Effects of exogenous proline on the physiological characteristics of Triticum aestivum L. and Lens culinaris Medik. under drought stress

Selma BEKKA, Ouzna ABROUS-BELBACHIR, Réda DJEBBAR

Abstract


Proline, which is an indicator of stress, is often considered as a good parameter for the testing of plants with good drought tolerance capacity. Thus, exogenous application of proline is a possible technique to avoid the deleterious effects of the drought on plant growth. The objectives of this study are to investigate the impact exogenous proline on the physiological behavior of two plant species, bread wheat, a monocot, and lentil, a dicot, under drought stress conditions. After several preliminary tests, optimal concentrations of exogenous proline were determined (6 mM for bread wheat and 2 mM for lentil) and both species were treated in normal and drought conditions. The results showed that water deficit affected both species leading to a reduction in growth, chlorophyll content and relative water content. Likewise, 15 % PEG-6000, which is equivalent to osmotic potential of -0.31MPa, caused a high accumulation of proline. In almost of cases we also noted a remarkable decrease in catalase (Cat), ascorbate peroxidase (APX) and gaiacol peroxidase (GPX) activities which was probably due to the oxidative stress caused by drought stress. The application of proline in stressful conditions reduced the deleterious effects caused by the stress on both species, due, particularly, to the accumulation of free endogenous proline and the increase of Cat, APX and GPX activities.


Keywords


Triticum aestivum L.; Lens culinaris Medik.; exogenous proline; drought tolerance

Full Text:

PDF

References


Akhzari, D., & Pessarakli, M. (2015). Effect of Drought Stress on Total Protein, Essential Oil Content, and Physiological Traits of Levisticum officinale Koch. Journal of Plant Nutrition, 39(10),1365-1371. doi:10.1080/01904167.2015.1109125

Alia, A., Prasad, K.V. S. K., Pardha Saradhi, P. (1995). Effect of zinc on free radical and proline in Brassica juncea and Cajanus cajan. Phytochemistry, 39(1), 45-47. doi:10.1016/0031-9422(94)00919-K

Abdelhamid, M.T., Rady, M. M., Osman, A. S., Abdalla, M. A. (2013). Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. Journal of Horticultural Science and Biotechnology, 88(4), 439–446. doi:10.1080/14620316.2013.11512989

Akcay, U. C., Ercan, O., Kavas, M., Yildiz, L., Yilmaz, C., Oktem, H. A., Yucel, M. (2010). Drought-induced oxidative damage and antioxidant responses in peanut (Arachis hypogaea L.) seedlings. Plant Growth Regulation, 61(1), 21-28. doi:10.1007/s10725-010-9445-1

Alam, M. M., Nahar, K., Hasanuzzaman, M., Fujita, M. (2014). Alleviation of osmotic stress in Brassica napus, B. campestris, and B. juncea by ascorbic acid application. Biolgia Plantarum, 58(4), 697-708. doi:10.1007/s10535-014-0447-0

Alia, Mohanty, P., Matysik, J. (2001). Effect of proline on the production of singlet oxygen. Amino Acids, 21 (2), 195-200. doi:10.1007/s007260170026

Antonić, D. S., Milošević, S., Cingel, A., Lojić, M., Trifunović-Momčilov, M., Petrić, M., Subotić A., Simonović, A. (2016). Effects of exogenous salicylic acid on Impatiens walleriana L. grown in vitro under polyethylene glycol-imposed drought. South African Journal of Botany, 105, 226–233. doi:10.1016/j.sajb.2016.04.002.

Ashraf, M., & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206-216. doi:10.1016/j.envexpbot.2005.12.006

Bajji, M., Kinet, J. M., Lutts, S. (2002). The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regulation, 36(1), 61–70. doi:10.1023/A:1014732714549

Bandurska, H. (2001). Does proline accumulated in leaves of water deficit stressed barley plantsconfine cell membrane injuries? II. Proline accumulation during hardening and its involvement in reducing membrane injuries in leaves subjected to severe osmotic stress. Acta Physiologiae Plantarum, 23(4), 483-490. doi:10.1007/s11738-001-0059-0

Bar-Nun, N., & Poljakoff-Mayber, A. (1977). Salinity Stress and the Content of Proline in Roots of Pisum sativum and Tamarix tetragyna. Annals of Botany Company, 41(1),173-179. doi:10.1093/oxfordjournals.aob.a085265

Barrs, H. D. (1968). Determination of water deficits in plant tissues. In: T.T Kozlowski (Eds) Water deficits and plant growth. New York, NY: Academic Press (pp. 235–368).

