonierbale, M. and Schafleitner, R. (2010). Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. Journal of Experimental Botany, 61: 2327-2343.
Forlani, G., Scainel, D. and Nielsen, E. (1997). Two ?1-pyrroline-5-carboxylate dehydrogenase, isoforms are expressed in cultured Nicotiana plumbaginifolia cells and are differentially modulated during the culture growth cycle. Planta, 20: 242-254
Fougere, F., Le Rudulier, D. and Streeter, J.G. (1991) .Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiology, 96: 1228-1236.
Fowler, S. and Thomashow, F. (2002). Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. The Plant Cell, 14: 8-15.
Funck, D., Stadelhofer, B. and Koch, W. (2008). Ornithine-a-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biology, 8: 40-52.
Gangopadhyay G, Basu S, Mukherjee B, Gupta S. (1997). Effects of salt and osmotic shocks on unadapted and adapted callus lines of tobacco. Plant Cell, Tissue and Organ Culture, 49: 45-52.
Ghanti, S.K.K., Sujata, K.G., Kumar, B.M.V., Karba, N.N., Reddy, K.J., Rao, M.S. and Kavi Kishor, P.B. (2011). Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biologia Plantarum, 55: 634-640.
Gleeson, D., LeluWalter, M. and Parkinson, M. (2005). Overproduction of proline in transgenic hybrid larch [Larix × leptoeuropaea (Dengler)] cultures renders them tolerant to cold, salt and frost. Molecular Breeding, 15(1): 21-29.
Guerzoni, J.T.S., Belintani, N.G., Moreira, R.M.P., Hoshimo, A.A., Domingues, D.S., Filho, J.C.B. and Vieira, L.G.E. (2014). Stress-induced ?1-pyrroline-5-carboxylate synthetase (P5CS) gene confers tolerance to salt stress in transgenic sugarcane. Acta Physiologiae Plantarum, 36(9): 2309-2319.
Han, K.H. and Hwang, C.H. (2003). Salt tolerance enhanced by transformation of a P5CS gene in carrot. Journal of Plant Biotechnology, 5: 149-153.
Hanson, A.D. and Hitz, W.D. (1982). Metabolic responses of mesophytes to plant water deficits. Annual Reviews of Plant Physiology, 33: 163-203.
Hanson, A.D., Rathinasabapathi, B., Rivoal, J., Burnet, M., Dillon, M.O. and Gage, D.A. (1994). Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proceedings of the National Academy of Science USA, 91(1): 306-310.
Hare, P.D. and Cress, W.A. (1997). Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation, 21(2): 79-102.
Hare, P.D., Cress, W.A. and Van Staden, J. (1998). Dissecting the roles of osmolyte accumulation during stress. Plant Cell and Environment, 21: 535-553.
Hellebust, J.A. (1976). Osmoregulation. Annual Review of Plant Physiology, 27: 485-505.
Hmida-Sayari, A., Gargouri-Bouzid, R., Bidani, A., Jaoua, L., Savoure, A. and Jaoua, S. (2005). Overexpression of D1-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Science, 169: 746-752.
Hong, Z., Lakkineni, K., Zhang, Z. and Verma, D.P.S. (2000). Removal of feedback inhibition of pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology, 122: 1129-1136.
Hongqi, Z., Croes, A.F. and Linskens, H.F. (1982). Protein synthesis in germinating pollen of Petunia: role of proline. Planta, 154: 199-203.
Hoque, M.A., Banu, M.N.A., Nakamura, Y., Shimoishi, Y. and Murata, Y. (2008). Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxifi cation systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology, 165: 813-824.
Hu, C.A, Delauney, A.J. and Verma, D.P. (1992). A bifunctional enzyme (?1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of National Academy of Science USA, 89(19): 9354-9358.
Hur, J., Hong Jong, K., Lee, C-H. and An, G., (2004). Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Science, 167: 417-426.
