Skip to main content
Log in

Endophytic infection modulates ROS-scavenging systems and modifies cadmium distribution in rice seedlings exposed to cadmium stress

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

Abstract

The relationship between endophytic infection and components of the Cd stress response was examined in the present study. Oryza sativa L. plants were grown in Hoagland’s nutrient solution with and without infection with the endophytic fungus JP4 under different cadmium (Cd) stress conditions (0, 50, 100, and 150 μM) for 2 weeks. Endophytic infection in the roots promoted rice seedling growth and decreased shoot Cd contents in comparison to non-infected treatments. Furthermore, the adsorbed Cd remained in the roots, and far less Cd was transported from the roots to the shoots. Compared to the non-infected rice seedlings, endophytic infection remarkably increased the pigment content, net photosynthetic rate (Pn), and chlorophyll fluorescence in all treatments, except for Fv/F0 values and chlorophyll b content in the 100 μM Cd treatment. Superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and glutathione reductase (GR) activity, as well as ascorbic acid (AsA) and glutathione (GSH) content, increased in EI seedlings relative to EF seedlings under Cd stress, while malondialdehyde (MDA) and H2O2 content decreased significantly. Inoculation of endophytic fungus JP4 in roots promoted rice seedling growth and ameliorated the negative effects of Cd stress on the growth of rice seedlings by triggering antioxidant systems and non-enzymatic systems, regulating photosynthetic activities and modifying the Cd distribution.

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

Similar content being viewed by others

References

  • Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113:548–570

    CAS  PubMed  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M, Khan NA (2008) Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regul 54:271–279

    CAS  Google Scholar 

  • Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric Ecosyst Environ 44:123–141

    Google Scholar 

  • Bu N, Li XM, Li YY, Ma CY, Ma LJ, Zhang C (2012) Effects of Na2CO3 stress on photosynthesis and antioxidative enzymes in endophyte infected and non-infected rice. Ecotoxicol Environ Saf 78:35–40

    CAS  PubMed  Google Scholar 

  • Cabrera C, Ortega E, Lorenzo ML, López MC (1998) Cadmium contamination of vegetable crops, farmlands, and irrigation waters. Rev Environ Contam Toxicol 154:55–81

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Caliope MA, Mariano GR, Humberto GM, Tania V (2017) Improved growth and control of oxidative stress in plants of Festuca arundinacea exposed to hydrocarbons by the endophytic fungus Lewia sp. Plant Soil 411:347–358

    Google Scholar 

  • Chao YY, Kao CH (2010) Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 336:39–48

    CAS  Google Scholar 

  • Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667

    Google Scholar 

  • Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann Bot106: 791–802

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costa H, Gallego SM, Tomaro ML (2002) Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Sci 162:939–945

    CAS  Google Scholar 

  • Dai H, Shan C, Zhao H, Jia G, Chen D (2017) Lanthanum improves the cadmium tolerance of Zea mays seedlings by the regulation of ascorbate and glutathione metabolism. Biol Plant 61:551–556

    CAS  Google Scholar 

  • Deng X, Xia Y, Hu W, Zhang H, Shen Z (2010) Cadmium-induced oxidative damage and protective effects of N-acetyl-l-cysteine against cadmium toxicity in Solanum nigrum L. J Hazard Mater 180:722–729

    CAS  PubMed  Google Scholar 

  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289

    CAS  Google Scholar 

  • Gajic G, Mitrovic M, Pavlovic P, Stevanovic B, Djurdjevic L, Kostic O (2009) An assessment of the tolerance of Ligustrum ovalifolium Hassk. to traffic-generated Pb using physiological and biochemical markers. Ecotox Environ Saf 72:1090–1101

    CAS  Google Scholar 

  • Hasan SA, Fariduddin Q, Ali B, Hayat S, Ahmad A (2009) Cadmium: toxicity and tolerance in plants. J Environ Biol 30:165–174

    CAS  PubMed  Google Scholar 

  • Havaux M, Gruszecki WI, Dupont I, Leblanc RM (1991) Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J Photochem Photobiol B: Biol 8:361–370

    CAS  Google Scholar 

  • He YM, Yang ZX, Li MR, Jiang M, Zhan FD, Zu YQ, Li T, Zhao ZW (2017) Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress. Environ Sci Pollut Res 24:18494–18504

    CAS  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

    CAS  PubMed  Google Scholar 

  • Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide acumulation. Plant Soil 298:231–241

    CAS  Google Scholar 

  • Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191

    CAS  Google Scholar 

  • Islam E, Liu D, Li TQ, Yang XE, Jin XF, Mahmood Q, Tian SK, Li JY (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926

    CAS  PubMed  Google Scholar 

  • Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186:1520–1526

    CAS  PubMed  Google Scholar 

  • Jana S, Choudhari MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354

    Google Scholar 

  • Kane KH (2011) Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ Exp Bot 71:337–344

