Skip to main content

Exogenous Proline-Mediated Abiotic Stress Tolerance in Plants: Possible Mechanisms

  • Chapter
  • First Online:

Abstract

Plants are subjected to many stresses (salinity, drought, heavy metals, temperature, etc.) that may limit their growth. As a result, plants exhibit a variety of adaptive strategies to mitigate the adverse effects of abiotic stresses. Among those strategies, the accumulation of compatible solute such as proline is the most common defensive mechanism adopted. Indeed, proline plays a highly beneficial role as an osmolyte. In addition, proline helps to stabilize subcellular structures and acts as a metal chelator. Proline may also activate the cellular antioxidant system and scavenge the reactive oxygen species (ROS). Accordingly, application of exogenous proline was investigated on plants to induce tolerance. Therefore, under salt conditions, exogenous proline might alleviate growth inhibition and ameliorate photosynthetic activity, mineral nutrition, and water status. Furthermore, it may regulate osmotic potential and decrease the effect of toxic ions by activating the enzymatic antioxidant system. Exogenous proline applied under drought stress has successfully improved physiological performance. In these conditions, these applications increased proline accumulation in cells and therefore reduce cell osmotic potential and maintain turgor. This osmotic adjustment may help plants to improve their biomass. Finally, the beneficial role of exogenous proline was also proved in plants subjected to metal stress. This organic compound may reduce the phytotoxic effects of metals through the formation of proline-metal complexes and the stimulation of enzymatic and nonenzymatic antioxidant systems. Besides, exogenous proline may protect plants subjected to metal contamination by stabilizing membranes and thereby preventing electrolyte leakage, improving water status, photosynthetic activity, and growth rate.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abdelhamid MT, Rady MM, Osman AS, Abdalla MA (2013) Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. J Hortic Sci Biotechnol 88:439–446

    Article  CAS  Google Scholar 

  • Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandhari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H (2011) Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biol Trace Elem Res 140:354–367

    Article  CAS  PubMed  Google Scholar 

  • Aleksza D, Horváth GV, Sándor G, Szabados L (2017) Proline accumulation is regulated by transcription factors associated with phosphate starvation. Plant Physiol 175(1):555–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali Q, Ashraf M, Shahbaz M, Humera H (2008) Ameliorative effect of foliar applied proline on nutrient uptake in water stressed maize (Zea mays L.) plants. Pak J Bot 40:211–219

    CAS  Google Scholar 

  • Ali Q, Anwar F, Ashraf M, Saari N, Perveen R (2013) Ameliorating effects of exogenously applied proline on seed composition, seed oil quality and oil antioxidant activity of maize (Zea mays L.) under drought stress. Int J Mol Sci 14:818–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amini S, Ghobadi C, Yamchi A (2015) Proline accumulation and osmotic stress: an overview of P5CS gene in plants. J Plant Mol Breed 3(2):44–55

    Google Scholar 

  • Anwar A, She M, Wang K, Riaz B, Ye X (2018) Biological roles of ornithine aminotransferase (OAT) in plant stress tolerance: present progress and future perspectives. Int J Mol Sci 19(11):3681

    Article  PubMed Central  CAS  Google Scholar 

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Aslam M, Saeed MS, Sattar S, Sajad S, Sajjad M, Adnan M, Iqbal M, Sharif MT (2017) Specific role of proline against heavy metals toxicity in plants. Int J Pure Appl Biosci 5(6):27–34

    Article  Google Scholar 

  • Ben Ahmed C, Magdich S, Ben Rouina B, Sensoy S, Boukhris M, Ben Abdullah F (2011) Exogenous proline effects on water relations and ions contents in leaves and roots of young olive. Amino Acids 40(2):565–573

    Article  CAS  PubMed  Google Scholar 

  • Bhagavan NV, Ha CE (2015) Chapter 3 - Amino acids. In: Essentials of medical biochemistry (Second edition) with clinical cases. Academic Press, Cambridge, USA, pp 21–29

