Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant

Ecology Letters

Volumn 8, Issue 12, 2005, Pages 1256-1263

  Lehtonen, Päivi ^a   Helander, Marjo ^a   Wink, Michael ^b   Sporer, Frank ^b   Saikkonen, Kari ^a,c  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c PLANT PRODUCTION RESEARCH   (Finland)

Author keywords

Alkaloids; Endophytic fungi; Hemiparasite; Herbivory; Lolium; Multitrophic interactions; Mutualism; Neotyphodium; Parasitism; Rhinanthus

Indexed keywords

ALKALOID; ENDOPHYTE; FUNGUS; GRASS; HEMIPARASITE; HERBIVORE; TROPHIC INTERACTION;

APHIDIDAE; AULACORTHUM SOLANI; BACTERIA (MICROORGANISMS); FUNGI; LOLIUM; NEOTYPHODIUM; NEOTYPHODIUM UNCINATUM; RHINANTHUS; RHINANTHUS SEROTINUS; SCHEDONORUS PRATENSIS;

EID: 28644449337     PISSN: 1461023X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2005.00834.x     Document Type: Article

References (58)

1. Adler, L.S. (2000). Alkaloid uptake increases fitness in a hemiparasitic plant via reduced herbivory and increased pollination. Am. Nat., 156, 92-99.
2. Adler, L.S. (2002). Host effects on herbivory and pollination in a hemiparasitic plant. Ecology, 83, 2700-2710.
3. Adler, L.S. (2003). Host species affects herbivory, pollination and reproduction in experiments with parasitic Castilleja. Ecology, 84, 2083-2091.
4. Adler, F.R. & Karban, R. (1994). Defended fortresses or moving targets -another model of inducible defenses inspired by military metaphors. Am. Nat., 144, 813-832.
5. Adler, L.S. & Wink, M. (2001). Transfer of alkaloids from hosts to hemiparasites in two Castilleja-Lupinus associations: analysis of floral and vegetative tissues. Biochem. Syst. Ecol., 29, 551-561.
6. Adler, L.S., Karban, R. & Sharon, S.Y. (2001). Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology, 82, 2032-2044.
7. Ahlholm, J.U., Helander, M., Lehtimäki, S., Wäli, P. & Saikkonen, K. (2002). Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos, 99, 173-183.
8. Amsler, C.D., McClintock, J.B. & Baker, B.J. (2001). Secondary metabolites as mediators of trophic interactions among Antarctic marine organisms. Am. Zool., 41, 17-26.
9. Bacon, C.W. (1993). Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric. Ecosyst. Environ., 44, 123-141.
10. Bekker, R.M., Verweij, G.L., Bakker, J.P. & Fresco, L.F.M. (2000). Soil seed bank dynamics in hayfield succession. J. Ecol., 88, 594-607.
11. Blackman, R.L. & Eastop, V.F. (2000). Aphids on the World's Crops. An Identification and Information Guide, 2nd edn. Wiley & Sons, Chichester.
12. Boros, C.A., Marshall, D.R., Caterino, C.R. & Stermitz, F.R. (1991). Chemistry of the Scrophulariaceae.18. Iridoid and phenylpropanoid glycosides from Orthocarpus spp alkaloid content as a consequence of parasitism on Lupinus. J. Nat. Prod., 54, 506-513.
13. Breen, J.P. (1993). Enhanced resistance to three species of aphids (Homoptera: Aphididae) in Acremonium endophyte-infected turfgrasses. J. Econ. Entomol., 86, 1279-1286.
14. Buitenhuis, R., Vet, L.E.M., Boivin, G. & Brodeur, J. (2005). Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids. Entomol. Exp. Appl., 114, 107-117.
15. Cheplick, G.P. & Clay, K. (1988). Acquired chemical defenses in grasses - the role of fungal endophytes. Oikos, 52, 309-318.
16. Clay, K. (1990). Comparative demography of three graminoids infected by systemic, clavicipitaceous fungi. Ecology, 71, 558-570.
17. Clay, K. & Holah, J. (1999). Fungal endophyte symbiosis and plant diversity in successional fields. Science, 285, 1742-1744.
18. Clay, K. & Schardl, C. (2002). Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat., 160, S99-S127.
19. Doebeli, M. & Knowlton, N. (1998). The evolution of interspecific mutualisms. Proc. Natl. Acad. Sci. USA, 96, 8676-8680.
20. Faeth, S.H. (2002). Are endophytic fungi defensive plant mutualists? Oikos, 98, 25-36.
21. Faeth, S.H. & Sullivan, T.J. (2003). Mutualistic asexual endophytesin a native grass are usually parasitic. Am. Nat., 161, 310-325.
22. Gange, A.C., Bower, E. & Brown, V.K. (2002). Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia, 131, 103-112.
23. Gange, A.C., Brown, V.K. & Aplin, D.M. (2003). Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol. Lett., 6, 1051-1055.
24. Gibson, C.C. & Watkinson, A.R. (1989). The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia, 78, 401-406.
25. Heie, O.E. (1994). The Aphidoidea (Hemiptera) of Fennoscandia and Denmark V. Fauna Entomologica Scandinavica, Vol. 28. Brill, Leiden.
26. Kelly, C.K. (1992). Resource choice in Cuscuta europea. Proc. Natl. Acad. Sci. USA, 89, 12194-12197.
