Fifty years ago I did my PhD researching an ascomycete fungus Epichloe typhinaand published some of the results in Transactions of the British Mycological Society (Kirby, 1961). Recently during a Mushroom and Toadstool walk on Westleton Common, Sheila Francis mentioned that she had seen a citation to my paper in a recent paper by Spooner & Kemp (2005). I had given up any study of the fungus after the paper was published to concentrate on the physiology of flowering in the cereals and grasses and so I was intrigued to find out how my work was still relevant. What I found was great changes in basic mycology, fungus systematics and the understanding of fungal sexuality.

I became interested in Epichloe typhina which causes choke of grasses as a schoolboy. It chokes off the grass inflorescence with a fungal stroma which in the later stages turns bright orange. Leicestershire, where I lived, was a county of long established permanent pasture and the fungus was widespread, particularly in ungrazed areas. I tried digging up infected plants and planting them in pots in the garden and found that the grass plant appeared healthy and vigorous while vegetative but the fungus reappeared in successive years when the grass flowered. This, combined with a developing interest in the effect of day-length on flowering (photoperiodism), led me to persuade the scholarship awarders that it was a suitable research topic for an aspiring young PhD student.

‘In my time’ there was one species of Epichloe, infecting a range of perennial grasses. It was not known how it spread from plant to plant and I think that I had a naïve impression that the endophyte fungus formed a stroma which produced conidia before the ascospore producing perithecia. I made no progress with plant to plant infection methods but I was able to show that in the vegetative plant the fungus was a benign endophyte with sparse hyphae growing between the cells of the plant tissue, but in the very early stages of floral initiation (long before the stem elongated and the inflorescence was visible) the fungus became rampant and formed a mass of hyphae. This generally completely choked the inflorescence, although the degree to which this occurred could be affected by artificially prolonging the day-length, which speeded up flowering and allowed the inflorescence to wholly or partially escape from the fungus.

There I left Epichloe typhina and apart from noticing a paper from the Welsh Plant Station at Aberystwyth which applied my ideas to induce severely infected lines of cocksfoot to flower and produce seed, I forgot about Epichloe. Oh, how things have changed! Epichloe has been split into six or more species, each specific to one or a few species of grass, the infection method and the sexuality have been worked out and the effect on grass growth and grazing animals has been established.

Of most interest to naturalists (and this is the main point of the story) is the relationship between the grass and the fungus, the sexuality of the fungus and a small fly. Epichloe is heterothallic and needs the union of two mating types to produce ascospores. The role of the fly, Botanophila sp. (Anthomyiidae) which lays its eggs on the fungal stroma, is to transfer spermatia (gametes), which are formed on the stroma, from one mating type to another. Feeding on the stroma it eats spermatia; later visiting another plant with a stroma of a different mating type it deposits spermatia, which pass unaffected through its gut, in its faeces where they may come into contact with the receptive hyphae of the developing perithecia of another mating type. Union of the gametes is followed by meiosis and the stroma turns bright orange and produces eight needle-shaped ascospores which are ejected and may infect other plants. The larvae of the fly feed on the fungus, concealing themselves in chambers made in the stroma.

This remarkable mutualistic association involving Epichloe, a grass plant, and a fly is another complex relationship similar to the one described by Peter Payne (White Admiral 70; 20) involving a mycorrhizal fungus, a tree and an orchid. Such associations provoke questions about how the balance between the different members is maintained. Why do not the fly larvae eat large portions of the stroma and reduce the spore output of the fungus or the parasitic orchid kill the mycorrhizal fungus? And in the Darwin centenary year we may perhaps reflect on how such complex relationships evolve. Some of the questions are within the scope of the garden naturalist. A close watch on the infected Holcus mollis plants in my garden to look at numbers of Botanophila larvae and their enemies is indicated for 2009.

References
Kirby, E. J. M. (1961). Host-parasite relations in the choke disease of grasses. Transactions of the British Mycological Society 44: 493 - 503.
Spooner, B. M. & S. L. Kemp (2005). Epichloe in Britain. Mycologist 19: 82-87.