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Effect of putrescine and proline on proflies of GABA, antioxidant activities in leaves of three Citrus species in response to low temperature stress

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Abstract

This study was carried out to assess antioxidant activities and defense role of putrescine and proline in leaves of three Citrus species under low temperature stress. Branches of three Citrus species (C. reticulata L., C. sinensis L. and C. paradisi L.), sprayed with putrescine 0, 5, 10 mM and proline 0, 15, 20 mM. 24 h after application, containers containing treated shoots exposed to temperatures 1, − 1 and − 3 °C for six hours. The amount of hydrogen peroxide, flavonoids, phenolic compounds and antioxidant capacity increased with temperature reduction to − 3 °C. HPLC analysis showed that low temperature (− 3 °C) induces the levels of Gamma Aminobutyric Acid (GABA) in leaves of all species. The comparison of the HPLC patterns of the three species showed that GABA levels in treated leaves increased than control. The application of different concentrations of putrescine and proline decreased production of hydrogen peroxide but improved antioxidative activities of leaves under low temperatures. Putrescine 10 mM and proline 20 mM showed the highest effects than the other levels. The highest value of hydrogen peroxide was observed in leaves of control (putrescine and proline 0 mM) under − 3 °C but its lowest level was seen in leaves treated with proline 20 mM and putrescine 10 mM in all three species of Citrus. The highest level of phenolic compounds, flavonoids and antioxidant capacity were observed in leaves treated with putrescine 10 mM and proline 20 mM at − 3 °C. Putrescine 10 mM and proline 20 mM showed the highest impact on reduction of the damages caused by low temperature stress.

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Abbreviations

GABA:

Gamma Aminobutyric Acid

ROS:

Reactive oxygen species

TCA:

Trichloroacetic acid

HPLC:

High Performance Liquid Chromatography

Put:

Putrescine

P:

Proline

References

  • Ali RM, Abbas HM, Kamal RK (2009) The effects of treatment with polyamines on dry matter and some metabolites in salinity–stressed chamomile and sweet majoram seedlings. Plant Soil Environ 55:477–483

    Article  CAS  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  CAS  PubMed  Google Scholar 

  • Bhusal RC, Mizutani F, Rutto KL (2002) Selection of rootstocks for flooding and drought tolerance in Citrus species. Pak J Biol Sci 5:509–512

    Article  Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Article  PubMed  PubMed Central  Google Scholar 

  • Bor M, Seckin B, Ozgur R, Yılmaz O, Ozdemir F, Turkan I (2009) Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutryric acid levels of sesame (Sesamum indicumL.). Acta Physiol Plant 31:655–659

    Article  CAS  Google Scholar 

  • Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  CAS  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant sci 140:103–125

    Article  CAS  Google Scholar 

  • Bressan R, Bohnert H, Zhu JK (2009) Abiotic stress tolerance: from gene discovery in model organisms to crop improvement. Mole Plant 2:1–2

    Article  CAS  Google Scholar 

  • Carina LA, Ingrid WL, Isabelle CD, Tonia VSL, Adeliana SO, Maria RAM, Edda LL, Mauricio PS (2004) Biological activity of proteins from pulps of tropical fruits. Food Chem 85:107–110

    Article  CAS  Google Scholar 

  • Chaum S, Siringam K, Juntawong J, Kirdmanee C (2010) Water relations, pigment stabilization, photosynthetic abilities and growth improvement in salt stressed rice plants treated with exogenous potassium nitrate application. Int J of Plant Prod 4:187–198

    CAS  Google Scholar 

  • De Palma M, Grillo S, Massarelli I, Costa A, Balogh G, Vigh L, Leone A (2008) Regulation of desaturase gene expression, changes in membrane lipid composition and freezing tolerance in potato plants. Mole Breeding 21:15–26

    Article  CAS  Google Scholar 

  • Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressedCucumis sativusroots and enhances short-term salinity tolerance. J of Plant Physio 165:1620–1635

    Article  CAS  Google Scholar 

  • Gill S, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo WW, Deng XX, Yi HL (2000) Somatic hybrids between navel orange and grapefruit for seedless triploid breeding. Euphytica 116:281–285

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Borhannuddin Bhuyan MHM, Zulfiqar F, Raza A, Mohsin SM, Al Mahmud J, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681

    Article  CAS  PubMed Central  Google Scholar 

  • Huang D, Lin C, Chen H, Lin YH (2004) Antioxidant and antiproliferative activities of sweet potato (Ipomoea batata L.) Lam (Tainong 57) constituents. Bot Bull Acad Sinica 45:179–186

    CAS  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and Plant Responses To Stress. Crit Rev Plant Sci 19(6):479–509

    Article  CAS  Google Scholar 

  • Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic alcium. Nature 352:524–526

    Article  CAS  PubMed  Google Scholar 

  • Kumar RR, Sharma SK, Rai GK, Singh K, Choudhury M, Dhawan G (2014) Exogenous application of putrescine at pre-anthesis enhances the thermotolerance of wheat (Triticum aestivum L.). Indian J Biochem Biophys 51:396–406

