Fungal endophytes and nematodes of agricultural and amenity grasses

In grasses, obligate mutualist fungal endophytes (Neotyphodium spp.) have ecological and economic significance because of the impact of fungal secondary metabolites on herbivores. These endophytes infect leaves and stems of healthy plants but have no marked pathogenic effects. A range of insect herbivores, including sap sucking aphids as well as biting herbivores, is affected by endophytes in tall fescue and perennial ryegrass. Endophyte-infected grasses can also cause toxicoses in grazing livestock. As well as protecting the plant from herbivory, these endophytes can increase plant yield, enhance root growth and modify water relations. Evidence for the effects of grass endophytes on root feeding nematodes is equivocal, perhaps reflecting the variety of interactions. None the less, there are striking examples of endophyte-infected grasses expressing very effective resistance to nematodes, not found in the endophyte-free host. These examples include nematodes for which natural genetic host resistance has proven elusive or difficult to manipulate. This article reviews relationships between Neotyphodium grass endophytes and root parasitic and other nematodes associated with grasslands. We review Lolium spp. and Festuca arundinacea and F. pratensis all native to Europe, temperate Asia, and North Africa. The more interesting phenomena involving endophytes are reported from countries where such grass species have been introduced, for example, from tall fescue in the United States of America and from perennial ryegrass, L perenne, in New Zealand. The review of nematode/endophyte interactions is grouped according to the mode of parasitism of the nematode concerned. It seems clear that to be affected by endophytes, nematodes must feed on endophyte-infected plants, perhaps ingesting toxins. Some nematodes may be tolerant of the toxins or may through their feeding habits or sites, avoid exposure to translocated toxins. In some case, the responses of plants to endophyte, such as wall thickening or anti-drought responses, may indirectly affect their host status for particular nematodes. The endophyte associations are maintained in USA and New Zealand grasses because of their beneficial features. In contrast, European bred forage grass cultivars generally have little or no endophyte infection. The symbiotic interaction is very complex with a good deal of variability. Future studies of endophyte impacts on nematodes should take account of the causes of variability in the interactions. This requires standardisation of grass genotype and fungus strain as well as biochemical characterisation of the combination. Environmental conditions need either to be controlled or at least measured to relate to effects on alkaloid production. It is also important to describe the feeding site and processes of the nematodes being studied. Control of these aspects will allow the development of experimental systems to test hypotheses about the relationship between parasite attributes and susceptibility to endophytes. Such studies have clear potential economic value, given that some combinations of grass and fungus provide fully effective resistance to nematodes not readily controlled either by natural genetic resistance or by other means. The use of selected endophytes on heterogeneous grass populations may offer durable control of nematodes to the benefit both of forage and amenity grass and to crops grown in rotations.