Skip to main content
SpringerLink
Log in

Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The effects of cadmium (Cd) on germination, and antioxidative enzyme activity (AEA) involving superoxide dismutase, catalase, peroxidase, and ascorbate peroxidase, and on amounts of malondialdehyde and proline present within Achnatherum inebrians, were determined for specimens infected (E+) vs. non-infected (E−) by Neotyphodium gansuense, and cultivated in the presence of various concentrations of CdCl2 (0, 50, 100, 200 and 300 μmol/l). Under high Cd concentrations (100, 200 and 300 μM), E+ (vs. E−) specimens exhibited a higher germination rate and index, and higher values for shoot length, root length and dry biomass, but there was no significant difference (P > 0.05) under low Cd concentrations (0 and 50 μM). AEA and the proline content increased, but malondialdehyde content declined in the E+ (vs. E−) specimens under high Cd concentrations (100, 200 and 300 μM). There was no significant difference (P > 0.05) under low Cd concentrations (0 and 50 μM). Endophyte infection was concluded to be of benefit to the germination and anti-oxidative mechanisms within A. inebrians under plant exposures to high CdCl2 concentrations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric Ecosyst Environ 41:23–142

    Google Scholar 

  • Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol 34:576–581

    CAS  PubMed  Google Scholar 

  • Barcelo J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37

    Article  CAS  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 1:764–775

    Article  Google Scholar 

  • Chaney RL (1993) Zn toxicity. In: Robson AD (ed) Zn in soils and plants. Developments in plants and soils sciences, vol 55. Kluwer, Dordrecht, pp 45–57

    Google Scholar 

  • Chen N (2008) Genetic diversity of drunken horse grass (Achnatherum inebrians) and effects of its endophyte infection on cold tolerance. MSc dissertation, Lanzhou University, China

  • Clairborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284

    Google Scholar 

  • Clay K (1987) Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 73:358–362

    Article  Google Scholar 

  • Conover MR (2003a) Impact of consuming tall fescue seeds infected with the endophytic fungus, Neotyphodium coenophialum, on reproduction of chickens. Theriogenology 59:1313–1323

    Article  PubMed  Google Scholar 

  • Conover MR (2003b) Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agric Ecosyst Environ 97:199–203

    Article  Google Scholar 

  • Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv Azad). J Exp Bot 52:1101–1109

    Article  CAS  PubMed  Google Scholar 

  • Eerens JPJ, Visker MHPW, Lucas RJ (1998) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment IV. Plant parasitic nematodes. N Z J Agric Res 41:209–217

    Google Scholar 

  • Ekmekçi Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

    Article  PubMed  CAS  Google Scholar 

  • Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67

    Article  Google Scholar 

  • Esterbauer HK, Cheeseman H (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Meth Enzymol 186:407–421

    Article  CAS  PubMed  Google Scholar 

  • Fabien M, Nathalle V, Adnan H, Alain C, Huguette S (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Plant Physiol 113:557–563

    Article  Google Scholar 

  • Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7:304–313

    Article  Google Scholar 

  • Fletcher LR, Harvey IC (1981) An association of a Lolium endophytes with ryegrass staggers. N Z Vet J 29:185–186

    CAS  PubMed  Google Scholar 

  • Gill PK, Sharma AD, Singh P, Bhullar SS (2003) Changes in germination, growth and soluble sugar contents of sorghum bicolor (L.) moench seeds under various abiotic stresses. Plant Growth Regul 40:157–162

    Article  CAS  Google Scholar 

  • Gou XY (2007) Effect of Neotyphodium endophyte on salt tolerance to drunken horse grass (Achnatherum inebrians). MSc dissertation, Lanzhou University, China

  • Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17

    CAS  Google Scholar 

  • Gupta AS, Robert P, Webb A, Scott H, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol 103:1067–1073

    PubMed  Google Scholar 

  • Gutterman Y (2000) Maternal effects on seeds during development. In: Fenner M (ed) Seeds. The ecology of the regeneration in plant communities. CAB International, London, pp 59–84

    Chapter  Google Scholar 

  • Hegedusü A, Erdei S, Horvath G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  Google Scholar 

  • Hill NS, Belesky DP, Stringer WC (1991) Competitiveness of tall fescue as influenced by Acremonium coenophialum. Crop Sci 31:185–190

    Google Scholar 

  • Latch GCM (1993) Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agric Ecosyst Environ 44:143–156

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Li CJ (2005) Biological and ecological characteristics of Achnatherum inebrians/Neotyphodium endophyte symbiont. PhD dissertation, Lanzhou University, China

  • Li HS (2000) Principle and techniques of botanic, chemical and physiological experiments. Senior Education Press, Beijing, pp 164–169 (194–197)

