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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Animal and Plant Health Inspection Service 2000 Serum copper concentrations of U.S. beef cattle. USDA Veterinary Services Information Sheet.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Bush L P, Wilkinson H H and Schardl C L 1997 Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol. 114, 1–7.
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.
Clay K and Schardl C 2002 Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist. 160 (Suppl.), 99–127.
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.
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.
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.
Fletcher L R and Harvey I C 1981 An association of aLolium endophyte with ryegrass staggers. New Zeal. Vet. J. 32, 185–186.
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.
Hewitt E J 1966 Sand and water culture methods used in the study of plant nutrition. Eastern Press, London.
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.
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.
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.
Justus M, Witte L and Hartmann T 1997 Levels and tissue distribution of loline alkaloids in endophyte-infectedFestuca pratensis. Phytochem. 44, 51–57.
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.
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.
Littell R C, Milliken G A, Stroup W W and Wolfinger R D 1996 SAS systems for mixed models. SAS Inst., Cary, N.C.
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.
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.
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.
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.
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.
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.
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.
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.
National Research Council 1996 Nutrient requirements of beef cattle. National Academy of Science. Washington, D.C.
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.
Parfitt R L 1979 The availability of P from phosphate-goethite bridging complexes. Desorption and uptake by ryegrass. Plant Soil 53, 55–65.
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.
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.
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.
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.
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.
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.
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.
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.
Suresh K and Subramanyam C 1998 Polyphenols are involved in copper binding to cell walls ofNeurospora crassa. J. Inorg. Biochem. 69, 209–215.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Malinowski, D.P., Zuo, H., Belesky, D.P. et al. Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected withNeotyphodium spp. endophytes. Plant Soil 267, 1–12 (2004). https://doi.org/10.1007/s11104-005-2575-y
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11104-005-2575-y