Skip to main content

Advertisement

SpringerLink
Log in

Proline-mediated changes in antioxidant enzymatic activities and the physiology of sugar beet under drought stress

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Drought stress (DS) is a major concern in the agricultural sector and, in particular, for sugar beet production and sugar content. As such several agricultural practices have been used to minimize yield losses from DS, and foliar application of proline is considered one such approach to improve drought tolerance in growing plants. Hence, the current study examined the proline-related improvements to induce drought tolerance in sugar beet plants. A field experiment was conducted at two locations (Shahrekord and Shalamzar) in Chaharmahal-Bakhtiari province, Iran. Experimental treatments comprised of three DS levels (well water: 100%; mild stress: 75%; severe stress: 50% water requirement of plant), and three proline applications (control: 0; low: 5 mM; high: 10 mM). DS caused a significant up-regulation in leaf proline content, malondialdehyde (MDA) content, hydrogen peroxide (H2O2) content, ascorbate peroxidase, catalase, and peroxidase enzymatic activities. This increase was more pronounced under proline application with concomitant down-regulation of MDA and H2O2 contents. DS also caused a decrease in leaf photosynthetic pigments, leaf relative water contents, membrane stability index and sugar beet root production; however, proline application mitigated these adverse DS effects. The study results suggest beneficial effects of proline applications, which is crucial to mitigation of the detrimental effects of DS in sugar beet by enhancing antioxidant enzymatic activities with concomitant reduction in MDA and H2O2 contents.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

Chl:

Chlorophyll

DS:

Drought stress

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

MSI:

Membrane stability index

POX:

Peroxidase

RWC:

Relative water contents

DS:

Drought stress

WW:

Well-water

MS:

Mild stress

SS:

Severe stress

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahmed CB, Rouina BB, Sensoy S, Boukhrissm Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive trees. J Agric Food Chem 58:4216–4222

    Article  Google Scholar 

  • Ali Q, Ashraf M, Athar HUR (2007) Exogenously applied proline at different growth stages enhances growth of two maize cultivars grown under water deficit conditions. Pak J Bot 39(4):1133–1144

    Google Scholar 

  • AL-Jbawi E, Abbas F (2013) The effect of length during water stress on sugar beet (Beta vulgaris L.) yield and quality. Persian Gulf Crop Protect 2(1):35–43

    Google Scholar 

  • Allen RG, Pereira LS, Raes D, Smith M (2000) FAO irrigation and drainage paper. Crop evapotranspiration 56:1–326

    CAS  Google Scholar 

  • Al-Shaheen MR, Soh A (2016) Effect of proline and gibberellic acid on the qualities and qualitative of corn (Zea maize L.) under the influence of different levels of the water stress. Int J Sci Res 6(5):752–756

    Google Scholar 

  • Arnon I (1996) Crop production in dry regions. Leonard Hill, London, 650 pp

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bajji M, Lutts S, Kinet JM (2000) Physiological changes after exposure to and recovery from polyethylene glycol-induced water deficit in callus cultures issued from durum wheat (Triticum durum Desf.) cultivars differing in drought resistance. J Plant Physiol 156:75–83

    Article  CAS  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    Article  CAS  Google Scholar 

  • Banchio E, Bogino PC, Zygadlo J, Giordano W (2008) Plant growth promoting rhizobacteria improves growth and essential oil yield in Origanum majorana L. Biochem Syst Ecol 36:766–771

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Ben AC, Ben Rouina B, Sensoy S, Boukhriss M, Ben Abdullah F (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216–4222

    Article  Google Scholar 

  • Boaretto LF, Carvalho G, Borgo L, Creste S, Landell MG, Mazzafera P, Azevedo RA (2014) “Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes. Plant Physiol Biochem 74:165–175

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Chen CT, Chen L, Lin CC, Kao CH (2001) Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci 160:283–290

    Article  CAS  Google Scholar 

  • Chrominski A, Halls S, Weber DJ, Smith BN (1989) Proline affects ACC to ethylene conversion under salt and water stresses in the halophyte Allenrolfea occidentalis. Environ Exp Bot 29:359–363

