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Oxidative stress and antioxidant responses of mulberry (Morus alba) plants subjected to deficiency and excess of manganese

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Abstract

The aim of the study was to relate the effects of deficiency and excess of Mn with the generation of reactive oxygen species (ROS) and altered cellular redox environment in mulberry (Morus alba L.) cv. Kanva-2 plants. Mn deficiency symptom appeared as mild interveinal chlorosis in middle leaves. Mn-excess did not produce any specific symptom. Leaf water potential (Ψ) was increased in Mn-deficient and Mn-excess mulberry plants. Mn-deficient leaves contained less Mn, less chloroplastic pigments and high tissue Fe, Zn and Cu concentrations. Starch content was increased with increasing Mn supply. While reducing sugar content increased in Mn-deficient and Mn-excess plants as well, non-reducing sugars remained unaffected in Mn-deficient plants and decreased in Mn-excess plants. Moreover, study of antioxidative responses, oxidative stress (H2O2 and lipid peroxidation) and cellular redox environment [dehydroascorbate (DHA)/ascorbic acid (AsA) ratio] in Mn-stressed mulberry plants was also undertaken. Both hydrogen peroxide and lipid peroxidation were enhanced in the leaves of Mn-deficient plants. Increased H2O2 concentration in Mn-excess leaves did not induce oxidative damage as indicated by no change in lipid peroxidation. The ratio of the redox couple (DHA/AsA) was increased both in Mn-deficient or Mn-excess plants. The activities of superoxide dismutase (EC 1.15.1.1) and catalase (EC 1.11.1.6) increased in Mn-deficient plants. The activity of ascorbate peroxidase (EC 1.11.1.11) increased with increasing Mn supply. The results suggest that deficiency or excess of Mn induces oxidative stress through enhanced ROS generation and disturbed redox couple in mulberry plants.

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Abbreviations

AsA:

Ascorbic acid

APX:

Ascorbate peroxidase

CAT:

Catalase

DHA:

Dehydroascorbate

DS:

Degree of succulence

DTT:

Dithiothreitol

POD:

Peroxidase

ROS:

Reactive oxygen species

RWC:

Relative water content

SOD:

Superoxide dismutase

SWC:

Specific water content

TCA:

Trichloroacetic acid

References

  • Allen MD, Kropat J, Tottey S, Del Campo JA, Merchant SS (2007) Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol 143:263–277. doi:10.1104/pp.106.088609

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. doi:10.1016/0003-2697(71)90370-8

    Article  PubMed  CAS  Google Scholar 

  • Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416. doi:10.1104/pp.59.3.411

    Article  PubMed  CAS  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of Nutrients: micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, USA, p 191-248. doi:10.1016/b978-0-12-384905-2.00007-8

  • Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917. doi:10.1105/tpc.109.073023

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I (1994) Activity of ascorbate-dependent H2O2-scavenging enzymes and leaf chlorosis are enhanced in magnesium- and potassium-deficient leaves, but not in phosphorus-deficient leaves. J Exp Bot 45:1259–1266. doi:10.1093/jxb/45.9.1259

    Article  CAS  Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704. doi:10.1111/j.1399-3054.2007.01042.x

    Article  PubMed  CAS  Google Scholar 

  • Fox TC, Guerinot ML (1998) Molecular biology of cation transport in plants. Ann Rev Plant Physiol Plant Mol Biol 49:669–696. doi:10.1146/annurev.arplant.49.1.669

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364. doi:10.1034/j.1399-3054.2003.00223.x

    Article  CAS  Google Scholar 

  • Fuhrs H, Gotze S, Specht A, Erban A, Gallien S, Heintz D, Van Dorsselaer A, Kopka J, Braun HP, Horst WJ (2009) Characterization of leaf apoplastic peroxidases and metabolites in Vigna unguiculata in response to toxic manganese supply and silicon. J Exp Bot 60:1663–1678. doi:10.1093/jxb/erp034

    Article  PubMed  Google Scholar 

  • Fuhrs H, Specht A, Erban A, Kopka J, Horst WJ (2011) Functional associations between the metabolome and manganese tolerance in Vigna unguiculata. J Exp Bot 63:329–340. doi:10.1093/jxb/err276

    Article  PubMed  Google Scholar 

  • González A, Steffen KL, Lynch JP (1998) Light and excess manganese: implications for oxidative stress in common bean. Plant Physiol 118:493–504. doi:10.1104/pp.118.2.493

    Article  PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1

    Article  PubMed  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition farnham royal, England: Commonwealth Agricultural Bureaux, Technical Communication No. 22 of the Commonwealth Bureau of Horticulture and Plantation Crops, East Malling, Maidstone, Kent

