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Non-enzymatic antioxidative defence in drought-stressed mulberry (Morus indica L.) genotypes

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Abstract

The present study investigated drought-induced responses of non-enzymatic antioxidants in four diverse mulberry genotypes (Morus indica L. S-36, M-5, MR-2 and V-1). Inside the glasshouse, potted plants were subjected to four water regimes for 75 days: (a) control: pots maintained at 100% pot water holding capacity (PC) (b) low water stress: 75% PC (c) medium water stress: 50% PC and (d) high water stress: 25% PC. Photosynthetic leaf gas exchange and non-enzymatic antioxidants including α-tocopherol, ascorbic acid (AA), glutathione, proline and total carotenoids were measured in leaves at regular intervals. Amongst all, V-1 was relatively drought tolerant and showed exceeded accumulation of α-tocopherol and AA-glutathione pool in association with higher carotenoids and proline contents. Susceptible S-36, M-5 and MR-2 could not induce any significant up-regulation in AA-glutathione pool leading to endogenous loss of α-tocopherol and more lipid peroxidation. Reactive oxygen species (ROS) like hydrogen peroxide (H2O2) and superoxide (O2 · −) showed apparent accumulation in water-stressed leaves and significantly contributed to lipid peroxidation in susceptible genotypes when compared to V-1. Our study demonstrated that proline, AA and glutathione were the major non-enzymatic antioxidants in mulberry with α-tocopherol and carotenoids as good additional indicators for drought stress tolerance. These non-enzymatic antioxidants can cumulatively render effective protection against oxidative damage and can be considered as reliable markers for screening drought-tolerant mulberry genotypes.

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References

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

    Article  CAS  Google Scholar 

  • Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM (2006) Immediate responses and adaptive strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 170:596–605

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Becana M, Aparicio-Tejo P, Irigoyen JJ, Sanchez-Diaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol 82:1169–1171

    Article  PubMed  CAS  Google Scholar 

  • Biasiolo M, Canal DAMT, Tornadore N (2004) Micromorphological characterization of ten mulberry cultivars (Morus spp.). Econ Bot 58:639–646

    Article  Google Scholar 

  • Bukhov NG, Carpentier R (2004) Effects of water stress on the photosynthetic efficiency of plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Netherlands, pp 623–635

    Google Scholar 

  • Chaitanya KV, Jutur PP, Sundar D, Reddy AR (2003) Water stress effects on photosynthesis in different mulberry cultivars. Plant Growth Regul 40:75–80

    Article  CAS  Google Scholar 

  • Chaitanya KV, Rasineni GK, Reddy AR (2009) Biochemical responses to drought stress in mulberry (Morus alba L.): evaluation of proline, glycine betaine and abscisic acid accumulation in five cultivars. Acta Physiol Planta 31:437–443

    Article  CAS  Google Scholar 

  • Chaves MM, Zarrouk O, Francisco R, Costa JM, Santos T, Regalado AP, Rodrigues ML, Lopes CM (2010) Grapevine under deficit irrigation: hints from physiological and molecular data. Ann Bot 105:661–676

    Article  PubMed  CAS  Google Scholar 

  • Cocozza C, Cherubini P, Regier N, Saurer M, Frey B, Tognetti R (2010) Early effects of water deficit on two parental clones of Populus nigra grown under different environmental conditions. Func Plant Biol 37:244–254

    Article  Google Scholar 

  • Collins A (2001) Carotenoids and genomic stability. Mutat Res 475:1–28

    Article  Google Scholar 

  • Connor DJ (2005) Adaptation of olive (Olea europaea L.) to water-limited environments. Aus J Agric Res 56:1181–1189

    Article  Google Scholar 

  • Dandin SB, Jayaswal J, Giridhar K (2003) Mulberry cultivation. In: Dandin SB, Jayaswal J, Giridhar K (eds) Handbook of Sericulture Technologies. Central Silk Board, Bangalore, pp 1–5

    Google Scholar 

  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    Article  CAS  Google Scholar 

  • Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 106:119–133

    Article  CAS  Google Scholar 

  • Efeoğlu B, Ekmekçi Y, Çiçek N (2009) Physiological responses of three maize cultivars to drought stress and recovery. S Afr J Bot 75:34–42

    Article  Google Scholar 

  • Elsheery N, Cao KF (2008) Gas exchange, chlorophyll fluorescence, and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol Planta 30:769–777