    Google Scholar 

  • Li F (2007) Effects of endophyte infection on drought resistance to drunken horse grass (Achnatherum inebrians). MSc dissertation, Lanzhou University, China

  • Li CJ, Gao JH, Ma B (2003) Seven diseases of drunken horse grass (Achnatherum inebrians) in China (In Chinese with english abstract). Pratacultural Sci 20:51–53

    Google Scholar 

  • Li CJ, Nan ZB, Gao JH, Tian P (2004a) Detection and distribution of Neotyphodium-Achnatherum inebrians association in China. In: Proceedings of 5th international Neotyphodium/grass interactions symposium. Arkansas, pp 210

  • Li CJ, Nan ZB, Paul VH, Dapprich P, Liu Y (2004b) A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon 90:141–147

    Google Scholar 

  • Li CJ, Zhang XX, Li F, Nan ZB, Schardl CL (2007a) Disease and pests resistance of endophyte infected and non-infected drunken horse grass. In: Popay A, Thom ER, (eds) Proceedings of the 6th international symposium on fungal endophytes of grasses. New Zealand Grassland Association, Dunedin, pp 111–114

  • Li CJ, Gao JH, Nan ZB (2007b) Interactions of Neotyphodium gansuense, Achnatherum inebrians, and plant-pathogenic fungi. Mycol Res 111:1220–1227

    Article  PubMed  Google Scholar 

  • Li CJ, Nan ZB, Li F (2008) Biological and physiological characteristics of Neotyphodium gansuense symbiotic with Achnatherum inebrians. Microbiol Res 163:431–440

    Article  CAS  PubMed  Google Scholar 

  • Li CJ, Nan ZB, Zhang CJ, Zhang CY, Zhang YH (2009) Effects of endophyte infected drunken horse grass on Chinese rabbit. J Agric Sci Technol 11(2):90–96 (In Chinese with English abstract)

    Google Scholar 

  • Maksymiec W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    Article  CAS  Google Scholar 

  • Malinowski DP, Leuchtmann A, Schmidt D, Nosberger J (1997) Symbiosis with Neotyphodium uncinatum endophyte may increase the competitive ability of meadow fescue. Agron J 89:833–839

    Google Scholar 

  • Malinowski DP, Belesky DP, Lewis GC (2005) Abiotic stresses in endophyte grasses. In: Craig AR, Charles PW, Donald ES (eds) Neotyphodium in cool-season grasses. pp 187–199

  • Meister B, Krauss J, Härri SA, Schneider MV, Müller CB (2006) Fungal endophyte symbionts affect aphid population size by reduction of adult lifespan and fecundity. Basic Appl Ecol 7:244–252

    Article  Google Scholar 

  • Melis T, Selim E, Faruk O, Soren H, Ismail C (2006) Antioxidant defense system and cadmium uptake in barley genotypes differing in cadmium tolerance. J Trace Elem Med Biol 20:181–189

    Article  CAS  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    CAS  PubMed  Google Scholar 

  • Moon CD, Jean-Jacques GJJ, Li CJ, Ravel C, Craven KD, Schardl CL (2007) New Neotyphodium endophyte species from the grass tribes stipeae and meliceae. Mycologia 99:895–905

    Article  CAS  PubMed  Google Scholar 

  • Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravier S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953

    Article  CAS  PubMed  Google Scholar 

  • Nan ZB, Li CJ (2000) Neotyphodium in native grasses in China and observations on endophyte-host interaction. In: Paul VH, Dapprich PD (eds) Proceedings of the 4th international Neotyphodium-grass interactions symposium. Soest, pp 41–50

  • Neil KL, Tiller RL, Faeth SH (2003) Big sacaton and endophyte-infected Arizona fescue germination under water stress. J Range Manage 56:616–622

    Article  Google Scholar 

  • Novas MV, Gentile A, Cabral D (2003) Comparative study of growth parameters on diaspores and seedlings between populations of Bromus setifolius from Patagonia, differing in Neotyphodium endophyte infection. Flora 198:421–426

    Google Scholar 

  • Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301

    Article  CAS  PubMed  Google Scholar 

  • Ouzounidou G, Moustakas M, Eleftheriou EP (1997) Physiologial and ultrastructural effects of cadmium on wheat (Triticum aestivum) leaves. Arch Environ Contam Toxicol 32:154–160

    Article  CAS  PubMed  Google Scholar 

  • Pedro EG, Pablo HM, Claudio MG, Roberto LB (2006) Effects of the Neotyphodium endophyte fungus on dormancy and germination rate of Lolium multiflorum seeds. Austral Ecol 31:767–775

