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

Abstract

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 nonexpression (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.

Variable Effects of Grass-Neotyphodium Associations on Cereal Leaf Beetle (Coleoptera: Chrysomelidae) Feeding, Development and Survival

“…Of note, however, is that incidental infestations of R. padi were repeatedly observed only on E-potted plants among E+ potted plants on a greenhouse bench (SL Clement, personal observations); thus, E+ W6 23409 may exhibit strong aphid repellent properties under some conditions. Loline alkaloid production by E+ tall fescue and meadow ryegrass, Lolium pratense (= meadow fescue, Festuca pratensis), has been associated with R. padi deterrence (Wilkinson et al 2000), leading to suggestions that grass-endophyte symbiota producing lolines could potentially be used to influence BYDV transmission in agricultural settings (Eichenseer et al 1991;Bultman and Bell 2003). Prior studies also showed that damaged E+ plants of tall fescue (Bultman et al 2004;Sullivan et al 2007) and Glyceria striata (Gonthier et al 2008) were more resistant to R. padi than undamaged E+ tests plants of both grasses.…”

Molecular Plant-Microbe Interactions That Cut the Mustard

“…There are also many endosymbiotic fungi, most notably in grasses, that increase plant growth and they have an added interesting feature in that many produce alkaloids with insecticidal activity (Wilkinson et al, 2000). This again illustrates the intricate and diverse complexity of plant-microbe interactions because it suggests that plant endosymbionts can have an added evolutionary advantage for the plant by deterring insect attack.…”

Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery

“…Peramine is an insect feeding deterrent and protects perennial ryegrass from the Argentine stem weevil, Listronotus bonariensis, a highly destructive insect pest in New Zealand (Rowan and Latch 1994;Tanaka et al 2005). Lolines are potent insecticidal and anti-aphid agents, not being implicated in any mammalian toxicoses (Jackson et al 1996;Wilkinson et al 2000). Obviously, the last of the aforementioned groups of alkaloids should provide for the most promising candidates to aid the agricultural arena.…”

“…Unique not only in structure, comprising a saturated 1-aminopyrrolizidine-ring system, with a highly strained ether bridge between C-2 and C-7 (Figure 10) (Petroski et al 1989), but also due to their potent, broad-spectrum insecticidal activities (Jackson et al 1996;Wilkinson et al 2000), loline alkaloids have remained a biosynthetic enigma till very recently (Blankenship et al 2005).…”