Skip to main content
Log in

Changes of antioxidative enzymes, lipid peroxidation and chlorophyll content in chickpea types colonized by different Glomus species under drought stress

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

In order to investigate the effects of Glomus species on some physiological characteristics of two chickpea types (Pirouz cultivar of Desi type and ILC-482 of Kabuli type) under non-stress (NS) and drought stress, an experiment was conducted using a factorial arrangement based on completely randomized design with three replications. Drought stress decreased shoot and total dry weight in plants. However inoculation of plants with mycorrhiza improved these traits. Leaf chlorophyll content was decreased, but leaf proline content and guaiacol peroxidases (EC 1.11.1.7) (POD), catalase (EC 1.11.1.6) (CAT), and ascorbate peroxidase (EC 1.11.1.11) (APX) activities were increased as a result of drought stress. Drought stress had no significant effect on soluble protein content and polyphenol oxidase (EC 1.10.3.1) (PPO) enzymatic activity in chickpea plants. In general, drought stress and especially severe drought stress increased membrane lipid peroxidation (MDA) in chickpea plants, which was more evident in non-inoculated than in inoculated plants. Inoculation of chickpea by AM significantly increased POD and PPO activities compared with non-inoculated chickpea, but had no effect on CAT activity and proline content of leaves. The reaction of chickpea cultivars to inoculation by AM species and irrigation levels were different. ILC-482 showed that antioxidant enzymes activities were more and thus less MDA compared with Pirouz cultivar. In general, the most POD and PPO activities were recorded for inoculated plants with G. etunicatum and G. versiform species, and the most APX activity was observed in plants inoculated with G. intraradices.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AM:

Arbuscular mycorrhiza fungal

APX:

ascorbate peroxidase

CAT:

catalase

MDA:

malondialdehyde

MDS:

moderate drought stress

NS:

non-stress

POD:

peroxidase

PPO:

polyphenol oxidase

SDS:

severe drought stress

References

  • Alguacil MM, Hernandez JA, Caravaea F, Portillo B, Roldan A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570

    Article  CAS  Google Scholar 

  • Al-Karaki GGN, McMichael B, ZAK J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Bartels D (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance. Trends Plant Sci 6:284–286

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldran RP, Teare ID (1973) Raipid determination of free proline for water studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Beer RF Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    Google Scholar 

  • Beltrano J, Carbone A, Montaldi ER, Guiamet JJ (1994) Ethylene as promoter of wheat grain maturation and ear senescence. Plant Growth Regul 15:107–112

    Article  CAS  Google Scholar 

  • Beltrano J, Ronco M, Montaldi ER (1999) Drought stress syndrome in wheat is proved by ethylene evolution and reversed by rewatering, aminoethoxyvinylglycine, or sodium benzoate. J Plant Growth Regul 18:59–64

    Google Scholar 

  • Beltrano J, Ronco MG (2007) Improved tolerance of wheat plants (Triticum aestivum L.) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum: Effect on growth and cell membrane stability. Braz J Plant Physiol 20(1):29–37

    Google Scholar 

  • Bowler C, Van Camp W, Van Montagu M, Inzé D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218

    CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Ann Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Sci 218:443–448

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Burke JJ, Mahan JR (1991) Environmental regulation of cellular protection systems. In: Gausman HW (ed) Plant Biochemical Regulators. Marcel Dekker, Inc, New York, pp 47–58

    Google Scholar 

  • Cakmak I, Horst J (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Hernandes JA, Roldan A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Sci 169:191–197

    Article  CAS  Google Scholar 

  • Creissen GP, Edwards AE, Mullineaux PM (1994) Glutathione reductase and ascorbate peroxidase. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 343–364

    Google Scholar 

  • Diego AM, Oliva MA, Carlos AM, Cambraia J (2003) Photosyntesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  Google Scholar 

  • Dionisio-Sese, Maribel L, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Egert M, Tevini M (2002) Influence of drought on some physiological parameters symptomatic for oxidative stress in leaves of chives (Allium schoenoprasum). Environ Exp Bot 48:43–49

    Article  CAS  Google Scholar 

  • Elstner EF (1987) Metabolism of activated oxygen species. In: Davies DD (ed) The Biochemistry of Plants.vol. II, Biochemistry of Metabolism. Academic, San Diego, CA, pp 252–315

    Google Scholar 

  • Francisco JP, Daniel V, Nilo M (2002) Ascorbic acid and flavonoid-peroxidase reaction as a detoxifying system of H2O2 in grapevine leaves. Phytochemistry 60:573–580

    Article  Google Scholar 

  • Girousse C, Bournoville R, Bonnemain JL (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111:109–113

    PubMed  CAS  Google Scholar 

  • Gunes A, Inal A, Adak MS, Bagci EG, Cicek N, Eraslan F (2008) Effect of drought stress implemented at pre- or post- anthesis stage some physiological as screening criteria in chickpea cultivars. Russian J Plant Physiol 55(1):59–67

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1985) Free radicals in biology and medicin. Clarendon, Oxford

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Clarendon, Oxford, UK

    Google Scholar 

  • Harborne JB (1984) Phytochemical Methods. A guide to modern techniques of plant analysis. Chapman and Hall, London, p 288

    Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal Symbiosis. London and New York: Academic Press

  • Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185

    Article  CAS  Google Scholar 

  • Hetrick BAD, Wilson GWT, Todd TC (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25

    Article  CAS  Google Scholar 

  • Jakob B, Heber U (1996) Photoproduction and detoxification of hydroxyl radicals in chloroplast and leaves in relation to photoinactivation of pohotosystems I and II. Plant Cell Physiol 37:629–35