    CAS  PubMed  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of Citrus. Plant physio 84:692–695

    Article  CAS  Google Scholar 

  • Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126

    Article  CAS  Google Scholar 

  • Liu WY, Zhang YF, Zhang DX (2012) Study on cold resistant genes in plants. J Shanxi Datong Univ 28:52–55

    CAS  Google Scholar 

  • Mancuso S (2000) Electrical resistance changes during exposure to low temperature measure chilling and freezing tolerance in olive tree (Olea europaea L.) plants. Plant Cell Environ 23:291–299

    Article  Google Scholar 

  • Mayer RR, Cherry JL, Rhodes D (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Phytochem 94:796–810

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mohammadrezakhani S, Hajilou J, Rezanejad F (2017) Evaluation of phenolic and flavonoid compounds in pollen grains of three Citrusspecies in response to low temperature. Grana 57:1–10

    Google Scholar 

  • Mohammadrezakhani S, Hajilou J, Rezanejad F, Zaare-Nahandi F (2019) Assessment of exogenous application of proline on antioxidant compounds in threeCitrusspecies under low temperature stress. J Plant Interact 14:347–358

    Article  CAS  Google Scholar 

  • Oh MM, Carey EE, Rajashekar CB (2009) Environmental stresses induce health-promoting phytochemicals in lettuce. Plant Physio Biochem 47:578–583

    Article  CAS  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A Rev Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

  • Pourmorad F, Hosseinimehr SJ, Shahabimajd N (2006) Antioxidant activity, phenol and flavonoid contents of some selected Iranian medicinal plants. Afr J Biotechnol 5:1142–1145

    CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E. Anal Biochem 269:337–341

    Article  CAS  PubMed  Google Scholar 

  • Rapisarda P, Bianco ML, Pannuzzo P, Timpanaro N (2008) Effect of cold storage on vitamin C, phenolics and antioxidant activity of five orange genotypes Citrus sinensis (L.) Osbeck. Postharvest Biol Technol 49:348–354

    Article  CAS  Google Scholar 

  • Razali N, Razab R, Junit SM, Aziz AA (2008) Radical scavenging and reducing properties of extracts of cashew shoots (Anacardium occidentale). Food Chem 111:38–44

    Article  CAS  Google Scholar 

  • Ruth G (2002) Oxidative stress and acclimation mechanisms in plants. The Arabidopisis Book, pp 1–20

  • Seppanen MM (2000) Characterize of freezing tolerance in Solanum commersonii (dun.) with special reference of the relationship between and oxidative stress. University of Helsinki department of production section of crop husbandry 56: 4–44

  • Shao HB, Chu LY, Wu G, Zhang JH, Lu ZH, Hu YC (2007) Changes of some anti-oxidative physiological indices under soil water deficits among 10 wheat (Triticum aestivum L.) genotypes at tillering stage. Colloids Surf B Biointerfaces 47:143149

    Google Scholar 

  • Shi QH, Ding F, Wang XF, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550

    Article  CAS  PubMed  Google Scholar 

  • Soost RK, Cameron JW (1975) Citrus. In: Janick J, Moore JN (eds) Advances in fruit breeding. IN, Purdue University Press, West Lafayette, pp 507–540

    Google Scholar 

  • Sun ZH, Ma XT (1999) Thermo stability of plasma membrane in citrus leaves. J Huazhong Agric Univ 18:375–377

    Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2011) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 14:691–699

    CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid raintreated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Vogt T (2010) Phenylpropanoid Biosynthesis. Mole Plant 3:2–10

    Article  CAS  Google Scholar 

  • Wallace W, Secor J, Schrader LE (1984) Rapid accumulation of γ-aminobutyric acidandalanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or mechanical manipulation. Plant Physio 75:170–175

    Article  CAS  Google Scholar 

  • Wang CY (1994) Chilling injury in horticultural commodities. Hortic Sci 29:986–988

    Google Scholar 

  • Yelenosky G (1985) Cold hardiness in Citrus. Hortic Rev 7:201–238

    Google Scholar 

  • Zhao HZ, Yang HQ (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic 116:442–447

    Article  CAS  Google Scholar 

  • ZhuJ DongCH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Horticultural Science, Faculty Agriculture, University of Tabriz, East Azerbaijan, Iran

    Soheila Mohammadrezakhani & Jafar Hajilou

  2. Plant Developmental Biology, Department of Biology, Shahid Bahonar University of Kerman, Kerman, Iran

    Farkhondeh Rezanejad

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  1. Soheila Mohammadrezakhani
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  2. Farkhondeh Rezanejad
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  3. Jafar Hajilou
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Correspondence to Soheila Mohammadrezakhani.

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Mohammadrezakhani, S., Rezanejad, F. & Hajilou, J. Effect of putrescine and proline on proflies of GABA, antioxidant activities in leaves of three Citrus species in response to low temperature stress. J. Plant Biochem. Biotechnol. 30, 545–553 (2021). https://doi.org/10.1007/s13562-020-00645-x

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  • DOI: https://doi.org/10.1007/s13562-020-00645-x

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