    Chapter  Google Scholar 

  • Butt M, Ayyub CM, Amjad M, Ahmad R (2016) Proline application enhances growth of chilli by improving physiological and biochemical attributes under salt stress. Pak J Agric Sci 53:43–49

    Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  PubMed  Google Scholar 

  • Dawood MG, Taie HAA, Nassar RMA, Abdelhamid MT, 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. S Afr J Bot 93:54–63

    Article  CAS  Google Scholar 

  • De Freitas PAF, de Souza MR, Marques EC, Prisco JT, Gomes-Filho E (2018) Salt tolerance induced by exogenous proline in maize is related to low oxidative damage and favorable ionic homeostasis. J Plant Growth Regul 37:911–924

    Article  CAS  Google Scholar 

  • De Freitas PAF, De Carvalho HH, Costa JH, De Souza MR, Da Cruz Saraiva KD, De Oliveira FDB, Gomes Coelho D, Tarquinio Prisco J, Gomes-Filho E (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38:403–416

    Article  PubMed  CAS  Google Scholar 

  • Deuschle K, Funck D, Hellmann H, Däschner K, Binder S, Frommer WB (2001) A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J 27(4):345–356

    Article  CAS  PubMed  Google Scholar 

  • Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN (2015) Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev 90(4):1065–1099

    Article  PubMed  Google Scholar 

  • Forlani G, Bertazzini M, Zarattini M, Funck D (2015) Functional characterization and expression analysis of rice δ1-pyrroline-5-carboxylate dehydrogenase provide new insight into the regulation of proline and arginine catabolism. Front Plant Sci 6:591

    PubMed  PubMed Central  Google Scholar 

  • Funck D, Eckard S, Müller G (2010) Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. BMC Plant Biol 10(1):70

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghaffari H, Tadayon MR, Nadeem M, Cheema M, Razmjoo J (2019) Proline-mediated changes in antioxidant enzymatic activities and the physiology of sugar beet under drought stress. Acta Physiol Plant 41:23

    Article  CAS  Google Scholar 

  • Gholami Zali A, Ehsanzadeh P (2018) Exogenous proline improves osmoregulation, physiological functions, essential oil, and seed yield of fennel. Ind Crop Prod 111:133–140

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery abiotic stress tolerance crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gleeson D, Lelu-Walter MA, Parkinson M (2004) Influence of exogenous L-proline on embryogenic cultures of larch (Larix leptoeuropaea Dengler), sitka spruce (Picea sitchensis (Bong.) Carr.) and oak (Quercus robur L.) subjected to cold and salt stress. Ann For Sci 61:125–128

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Alam M, Rahman A, Hasanuzzama M, 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 Res Int 2014:Article ID 757219, 17 pages

    Google Scholar 

  • Hasanuzzaman M, Fujita M, Oku H, Islam MT (eds) (2019) Plant tolerance to environmental stress: role of phytoprotectants, 1st edn. CRC Press, Boca Raton, USA, p 448

    Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heuer B (2010) Role of proline in plant response to drought and salinity. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press, Boca Raton, pp 213–238

    Google Scholar 

  • Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoque MA, Banu MN, Okuma E, Amako K, Nakamura Y, Shimoishi Y (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol 64:1457–1468

    Article  CAS  Google Scholar 

  • Hossain MA, Hoque MA, Burritt DJ, Fujita M (2014) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad P (ed) Oxidative damage to plants. Academic press, Cambridge, USA, pp 477–522

    Google Scholar 

  • Huang TC, Teng CS, Chang JL, Chuang HS, Ho CT, Wu ML (2008) Biosynthetic mechanism of 2-acetyl-1-pyrroline and its relationship with Δ1-pyrroline-5-carboxylic acid and methylglyoxal in aromatic rice (Oryza sativa L.) callus. J Agric Food Chem 56:7399–7404

    Article  CAS  PubMed  Google Scholar 

  • Iqbal MJ (2018) Role of osmolytes and antioxidant enzymes for drought tolerance in wheat. In: Fahad S (ed) Global wheat production. IntechOpen. https://doi.org/10.5772/intechopen.75926. Available from: https://www.intechopen.com/books/global-wheat-production/role-of-osmolytes-and-antioxidant-enzymes-for-drought-tolerance-in-wheat

