Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass

Abstract

Several endophytic fungi of the genus Neotyphodium form symbiotic associations with Lolium spp. grasses and are renowned for production of bioactive alkaloids such as ergot alkaloids. Some of these endophytes make their grass partners less suitable as hosts for endoparasitic nematodes, including Pratylenchus spp. The potential for ergot alkaloids to affect nematode motility was investigated in vitro. Ergovaline, the ergot alkaloid pathway end product of several Neotyphodium spp., was the only ergot alkaloid tested that inhibited motility of Pratylenchus scribneri. The association of ergot alkaloids with nematode population suppression was examined in glasshouse experiments with strains of the perennial ryegrass endophyte Neotyphodium sp. isolate Lp1 (syn. Neotyphodium lolii × Epichloë typhina) that have been genetically modified to lack ergot alkaloids or to have an altered ergot alkaloid profile. Populations of P. scribneri were significantly smaller in pots of perennial ryegrass containing the wild-type, ergot alkaloid-producing endophyte than in pots of endophyte-free perennial ryegrass. Elimination of certain complex ergot alkaloids (ergovaline and lysergic acid amides) in one gene knockout strain, or complete elimination of ergot alkaloids in another, did not affect the ability of the endophyte to suppress populations of nematode. Presence and concentrations of ergot alkaloids in pseudostems were as expected based on presence and genotype of endophyte in each plant, but frequently were undetectable or in low concentration in roots. The data indicate that ergot alkaloids do not contribute significantly to the endophyte-associated suppression of Pratylenchus spp.

The Effect of Endophytic Fungi on Nematode Populations in Summer-dormant and Summer-active Tall Fescue

“…Ky312 is a poor host for stunt and ring nematodes, but a good host for spiral nematode. In previous work, the wild type endophyte has been shown to suppress lesion nematode populations, (Timper et al, 2005;Panaccione et al, 2006;Bacetty et al, 2009;Timper and Bouton 2012), whereas Kimmons et al (1990) found no difference in spiral nematode numbers in pots containing either endophytefree or endophyte-infected (toxic) tall fescue. Results from this study support this previous study, but we also show no difference between TMQ+ (AR584 novel endophyte) and TMQ2.…”

“…Ergot alkaloid-producing endophytes have been shown to reduce population densities of lesion nematode (Pratylenchus scribneri) (Panaccione et al, 2006;Bacetty et al, 2009), whereas novel endophyte resistance to lesion nematodes in summer-active cultivars was dependent on the endophyte strain and the tall fescue cultivar (Timper et al, 2005). Comparison of a transgenic nonergot alkaloidproducing strain (deletion of the dmaW gene encoding the first step of ergot alkaloid production) to the wild type strain showed endophyte-associated suppression of P. scribneri in perennial ryegrass was still evident suggesting other mechanisms might be responsible for the suppression (Panaccione et al, 2006). Reduction in root-knot nematode (Meloidogyne marylandi) population densities by ergot alkaloid-producing endophyte infected tall fescue plants has also been reported (Elmi et al, 1999).…”

“…Reduction in root-knot nematode (Meloidogyne marylandi) population densities by ergot alkaloid-producing endophyte infected tall fescue plants has also been reported (Elmi et al, 1999). Each of these studies was conducted with summer-active tall fescue cultivars (Timper et al, 2005;Bacetty et al, 2009) or perennial ryegrass (Panaccione et al, 2006) and may not translate to effects seen with summer-dormant varieties. Therefore, our objective was to evaluate nematode population densities in novel endophyte-infected and endophyte-free summer-dormant and summer-active tall fescue compared to the common toxic endophyte-infected (Kentucky 31+) and endophyte-free summer-active tall fescue.…”

Fungal endophytes and their interaction with plant pathogens: a review

“…as those observed in ergot alkaloid producing strains (Timper et al, 2005). In contrast, other experiments showed that the amount of ergot alkaloids translocated to roots is very small, and experiments with Neotyphodium knockout mutants having their pathway of ergot alkaloid synthesis disrupted suggested that these alkaloids are not responsible for the inhibition of nematode populations in endophyte infected plants (Panaccione et al, 2006). Nevertheless, other types of alkaloids with antiherbivore activity are produced by Neotyphodium species, and chemical changes such as the production of phenolic compounds do occur in Neotyphodium-infected roots (Malinowski and Belesky, 2000).…”

Tall Fescue ‘Jesup (Max‐Q)’: Meloidogyne incognita Development in Roots and Nematotoxicity

“…Methanolic root extracts from E+ tall fescue Jesup (ergot alkaloid-producing endophyte; nonhost to P. scribneri) were nematostatic and repellant to P. scribneri when prepared from plants grown 45 d or more, whereas root extracts from E-tall fescue (no endophyte, susceptible plant) were attractive to the nematode (Bacetty et al, 2009a(Bacetty et al, , 2009b. Several purified ergot alkaloids, identified as compounds produced in Neotyphodiumassociated tall fescue and perennial ryegrass (Lolium perenne L.), were repellant to P. scribneri, and those that inhibited nematode motility were either nematotoxic or nematostatic (Panaccione et al, 2006;Bacetty et al, 2009aBacetty et al, , 2009b. It is interesting to note that even though alkaloids produced in the E+ plants could be nematotoxic, root extracts from these plants were not nematicidal to P. scribneri.…”