Ibragimova, S.S., Kolodyazhnaya, S.Y., Gerasimova, S.V. and Kochetov, A.V. (2012). Partial suppression of gene encoding proline dehydrogenase enhances plant tolerance to various abiotic stresses. Russian Journal of Plant Physiology, 59: 88-96.
Ibragimova, S.M., Trifonova, E.A., Filipenko, E.A. and Shymny, V.K. (2015). Evaluation of salt tolerance of transgenic tobacco plants bearing the P5CS1 gene of Arabidopsis thaliana. Russian Journal of Genetics, 51(12): 1181-1188.
Jazii, R.F., Yamchi, A., Hajirezaei, M., Abbasi, A.R. and Karkhane, A.A. (2011). Growth assessments of Nicotiana tabaccum cv. Xanthi transformed with Arabidopsis thaliana P5CS under salt stress. African Journal of Biotechnology, 10: 8539-8552.
Jones, M.M., Osmond, C.B. and Turner, N.C. (1980). Accumulation of solutes in leaves of sorghum and sunflower in response to water deficits. Australian Journal of Plant Physiology, 7: 193-205.
Kant, S., Kant, P., Raveh, E., and Barak, S. (2006). Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell and Environment, 29: 1220-1234.
Karthikeyan, A., Pandian, S.K. and Ramesh, M. (2011). Transgenic indica rice cv. ADT 43 expressing a ?1-pyrroline-5-carboxylate synthetase (P5CS) gene from Vigna aconitifolia demonstrates salt tolerance. Plant Cell Tissue and Organ Culture, 107: 383-395.
Kavi Kishor, P.B., Hong, Z., Miao, G., Hu, C.A.A. and Verma, D.P.S. (1995). Over expression of ?1-pyrroline-5-carboxylate synthetase increases proline overproduction and confers osmotolerance in transgenic plants. Plant Physiology, 108: 1387-1394.
Kavi Kishor, P.B., Sangam, S., Amrutha, R.N., Laxmi, P.S., Naidu, K.R., Rao, K.R.S. S., Rao, S., Reddy, K.J.,
Theriappan, P. and Sreenivasulu, N. (2005). Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Current Science, 88: 424-438.
Kazuo, S. and Kazuko, Y.S. (2006). Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany, 58(2): 221-227.
Kemble, A.R. and Macpherson, H.T. (1954). Liberation of amino acids in perennial rye grass during wilting. Biochemistry Journal, 58(1): 46-49.
Ketchum, R.E.B, Warren, R.C., Klima, L.J., Lopez-Gutierrez, F. and Nabors, M.W. (1991). The mechanism and regulation of proline accumulation in suspension cultures of the halophytic grass Distichlis spicata L. Journal of Plant Physiology, 137: 368-374.
Kochetov, A.V., Titov, S.E., Kolodyazhnaya, Y.S., Komarova, M.L., Kovel, V.S., Makarova, N.N., Ilyinskyi, Y.Y., Trifonova, E.A. and Shummy, V.K. (2004). Tobacco transformants bearing antisense suppressor of proline dehydrogenase gene are characterized by higher proline content and cytoplasm osmotic pressure. Russian Journal of Genetics, 40: 216-218.
Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T. and Wang, X. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology, 130: 2129-2141.
Kumar, V., Shriram, V., Kavi Kishor, P.B., Jawali, N. and Shitole, M.G. (2010). Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over expressing P5CSF129A gene. Plant Biotechnology Reports, 4: 37-48.
Kuznetsov, V.V. and Shevyakova, N.I. (1999). Proline under stress: Biological role, metabolism, and regulation. Russian Journal of Plant Physiology, 46: 274-287.
LaRosa, P. C., Rhodes, D., Rhodes, J. C., Bressan, R. A. and Csonka, L. N., (1991). Elevated accumulation of proline in NaCl-adapted tobacco cells is not due to altered ?1-pyrroline-5-carboxylate reductase. Plant Physiology, 96: 245-250.
Leigh, R.A., Ahmad, N. and Wyn Jones, R.G. (1981). Assessment of glycine betaine and proline compartmentation by analysis of isolated beet vacuoles. Planta, 153: 34-41.
