Plant and Soil

, Volume 267, Issue 1–2, pp 1–12

Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected withNeotyphodium spp. endophytes

  • D. P. Malinowski
  • H. Zuo
  • D. P. Belesky
  • G. A. Alloush
Article

Abstract

Infection of tall fescue (Festuca arundinacea Schreb.) with its endemicNeotyphodium coenophialum-endophyte (Morgan-Jones and Gams) Glenn, Bacon and Hanlin appears to reduce copper (Cu) concentrations in forage and serum of grazing animals, contributing to a range of immune-related disorders. A greenhouse experiment was conducted to identify effects of novel endophyte strains on Cu acquisition by tall fescue (Festuca arundinacea Schreb.) varieties Grasslands Flecha and Jesup infected with a novel, non ergot producing endophyte strain AR542, and two perennial ryegrass (Lolium perenne L.) varieties Aries and Quartet infected with a novel, non lolitrem B producing strain AR1, and their noninfected (E−) forms. Individual endophyte/grass associations were cultivated in nutrient solutions at 1.0 (P+) and 0.0 mM (P−) phosphorus concentrations. The Cu2+-binding activity of extracellular root exudates, and concentrations of Cu and other heavy metals in roots and shoots were measured. Extracellular root exudates of AR542-infected vs. E− tall fescue had higher Cu2+-binding activity only in P− nutrient solution as shown by lower concentration of free Cu2+ (0.096 vs. 0.188 mmol Cu2+ g−1 root DM, respectively). The Cu2+-binding activity by root exudates of perennial ryegrass was not affected by endophyte infection, but was higher (i.e., lower concentration of free Cu2+) in P− vs. P+ nutrient solution (0.068 vs. 0.114 mmol Cu2+ g−1 root DM). In this hydroponic experiment, Cu concentrations in shoots of both grasses were not a function of Cu2+-binding activity and endophyte effects on heavy metal concentrations in shoots and roots were specific for each variety. The Cu2+-binding activity of extracellular root exudates may affect Cu accumulation by field-grown, endophyte-infected tall fescue under P-limiting growth conditions and warrants verification by more specific methods.

