BSPP Presidential Meeting 1999

Biotic Interactions in Plant-pathogen Associations

Session II - Interactions with fungi

Epichlo grass endophytes and their interaction with a symbiotic fly.
Adrian Leuchtmann.

Geobotanisches Institut ETH, Zollikerstrasse 107, CH-8008 Zrich, Switzerland.

Epichlo grass endophytes (Ascomycota) and related asexual species form systemic associations with many pooid grasses in temperate regions of the Northern hemisphere. During sexual reproduction the fungus produces reproductive structures (stromata) on aborted host inflorescence referred to as choke disease. Host specific fungal species are self-incompatible (heterothallic) and need to be fertilized by spermatia of opposite mating type. The vector for transferring spermatia are specialized flies of genus Botanophila which ingest spermatia and pass them through their gut. Female flies lay eggs on young fungal stromata and after fertilization hatching larvae feed on developing perithecia as their exclusive food source. Thus, Botanophila flies live in a symbiotic relationship with Epichlo fungi, and dependence on stromata as food source should promote specialization (as a consequence of sexual incompatibility among different Epichlo taxa). Investigations were made to examine whether flies are specialized on host grasses and their Epichlo fungi, and how flies could recognize different hosts. Distribution of fly genotypes collected from different hosts did not indicate specific preference. However, field observations and the absence of mating among different host strains in experimental field plots clearly suggested specificity of flies. Volatile compounds collected and analyzed from infected host plants showed different patterns with each host association. Thus, volatiles could serve as specific attractants. We hypothesize that flies may be unspecific initially when hatching, then after first contact with a stroma learn to specifically recognize other stromata of the same host association.

Influence of virus spread on the outcome of interspecific hybridisation between fungal pathogens
Clive M. Brasier.

Forest Research Agency, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UK. 

Two highly destructive pandemics of Dutch elm disease have occurred across the Northern Hemisphere this century. Each has been caused by the spread of a different, introduced ascomycete pathogen. First to appear, in the early 1900s, was the moderately aggressive Ophiostoma ulmi. This was followed, from the 1940s onwards, by the spread of the highly aggressive O. novo-ulmi, which has rapidly replaced the O. ulmi in the process. Interspecific hybridisation in fungi is considered rare, but several lines of evidence show that interspecific hybridisation has occurred between O. ulmi and O. novo-ulmi during the replacement period; although the resulting hybrids are transient and unfit.

When O. novo-ulmi arrived in Europe, the resident O. ulmi population was highly heterogenic with regard to vegetative compatibility (vc) loci and mating type. In contrast, the immigrant O. novo-ulmi spread initially as single vegetative compatibility type/single mating type clones. Thereafter, the O. novo-ulmi population rapidly (5-6 yr) became heterogenic for vc types and mating type and the clones disappeared. In North America, however, similar O. novo-ulmi clones survived much longer (50 yr); and the rate of appearance of new vc types/mating types has been slow. In New Zealand, an immigrant vc clone has survived 10 yr without significant genetic change.

Underlying differences between the European, North American and New Zealand situations indicate (i) that O. ulmi must be present for the heterogenenicity to occur in the O. novo-ulmi population; (ii) that deleterious fungal viruses must be abundant in the O. novo-ulmi clones for the change to heterogenenicity to be rapid; (iii) that it is the spread of the viruses that favours the survival of the new vc types over the original vc clone.

Research in progress (M. Paoletti, K. W. Buck and C. M. Brasier, unpublished) is consistent with a hypothesis that the new vc loci, and possibly also new mating type loci, are acquired by the O. novo-ulmi clones from O. ulmi through introgression. Virus pressure, therefore, appears to be a significant influence on the outcome of a major fungal hybridisation event.

Fungal endophytes and nematodes of agricultural and amenity grasses
Roger Cook and 2Graham.C. Lewis
Institute of Grassland and Environmental Research, Aberystwyth, Ceredigion, SY23 3EB, Wales, UK.
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Institute of Grassland and Environmental Research, North Wyke, Okehampton, Devon, EX20 2SB, UK

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.

Feeding on plant-pathogenic fungi by invertebrates: relationships to saprophytic and mycorrhizal systems
Terence P. McGonigle & M. Hyakumuchi.
Faculty of Agriculture, Gifu University, Gifu 501-1193, Japan.

What is the significance of grazing on plant-pathogenic fungi by invertebrates? Such grazing certainly occurs, but the extent to which it modifies pathogenic interactions is unclear. Here, we consider feeding on fungi in broad terms by arthropods, nematodes, annelids, and protozoa. Understanding the impact of feeding is important when extending laboratory data on plant-pathogen interactions into the field. A summary of relevant published studies from pathogenic systems will be made. These studies will then be evaluated in terms of what can be learned from saprotrophic and mycorrhizal systems, as outlined below. Grazing can affect ecosystem function and fungal community structure. Effects on saprotrophic and mycorrhizal systems can be direct, such as by the excretion of nitrogen from the bodies of the grazers, which contributes to mineralisation. Indirect effects are possible as by the action of comminution and mixing of substrate, inoculum dispersal, and changes in vigour of the grazed fungus, all of which can modify mineralisation or immobilisation by the microbes. These indirect effects on mineralisation are important for saprotrophic fungi, but they may also be relevant for certain mycorrhizal fungi with limited saprotrophic capabilities. Effects of grazing on the collection of nutrients from soil and the transfer of them to the plant in mycorrhizal systems are mostly negative. However, at low animal densities a stimulation of mycorrhizal function can occur, which is perhaps related to a stimulation of fungal activity. Available data for effects on fungal community structure are mostly for saprotrophic systems. Under controlled conditions, selective grazing has been shown to modify fungal communities by either suppression of a fungus that was otherwise dominant, or by further polarising competitive interactions by grazing on less-dominant fungi. These processes serve to increase and reduce fungal diversity, respectively. Further, grazing can act to facilitate the transition of fungal communities from early to late stages of succession. Conclusions relevant to pathogenic systems will be drawn, and these will be discussed in terms of the co-occurrence of pathogenic, saprotrophic, and mycorrhizal fungi through the connected pathway of soil, root, shoot, and air.