Leisinger, T. (1987). Biosynthesis of proline. In: Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Neidhardt, F.C., Ingraham, J.L., Low, K.B., Magasanik, B., Schaechter, M. and Umbarger, H.E. (eds.). American Society for Microbiology, Washington, DC. pp. 346-351.
Li, S., Du, Y.P., Wu, Z.Y., Huang, C.L., Zhang, X.H., Wang, Z.X. and Jia, G.X. (2013). Excision of a selectable marker in transgenic lily (Sorbonne) using the Cre/loxP DNA excision system. Canadian Journal of Plant Science, 93: 903-912.
Liu, J., Ishitani, M., Halfter, U., Kim, C.S. and Zhu, J.K. (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the National Academy of Sciences, USA, 97: 3730-3734.
Liu D., He, S., Zhai, H., Wang, L., Zhao, Y.B., Wang, R. and Liu. Q. (2014). Overexpression of IbP5CR enhances salt tolerance in transgenic sweet potato. Plant Cell, Tissue and Organ Culture 117: 1-16.
Ma, L., Zhou, E., Gao, L., Mao, X., Zhou, R. and Jia, J. (2008). Isolation, expression analysis and chromosomal location of P5CR gene in common wheat (Triticum aestivum L.). South African Journal of Botany, 74: 705-712.
Madan, S., Nainawatee H.S., Jain, R.K., Chowdhury, J.B. (1995). Proline and proline metabolising enzymes in in-vitro selected NaCl-tolerant Brassica juncea L. under salt stress. Annals of Botany, 76: 51-57.
Mahboobeh, R. and Akbar, E.A. (2013). Effect of salinity on growth, chlorophyll, carbohydrate and protein contents of transgenic Nicotiana plumbaginifolia overexpressing P5CS gene. E3 Journal of Environmental Research and Management, 4: 163-170.
Mani, S., Van de Cotte, B., Van Montagu, M. and Verbruggen, N. (2002). Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiology, 128: 73-83.
Martin J.H. (1930). The comparative drought resistance of sorghums and corn. Agronomy Journal, 22: 993-1003.
McCue, K.F. and Hanson, A.D. (1990). Drought and salt tolerance: towards understanding and application. Trends in Biotechnology, 8: 358-362.
Miller, G., Honig, A., Stein, H., Suzuki, N., Mittler, R. and Zilberstein, A. (2009). Unraveling ?1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. Journal of Biological Chemistry, 284(39): 26482-26492.
Mitchell, H.J., Ayliffe, M.A., Rashid, K.Y. and Pryor, A.J. (2006). A rust inducible gene from flax is involved in proline catabolism. Planta, 223: 213-222.
Molinari, H.B.C., Filho, J.C.B., Kobayashi, A.K., Pileggi, M., Junior, R.P.L. and Pereira, L.F.P. (2004). Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. × Poncirus trifoliate L. Raf.) overproducing proline. Plant Science, 167: 1375-1381.
Molinari, H.B.C., Marur, C.J., Daros, E., Campos, M.K.F., Carvalho, J.F.R.P., Filho, J.C.B., Pereira, L.F.P. and Vieira, L.G.E. (2007). Evaluation of the stress-inducible production of proline in transgenic sugarcane: osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum, 130: 218-229.
Monteoliva, M.I, Rizzi, Y.S., Cecchini, N.M., Hajirezaei, M.R. and Alvarez, M.E. (2014). Context of action of proline dehydrogenase (ProDH) in the hypersensitive response of Arabidopsis. BMC Plant Biology, 14: 21-32.
Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytologist, 167: 645-663.
Munns, R. and Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59: 651-681.
Naidu, B.P., Paleg, L.G., Aspinall, D., Jennings, A.C., Jones, G.P. (1991). Amino acid and glycine betaine accumulation in cold stressed wheat seedlings. Phytochemistry, 30: 407-409.
