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Contribution of Fungal Loline Alkaloids to Protection from Aphids in a Grass-Endophyte Mutualism

October 2000 , Volume 13 , Number  10
Pages  1,027 - 1,033

Heather H. Wilkinson , 1 Malcolm R. Siegel , 1 Jimmy D. Blankenship , 1 Allison C. Mallory , 1 Lowell P. Bush , 2 and Christopher L. Schardl 1

1Department of Plant Pathology, University of Kentucky, Lexington 40546-0091, U.S.A.; 2Department of Agronomy, University of Kentucky, Lexington 40546-0091, U.S.A.

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Accepted 17 May 2000.

Fungal endophytes provide grasses with enhanced protection from herbivory, drought, and pathogens. The loline alkaloids (saturated 1-aminopyrrolizidines with an oxygen bridge) are fungal metabolites often present in grasses with fungal endophytes of the genera Epichloë or Neotyphodium. We conducted a Mendelian genetic analysis to test for activity of lolines produced in plants against aphids feeding on those plants. Though most loline-producing endophytes are asexual, we found that a recently described sexual endophyte, Epichloë festucae, had heritable variation for loline alkaloid expression (Lol+) or non-expression (Lol¯). By analyzing segregation of these phenotypes and of linked DNA polymorphisms in crosses, we identified a single genetic locus controlling loline alkaloid expression in those E. festucae parents. We then tested segregating Lol+ and Lol¯ full-sibling fungal progeny for their ability to protect host plants from two aphid species, and observed that alkaloid expression cosegregated with activity against these insects. The in planta loline alkaloid levels correlated with levels of anti-aphid activity. These results suggested a key role of the loline alkaloids in protection of host plants from certain aphids, and represent, to our knowledge, the first Mendelian analysis demonstrating how a fungal factor contributes protection to plant-fungus mutualism.

Additional keywords: amplified fragment length polymorphism (AFLP), Festuca, Lolium spp., Rhopalosiphum padi, Schizaphis graminum.

© 2000 The American Phytopathological Society