Key words

copper Festuca arundinacea Lolium perenne Neotyphodium novel endophytes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Animal and Plant Health Inspection Service 2000 Serum copper concentrations of U.S. beef cattle. USDA Veterinary Services Information Sheet.Google Scholar
  2. Bacon C W, Lyons P C, Porter J K and Robbins J D 1986 Ergot toxicity from endophyte-infected grasses.: A review. Agron. J. 78, 106–116.CrossRefGoogle Scholar
  3. Bagley C V, Stenquist N J and Worwood D R 1997 Copper deficiency in Utah. Animal Health Fact Sheet 11. Cooperative Extension Service, Utah State University, Logan, UT.Google Scholar
  4. Ball O J-P and Tapper B A 1999 The production of loline alkaloids in artificial and natural grass/endophyte associations.In Proc. 52nd N.Z. Plant Protection Conf. 9–13 August 1999. Ed. N Z Auckland. pp. 264–269.Google Scholar
  5. Belguendouz L, Fremont L and Linard A 1997 Resveratrol inhibits metal ion-dependent and independent peroxidation of porcine low-density lipoproteins. Biochem. Pharm. 53, 1347–1355.PubMedCrossRefGoogle Scholar
  6. Bitton G, Jung K and Koopman B 1994 Evaluation of a microplate assay specific for heavy metal toxicity. Arch. Environ. Contam. Toxicol. 27, 25–28.PubMedCrossRefGoogle Scholar
  7. Bluett S, Thom E R, Clark D A and Tapper B 2001 Milk production and composition from cows grazing perennial ryegrass infected with a novel endophyte (AR1).In Proc. 4th InternationalNeotyphodium/Grass Interaction Symposium. 27–29 September 2000. Eds. V H Paul and P D Dapprich. pp. 195–199. Soest, Germany.Google Scholar
  8. Bouton J 2001 The use of endophytic fungi for pasture improvement in the USA.In Proc. 4th Int.Neotyphodium/Grass Interaction Symposium. 27–29 September 2000 Eds. V H Paul and P D Dapprich. pp. 163–168. Soest, Germany.Google Scholar
  9. Bouton J, Hill N, Hoveland C, McCann M, Thompson F, Hawkins L and Latch G 2001 Performance of tall fescue cultivars infected with non-toxic endophytes.In Proc. 4th Int.Neotyphodium/Grass Interactions Symposium. 27–29 September 2000. Eds. V H Paul and P D Dapprich. pp. 179–185. Soest, Germany.Google Scholar
  10. Bouton J H, Latch G C M, Hill N S, Hoveland C S, McCann M A, Watson R H, Parish J A, Hawkins L L and Thompson F N 2002 Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron. J. 94, 567–574.CrossRefGoogle Scholar
  11. Brown J E, Khodr H, Hider R C and Rice-Evans C A 1998 Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties. Biochem. J. 330, 1173–1178.PubMedGoogle Scholar
  12. Bush L P, Wilkinson H H and Schardl C L 1997 Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol. 114, 1–7.PubMedGoogle Scholar
  13. Christensen M J, Simpson W R and Samarrai T Al 2000 Infection of tall fescue and perennial ryegrass plants by combinations of differentNeotyphodium endophytes. Mycol. Res. 104, 974–978.CrossRefGoogle Scholar
  14. Clay K and Schardl C 2002 Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist. 160 (Suppl.), 99–127.Google Scholar
  15. Dennis S B, Allen V G, Saker K E, Fontenot J P, Ayad J Y M and Brown C P 1998 Influence ofNeotyphodium coenophialum on copper concentration in tall fescue. J. Anim. Sci. 76, 2687–2693.PubMedGoogle Scholar
  16. Dousset S, Morel J L, Jacobson A and Bitton G 2001 Copper binding capacity of root exudates of cultivated plants and associated weeds. Biol. Fertil. Soils 34, 230–234.CrossRefGoogle Scholar
  17. Fletcher L R and Easton H S 1997 The evaluation and use of endophytes for pasture improvement. InNeotyphodium. Eds. C W Bacon and N S Hill. pp. 209–227. Plenum Press. New York.Google Scholar
  18. Fletcher L R and Harvey I C 1981 An association of aLolium endophyte with ryegrass staggers. New Zeal. Vet. J. 32, 185–186.Google Scholar
  19. Gahoonia T S, Claasen N and Jungk A 1992 Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate. Plant Soil 140, 241–248.CrossRefGoogle Scholar
  20. Hewitt E J 1966 Sand and water culture methods used in the study of plant nutrition. Eastern Press, London.Google Scholar
  21. Holmgren G G S, Meyer M W, Chaney R L and Daniels R B 1993 Cadmium, lead, zinc, copper, and nickel in agricultural soils of the United States of America. J. Environ. Qual. 22, 335–348.CrossRefGoogle Scholar
  22. Jupp A P and Newman E I 1987 Phosphorus uptake from soil byLolium perenne during and after severe drought. J. Appl. Ecol. 24, 979–990.Google Scholar
  23. Ju Y, Sacalis J N and Still C C 1998 Bioactive flavonoids from endophyte-infected blue grass (Poa ampla). J. Agric. Food Chem. 46, 3785–3788.Google Scholar
  24. Justus M, Witte L and Hartmann T 1997 Levels and tissue distribution of loline alkaloids in endophyte-infectedFestuca pratensis. Phytochem. 44, 51–57.CrossRefGoogle Scholar
  25. Koshino H, Terada S, Yoshihara T, Sakamura S, Shimanuki T, Sato T and Tajimi A 1988 Three phenolic acid derivates from stromata ofEpichloë typhina onPhleum pratense. Phytochem. 27, 1333–1338.CrossRefGoogle Scholar
  26. Lewis G C, Bakken A K, MacDuff J H and Raistrick N 1996 Effect of infection by the endophytic fungusAcremonium lolii on growth and nitrogen uptake by perennial ryegrass (Lolium perenne) in flowing solution culture. Ann. Appl. Biol. 129, 451–460.CrossRefGoogle Scholar
  27. Littell R C, Milliken G A, Stroup W W and Wolfinger R D 1996 SAS systems for mixed models. SAS Inst., Cary, N.C.Google Scholar
  28. Malinowski D P, Alloush G A and Belesky D P 1998a Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyteNeotyphodium coenophialum. Plant Soil 205, 1–12.CrossRefGoogle Scholar