    Article  CAS  Google Scholar 

  • Dadkhah AR, Grrifiths H (2006) The effect of salinity on growth, inorganic ions and dry matter partitioning in sugar beet cultivars. J Agric Sci Tech 8:199–210

    Google Scholar 

  • Dawood MG (2016) Influence of osmoregulators on plant tolerance to water stress. Sci Agric 13(1):42–58

    CAS  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    Article  CAS  Google Scholar 

  • FAOSTAT (2018) http://faostat.fao.org/site

  • Farissi M, Bouizgaren A, Faghire M, Bargaz A, Ghoulam C (2013) Agrophysiological and biochemical properties associated with adaptation of Medicago sativa populations to water deficit. Turk J Bot 37:1166–1175

    Article  CAS  Google Scholar 

  • Foroozesh P, Majidi Heravan E, Bihamta MR, Fatollah Taleghani D, Habibi D (2012) Physiological evaluation of sugar beet genotypes under water stress. Am Eurasian J Agric Environ Sci 12:820–826

    CAS  Google Scholar 

  • Handa S, Handa AK, Hasegawa PM, Bressan RA (1986) Proline accumulation and the adaptation of cultured plant cells to water stress. Plant Physiol 80:938–945

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (2003) A regulatory role for proline metabolism in stimulating Arabidopsis thaliana seed germination. Plant Growth Regul 39:41–50

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Alam MM, Rahman A, Hasanuzzaman 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 757219:1–17

    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  Google Scholar 

  • Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Anal Biochem 55:554–562

    Article  CAS  Google Scholar 

  • Hong Z, Lakkineni K, Zhang Z, Verma DP (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  Google Scholar 

  • Hoque MA, Banu MN, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata 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 164:1457–1468

    Article  CAS  Google Scholar 

  • Hossain MA, Fujita M (2010) Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiol Mol Biol Plants 16(1):19–29

    Article  CAS  Google Scholar 

  • Imlay JA (2002) Cellular defense against superoxide and hydrogen peroxide. Annl Rev Biochem 77:755–776

    Article  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induce changes in concentration of proline and total soluble sugar in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Irshad M, Honna T, Eneji AE, Yamamoto S (2002) Wheat response to nitrogen source under saline conditions. J Plant Nutr 2512:2603–2612

    Article  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Banu MN, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597

    Article  CAS  Google Scholar 

  • Jinyou D, Xiaoyang C, Wei L, Qiong G (2004) Osmoregulation mechanism of drought stress and genetic engineering strategies for improving drought resistance in plants. For Stud China 6(2):56–62

    Article  Google Scholar 

  • Kadkhodaie A, Zahedi M, Razmjoo J, Pessarakli M (2014) Changes in some anti-oxidative enzymes and physiological indices among sesame genotypes (Sesamum indicum L.) in response to soil water deficits under field conditions. Acta Physiol Plant 36:641–650

    Article  CAS  Google Scholar 

  • Kibria MG, Farzana K, Abdul Matin M, Anamul Hoque MA (2016) Mitigating water stress in wheat (BARI Gom-26) by exogenous application of proline. Fundam Appl Agric 1(3):118–123

    Google Scholar 

  • Kishor PBK, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Review Curr Sci 88(3):424–438

    CAS  Google Scholar 

  • Kumar NS, Zhu W, Liang X, Zhang L, Demers AJ, Zimmerman MC, Simpson MA, Becker DF (2012) Proline dehydrogenase is essential for proline protection against hydrogen peroxide-induced cell death. Free Radic Biol Med 53:1181–1191

    Article  Google Scholar 

  • Liang X, Zhang L, Natarajan SK, Becker D (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011

    Article  CAS  Google Scholar 

  • Liu C, Liu Y, Guo K, Fan D, Li G, Zheng Y, Yu L, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183

    Article  CAS  Google Scholar 

  • Madhava KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aus J Crop Sci 4(8):580–585

    CAS  Google Scholar 

  • Mansour MMF (2000) Nitrogen containing compound and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Mansuri M, Babazadeh H, Emdad MR, Taleghani D (2017) effect of deficit irrigation management on qualitative and quantitative yield of sugar beet (Beta vulgaris L.) in Karaj, Iran. Appl Ecol Env Res 16(1):455–466

