STIMULATION OF SEX ORGAN FORMATION IN PHYTOPHTHORA BY ANTAGONISTIC SPECIES OF TRICHODERMA
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1 195 New Phytol. STIMULATION OF SEX ORGAN FORMATION IN PHYTOPHTHORA BY ANTAGONISTIC SPECIES OF TRICHODERMA II. ECOLOGICAL IMPLICATIONS BY C. M. Forest Research Station, Alice Holt Lodge, Farnham, Surrey {Received 21 August 1974) SUMMARY Evidence for the occurrence of the 'Trichoderma effect' in nature is reviewed. It is considered that the effect may be a specifically evolved defence mechanism, and that root inhabiting species of Phytophthora may be more ecologically specialized for response to Trichoderma than others. It is suggested that the 'Trichoderma effect' and similar phenomena could influence speciation in heterothallic Phytophthora species. INTRODUCTION Most Phytophthora diseases are soil-borne but available evidence suggests that in the absence of an adequate food base, the mycelium is often short lived and subject to lysis (e.g. Legge, 1953; Vujicic and Park, 1964; Tsao, 1969). Survival of many species in soil is probably dependent upon the formation of the more resistant oospores and chlamydospores (Legge, 1953; Vujicic and Park, 1964; Mircetich and Zentmyer, 1966; Tsao, 1969). Approximately one third of the forty-two species of Phytophthora recognized by Waterhouse (1963) are heterothallic, and it has been assumed that the formation of oospores by these heterothallic species in nature requires the presence of both compatibility or mating types, Ai and A2. However, recent observations have shown that volatiles from antagonistic isolates of the common soil saprophyte Trichoderma can induce oospore formation by selfing in single A2 isolates of certain Phytophthora species in vitro (Brasier, 1967, 1971, 1975; Pratt et al, 1972). Moreover, a similar phenomenon has been reported from soil (Reeves and Jackson, 1972). This information may be of considerable ecological significance since, in a diploid organism, formation of oospores in response to Trichoderma in nature would not only provide a means of survival but also a potential source of genetic variation. The present paper considers evidence for the phenomenon in nature and examines some possible implications for the ecology and phylogenetics of heterothallic Phytophthora species. EVIDENCE FROM SOIL EXPERIMENTS Much of the evidence for the 'Trichoderma effect' in nature comes from soil baiting experiments with Phytophthora cinnamomi. The first indication can be found in the data of Mircetich and Zentmyer (1966), who obtained oospores within fifteen days when they buried washed mycelial mats of P. cinnamomi in vials of unsterile soil. The isolate used was an A2 (G. A. Zentmyer, personal communication).
2 196 C. M. BRASIER While many soil organisms, such as bacteria (Mukerjee and Roy, 1962; Brasier, 1972a, b) could be involved, critical evidence for the implication of Trichoderma was provided by Reeves and Jackson (1972), who buried mycelial mats of an A2 isolate of Phytophthora cinnamomi, together with small sections of root, in pots containing five different soils. Oospores formed within the root sections in three soils within 6-8 days and were conspicuously associated in each case with the presence of sporing Trichoderma viride mycelium. Examination showed that in the soils T. viride was abundant, whereas in the other two it was apparently absent. Rapid lysis of the Phytophthora mycelium also occurred in the active soils. It was concluded that P. cinnamomi would form oospores in these soils provided that suitable nutrients were available and active Trichoderma viride was present. Brasier (1972b and unpublished results) buried mycelial mats of Ai and A2 isolates of Phytophthora cinnamomi separately in pots containing a clay soil from under oak woodland and a sandy soil from beneath spruce woodland. Clumps of oospores developed on the mycelium of the A2 isolates (Pi 16) in both soils whereas the Ai isolate (Pi73) remained sterile in all treatments. Trichoderma isolates obtained from both these soils were shown to be active by the volatile method (Brasier, 1975). It was presumed from the differential response of the Ai and A2 isolates that the oospores of Pi 16 were most probably induced by Trichoderma. This evidence strongly suggests that at least with the common root pathogen Phytophthora cinnamomi, the 'Trichoderma effect' does occur in soil and in host tissues. ECOLOGICAL AND PHYLOGENETICAL IMPLICATIONS Since the initial work of Weindling (1932) it has been widely considered that antagonistic Trichodermas are potentially capable of suppressing populations of soil-borne fungal pathogens (see Garrett, 1970). They are therefore likely to influence the survival of Phytophthora spp. where the two organisms come into proximity. Although most soils appear to be inhabited by Trichoderma species, limited information is available on their distribution in soil or on root surfaces, and that available prior to the reclassification of the genus by Rifai (1969) is difficult to interpret owing to the uncertain taxonomic position of the isolates