Fungal loline alkaloids in grass–endophyte associations confer resistance to the rice leaf bug, Trigonotylus caelestialium

Abstract

Plant symbiotic fungi (endophytes) of the genus Neotyphodium [anamorphs, asexual derivatives of Epichloë (Ascomycota: Clavicipitaceae)] often associate with grass species of the subfamily Pooideae, which includes important forage and turf species. These endophytes are known to produce a range of alkaloids that enhance their host's resistance to insects or are toxic to grazing animals. Among the alkaloids, loline alkaloids (saturated 1-aminopyrrolizidines) are generally observed in the highest concentrations in many Neotyphodium -grass symbiotic associations, and are known to be toxic to insects but not to mammals. Some Neotyphodium -infected grasses have enhanced resistance to rice leaf bug, Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae), one of the major pests for rice production in Japan. Our laboratory experiments quantified the effects of purified loline ( N-formylloline) and in planta synthesis of loline alkaloids by meadow fescue [ Lolium pratense (Huds.) S.J. Darbyshire (syn. Festuca pratensis Huds.)]-Neotyphodium uncinatum (Gams, Petrini & Schmidt) Glenn, Bacon & Hanlin and Italian ryegrass ( Lolium multiflorum Lam.)-Neotyphodium occultans Moon, Scott & Christensen associations on the development and survival of T. caelestialium . No-choice feeding assays with laboratory populations of the insect revealed that their growth was significantly decreased by the infected grasses, and the effect was greater for N. uncinatum than for N. occultans , in keeping with differences in N-formylloline concentrations in the plants. Artificial feeding of N-formylloline through feeding sachets indicated that the chemical has an adverse effect on survival of larvae, even at the lowest concentration tested (50 μ g/g), which was considerably lower than the typical concentrations in many Neotyphodium -grass association s . The results confirmed the ability of Neotyphodium -infected forage grasses to control T. caelestialium propagation in meadows, which may cause damages to nearby rice paddies.

Evaluating the fungal endophyte Neotyphodium occultans for resistance to the rice leaf bug, Trigonotylus caelestialium, in Italian ryegrass, Lolium multiflorum

“…Some N. occultans-infected Italian ryegrass used in this study showed excellent resistance to T. caelestialium, similar to N. lolii-infected perennial ryegrass (Shiba & Sugawara, 2005) and N. uncinatum-infected meadow fescue (Shiba & Sugawara, 2009). The feeding preference and the survival rate of this insect were considerably lower on infected plants than on uninfected ones, and the higher the in planta N-formylloline concentration, the greater the adverse effects on the insect.…”

“…This hypothesis is derived from the toxic effect of the chemical to the insect as indicated by the force feeding of the purified chemical performed in Shiba & Sugawara (2009). Significant correlation between N-formylloline concentration in plants and the survival of the insects was observed when they were reared on the inflorescences of N. occultans-infected Italian ryegrass. These results indicate that N. occultans-infected Italian ryegrass deterred feeding of T. caelestialium.…”

“…Perennial ryegrass, Lolium perenne L., with Neotyphodium lolii (Latch, Christensen & Samuels) Glenn, Bacon & Hanlin shows a strong feeding deterrence to T. caelestialium, and all larvae on infected leaves died from starvation (Shiba & Sugawara, 2005). Artificial feeding of purified N-formylloline indicated that the chemical has an adverse effect on survival of the insect, even at lower concentrations than typically present in many Neotyphodium-grass associations (Shiba & Sugawara, 2009). N-formylloline, the most abundant loline alkaloid produced by Neotyphodium endophytes, has been shown to confer resistance to this insect species.…”

Effects of alkaloids from fungal endophytes in grass–Epichloëassociations on survival of the sorghum plant bug (Stenotus rubrovittatus)

“…The survival of S. rubrovittatus fed on the N ‐formylloline was investigated using a membrane‐feeding assay as described previously (Shiba and Sugawara ). Purified N ‐formylloline (extracted and purified from endophyte‐infected meadow fescue [ Festuca pratensis Huds.…”

“…(). The Epichloë ‐produced alkaloid, N ‐formylloline, has been shown to confer resistance to this insect species on the host grasses, concentration dependently (Shiba and Sugawara ; Shiba et al . ).…”