    Article  Google Scholar 

  • Marcińska I, Czyczyło-Mysza I, Skrzypek E, Grzesiak MT, Janowiak F, Filek M, Dziurka M, Dziurka K, Waligórski P (2013) Alleviation of osmotic drought effects by exogenous application of salicylic or abscisic acid on wheat seedlings. Int J Mol Sci 14:13171–13193

    Article  Google Scholar 

  • Matysik J, Alia BB, Monthy P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Ober ES, Rajabi A (2010) Abiotic stress in sugar beet. Sugar Tech 12:294–298

    Article  CAS  Google Scholar 

  • Ozturk L, Demir Y (2002) In vivo and in vitro protective role of proline. Plant Growth Regul 38:259–264

    Article  CAS  Google Scholar 

  • Phang JM, Liu W, Zabirnyk O (2010) Proline metabolism and microenvironmental stress. Annu Rev Nutr 30:441–463

    Article  CAS  Google Scholar 

  • Raymond MJ, Smirnoff N (2002) Proline metabolism and transport in maize seedlings at low water potential. Annals Bot 89:813–823

    Article  CAS  Google Scholar 

  • Refay YA (2010) Root yield and quality traits of three sugar beet (Beta vulgaris L.) varieties in relation to sowing date and stand densities. World J Agri Sci 6(5):589–594

    Google Scholar 

  • Reza S, Heidari R, Zare S, Norastehnia A (2006) Antioxidant response of two salt-stressed barley varieties in the presence or absence of exogenous proline. Gen App Plant Physiol 32:233–251

    Google Scholar 

  • Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56

    Article  CAS  Google Scholar 

  • SAS Institute (2002) The SAS system for windows. In: Released 9.1. SAS Inst., Cary, NC

    Google Scholar 

  • Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354

    Article  Google Scholar 

  • Srivastava AK, Suprasanna P, Srivastava S, D’Souza SF (2010) Thiourea mediated regulation in the expression profile of aquaporins and its impact on water homeostasis under salinity stress in Brassica juncea roots. Plant Sci 178:517–522

    Article  CAS  Google Scholar 

  • Valentovic P, Luxova M, Kolarovic L, Gasparikova O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ 52(4):186–191

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yang SL, Lan SS, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166:1694–1699

    Article  CAS  Google Scholar 

  • Yang Y, Zhang Y, Wei X, You J, Wang W, Lu J, Shi R (2011) Comparative antioxidative responses and proline metabolism in two wheat cultivars under short term lead stress. Ecotoxicol Environ Saf 74:733–740

    Article  CAS  Google Scholar 

  • Yeilaghi H, Arzani A, Ghaderian M, Fotovat R, Feizi M, Pourdad SS (2012) Effect of salinity on seed oil content and fatty acid composition of safflower (Carthamus tinctorius L.) genotypes. Food Chem 130:618–625

    Article  CAS  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    Article  CAS  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agronomy, Faculty of Agriculture, Shahrekord University, Shahrekord, Iran

    Hamideh Ghaffari & Mahmoud Reza Tadayon

  2. School of Science and the Environment, Grenfell Campus, Memorial University of Newfoundland, Corner Brook, A2H 5G4, Canada

    Muhammad Nadeem & Mumtaz Cheema

  3. Department of Agronomy and Plant Breeding, Faculty of Agriculture, Isfahan University of Technology, Isfahan, Iran

    Jamshid Razmjoo

  4. Department of Environmental Sciences, COMSATS University of Islamabad, Vehari Campus, Islamabad, Pakistan

    Muhammad Nadeem

Authors
  1. Hamideh Ghaffari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahmoud Reza Tadayon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Nadeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mumtaz Cheema
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jamshid Razmjoo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahmoud Reza Tadayon.

Additional information

Communicated by R. Aroca.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghaffari, H., Tadayon, M.R., Nadeem, M. et al. Proline-mediated changes in antioxidant enzymatic activities and the physiology of sugar beet under drought stress. Acta Physiol Plant 41, 23 (2019). https://doi.org/10.1007/s11738-019-2815-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-019-2815-z

Keywords

Search

Navigation