concerned. However, Gibbs (1967) found the commonest Trichoderma on pine root surfaces to be T. viride, followed by T. polysporum, T. hamatum and T. piluliferum respectively. T. harzianum and T. koningii were also present, but of far less significance. Thus the four species-groups shown to be active in stimulating sexual reproduction in Phytophthora, Trichoderma viride, T. polysporum, T. piluliferum and T. koningii (Brasier, 1975) are all potential root surface fungi. T. viride, in particular, is common in decaying bark (Webster, 1964), on live tree root surfaces and in soil (Gibbs, 1967), and has often been noted as replacing primary pathogens in woody material. It is therefore likely to be an early invader of root and bark tissue damaged by Phytophthora attack. Within host tissue the formation of oospores by Phytophthora at the approach of such an antagonist would clearly be of survival value. In particular a response to volatiles (Brasier, 1971) or non-volatile diffusates might secure oospore formation before physical contact between the two fungi occurred. The rapid production of oospores by P. cinnamomi in response to Trichoderma isolates producing volatile antibiotics (Brasier, 1975) suggests that, in this species at least, the effect is more likely to be a specifically evolved defence mechanism than a purely chance phenomenon. Thus, in the presence of active Trichoderma a root-invading Phytophthora
3 Ecological implications of effect of Trichoderma on Phytophthora 197 equipped with such a defence mechanism would possibly be at a selective advantage over one not so endowed. Here, evidence of variation in ability of different heterothallic species to respond to Trichoderma (Brasier, 1975) is of particular interest. The two species notable for ready response to Trichoderma, Phytophthora cinnamomi and P. cambivora are both common pathogens on roots of woody hosts in Britain. P. palmivora forms i and 2 (Waterhouse, 1974; cf. also P. arecae and P. meadii), which often attack aerial parts of woody hosts apparently do not respond to Trichoderma viride, whereas the black pepper form of Phytophthora palmivora, which attacks roots of another woody host {Piper nigrum) from the soil, does. Other species including Phytophthora nicotianae, P. cryptogea, and P. drechsleri which were apparently polymorphic for response, and P. infestans which responded weakly and erratically, need further investigation. Nevertheless the present evidence suggests that heterothallic Phytophthora species common on roots of woody hosts may be more ecologically specialized for response to Trichoderma than others. If it is accepted that in the root invading species such as Phytophthora cinnamomi, P. cambivora and P. palmivora (black pepper form) response to Trichoderma is an important ecological attribute, the frequency of Ai and A2 types of these species assumes a new significance. In an investigation of Phytophthora palmivora (black pepper form) from Piper nigrum in Sarawak, Brasier (1972a) found eleven A2 and three Ai isolates. In a survey of isolates of Phytophthora cambivora and P. cinnamomi from roots of trees and shrubs in Britain, among fifteen isolates of P. cambivora twelve were of the A2 and three were of the Ai compatibility type, and all twenty-eight isolates of P. cinnamomi were A2 (Brasier, 1972b). The apparent absence of the Ai of P. cinnamomi in Britain may be due to historical accident of introduction. However, while P. cinnamomi is a successful species of world-wide distribution, even in countries where the Ai has been found it is often rare or infrequent. (Galindo and Zentmyer, 1964; Pratt, Heather and Shepherd, 1972). From this it appears that in P. cinnamomi, in particular, the chances of oospores being formed by the pairing of Ai and A2 isolates in nature is extremely small, and that the formation of oospores by selfing of single isolates in response to Trichoderma or other agencies may be of greater importance. It is possible that the compatibility system is degenerating in this species, and that genetical isolation of Ai and A2 types is occurring. This situation would be accelerated if selfing of A2 produced only A2 isolates among oospore progeny, but the genetic control of compatibility type is still to be resolved. However, it is apparent that ecological specialization towards response to Trichoderma and other agencies could lead to speciation and other complex phylogenetic relationships in the heterothallic species. Such a phenomenon might account for the occurrence of two ecotypes among isolates of Phytophthora drechsleri from Eucalypt forests in Australia, one A2 and responsive to Trichoderma, the other sterile and nonresponsive (Shepherd and Pratt, 1973). ACKNOWLEDGMENTS I am much indebted to my colleagues Dr J. N. Gibbs and Dr M. Anderson for helpful discussion of the manuscript. REEERENCES (1967). Physiology of reproduction in Phytophthora. Ph.D. Thesis, University of Hull. (1971). Induction of sexual reproduction in single A2 isolates of Phytophthora by Trichoderma viride. Nature New BioL Lond., 231, 283. BRASIER, C. M. BRASIER, C. M.
