Summary 1 Summary All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.

https://courses.washington.edu/cfr523/documents/2009TansleyReview.pdf

Fungal endophytes: diversity and functional roles.

Mutualistic interactions between species are receiving increased attention from ecologists, although research lags far behind analogous work on competition or predator-prey interactions. Most research has focused on rather showy mutualisms such as pollination or fruit dispersal and has suggested that mutualisms are more important in tropical communities than in temperate communities (67). Plant-microbial mutualisms, in contrast, have prompted little ecological research. Plant-microbial associations are more difficult to observe and manipulate than plant-animal associations. Many plants are always infected (e.g. legumes by rhizobia, forest trees by mycorrhizal fungi), so it is easy to consider the microorganisms merely as a special type of plant organ. Further, plant-microbial mutualisms historically have been outside the realm of ecology, in other areas of biology like microbiology and mycology. Recent research has revealed a widespread mutualistic association between grasses, our most familiar and important plant family, and endophytic fungi. Asymptomatic, systemic fungi that occur intercellularly within the leaves, stems, and reproductive organs of grasses have dramatic effects on the physiology, ecology, and reproductive biology of host plants. Through the production of toxic alkaloids, endophytic fungi defend their host plants against a wide range of insect and mammalian herbivores. Poisoning of domestic livestock has spurred a great deal of research on endophytic fungi in pasture grasses. This research has shown clearly that plants benefit from

Fungal endophytes of grasses.

The occurrence of the alkaloidsN-formyl andN-acetyl loline, peramine, lolitrem B, and ergovaline and the response of aphids to plants containing these compounds were determined in species and cultivars ofFestuca,Lolium, and other grass genera infected with fungal endophytes (Acremonium spp., andEpichloe typhina). Twenty-nine of 34 host-fungus associations produced one or more of the alkaloids, most frequently peramine or ergovaline. Three alkaloids (lolines, peramine, and ergovaline) were found in tall fescue and in perennial ryegrass infected withA. coenophialum, while peramine, lolitrem B, and ergovaline were present in perennial ryegrass and in tall fescue infected withA. lolii and inF. longifolia infected withE. typhina. WhileA. coenophialum andA. lolii produced similar patterns of alkaloids regardless of the species or cultivar of grass they infected, isolates ofE. typhina produced either no alkaloids or only one or two different alkaloids in the grasses tested. Aphid bioassays indicated thatRhopalosiphum padi andSchizaphis graminum did not survive on grasses containing loline alkaloids and thatS. graminum did not survive on peramine-containing grasses. Ergovaline-containing grasses did not affect either aphid.

Fungal endophyte-infected grasses: Alkaloid accumulation and aphid response.

https://www.cell.com/trends/plant-science/pdf/S1360-1385(06)00188-9.pdf

Model systems in ecology: dissecting the endophyte–grass literature

Synthesis of natural products containing the pyrrolic ring.

Infection of ryegrass (Lolium perenne) by an endophytic fungus (Acremonium loliae) confers resistance against the Argentine stem weevil (Listronotus bonariensis). Extracts from ryegrass clones, infected and uninfected with A. loliae, were compared in a feeding choice bioassay, and several fractions were identified which affected stem weevil feeding behavior. One stem weevil feeding deterrent, peramine C12H17N5O, has been isolated from infected ryegrass and partially characterized as a basic indole derivative. Extracts from culturedA. loliae had no effect on stem weevil feeding behavior nor was peramine detected in the fungal cultures examined. Peramine and the other active substances are hydrophilic in contrast to the lipophilic properties reported for the neurotoxic lolitrems also isolated from ryegrass infected with A. loliae and associated with causing ryegrass staggers disorder in livestock. It is suggested that ryegrass staggers and stem weevil feeding deterrency may arise by different biochemical mechanisms.

D L Gaynor

Papers

Isolation of feeding deterrents against argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae.