Concepts in Fungal Nutrition and the Origin of Biotrophy

Summary 1. Since use of the terms, symbiosis and obligate parasitism, is ambiguous, an attempt is made to re‐impose precision by a re‐evaluation of basic concepts. 2. For symbiosis, there should be a return to a concept closer to that of de Bary's original, embracing those parasitic and mutualistic associations which involve permanent, intimate contact. 3. Culturability should be abandoned as a criterion for classifying fungal behaviour. 4. Instead of culturability, emphasis should be placed on the ecological and nutritional behaviour of fungi, permitting the recognition of five groups: obligate saprotrophs, facultative necrotrophs, obligate necrotrophs, facultative biotrophs and obligate biotrophs. 5. Since environmental conditions can determine whether the nutrition of a fungus is biotrophic or necrotrophic, a scheme, speculative but amenable to experimental test, for the origin of biotrophy is proposed. This involves the interplay of alterations to patterns of translocation produced by fungally‐induced changes in hormonal balance in infected plants and catabolite repression of degradative enzymes of the fungus. 6. The dependence of mutualistic symbiosis on the maintenance of biotrophy is stressed. 7. Based on the nutrition of the diverse kinds of fungi involved in mycorrhizas, a re‐alignment of groupings of mycorrhizal associations is proposed. This directs research towards seeking generalizations within, and differences between, four clearly defined groups (sheathing, vesicular‐arbuscular, orchidaceous and ericaceous) instead of, as at present, within and between two (variously termed ectotrophic and endotrophic or ectomycorrhiza and endomycorrhiza), the second of which is highly artificial. Earlier drafts of the paper were read by Professors J. L. Harley, L. B. Thrower and S. D. Garrett, and Drs M. J. Carlile, B. C. Clifford, G. Hadley, P. M. Holligan, D. M. Losel and D. C. Smith. I am most grateful for their advice on specific points. Many, but not all, of their comments have been incorporated and I must stress that some views expressed, particularly with regard to the classification of mycorrhizas, are at variance with those of some of these colleagues.