27. Kelly, C.K. & Horning, K. (1999). Acquisition order and resource value in Cuscuta attenuate. Proc. Natl. Acad. Sci. USA, 96, 13319-13322.
28. Kemmers, R.H., van Delft, S.P.J., Madaras, M., Hoosbeek, M., Vos, J. & van Breemen, N. (2004). Ecopedological Explorations of Three Calcareous Rich Fens in the Slovak Republic. Alterra-rapport 887, Alterra. Green World Research, Wageningen.
29. Lehtonen, P., Helander, M. & Saikkonen, K. (2005). Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia, 142, 38-45.
30. Marvier, M.A. (1996). Parasitic plant-host interactions: plant performance and indirect effects on parasite-feeding herbivores. Ecology, 77, 1398-1409.
31. Marvier, M.A. (1998). A mixed diet improves performance and herbivore resistance of a parasitic plant. Ecology, 79, 1272-1280.
32. Morris, W.F. (1996). Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology, 77, 1451-1462.
33. Omacini, M., Chaneton, E.J., Ghersa, C.M. & Muller, C.B. (2001). Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature, 409, 78-81.
34. Polunin, O. (1969). Flowers of Europe. Oxford University Press, London.
35. Press, M.C. (1989). Autotrophy and heterotrophy in root hemi-parasites. Trends Ecol. Evol., 4, 258-263.
36. Press, M.C. & Graves, J.D. (1995). Parasitic Plants. Chapman & Hall, London.
37. Press, M.C. & Phoenix, G.K. (2005). Impacts of parasitic plants on natural communities. New Phytol., 166, 737-751.
38. Puustinen, S. & Mutikainen, P. (2001). Host-parasite-herbivore interactions: implications of host cyanogenesis. Ecology, 82, 2059-2071.
39. Saikkonen, K. (2000). Kentucky-31, far from home. Science, 287, 1887.
40. Saikkonen, K., Faeth, S.H., Helander, M. & Sullivan, T.J. (1998). Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst., 29, 319-343.
41. Saikkonen, K., Helander, M., Faeth, S.H., Schulthess, F. & Wilson, D. (1999). Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia, 121, 411-420.
42. Saikkonen, K., Ahlholm, J., Helander, M., Lehtimäki, S. & Niemeläinen, O. (2000). Endophytic fungi in wild and cultivated grasses in Finland. Ecography, 23, 360-366.
43. Saikkonen, K., Wäli, P., Helander, M. & Faeth, S.H. (2004). Evolution of endophyte-plant symbioses. Trends Plant Sci., 9, 275-280.
44. Salonen, V. & Lammi, A. (2001). Effects of root hemiparasitic infection on host performance: Reduced flower size and increased flower asymmetry. Ecoscience, 8, 185-190.
45. Salonen, V., Setälä, H. & Puustinen, S. (2000). The interplay between Pinus sylvestris, its root hemiparasite Melampyrum pratense, and ectomycorrhizal fungi: Influences on plant growth and reproduction. Ecoscience, 7, 195-200.
46. Schardl, C.L., Leuchtmann, A. & Spiering, M.J. (2004). Symbiosis of grasses with seedborne fungal endophytes. Annu. Rev. Plant. Biol., 55, 315-340.
47. Schneider, M.J. & Stermitz, F.R. (1990). Uptake of host plant alkaloids by root parasitic Pedicularis species. Phytochemistry, 29, 1811-1814.
48. Scriber, J.M. (1983). Host-plant suitability (1984). In: Chemical Ecology of Insects (eds Bell, W.J. & Carde, R.T.). Chapman & Hall, New York, NY, pp. 159-204.
49. Siegel, M.R. & Bush, L.P. (1996). Defensive chemicals in grass-fungal endophyte associations. Recent Adv. Phytochem., 30, 81-118.
50. Siegel, M.R. & Bush, L.P. (1997). Toxin production in grass/endophyte associations. In: The Mycota. V. Plant Relationships, Part A (eds Carroll, G.C. & Tudzynski, P.). Springer-Verlag, Berlin, pp. 185-207.
51. Simms, E.L. & Taylor, D.L. (2002). Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr. Comp. Biol., 42, 369-380.
52. Strauss, S.Y. & Irwin, R.E. (2004). Ecological and evolutionary consequences of multispecies plant-animal interactions. Ann. Rev. Ecol. Evol., 35, 435-466.
53. Thompson, J.N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, IL.
54. Tofern, B., Kaloga, M., Witte, L., Hartmann, T. & Eich, E. (1999). Occurrence of loline alkaloids in Argyreia mollis (Convolvulaceae). Phytochemistry, 51, 1177-1180.
55. West, S.A., Kiers, E.T., Simms, E.L. & Denison, R.F. (2002). Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc. R. Soc. Lond. B, 269, 685-694.
56. Westbury, D.B. (2004). Rhinanthus minor L. J. Ecol., 92, 906-927.
57. Woldemichael, G.M. & Wink, M. (2002). Concomitant occurrence of pyrrolizidine and quinolizidine alkaloids in the hemiparasite Osyris alba L. (Santalaceae). Biochem. Syst. Ecol., 30, 264-276.
58. Wootton, J.T. (1993). Indirect effects and habitat use in an intertidal community - interaction chains and interaction modifications. Am. Nat., 141, 71-89.