    Google Scholar 

  • Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiol Mol Biol Plants 17(3):203–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kavi Kishor PB, HimaKumari P, Sunita MSL, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim GB, Nam YW (2013) A novel Δ1-pyrroline-5-carboxylate synthetase gene of Medicago truncatula plays a predominant role in stress-induced proline accumulation during symbiotic nitrogen fixation. J Plant Physiol 170(3):291–302

    Article  CAS  PubMed  Google Scholar 

  • Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39(4):949–962

    Article  CAS  PubMed  Google Scholar 

  • Merwad ARM, Desoky ESM, Rady MM (2018) Response of water deficit-stressed Vigna unguiculata performances to silicon, proline or methionine foliar application. Sci Hortic 228:132–144

    Article  CAS  Google Scholar 

  • Messedi D, Farhani F, Hamed KB, Trabelsi NAJLA, Ksouri R, Habib-Ur-Rehman Athar CA (2016) Highlighting the mechanisms by which proline can confer tolerance to salt stress in Cakile maritima. Pak J Bot 48:417–427

    CAS  Google Scholar 

  • Murahama M, Yoshida T, Hayashi F, Ichino T, Sanada Y, Wada K (2001) Purification and characterization of δ1-pyrroline-5-carboxylate reductase isoenzymes, indicating differential distribution in spinach (Spinacia oleracea L.) leaves. Plant Cell Physiol 42(7):742–750

    Article  CAS  PubMed  Google Scholar 

  • Murmu K, Murmu S, Kumar Kundu C, Sekhar Bera P (2017) Exogenous proline and glycine betaine in plants under stress tolerance. Int J Curr Microbiol App Sci 6(9):901–913

    Article  CAS  Google Scholar 

  • Noreen S, Akhter MS, Yaamin T, Arfan M (2018) The ameliorative effects of exogenously applied proline on physiological and biochemical parameters of wheat (Triticum aestivum L.) crop under copper stress condition. J Plant Interact 13:221–230

    Article  CAS  Google Scholar 

  • Orsini F, Pennisi G, Mancarella S, Al Nayef M, Sanoubar R, Nicola S, Gianquinto G (2018) Hydroponic lettuce yields are improved under salt stress by utilizing white plastic film and exogenous applications of proline. Sci Hortic 233:283–293

    Article  Google Scholar 

  • Osman HS (2015) Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann Agric Sci 60:389–402

    Article  Google Scholar 

  • Oukarroum A, El Madidi S, Strasser RJ (2012) Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): a chlorophyll a fluorescence study. Plant Biosyst 146:1037–1043

    Article  Google Scholar 

  • Pál M, Tajti J, Szalai G, Peeva V, Végh B, Janda T (2018) Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Sci Rep 8:12839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pérez-Arellano I, Carmona-Álvarez F, Martínez AI, Rodríguez-Díaz J, Cervera J (2010) Pyrroline-5-carboxylate synthase and proline biosynthesis: from osmotolerance to rare metabolic disease. Protein Sci 19(3):372–382

    PubMed  PubMed Central  Google Scholar 

  • Rai AN, Penna S (2013) Molecular evolution of plant P5CS gene involved in proline biosynthesis. Mol Biol Rep 40(11):6429–6435

    Article  CAS  PubMed  Google Scholar 

  • Rana V, Ram S, Nehra K (2017) Review proline biosynthesis and its role in abiotic stress. IJAIR 6(3):473–478

    Google Scholar 

  • Rasheed R, Ashraf MA, Hussain I, Haider MZ, Kanwal U, Iqbal M (2014) Exogenous proline and glycinebetaine mitigate cadmium stress in two genetically different spring wheat (Triticum aestivum L.) cultivars. Braz J Bot 37:399–406

    Article  Google Scholar 

  • Roychoudhury A, Banerjee A, Lahiri V (2015) Metabolic and molecular-genetic regulation of proline signaling and itscross-talk with major effectors mediates abiotic stress tolerance in plants. Turk J Bot 39(6):887–910