Nanjo T., Kobayashi, M., Yoshiba, Y., Sanada, Y., Wada, K., Tsukaya, H., Kakubari, Y., Yamagushi-Shinozaki, K. and Shinozaki, K. (1999). Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. The Plant Journal, 18: 185-193.
Nash, D., Paleg, L.G. and Wiskich, J.T. (1982). Effect of proline, betaine and some other solutes on the heat stability of mitochondrial enzymes. Australian Journal of Plant Physiology, 9: 47-57.
Ober, E.S., and Sharp, R.E. (1994). Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. 1. Requirement for increased levels of abscisic acid. Plant Physiology, 105: 981-987.
Pahlich, E., Kerres, R. and Jager, H.J. (1983). Influence of water stress on the vacuole/extravacuole distribution of proline in protoplasts of Nicotiana rustica. Plant Physiology, 72: 590-591.
Paleg, L.G., Douglas, T.J., van Daal, A. and Keech, D.B. (1981). Proline, betaine and other organic solutes
protect enzymes against heat inactivation. Australian Journal of Plant Physiology, 8: 107-114.
Parida, A.K., Dagaonkar, V.S., Phalak, M.S., and Aurangabadkar, L.P. (2008). Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery. Acta Physiologiae Plantarum, 30: 619-627.
Petrusa, LM and Winicov, I. (1997). Proline status in salt tolerant and salt sensitive alfalfa cell lines and plants in response to NaCl. Plant Physiology and Biochemistry, 35: 303-310.
Phang, J. M. (1985). The regulatory functions of proline and pyrroline- 5-carboxylic acid. Current Topics in Cell Regulation, 25:91–132.
Priya, A.M., Krishnan, S.R. and Ramesh, M. (2015). Ploidy stability of Oryza sativa. L cv. IR64 transformed with the moth bean P5CS gene with significant tolerance against drought and salinity. Turkish Journal of Biology, 39: 407-416.
Pollard, A. and Wyn, J.R.G. (1979). Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta, 144: 291-298.
Razavizadeh, R. and Ehsanpour, A.A. (2009). Effects of salt stress on proline content, expression of ?1-pyrroline-5-carboxylate synthetase, and activities of catalase and ascorbate peroxidase in transgenic tobacco plants. Biology Letters, 46: 63-75.
Rayapati, P.J. and Stewart, C.R. (1991). Solubilization of proline dehydrogenase from maize (lea mays L.) mitochondria. Plant Physiology, 95: 787-791.
Rhodes, D. (1987). Metabolic responses to stress. In: The Biochemistry of Plants, Davies, D.D. (eds.), vol. 12. Academic Press, New York, pp. 201-241.
Rhodes, D. and Handa, S. (1989). Amino acid metabolism in relation to osmotic adjustment in plant cells. In: Environmental Stress in Plants: Biochemical and Physiological Mechanisms, NATO ASI Series, vol. G19, Cherry, J.H. (eds.), Springer, Berlin, pp. 41-62.
Rhodes, D., Nadolska-Orczyk A., Rich P.J. (2002). Salinity, osmolytes and compatible solutes In: Lauchli A, Luttge U, eds. Salinity, Environment, Plant, Molecules. Netherlands: Al-Kluwer Academic Publishers, pp. 181-204.
Rhodes, D., Verslues, P.E. and Sharp, R.E. (1999). Role of amino acids in abiotic stress resistance. In: Plant Amino Acids: Biochemistry and Biotechnology, Singh, B.K. (eds.) Marcel Dekker, NY, pp. 319-356.
Ribarits, A., Abdullaev, A., Tashpulatov, A., Richter, A., Heberle-Bors, E. and Touraev, A. (2007). Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development. Planta, 225: 1313-1324.
Rice Knowledge Management Portal (2011). www.rkmp.co.in www.rkmp.iari.res.in.
Rodriguez, R. and Redman, R. (2005). Balancing the generation and elimination of reactive oxygen species. Proceedings of National Academy of Science USA, 102: 3175-3176.