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Griffith OW, Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (s-n-butylhomocysteine sulfoximine). J Biol Chem 254:7558–7560

    PubMed  CAS  Google Scholar 

  • Guha A, Rasineni GK, Reddy AR (2010) Drought tolerance in mulberry: a physiological approach with insights to growth dynamics and leaf yield production. Exp Agric 46:471–488

    Article  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 

  • Hernandez JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2 · −/H2O2 production in the apoplast of pea leaves, its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed  CAS  Google Scholar 

  • Hong-Bo S, Li-Ye C, Ming-An S, Jaleel CA, Hong-Mei M (2008) Higher plant antioxidants and redox signalling under environmental stresses. C R Biol 331:433–441

    Article  Google Scholar 

  • Kamal-Eldin A, Appelqvist LA (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701

    Article  PubMed  CAS  Google Scholar 

  • Keyes WJ, Lynn GD, Erbil WK, Taylor JV, Apkarianb RP (2002) H2O2 in interspecies signaling: a new role in host detection. Microsco Microanal 8:962–963

    Google Scholar 

  • Kotresha D, Rao AP, Srinivas N, Vidyasagar GM (2007) Antioxidative response to drought and high temperature stress in selected mulberry genotypes. Physiol Mol Biol Plants 13:57–63

    CAS  Google Scholar 

  • Lawlor DW (1995) The effects of water deficit on photosynthesis. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific Publishers Ltd, Oxford, pp 129–160

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Methods in enzymology.vol 148, pp 350–382

  • LiXin Z, ShengXiu L, ZongSuo L (2009) Differential plant growth and osmotic effects of two maize (Zea mays L.) cultivars to exogenous glycinebetaine application under drought stress. Plant Growth Regul 58:297–305

    Article  Google Scholar 

  • Maherali H, DeLucia EH (2001) Influence of climate-driven shifts in biomass allocation on water transport and storage in ponderosa pine. Oecologia 129:481–491

    Google Scholar 

  • Marron N, Maury S, Rinaldi C, Brignolas F (2006) Impact of drought and leaf development stage on enzymatic antioxidant system of two Populus deltoides × nigra clones. Ann Forest Sci 63:323–327

    Article  CAS  Google Scholar 

  • Meyer AJ (2008) The integration of glutathione homeostasis and redox signalling. J Plant Physiol 165:1390–1403

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosyn Res 86:459–474

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    Article  PubMed  Google Scholar 

  • Munné-Bosch S, Peñuelas J (2004) Drought-induced oxidative stress in strawberry (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Sci 166:1105–1110

    Article  Google Scholar 

  • Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjorkman O (2001) Photoprotection in a zeaxanthin-and lutein-deficient double mutant of Arabidopsis. Photosyn Res 67:139–145

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  PubMed  CAS  Google Scholar 

  • Omaye ST, Turnbull JD, Sauberilich HE (1979) Selected methods for the determination of ascorbic acid in animal cells, tissues and fluids. In: Methods in enzymology. New York, Academic Press, pp 3–11

  • Pinheiro HA, Damatta FM, Chaves ARM, Fontes EPB, Loureiro ME (2004) Drought tolerance in relation to protection against oxidative stress in clones of Coffea canephora subjected to long-term drought. Plant Sci 167:1307–1314

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Jutur PP, Sumitra K (2004a) Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environ Exp Bot 52:33–42

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004b) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Jutur PP, Gnanam A (2005) Photosynthesis and oxidative stress responses to water deficit in five different mulberry (Morus alba L.) cultivars. Physiol Mol Biol Plants 11:291–298

    CAS  Google Scholar 

  • Savoure A, Jaoua S, Hua X-J, Ardiles W, Van Montagu M, Verbruggen N (1995) Isolation, characterization, and chromosomal location of a gene encoding the D1-pyrroline-5 carboxylate synthetase in Arabidopsis thaliana. FEBS Lett 372:13–19

    Article  PubMed  CAS  Google Scholar 

  • Schwanz P, Polle A (1998) Antioxidative systems, pigment and protein contents in leaves of adult Mediterranean oak species (Quercus pubescens and Q. ilex) with lifetime exposure to elevated CO2. New Phytol 140:411–423

    Article  CAS  Google Scholar 

  • Shao H-B, Chu L-Y, Lu Z-H, Kang C-M (2008) Primary antioxidant free radical scavenging and redox signalling pathways in higher plant cells. Int J Biol Sci 4:8–14