    Article  CAS  Google Scholar 

  • Satoh R, Fujita Y, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2004) A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in Arabidopsis. Plant Cell Physiol 45:309–317

    Article  CAS  PubMed  Google Scholar 

  • Savouré A, Hua XJ, Bertauche N, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet 254(1):104–109

    Article  PubMed  Google Scholar 

  • Shahid MA, Balal RM, Pervez MA, Abbas T, Aqeel MA, Javaid MM, 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. Turk J Bot 38:914–926

    Article  CAS  Google Scholar 

  • Shetty K (1997) Biotechnology to harness the benefits of dietary phenolics; focus on Lamiaceae. Asia Pac J Clin Nutr 6:162–171

    CAS  PubMed  Google Scholar 

  • Signorelli S, Dans PD, Coitiño EL, Borsani O, Monza J (2015) Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions. PLoS One 10(3):e0115349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh A, Sharma MK, Sengar RS (2017) Osmolytes: Proline metabolism in plants as sensors of abiotic stress. JANS 9(4):2079–2092

    Article  CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Sobahan MA, Arias CR, Okuma E, Shimoishi Y, Nakamura Y, Hirai Y, Mori IC, Murata Y (2009) Exogenous proline and glycinebetaine suppress apoplastic flow to reduce Na+ uptake in rice seedlings. Biosci Biotechnol Biochem 73:2037–2042

    Article  CAS  PubMed  Google Scholar 

  • 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 Sci 166:941–948

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97

    Article  CAS  PubMed  Google Scholar 

  • Székely G, Ábrahám E, Cséplő Á, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53(1):11–28

    Article  PubMed  CAS  Google Scholar 

  • Teh CY, Shaharuddin NA, Ho CL, Mahmood M (2016) Exogenous proline significantly affects the plant growth and nitrogen assimilation enzymes activities in rice (Oryza sativa) under salt stress. Acta Physiol Plant 38:151

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  CAS  PubMed  Google Scholar 

  • Verdoy D, Coba De La Peña T, Redondo FJ, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29:1913–1923

    Article  CAS  PubMed  Google Scholar 

  • Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book/American Society of Plant Biologists 8:e0140

    Google Scholar 

  • Wei C, Cui Q, Zhang XQ, Zhao YQ, Jia GX (2016) Three P5CS genes including a novel one from Lilium regale play distinct roles in osmotic, drought and salt stress tolerance. J Plant Biol 59(5):456–466

    Article  CAS  Google Scholar 

  • Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schutze K, Alonso R, Harter K, Vicente-Carbajosa J, Droge-Laser W (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wutipraditkul N, Wongwean P, Buaboocha T (2015) Alleviation of salt-induced oxidative stress in rice seedlings by proline and/or glycinebetaine. Biol Plant 59:547–553

    Article  CAS  Google Scholar 

  • You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant

    Book  Google Scholar 

  • Zhang L, Becker DF (2015) Connecting proline metabolism and signaling pathways in plant senescence. Front Plant Sci 6:552

    PubMed  PubMed Central  Google Scholar 

  • Zouari M, Ben Ahmed C, Zorrig W, Elloumi N, Rabhi M, Delmail D, Ben Rouina B, Labrousse P, Ben Abdallah F (2016a) Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.). Ecotoxicol Environ Saf 128:100–108

    Article  CAS  PubMed  Google Scholar 

  • Zouari M, Ben Ahmed C, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Ben Abdallah F, Ben Rouina B (2016b) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128:195–205

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pascal Labrousse .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Zouari, M., Hassena, A.B., Trabelsi, L., Rouina, B.B., Decou, R., Labrousse, P. (2019). Exogenous Proline-Mediated Abiotic Stress Tolerance in Plants: Possible Mechanisms. In: Hossain, M., Kumar, V., Burritt, D., Fujita, M., Mäkelä, P. (eds) Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-27423-8_4

Download citation

Publish with us

Policies and ethics