    Article  Google Scholar 

  • Pinkerton BW, Rice JS, Undersander DJ (1990) Germination in Festuca arundinacea as affected by the fungal endophyte, Acremonium coenophialum. In: Quinsenberry SS, Joost RE (eds) Proceedings of the international symposium: on acremonium/grass interactions. New Orleans, pp 176

  • Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue. Crop Sci 32:1060–1061

    Article  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Schardl CL, Leuchtmann A (2004) The Epichloë endophytes of grasses and the symbiotic continnuum. In: Dighton J, White JF, Oudemans P (eds) The fungal community. CRC Press, Boca Raton, pp 475–503

    Google Scholar 

  • Semane B, Cuypers A, Smeets K, Belleghem F, Horemans N, Schat H, Van-gronsveld J (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Plant Physiol 129:519–528

    Article  CAS  Google Scholar 

  • Siegel MR, Latch GCM, Johnson MC (1987) Fungal endophytes of grasses. Annu Rev Phytopathol 25:293–315

    Article  Google Scholar 

  • Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990) Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3315

    Article  CAS  Google Scholar 

  • Uraguchi S, Watanabe I, Yoshitomi A, Kiyono M, Kuno K (2006) Characteristics of cadmium accumulation and tolerance in novel Cd-accumulating crops, Avena strigosa and Crotalaria juncea. J Exp Bot 57:29–55

    Article  Google Scholar 

  • Van Assche F, Clijsters H (1986a) Inhibition of photosynthesis by treatment of Phaseolus vulgaris with toxic concentration of Zn: effects on electron transport and photophosphorylation. Plant Physiol 66:717–721

    Article  Google Scholar 

  • Van Assche F, Clijsters H (1986b) Inhibition of photosynthesis in Phaseolus vulgaris by treatment with toxic concentration of Zn: effects on ribulose-1, 5-bisphosphate carboxylase/oxygenase. J Plant Physiol 125:355–360

    Google Scholar 

  • Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294

    Article  CAS  PubMed  Google Scholar 

  • West CP, Izekor E, Robbins RT, Gergerich R, Mahmood T (1990) Acremonium coenophialum effects on infestations of barley yellow dwarf virus and soil-borne nematodes and insects in tall fescue. In: Proceedings of the international symposium on acremonium/grass interactions. pp 196–198

  • White JF, Morgan-Jones G (1987a) Endophyte-host associations in forages VII. Acremonium chisosum, a new species isolated from Stipa eminens in Texas. Mycotaxon 28:179–189

    Google Scholar 

  • White JF, Morgan-Jones G (1987b) Endophyte-host associations in forage grasses. IX. Concerning Acremonium typhinum, the anamorph of Epichloë typhina. Mycotaxon 29:289–500

    Google Scholar 

  • White JF, Morgan-Jones G (1987c) Endophyte-host associations in forage grasses. X. Cultural studies on some species of Acremonium sect. albo-lanosa, including a new species, A. starrii. Mycotaxon 30:87–95

    Google Scholar 

  • Zhang YP, Nan ZB (2007) Growth and anti-oxidative systems change in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193:377–386

    Article  CAS  Google Scholar 

  • Zhang FQ, Zhang HX, Wang GP, Xu LL, Shen ZG (2009) Cadmium-induced accumulation of hydrogen peroxide in the leaf apoplast of Phaseolus aureus and Vicia sativa and the roles of different antioxidant enzymes. J Hazard Mater. doi:10.1016/j.jhazmat.2009.02.002

Download references

Acknowledgments

We wish to thank Dr. Peter Long for polishing the English and Dr. Fenqin Zhang for providing beneficial discussion of the manuscript. This research was financially supported by the National Basic Research Program of China (2007CB108902), National Key Technology R & D Program of China (2008BADB3B05) & National Nature Science Foundation of China (30771531).

Author information

Authors and Affiliations

  1. Key Laboratory of Grassland Agro-Ecosystems, Ministry of Agriculture; College of Pastoral Agriculture Science and Technology, Lanzhou University, P. O. Box 61, 730000, Lanzhou, Gansu, People’s Republic of China

    Xingxu Zhang, Chunjie Li & Zhibiao Nan

  2. College of Resources and Environmental Sciences, Lanzhou University, 730000, Lanzhou, Gansu, People’s Republic of China

    Xiaomei Fan

Authors
  1. Xingxu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomei Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chunjie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhibiao Nan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chunjie Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, X., Fan, X., Li, C. et al. Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul 60, 91–97 (2010). https://doi.org/10.1007/s10725-009-9422-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-009-9422-8

Keywords

Search

Navigation