4 C. M. BRASIER BRASIER, C. M. (1972a). Observations on the sexual mechanism in Phytophthora palmivora and related species. Trans. Br. tnycol. Soc, 58, 237. BRASIER, C. M. (1972b). The Trichoderma effect. Rep. Forest Res. Lond., (1972) pp and Plate 4. BRASIER, C. M. (1975). Stimulation of sex organ formation in Phytophthora by antagonistic species of Trichoderma. I. The effect in vitro. New Phytol., 74, 183. GARRETT, S. D. (1970). Pathogenic Root-infecting Fungi. Cambridge University Press. GALINDO, J. & ZENTMYER, G. A. (1964). Mating types in Phytophthora cinnamomi. Phytopathology, 54, 238. GiBBS, J. N. (1967). A study of the epiphytic growth habit of Fomes annosus. Ann. Bot. N.S., 31, 755. LEGGE, B. H. (1953)- Studies of species 0/Phytophthora. Ph.D. Thesis, University of Birmingham. MIRCETICH, S. M. & ZENTMYER, G. A. (1966). Production of oospores and chlamydospores of Phytophthora cinnamomi in roots and soil. Phytopathology, 56, MuKERjEE, N. & ROY, A. B. (1962). Microbial influence on the formation of oospores in culture by Phytophthora parasitica var. subdariffae. Phytopathology, 52, 583. PRATT, B. H., HEATHER, W. A. & SHEPHERD, C. J. (1972). Transcontinental occurrence of Ai and A2 strains of Phytophthora cinnamomi in Australia. Amt. J. biol. Sci., 25, PRATT, B. H., SEDGLEY, J. H., HEATHER, W. A. & SHEPHERD, C. J. (1972). Oospore production in Phytophthora cinnamomi in the presence of Trichoderma koningii. Aust. J. biol. Sci., 25, 861. REEVES, R. J. & JACKSON, R. M. (1972). Induction of Phytophthora cinnamomi oospores in soil by Trichoderma viride. Trans. Br. my col. Soc, 47, 455. RiFAi, M. (1969). A revision of the genus Trichoderma. Mycol. Pap No SHEPHERD, C. J. & PRATT, B. H. (1973). Separation of two ecotypes of Phytophthora drechsleri. Tucker occurring in Australian native forests. Aust. J. biol. Sci., 26, TSAO, P. H. (1969). Studies on the saprophytic behaviour of Phytophthora parasitica in soil. Proc. First Internat. Citrus Symp., 3, VujifiiK, R. & PARK, D. (1964). Behaviour of Phytophthora erythroseptica in soil. Trans. Br. mycol. Soc 47, 455- WATERHOUSE, G. M. (1963). Key to the species oi Phytophthora de Bary. Mycol. Pap., No. 92. WATERHOUSE, G. M. (1974). Phytophthora palmivora and some related species. In: Phytophthora Disease of Cocoa (Ed. by P. H. Gregory), pp Longman Group, London. WEBSTER, J. (1964). Culture studies on Hypocrea and Trichoderma. I. Comparison of perfect and imperfect states of H. gelatinosa, H. rufa and Hypocrea Sp. i. Trans. Br. mycol. Soc, 47, 75. WEINDLING, R. (1932). Trichoderma lignorum as a parasite of other soil fungi. Phytopathology, 22, 837.
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