    Google Scholar 

  • Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and isoenzymes in embryogenic and non-embryogenic ‘Shamouti’ orange ovular callus lines. Plant Cell Physiol 18:463–467

    CAS  Google Scholar 

  • Kucerova D, Kollarova K, Zelko I, Vatehova Z, Liskova D (2014) Galactoglucomannan oligosaccharides alleviate cadmium stress in Arabidopsis. J Plant Physiol 171:518–524

    CAS  PubMed  Google Scholar 

  • Law MY, Charles SA, Halliwelll B (1983) Glutathione and ascorbic acid in spinach (Spinach oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. Biochem J 210:899–903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both Cu/Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    CAS  PubMed  Google Scholar 

  • Li T, Liu MJ, Zhang XT, Zhang HB, Sha T, Zhao ZW (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074

    CAS  PubMed  Google Scholar 

  • Li XM, Bu N, Li YY, Ma LJ, Xin SG, Zhang LH (2012) Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. J Hazard Mater 213–214:55–61

    PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    CAS  Google Scholar 

  • Likar M, Regvar M (2013) Isolates of dark sepatate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil 370:593–604

    CAS  Google Scholar 

  • Liu RJ, Chen YL (2007) Mycorrhizology. Science Press, Beijing, pp 1–447

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ma F, Cheng L (2003) The sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate–glutathione pathway than the shaded peel. Plant Sci 165:819–827

    CAS  Google Scholar 

  • Ma LJ, Li XM, Bu N, Li N (2010) An alginate-derived oligosaccharide enhanced wheat tolerance to cadmium stress. Plant Growth Regul 62:71–76

    CAS  Google Scholar 

  • Migocka M, Kosieradzka A, Papierniak A, Maciaszczyk-Dziubinska E, Posyniak E, Garbiec A, Filleur S (2015) Two metal-tolerance proteins, MTP1 and MTP4, are involved in Zn homeostasis and Cd sequestration in cucumber cells. J Exp Bot 66(3):1001–1015

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Monnet F, Vaillant N, Hitmi A, Coydret A, Sallanon H (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plant 113:557–563

    CAS  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    CAS  PubMed  Google Scholar 

  • Rennenberg H, Brunold C (1994) Significance of glutathione metabolism in plants under stress. Prog Bot 55:142–156

    CAS  Google Scholar 

  • Sarwar N, Saifullah Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937

    CAS  PubMed  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    CAS  Google Scholar 

  • Shamsi IH, Wei K, Zhang GP, Jilani G, Hassan MJ (2008) Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. Biol Plant 52:165–169

    CAS  Google Scholar 

  • Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919

    CAS  PubMed  Google Scholar 

  • Talaat NB (2015) Effective microorganisms improve growth performance and modulate the ROS-scavenging system in common bean (Phaseolus vulgaris L.) plants exposed to salinity stress. J Plant Growth Regul 34:35–46

    CAS  Google Scholar 

  • Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A (2012) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Ann Bot 110:433–443

    PubMed  PubMed Central  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    CAS  PubMed  Google Scholar 

  • Wang YP, Huang J, Gao YZ (2012) Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS ONE 7: e48669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JL, Li T, Liu GY, Smith JM, Zhao ZW (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Rep 6:22028

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yu F, Gu Y, Zhang Q, Bu N (2016) The identification of a fungal endophyte of Suaeda salsa and preliminarily research on active products of promoting growth. Biotech Bull 32:151–157 (in Chinese)

    Google Scholar 

  • Zhang XX, Li CJ, Nan ZB (2010) Effects of cadmium stress on growth and antioxidantive systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazdard Mater 175:703–709

    CAS  Google Scholar 

  • Zhang XX, Li CJ, Nan ZB (2012) Effects of cadmium stress on seed germination and seedling growth of Elymus dahuricus infected with the neotyphodium endophyte. Sci China: Life Sci 55:793–799

    CAS  Google Scholar 

  • Zhao Y, Yu F, Guo MM, Bu N (2015) Isolation, identification and growth-promoting effect of Suaeda salsa endophyte fungi JP3. J Shenyang Norm Univ 33:116–120

    CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31600314), and the Shenyang City Science and Technology Plan (F16-205-1-50), Major incubating project of Shenyang Normal University (ZD201705), Liaoning Province Science and Technology Plan Progect (No. 2017208001) and the Liaoning Province Natural Science Foundation (2015020762).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cuimei Yu.

Additional information

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

Ma, L., Li, X., Wang, L. et al. Endophytic infection modulates ROS-scavenging systems and modifies cadmium distribution in rice seedlings exposed to cadmium stress. Theor. Exp. Plant Physiol. 31, 463–474 (2019). https://doi.org/10.1007/s40626-019-00159-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-019-00159-5

Keywords

Navigation