Ben Ahmed, C. S., Magdich, S., Ben Rouina, B., Sensoy, S., Boukhris, M., Ben Abdullah, F. (2010). Exogenous proline effects on water relations and ions contents in leaves and roots of young olive. Amino Acids, 40(2), 565-573. doi:10.1007/s00726-010-0677-1

Ben Hassine, A., Ghanem M. E., Bouzid, S., 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(6), 1315-1326. doi:10.1093/jxb/ern040

Bradford, M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principal of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi:10.1016/0003-2697(76)90527-3

Carvalho, M. H. (2008). Drought Stress and Reactive Oxygen Species. Plant Signaling and Behavior, 3(3), 156- 165. doi:10.4161/psb.3.3.5536

Dawood, M. G., Taie, H. A. A., Nassar, R. M. A., Abdelhamid, M. T., Schmidhalter, U. (2014). The changes induced in the physiological, biochemical and anatomical characteristics of Vicia faba by the exogenous application of proline under seawater stress. South African Journal of Botany, 93, 54–63. doi:10.1016/j.sajb.2014.03.002

Delauney, A. J., & Verma, D. P. S. (1993). Proline biosynthesis and osmoregulation in plants. The Plant Journal, 4(2), 215-223. doi:10.1046/j.1365-313X.1993.04020215.x

Demir, Y., & Kocacaliskan, I. (2002). Effect of NaCl and proline on bean seedling cultured in vitro. Biologia Plantarum, 45(4), 597–599. doi:10.1023/A:1022343101727

Dorey, S., Baillieul, F., Saindrenan, P., Fritige, B., Kaufmann, S. (1998). Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Molecular Plant-Microbe Interactions, 11(11), 1102–11090. doi:10.1094/MPMI.1998.11.11.1102

Dubey, R., & Rani, M. (1990). Influence of NaCl salinity on the behavior of protease. Amino peptidase and carboxypeptidase's in the seedlings in relation to salt. Australian Journal of Plant Physiology, 17, 215 – 221. doi:10.1071/PP9900215

Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S. M. A. (2009). Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development, 29(1), 185–212. doi:10.1051/agro:2008021

Gleeson, D., Lelu-Walter, M. A., Parkinson, M. (2004). 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. doi:10.1007/s11032-004-1363-3

Gondim, F. A., Gomes-Filho, E., Costa, J. H., Alencar, N. L. M., Prisco, J. T. (2012). Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiology and Biochemistry, 56, 62-71. doi:10.1016/j.plaphy.2012.04.012

Handa, S., Handa, A. K., Hasegawa, P. M., Bressan, R. A. (1986). Proline accumulation and the adaptation of culture cultured plant cells to water stress. Plant Physiology, 80(4), 938-945. doi:10.1104/pp.80.4.938

Hasanuzzaman, M., Alam, M., Rahman, A., Hasanuzzaman, Md., Nahar, K., Fujita, M. (2014). Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Research International, ID 757219, 1-17. doi:10.1155/2014/757219

Ignatova, Z., & Gierasch, L. M. (2006). Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant. Proceedings of the National Academy of Sciences, 103(36), 13357–13361. doi:10.1073/pnas.0603772103

Ji, H., Liu, L., Li, K., Xie, Q., Wang, Z., Zhao, X., Xia Li, X. (2014). PEG-mediated osmotic stress induces premature differentiation of the root apical meristem and outgrowth of lateral roots in wheat. Journal of Experimental Botany, 65(17), 4863-4872. doi:10.1093/jxb/eru255.

Khalil, S. E., & El-Noemani, A. A. (2012). Effect of irrigation intervals and exogenous proline application in improving tolerance of garden cress plant (Lepidium sativum L.) to water stress. Journal of Applied Sciences Research, 8(1),157-167.