    Article  CAS  Google Scholar 

  • Kehri HK, Chandra S (1990) VAM association in urd as affected by water stress condition in soil and foliar spray. Acta Bot Ind 18:316–318

    Google Scholar 

  • Kishor PB, Hong Z, Miao GH, Hu CA, Verma DPS (1995) Overexpression of D1-pyrroline- 5-carboxilate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–94

    PubMed  CAS  Google Scholar 

  • Koide RT, Schreiner RP (1992) Regulation of the vesicular arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557–581

    Article  CAS  Google Scholar 

  • Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic, San Diego, Calif

    Google Scholar 

  • Kumar KB, Khan PA (1982) Peroxidase and polyphenoloxidase in excisedragi (Eleusine coracana cv. PR 202) leaves during senescence. Ind J Exp Bot 20:412–416

    CAS  Google Scholar 

  • Lacan D, Baccou JC (1998) High levels of antioxidant enzymes correlate with delayed senescence in nonnetted muskmelon fruits. Planta 204:377–382

    Article  CAS  Google Scholar 

  • Lambais MR, Rios-Ruiz WE, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160:421–428

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoides and chlorophylls ‘a’ and ‘b’ of leaf extract in different solvent. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • McArthur DAJ, Knowles NR (1993) Influence of VAM fungi and nutrition on growth, development, and mineral nutrition of potato. Plant Physiol 102:771–782

    PubMed  CAS  Google Scholar 

  • Malecka A, Jarmuszkiewicz W, Tomaszewska B (2001) Antioxidative defense to lead stress in subcellular compartments of pea root cells. Acta Biochim Pol 48:687–698

    PubMed  CAS  Google Scholar 

  • Malhotra RS, Pundir RPS, Slinkard AE (1987) Genetic resources of chickpea. In: Saxena MC, Singh KB (eds) The Chickpea. CAB International Cambrian News, Aberystwyth, pp 67–81

    Google Scholar 

  • Mathur N, Vyas A (2000) Influence of arbuscular mycorrhizae on biomass production, nutrient uptake and physiological changes in Ziziphus mauritana Lam. under water stress. J Arid Environ 45:191–195

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild DL, Swan GA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352

    Article  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 

  • Nayyar H, Singh S, Kaur S, Kumar SD, Upadhyaya H (2006) Different sensitivity of macrocarpa and microcarpa types of chickpea (Cicer arietinum L.) to water stress:association of contrasting stress response with oxidative injury. Journal Integrative Plant Biology 48(1):1318–1329

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–79

    Article  PubMed  CAS  Google Scholar 

  • Palma JM, Longa MA, del Rio LA, Arines J (1993) Supperoxide dismutase in vesicular arbuscular-mycorrhizal red clover plants. Physiol Plant 87:77–83

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T British Mycol Soc 55:158–161.l

    Article  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhiz soybean plants and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    Article  CAS  Google Scholar 

  • Rachel EK, Reddy SR, Reddy SM (1992) Seedling preinoculation with AM fungi on transplant survival and growth of sunflower. Proc Natl Acad Sci Ind B 62:429–432

    Google Scholar 

  • Robinson DA, Campbell CS, Hopmans JW, Hornbuckle BK, Jones SB, Knight R, Ogden F, Selker J, Wendroth O (2008) Soil moisture measurement for ecological and hydrological watershed-scale observatories. A review Vadose Zone J 7:358–389

    Article  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333

    Article  CAS  Google Scholar 

  • Sairam RK, Rao KV, Srivastava GC (2004) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046

    Article  Google Scholar 

  • Seel WE, Hendry GAF, Lee JA (1992) The combined effect of desiccation and irradiance on mosses from xeric and hydric habitats. J Exp Bot 43:1023–1030

    Article  Google Scholar 

  • Singh KB, Ocampo B (1997) Exploitation of wild Cicer species for yield improvement in chickpea. Theor Appl Genet 95:418–423

    Article  Google Scholar 

  • Sinha S, Saxena R, Singh S (2005) Chromium induced lipid peroxidation in the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58:595–604

    Article  PubMed  CAS  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 

  • Smith SE, Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu Rev Plant Physiol 39:221–244

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, Calif

    Google Scholar 

  • Sun W, Montagu MV, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    PubMed  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 4:186–191

    Google Scholar 

  • Whalley WR (1993) Considerations on the use of time-domain reflectometry (TDR) for measuring soil water content. J Soil Sci 44:1–9

    Article  Google Scholar 

  • Wu QS, Zou YN (2009) Mycorrhiza has a direct effect on reactive oxygen metabolism of drought-stressed citrus. Plant Soil Environ 55(10):436–442

    CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX (2006) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. Eur J Soil Biol 42:166–172

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX, Wang MY (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48:147–154

    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 

  • ZhongQun H, ChaoXing H, ZhiBin Z, ZhiRong Z, HuaiSong W (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids and Surfaces B: Biointerfaces 59(2):128–133

    Article  Google Scholar 

Download references

Acknowledgment

We are grateful to the University of Kurdistan for financial support of this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yousef Sohrabi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sohrabi, Y., Heidari, G., Weisany, W. et al. Changes of antioxidative enzymes, lipid peroxidation and chlorophyll content in chickpea types colonized by different Glomus species under drought stress. Symbiosis 56, 5–18 (2012). https://doi.org/10.1007/s13199-012-0152-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-012-0152-8

Keywords

Navigation