  • Hiltbrunner E, Flückiger W (1996) Manganese deficiency of silver fir trees (Abies alba) at a reforested site in the Jura mountains, Switzerland: aspects of cause and effect. Tree Physiol 16:963–975. doi:10.1093/treephys/16.11-12.963

    Article  PubMed  CAS  Google Scholar 

  • Husted S, Laursen KH, Hebbern CA, Schmidt SB, Pedas P, Haldrup A, Jensen PE (2009) Manganese deficiency leads to genotype-specific changes in fluorescence induction kinetics and state transitions. Plant Physiol 150:825–833. doi:10.1104/pp.108.134601

    Article  PubMed  CAS  Google Scholar 

  • Kang BT, Fox RL (1980) A methodology for evaluating the manganese tolerance of cowpea (Vigna unguiculata) and some preliminary results of field trials. Field Crops Res 3:199–210. doi:10.1016/0378-4290(80)90028-3

    Article  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152. doi:10.1146/annurev-arplant-042811-105522

    Article  PubMed  CAS  Google Scholar 

  • Kumar P, Tewari RK, Sharma PN (2007) Excess nickel–induced changes in antioxidative processes in maize leaves. J Plant Nutr Soil Sci 170:796–802. doi:10.1002/jpln.200625126

    Article  CAS  Google Scholar 

  • Kumar P, Tewari RK, Sharma PN (2010) Sodium nitroprusside-mediated alleviation of iron deficiency and modulation of antioxidant responses in maize plants. AoB Plants 2010: plq002-plq002. doi:10.1093/aobpla/plq002

  • Lanquar V, Ramos MS, Lelievre F, Barbier-Brygoo H, Krieger-Liszkay A, Kramer U, Thomine S (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol 152:1986–1999. doi:10.1104/pp.109.150946

    Article  PubMed  CAS  Google Scholar 

  • Law M, Charles S, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903

    PubMed  CAS  Google Scholar 

  • Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH, Li Y, Yang GH (2010) Effects of manganese-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol 10:42. doi:10.1186/1471-2229-10-42

    Article  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Lester Packer RD (ed) Methods in enzymology, vol 148. Academic Press, USA, pp 350–382. doi:10.1016/0076-6879(87)48036-1

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Mengel K, Kirkby EA (2001) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220. doi:10.1093/jxb/erq282

    Article  PubMed  CAS  Google Scholar 

  • Millaleo R, Reyes-Díaz M, Alberdi M, Ivanov AG, Krol M, Hüner NPA (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64:343–354. doi:10.1093/jxb/ers339

    Article  PubMed  CAS  Google Scholar 

  • Montgomery R (1957) Determination glycogen. Arch Biochem Biophys 67:378–386

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay MJ, Sharma A (1991) Manganese in cell metabolism of higher plants. Bot Rev 57:117–149

    Article  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 

  • Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  • Pearson JN, Rengel Z (1997) Genotypic differences in the production and partitioning of carbohydrates between roots and shoots of wheat grown under zinc or manganese deficiency. Ann Bot 80:803–808. doi:10.1006/anbo.1997.0523

    Article  CAS  Google Scholar 

  • Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466. doi:10.1104/pp.108.118851

    Article  PubMed  CAS  Google Scholar 

  • Piper CS (1942) Soil and plant analysis. Hassel Press, Adelaide

    Google Scholar 

  • Polle A, Chakrabarti K (1994) Effects of manganese deficiency on soluble apoplastic peroxidase activities and lignin content in needles of Norway spruce (Picea abies). Tree Physiol 14:1191–1200

    Article  PubMed  CAS  Google Scholar 

  • Polle A, Chakrabarti K, Chakrabarti S, Seifert F, Schramel P, Rennenberg H (1992) Antioxidants and manganese deficiency in needles of Norway spruce (Picea abies L.) trees. Plant Physiol 99:1084–1089

    Article  PubMed  CAS  Google Scholar 

  • Rosas A, Rengel Z, de la Luz Mora M (2007) Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover. J Plant Nutr 30:253–270. doi:10.1080/01904160601118034

    Article  CAS  Google Scholar 

  • Shamachary, Jolly MS (1988) A simple device for quick determination of mulberry leaf area in field. Indian J Seric 27:51–54

    Google Scholar 

  • Sharma PN, Kumar P, Tewari RK (2004) Early signs of oxidative stress in wheat plants subjected to zinc deficiency. J Plant Nutr 27:451–463. doi:10.1081/pln-120028873

    Article  CAS  Google Scholar 

  • Silber A, Bar-Tal A, Levkovitch I, Bruner M, Yehezkel H, Shmuel D, Cohen S, Matan E, Karni L, Aktas H, Turhan E, Aloni B (2009) Manganese nutrition of pepper (Capsicum annuum L.): growth, Mn uptake and fruit disorder incidence. Sci Hortic 123:197–203. doi:10.1016/j.scienta.2009.08.005