Roosens, N.H., Bitar, F.A., Loenders, K., Angenon, G. and Jacobs, M. (2002). Overexpression of ornthine-?-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Molecular Breeding, 9: 73-80.
Roxas, V.P., Smith, R.K., Allen, E.R. and Allen, R.D. (1997). Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnology, 15: 988-991.
Sairam, R.K., Srivastava, G.C., Agarwal, S. and Meena, R.C. (2005). Differences in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum, 49(1): 85-91.
Samaras, Y., Bressan, R.A., Csonka, L.N., Garcia-Rios, M.G., Paino, D'Urzo, M. and Rhodes, D. (1995). Proline accumulation during drought and salinity. In: Environment and Plant Metabolism: Flexibility and Acclimation, Bios Scientific Publishers, Oxford, pp. 161-187.
Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z. and Nagamura, Y. (2005). The map-based sequence of the rice genome. Nature, 436: 793-800.
Sawahel, W. A. and Hassan, A. H., (2002). Generation of transgenic wheat plants producing high levels of the osmoprotectant proline. Biotechnology Letters, 24: 721-725.
Schat, H., Sharma, S.S. and Vooijs, R. (1997). Heavy metalinduced accumulation of free proline in a metaltolerant and a nontolerant ecotype of Silene vulgaris. Physiologia Plantarum, 101: 477-482.
Schwacke, R., Grallath, S., Breitkreuz, K.E., Stransky, E., Stransky, H., Frommer, W.B., and Rentsch, D. (1999). LeProT1, a transporter for proline, glycine betaine, and ?-amino butyric acid in tomato pollen. Plant Cell, 11: 377-392.
Seki, M., Kamei, A., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2003). Molecular responses to drought, salinity and frost: common and different paths for plant protection. Current Opinion in Biotechnology, 14: 194-199.
Seki, M., Narusaka, M., Ishida, J., Nanjo, T. and Fujita, M. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant Journal, 31: 279-92.
Serraj, R. and Sinclair, T.R. (2002). Osmolyte accumulation: can it really help increase crop yield under drought
conditions. Plant Cell Environment, 25: 333-341.
Serrano, R., Mulet, J.M., Rios, G., Marquez, J.A., Larrinoa, I.F., Leube, M.P., Mendizabal, I., Pascual-Ahuir, A., Proft, M., Ros, R. and Montesinos, C. (1999). A glimpse of the mechanisms of ion homeostasis during salt stress. Journal of Experimental Botany, 50: 1023-1036.
Sharma, S.S. and Dietz, K.J. (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57: 711-726.
Sharma, S., and Verslues, P.E. (2010). Mechanisms independent of ABA or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell and Environment, 33: 1838-1851.
Shen, B., Hohmann, S., Jensen, R.G. and Bohnert, H.J. (1999). Roles of sugar alcohols in osmotic stress adaptation. Replacement of glycerol by mannitol and sorbitol in yeast. Plant Physiology, 121: 45-52.
Siripornadulsil, S., Traina, S., Verma, D.P.S. and Sayre, R.T. (2002). Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell, 14: 2837-2847.
Smirnoff, N. and Cumbes, Q.J. (1989). Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry, 28: 1057-1060.
Sokhansanj, A., Noori, S.A.S. and Niknam, V. (2006). Comparison of bacterial and plant genes participating in proline biosynthesis with Osmotin gene, with respect to enhancing salinity tolerance of transgenic tobacco plants. Russian Journal of Plant Physiology, 53: 110-115.
Somero, G.N. (1986). Protons, osmolytes, and fitness of internal milieu for protein function. American Journal of Physiology, 251: 197-213.
Srinivas, V. and Balasubramanian, D. (1995). Proline is a protein-compatible hydrotrope. Langmuir, 11: 2830-2833.
Stephanopoulos, G. (1999). Metabolic fluxes and metabolic engineering. Metabolic Engineering, 1: 1-11.