Khedr, A. H. A., Abbas, M. A., Wahid, A. A. A., Quick, W. P., Abogadallah, G. M. (2003). Proline induces the expression of salt-stress responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. Journal of Experimental Botany, 54(392), 2553–2562. doi:10.1093/jxb/erg277

Kibria, M. G., Farzana, K. Md., Matin, A., Hoque, Md. A. (2016). Mitigating water stress in wheat (BARI Gom 26) by exogenous application of proline. Fundamental and Applied Agriculture, 1(3), 118-123.

Lehmann, S., Funck, D., Szabados, L., Rentsch, D. (2010). Proline metabolism and transport in plant development. Amino Acids, 39(4), 949-962. doi:10.1007/s00726-010-0525-3

Li, P., Zhang, Y., Wu, X., Liu, Y. (2018). Drought stress impact on leaf proteome variations of faba bean (Vicia faba L.) in the Qinghai–Tibet Plateau of China. 3 Biotech, 8(110), 1-12.

Liang, X., Zhang, L., Natarajan, S.K. Becker, D.F. (2013). Proline Mechanisms of Stress Survival. Antioxidants & Redox Signaling, 19, 988- 1011. doi:10.1089/ars.2012.5074

Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: Pigments of Photosynthetic Biomembranes. Methodes in Enzymology, 148, 350-382. doi:10.1016/0076-6879(87)48036-1

Lokhande, V. H., Nikam, T. D., Penna, S. (2001). Differential Osmotic Adjustment to Iso-osmotic NaCl and PEG Stress in the in vitro Cultures of Sesuvium portulacastrum (L.). L. Journal of Crop Science and Biotechnology, 13(4), 251-256. doi:10.1007/s12892-010-0008-9

MacAdam, J. W., Nelson, C. J., Sharpe, R.E. (1992). Peroxidase activity in the leaf elongation zone of tall fescue. Plant Physiology, 99, 872-878. doi:10.1104/pp.99.3.872

Magné, C., & Larher, F. (1992). High sugar content of extracts interfers with colorimetric determination of amino Acids and free proline. Analytical Biochemistry, 200(1), 115-118. doi:10.1016/0003-2697(92)90285-F

Mani, S., Van De Cotte, B., Van Montagu, M., Verbruggen, N. (2002). Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiology, 128(1), 73–83. doi:10.1104/pp.010572

Medeiros, M. J. L., Silva, M. M. A., Granja, M. M. C., De Souza Silva Júnior, G., Camara, T., Willadino, L. (2015). Effect of exogenous proline in two sugarcane genotypes grown in vitro under salt stress. Acta Biológica Colombiana, 20(2), 57-63.

Meeta, J., Mini, M., Rekha, G. (2013). Effect of PEG-6000 I mposed Water Deficit on Chlorophyll Metabolism in Maize Leaves. Journal of Stress Physiology & Biochemistry, 9, 262-271.

Molla, M. R., Ali, M. R., Hasanuzzaman, M., Al-Mamu, M. H., Ahmed, A., Nazim UD-Dowla, M. A. N., Rohman, Md. M. (2014). Exogenous proline and betaine-induced upregulation of glutathione transferase and glyoxalase I in lentil (Lens culinaris) under drought stress. Notulae Botanicae Horti Agrobotanici Cluj-NapocaNorth America, 42(1), 73–80. doi:10.15835/nbha4219324

Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867-880.

Noctor, G., & Foyer, C. H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 249 –279. doi:10.1146/annurev.arplant.49.1.249

Okuma, E., Soeda, K., Tada, M., Murata, Y. (2000). Exogenous proline mitigates the inhibition of growth of Nicotiana tabacum cultured cells under saline conditions. Soil Science and Plant Nutrition, 46(1), 257-263. doi:10.1080/00380768.2000.10408781

Ozden, M., Demirel, U., Kahraman, A. (2009). Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Scientia Horticulturae, 119(2), 163–168. doi:10.1016/j.scienta.2008.07.031

Passioura, J. (2007). The drought environment: physical, biological and agricultural perspectives. Journal of Experimental Botany, 58(2), 113-117. doi:10.1093/jxb/erl212

Rady, M., & Hemida, K. A. (2016). Sequenced application of ascorbate-proline-glutathione improves salt tolerance in maize seedlings. Ecotoxicology and Environmental Safetyn, 133, 252–259. doi:10.1016/j.ecoenv.2016.07.028