    Article  CAS  Google Scholar 

  • Sinha P, Dube BK, Chatterjee C (2006) Manganese stress alters phytotoxic effects of chromium in green gram physiology (Vigna radiata L.) cv. PU 19. Environ Exp Bot 57:131–138. doi:10.1016/j.envexpbot.2005.05.003

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Rad Biol Med 18:321–336

    Article  PubMed  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN, Bisht SS (2002) Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 162:381–388. doi:10.1016/s0168-9452(01)00578-7

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Tewari N, Srivastava S, Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responses—influence on the activity and expression of superoxide dismutase in maize. Plant Sci 166:687–694. doi:10.1016/j.plantsci.2003.11.004

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Neetu Sharma PN (2005) Signs of oxidative stress in the chlorotic leaves of iron starved plants. Plant Sci 169:1037–1045. doi:10.1016/j.plantsci.2005.06.006

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2006a) Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants. Sci Hortic 108:7–14. doi:10.1016/j.scienta.2005.12.006

    Article  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2006b) Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta 223:1145–1153. doi:10.1007/s00425-005-0160-5

    Article  PubMed  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2007) Oxidative stress and antioxidant responses in young leaves of mulberry plants grown under nitrogen, phosphorus or potassium deficiency. J Integr Plant Biol 49:313–322. doi:10.1111/j.1744-7909.2007.00358.x

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2008) Morphology and physiology of zinc-stressed mulberry plants. J Plant Nutr Soil Sci 171:286–294. doi:10.1002/jpln.200700222

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2010a) Morphology and oxidative physiology of sulphur-deficient mulberry plants. Environ Exp Bot 68:301–308. doi:10.1016/j.envexpbot.2010.01.004

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2010b) Morphology and oxidative physiology of boron-deficient mulberry plants. Tree Physiol 30:68–77. doi:10.1093/treephys/tpp093

    Article  PubMed  CAS  Google Scholar 

  • Tewari RK, Watanabe D, Watanabe M (2012) Chloroplastic NADPH oxidase-like activity-mediated perpetual hydrogen peroxide generation in the chloroplast induces apoptotic-like death of Brassica napus leaf protoplasts. Planta 235:99–110. doi:10.1007/s00425-011-1495-8

    Article  PubMed  CAS  Google Scholar 

  • Wei Yang TJ, Perry PJ, Ciani S, Pandian S, Schmidt W (2008) Manganese deficiency alters the patterning and development of root hairs in Arabidopsis. J Exp Bot 59:3453–3464. doi:10.1093/jxb/ern195

    Article  Google Scholar 

  • Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Ann Bot 83:175–182. doi:10.1006/anbo.1998.0811

    Article  CAS  Google Scholar 

  • Yu Q, Osborne L, Rengel Z (1998) Micronutrient deficiency changes activities of superoxide dismutase and ascorbate peroxidase in tobacco plants. J Plant Nutr 21:1427–1437. doi:10.1080/01904169809365493

    Article  CAS  Google Scholar 

  • Yu Q, Osborne LD, Rengel Z (1999) Increased tolerance to Mn deficiency in transgenic tobacco overproducing superoxide dismutase. Ann Bot 84:543–547. doi:10.1006/anbo.1999.0951

    Article  CAS  Google Scholar 

  • Zanão Júnior LA, Fontes RLF, César J, Neves L, Korndörfer GH, de Ávila VT (2010) Rice grown in nutrient solution with doses of manganese and silicon. R Bras Ci Solo 34:1629–1639

    Article  Google Scholar 

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Acknowledgments

Author R. K. Tewari is grateful to the Council of Scientific and Industrial Research (CSIR), New Delhi, India for senior research fellowship. Authors are also thankful to Dr. Neetu and Dr. P. K. Singh for their support in the experiments.

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There is no conflict of interest.

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  1. Rajesh Kumar Tewari

    Present address: Biosphere Impact Studies, Belgian Nuclear Research Center (SCK·CEN), Boeretang 200, 2400, Mol, Belgium

Authors and Affiliations

  1. Department of Botany, University of Lucknow, Lucknow, 226007, India

    Rajesh Kumar Tewari, Praveen Kumar & Parma Nand Sharma

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  1. Rajesh Kumar Tewari
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Correspondence to Rajesh Kumar Tewari.

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Communicated by U. Feller.

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Tewari, R.K., Kumar, P. & Sharma, P.N. Oxidative stress and antioxidant responses of mulberry (Morus alba) plants subjected to deficiency and excess of manganese. Acta Physiol Plant 35, 3345–3356 (2013). https://doi.org/10.1007/s11738-013-1367-x

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  • DOI: https://doi.org/10.1007/s11738-013-1367-x

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