    Article  CAS  Google Scholar 

  • Shvaleva AL, Costa E, Silva F, Breia E, Jouve J, Hausman JF, Almeida MH, Maroco JP, Rodrigues ML, Pereira JS, Chaves MM (2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol 26:239–248

    Article  PubMed  CAS  Google Scholar 

  • Šircelj H, Tausz M, Grill D, Batic F (2007) Detecting different levels of drought stress in apple trees (Malus domestica Borkh.) with selected biochemical and physiological parameters. Sci Hort 113:362–369

    Article  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    Article  CAS  Google Scholar 

  • Susheelamma BN, Jolly MS, Giridhar K, Sengupta K (1990) Evaluation of germplasm genotypes for the drought resistance in mulberry. Sericologia 30:327–340

    Google Scholar 

  • Tausz M, Hietz P, Briones O (2001) The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of Mexican cloud forest. Aus J Plant Physiol 28:775–783

    CAS  Google Scholar 

  • Tausz M, Wonisch A, Grill D, Morales D, Jiménez MS (2003) Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation. J Exp Bot 54:1505–1510

    Article  PubMed  CAS  Google Scholar 

  • Terman A, Brunk UT (2006) Oxidative stress, accumulation of biological ‘garbage’, and aging. Antioxid Redox Signal 8:197–204

    Article  PubMed  CAS  Google Scholar 

  • Trebst A, Depka B, Holländer-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 516:156–160

    Article  PubMed  CAS  Google Scholar 

  • Turner NC (1979) Drought resistance and adaptation to water deficits in crop plants. In: Mussel H, Staples RC (eds) Stress Physiology in Crop Plants. Wiley, New York, pp 343–372

    Google Scholar 

  • Wu G, Wei ZK, Shao HB (2007) The mutual responses of higher plants to environment: physiological and microbiological aspects. Biointerfaces 59:113–119

    Article  CAS  Google Scholar 

  • Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    Article  PubMed  CAS  Google Scholar 

  • Yanbao L, Chunying Y, Chunyang L (2006) Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol Planta 127:182–191

    Article  Google Scholar 

  • Yen GC, Wu SC, Duh PD (1996) Extraction and identification of antioxidant components from the leaves of mulberry (Morus alba L.). J Agric Food Chem 44:1687–1690

    Article  CAS  Google Scholar 

  • Yildiz-Aktas L, Dagnon S, Gurel A, Gesheva E, Edreva A (2009) Drought tolerance in cotton: involvement of non-enzymatic ROS-scavenging compounds. J Agron Crop Sci 195:247–253

    Article  CAS  Google Scholar 

  • Yin C, Peng Y, Zang R, Zhu Y, Li C (2005) Adaptive responses of Populus kangdingensis to drought stress. Physiol Planta 123:445–451

    Article  CAS  Google Scholar 

  • Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge the financial assistance of Department of Science and Technology (DST), Government of India, New Delhi (Grant SR/SO/PS-27/05). We are grateful to Dr. S Masilamani, Scientist C (Regional Sericultural Research Station, Salem, India) for providing the mulberry cuttings. We acknowledge the Central Instruments Laboratory (CIL) of University of Hyderabad, Hyderabad, India for the help on Confocal Fluorescence Microscopy. A.G. gratefully acknowledges the research fellowship granted by DST, India and University of Hyderabad, India. D.G. and G.K.R acknowledge the senior research fellowships granted by CSIR (Council of Scientific and Industrial Research, Government of India). We also thank our field assistant Mr K. Vinod for raising and maintenance of mulberry saplings for this experiment.

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  1. Photosynthesis and Plant Stress Biology Laboratory, Department of Plant Sciences, University of Hyderabad, Hyderabad, 500046, India

    Anirban Guha, Debashree Sengupta, Girish Kumar Rasineni & Attipalli Ramachandra Reddy

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  1. Anirban Guha
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  2. Debashree Sengupta
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  3. Girish Kumar Rasineni
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  4. Attipalli Ramachandra Reddy
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Correspondence to Attipalli Ramachandra Reddy.

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Communicated by M. Adams.

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Guha, A., Sengupta, D., Rasineni, G.K. et al. Non-enzymatic antioxidative defence in drought-stressed mulberry (Morus indica L.) genotypes. Trees 26, 903–918 (2012). https://doi.org/10.1007/s00468-011-0665-4

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  • DOI: https://doi.org/10.1007/s00468-011-0665-4

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