Stewart, G.R. and Lee, J.A. (1974). The role of proline accumulation in halophytes. Planta, 120: 279-289.
Stewart, C.R., Boggess, S.F., Aspinall, D. and Paleg, L.G. (1977). Inhibition of proline oxidation by water stress. Plant Physiology, 59: 930-932.
Stewart G.R. and Larher, F. (1980). Accumulation of amino acids and related compounds in relation to environmental stress. In: The Biochemistry of Plants. Mifflin, B.J. (eds), vol. 5, Academic Press, New York, pp. 609-635.
Stewart, C.R. (1981). Proline accumulation: Biochemical aspects. In: Physiology and Biochemistry of Drought Resistance in Plants, Paleg, L.G. and Aspinall, D. (eds.) Academic Press, Sydney, pp. 243-259.
Stines, A.P., Naylor, D.J., Hoj, P.B. and van Heeswijck, R. (1999). Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of ?1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiology, 120: 923-931.
Strizhov N, Abrahám E, Okrész L, Blickling S, Zilberstein A, Schell J, (1997). Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant Journal, 12: 557-569
Su, J., Wu, R. (2004). Stress inducible synthesis of proline in transgenic rice confers faster growth under stress
conditions than that with constitutive synthesis. Plant Science, 166: 941-948.
Surekha, C., Nirmala Kumari, K., Aruna, L.V., Suneetha, G., Arundhati, A. and Kishor, P.B.K. (2014). Expression of the Vigna aconitifolia P5CSF129A gene in transgenic pigeonpea enhances proline accumulation and salt tolerance. Plant Cell Tissue and Organ Culture, 116: 27-36.
Surender Reddy, P., Jogeswar, G., Rasineni, G.K., Maheswari, M., Reddy, A.R., Varshney, R.K. and Kavi Kishor, P.B. (2015). Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum (Sorghum bicolor L. Moench). Plant Physiology and Biochemistry, 94: 104-113.
Szekely, G., Abraham, E., Cselo, A., Rigo, G., Zsigmond, L., Csiszar, J., Ayaydin, F., Strizhov, N., Jasik, J., Schmelzer, E., Koncz, C. and Szabados, L. (2008).
Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant Journal, 53: 11-28.
Szymon, K., Lukasz, Q., Katarzyna, L., Stanley, L. and Malgorzata, G. (2015). Enhanced expression of the proline synthesis gene P5CSA in relation to seed osmopriming improvement of Brassica napus germination under salinity stress. Journal of Plant Physiology, 183: 1-12.
Tal, M. and Katz, A. (1980). Salt tolerance in the wild relatives of the cultivated tomato: the effect of proline on the growth of callus tissue of Lycopersicon esculentum and L. peruvianum under salt and water stress. Z. Pflanzenphysiol, 98: 283-288.
Tanner, J. (2008). Structural biology of proline catabolism. Amino Acids, 35: 719-730.
Taylor, C.B. (1996). Proline and water deficit: ups and downs. Plant Cell, 8: 1221-1224.
Thomas, J.C., De Armond, R.L. and Bohnert, H.J. (1992). Influence of NaCl on growth, proline, and
phosphoenolpyruvate carboxylase levels in Mesembryanthemum crystallinum suspension cultures. Plant Physiology, 98: 626-631.
Thompson, J.F. (1980). Arginine synthesis, proline synthesis, and related processes. In: The Biochemistry of Plants, Mifflin, B.J. (eds.), vol. 5, Academic Press, New York, pp. 375-403.
Timasheff, S.N. (1993). The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annual Review of Biophysical and Biomolecular Structures, 22: 67-97.
Treichel, S. (1986). The influence of NaCl on ?1-pyrroline-5-carboxylate reductase (P5CR) in proline-accumulating cell suspension cultures of Mesembryanthemum nodiflorum and other halophytes. Plant Physiology, 67: 173-181.
Ueda, A., Shi, W., Shimada, T., Miyake, H. and Takabe, T. (2008). Altered expression of barley proline transporter causes different growth responses in Arabidopsis. Planta, 227(2): 277-86.