  29. Malinowski D P, Alloush G A and Belesky D P 2000 Leaf endophyteNeotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 227, 115–126.CrossRefGoogle Scholar
  30. Malinowski D P and Belesky D P 1999a Endophyte infection enhances the ability of tall fescue to utilize sparingly available phosphorus. J. Plant Nutr. 22, 835–853.Google Scholar
  31. Malinowski D P and Belesky D P 1999b Infection with leaf fungal endophyteNeotyphodium coenophialum increases aluminum sequestration on root surfaces of tall fescue. J. Plant Nutr. 22, 1335–1349.Google Scholar
  32. Malinowski D P and Belesky D P 2000 Adaptations of endophyteinfected cool-season grasses to environmental stresses: Mechanisms of drought and mineral stress tolerance. Crop Sci. 40, 923–940.CrossRefGoogle Scholar
  33. Malinowski D P, Belesky D P, Hill N S, Baligar V C and Fedders J M 1998b Influence of phosphorus on the growth and ergot alkaloid content ofNeotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.). Plant Soil 198, 53–61.CrossRefGoogle Scholar
  34. Mira L, Fernandez M T, Santos M, Rocha R, Florêncio M H and Jennings K R 2002 Interactions of flavonoids with iron and copper ions: A mechanism for their antioxidant activity. Free Rad. Res. 36, 1199–1208.CrossRefGoogle Scholar
  35. Monnet F, Vaillant N, Hitmi A, Coudret A and Sallanon H 2001 EndophyticNeotyphodium lolii induced tolerance to Zn stress inLolium perenne. Physiol. Plantarum 113, 557–563.Google Scholar
  36. National Research Council 1996 Nutrient requirements of beef cattle. National Academy of Science. Washington, D.C.Google Scholar
  37. Oliver J W, Schulze A E, Rohrbach B W, Fribourg H A, Ingle T and Waller J C 2000 Alterations in hemograms and serum biochemical analytes of steers after prolonged consumption of endophyte-infected tall fescue. J. Anim. Sci. 78, 1029–1035.PubMedGoogle Scholar
  38. Parfitt R L 1979 The availability of P from phosphate-goethite bridging complexes. Desorption and uptake by ryegrass. Plant Soil 53, 55–65.CrossRefGoogle Scholar
  39. Pennell C and Ball O J-P 1999 The effects ofNeotyphodium endophytes in tall fescue on pasture mealy bug (Balanococcus poae).In Proc. 52nd N. Z. Plant Protection Conf. 9–13 August 1999. pp. 259–263. Auckland, N.Z.Google Scholar
  40. Popay A J, Baltus J G and Pennell G L 2001 Insect resistance in perennial ryegrass with toxin-freeNeotyphodium endophytes.In Proc. 4th Int.Neotyphodium/Grass Interaction Symposium. 27–29 September 2000. Eds. V H Paul and P D Dapprich. pp. 187–193. Soest, Germany.Google Scholar
  41. Powell R G, TePaske M R, Plattner R D, White J F and Clement S L 1994 Isolation of resveratrol fromFestuca versuta and evidence for the widespread occurrence of this stilbene in the Poaceae. Phytochem. 35, 335–338.CrossRefGoogle Scholar
  42. Römheld, V. 1991. The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: An ecological approach. Plant Soil 130, 127–134.Google Scholar
  43. Saker K E, Allen V G, Kalnitsky J, Thatcher C D, Swecker W S, Jr. and Fontenot J P 1998 Monocyte immune cell response and copper status in beef steers that grazed endophyte-infected tall fescue. J. Anim. Sci. 76, 2694–2700.PubMedGoogle Scholar
  44. Schosseler P M, Wehrli B and Schweiger A 1997 Complexation of copper(II) with carbonate ligands in aqueous solution: A cw and pulse EPR study. Inorg. Chem. 36, 4490–4499.PubMedCrossRefGoogle Scholar
  45. Stoszek M J, Mika P G, Oldfield J E and Weswig P H 1986 Influence of copper supplementation on blood and liver copper in cattle fed tall fescue or quackgrass. J. Anim. Sci. 62, 263–271.PubMedGoogle Scholar
  46. Stoszek M J, Oldfield J E, Carter G E and Weswig P H 1979 Effect of tall fescue and quackgrass on copper metabolism and weight gains of beef cattle. J. Anim. Sci. 48, 893–899.Google Scholar
  47. Suresh K and Subramanyam C 1998 Polyphenols are involved in copper binding to cell walls ofNeurospora crassa. J. Inorg. Biochem. 69, 209–215.CrossRefGoogle Scholar
  48. Tapper B A and Latch G C M 1999 Selection against toxin production in endophyte-infected perennial ryegrass.In Ryegrass endophyte: An essential New Zealand symbiosis. Eds. D R Woodfield and C Matthew. pp. 107–111. Grassl. Res. and Practice Ser. 7. New Zealand Grassl. Assoc., Palmerston North, New Zealand.Google Scholar
  49. Treeby M, Marschner H and Römheld V 1989 Mobilization of iron and other micronutrient cations from calcareous soil by plantborne, microbial and synthetic metal chelators. Plant Soil 114, 217–226.CrossRefGoogle Scholar
  50. Vazquez-de-Aldana B R, Garcia-Criado B, Zabalgogeazcoa I and Garcia-Ciudad A 1999 Influence of fungal endophyte infection on nutrient element content of tall fescue. J. Plant Nutr. 22, 163–176.CrossRefGoogle Scholar
  51. Wilkinson H H and Schardl C L 1997 The evolution of mutualism in grass-endophyte associations. InNeotyphodium. Eds. C W Bacon and N S Hill. pp. 13–25. Plenum Press, New York.Google Scholar
  52. Zhang Y J, Bryan N D, Livens F R and Jones M N 1996 Complexing of metal ions by humic substances. Humic and Fulvic Acids. ACS Symposium Series 651, 194–206.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • D. P. Malinowski
    • 1
  • H. Zuo
    • 1
  • D. P. Belesky
    • 2
  • G. A. Alloush
    • 3
  1. 1.Texas Agricultural Experiment StationTexas A&M UniversityVernonUSA
  2. 2.United States Department of Agriculture, Agricultural Research ServiceAppalachian Farming Systems Research CenterBeaverUSA
  3. 3.Department of Soil Science and Plant NutritionTishreen UniversityLattakiaSyria

Personalised recommendations