Rajendrakumar, C. S., Reddy, B. V., Reddy, A. R. (1994). Proline-protein interactions: protection of structural and functional integrity of M4 lactate dehydrogenase. Biochemical and Biophysical Research Communications, 201 (2), 957–963. doi:10.1006/bbrc.1994.1795

Rasheed, R., Ashraf, M. A., Hussain, I., Haider, M. Z., Kanwal, U., Iqbal, M. (2014). Exogenous proline and glycine betaine mitigate cadmium stress in two genetically different spring wheat (Triticum aestivum L.) cultivars. Brazilian Journal of Botany, 37(4), 399-406. doi:10.1007/s40415-014-0089-7

Ranjbarfordoei, A ., Samson, R., Damne, P. V., Lemeur, R. (2000). Effects of Drought Stress Induced by PolyethyleneGlycol on Pigment Content and Photosynthetic Gas Exchange of Pistacia khinjuk and P mutica. Photosynthetic, 38(3), 443-447. doi:10.1023/A:1010946209484

Rentsch, D., Hirner, B., Schmelzer, E., Frommer, W. B. (1996). Salt stressinduced proline transporters and salt stress-repressed broadspecificity amino acid permeases identified by suppression of a yeast amino acid permease- targeting mutant. The Plant Cell, 8(8),1437-1446. doi:10.1105/tpc.8.8.1437

Samota, M .K., Sasi., M., Singh, A. (2017). Impact of Seed Priming on Proline Content and Antioxidant Enzymes to Mitigate Drought Stress in Rice Genotype. International Journal of Current Microbiology and Applied Sciences, 6, 2459-2466. doi:10.20546/ijcmas.2017.605.275

Savouré, A., Jaoua, S., Hua, X. J., Ardiles, W., Van Montagu, M., Verbruggen, N. (1995). Isolation, characterization, and chromosomal location of a gene encoding the ∆1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Letters, 372, 13–19. doi:10.1016/0014-5793(95)00935-3

Schobert, C., Köckenberger, W., Komor, E. (1988). Uptake of amino acids by plants from the soil: A comparative study with castor bean seedlings grown under natural and axenic soil conditions. Plant and Soil, 109(9), 181-188. doi:10.1007/BF02202082

Sepehr, M. F., Ghorbanli, M ., Amini, F. (2012).The effect of water stress on nitrate reductase activity, and nitrogen and phosphorus contents in Cuminum cyminum L.. Pakistan Journal of Botany, 44(3), 899-903

Shahid, M. A., Balal, R. M., Pervez, M. A., Abbas, T., Aqeel, M. A., Javaid, M. M., Garcia-Sanchez, F. (2014). Exogenous proline and proline-enriched Lolium perenne leaf extract protects against phytotoxic effects of nickel and salinity in Pisum sativum by altering polyamine metabolism in leaves. Turkish Journal of Botany, 38, 914-926. doi:10.3906/bot-1312-13

Sharma, S. S., & 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(4),711–526. doi:10.1093/jxb/erj073

Singh, M., Singh, V. P., Dubey, D., Prasad, S. M. (2015). Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicology and Environmental Safety, 117, 164–173. doi:10.1016/j.ecoenv.2015.03.021

Smirnoff, N. (1995). Antioxidant systems and plant response to the environment. In: Smirnoff V (Eds.), Environment and Plant Metabolism: Flexibility and Acclimation, BIOS Scientific Publishers, Oxford, UK.

Szabados, L., & Savouré, A. (2009). Proline: a multifunctional amino acid. Trends in Plant Science, 15(2), 89–97. doi:10.1016/j.tplants.2009.11.009

Troll, W., & Lindsey, J. (1955). A photometric method for the determination of proline. Journal of Biological Chemistry, 215(2), 655-660.

Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids. 35(4), 753-759. Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology, 208, 2819-2830.

Yuan, Z., Wang, C., Li, S. X., Tai, F. (2014). Effects of different plant hormones or PEG seed soaking on maize resistance to drought stress. Canadian Journal of Plant Science, 94(8), 1491-1499. doi:10.4141/cjps-2014-110




DOI: http://dx.doi.org/10.14720/aas.2018.111.2.20

Refbacks

  • There are currently no refbacks.


Copyright (c) 2018 selma bekka

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

 

Acta agriculturae Slovenica is an Open Access journal published under the terms of the Creative Commons CC BY License.

                           


eISSN 1854-1941