Vendruscoloa, E.C.G., Schusterb, I., Pileggic, M., Scapimd, C.A., Molinarie, H.B.C., Marure, C.J. and Vieirae L.G.E. (2007). Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology, 164: 1367-1376.
Verbruggen, N. and Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids, 35: 753-759.
Verbruggen, N., Hua, X.J., May, M. and Van Montagu, M. (1996). Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proceedings of National
Academy of Science USA, 93: 8787-8791.
Verdoy, D., de la Pena, T.C., Redondo, F.J., Lucas, M.M. and Pueyo, J.J. (2006). Transgenic Medicago truncatula plants that accumulate proline display nitrogen fixing activity with enhanced tolerance to osmotic stress. Plant, Cell and Environment, 29: 1913-1923.
Verma, D.P.S. (1999). Osmotic stress tolerance in plants: Role of proline and sulfur metabolisms. In: Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants. Landes Company, Texas, USA, pp. 153-168.
Voetberg, G.S. and Sharp, R.E. (1991). Growth of the maize primary root tip at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiology, 96: 1125-1130.
Widodo, John, H.P., Ed, N., Mark, T., Antony, B. and Ute, R. (2009). Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany, 60: 4089-4103.
Williamson, C. L. and Slocum, R. D. (1992). Molecular cloning and evidence for osmoregulation of the D 1 -pyrroline-5-carboxylate reductase (proC) gene in pea (Pisum sativum L.). Plant Physiology, 100: 1464–1470
Wu, S.J., Ding, L. and Zhu, J.K. (1996). SOS1 a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell, 8: 617-627.
Wu, L.Q., Fan, Z.M., Guo, L., Li, Y.Q., Zhang, W.J., Qu, L.J. and Chen, Z.L. (2003). Over-expression of an Arabidopsis delta-OAT gene enhances salt and drought tolerance in transgenic rice. Chinese Science Bulletin, 48: 2594-2600.
Wyn, J.R.G., Storey, R., Leigh, R.A., Ahmad, N. and Pollard. A. (1977). A hypothesis on cytoplasmic osmoregulation. In: Regulation of Cell Membrane Activities in Plants. Marre, E. and Cifferi, O. (eds.), Elsevier, Amsterdam, pp. 121-136.
Yamchi A., Jazii, F.R., Mousav, A., Karkhane, A.A. and Re, S. (2007). Proline accumulation in transgenic tobacco as a result of expression of Arabidopsis ?1-pyrroline-5-carboxylate synthetase (P5CS) during osmotic stress. Journal of Plant Biochemistry and Biotechnology, 16: 9-15.
Yancey, P.H. (1994). Compatible and counteracting solutes. In: Cellular and Molecular Physiology of Cell Volume Regulation. Strange, K. (eds.), CRC Press, Boca Raton, pp. 81-109.
Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D. and Somero, G.N. (1982). Living with water stress: evolution of osmolytes systems. Science, 217: 1214-1222.
You, J., Hu, H. and Xiong L. (2012). An ornithine ?-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Science, 197: 59-69.
Yu, C., Wan, A.S, Auinbt, Z.A. and Quzac, G.J. (1983). Transport of glycine, serine, and proline into spinach leaf mitochondria. Archives of Biochemistry and Biophysics, 227: 180-187.
Zhang, C.S., Lu, Q. and Verma, D.P.S. (1995). Removal of feedback inhibition of ?1-pyrroline-5-carboylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. Journal of Biological Chemistry, 270: 20491-20496.
Zhu, B., Su, J., Chang, M., Verma, D. P. S., Fan, Y. L. and Wu, R. (1998). Overexpression of a ?1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Science, 139: 41-48.
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How to Cite

Osmolytes: Proline metabolism in plants as sensors of abiotic stress. (2017). Journal of Applied and Natural Science, 9(4), 2079-2092. https://doi.org/10.31018/jans.v9i4.1492