The Nature and Application of Biocontrol Microbes II: Trichoderma spp. Trichoderma: Systematics, the Sexual State, and Ecology

Samuels, G. J. 2006. Trichoderma: Systematics, the sexual state, and ecology. Phytopathology 96:195-206. A chronology is presented that charts the development of a genus and species concept in Trichoderma. Eighty-nine species of Trichoderma have been named, and several species of Hypocrea have been linked to unnamed Trichoderma anamorphs. Eighty-three taxa of Trichoderma and their teleomorphs, Hypocrea spp., have been included in phylogenetic analyses, including 11 species of Hypocrea with unnamed Trichoderma anamorphs. Phylogenetic analyses show that Trichoderma and Hypocrea are congeneric. Trichoderma species not linked to Hypocrea teleomorphs are derived from among species that are linked to teleomorphs, indicating sexual and asexual lineages are not independent of each other. Many more species remain to be discovered and described. Molecular phylogenetic analyses have revealed the existence of more species than have been recognized on the basis of morphology alone. A suggestion is made to modify the International Code of Botanical Nomenclature to enable adoption of a single generic name for Trichoderma/Hypocrea, with Trichoderma being the older and more utilitarian name. As increasing numbers of species are studied, the few morphological characters of anamorph and teleomorph have reached their limit for defining species. DNA-based characters have assumed an indispensable role. Exploration of new niches, such as within tree trunks and new geographic locations, have resulted in a substantial increase in the number of species of Trichoderma. Trichoderma is usually considered a genus of free-living soil fungi but evidence suggests that Trichoderma species may be opportunistic, avirulent plant symbionts as well as parasites of other fungi. Members of the genus Trichoderma are universally present in soils, although individual species may be either cosmopolitan (e.g., T. harzianum) or limited (e.g., T. viride) in their geographic distribution. To facilitate identification of species, a list of correctly identified strains of Trichoderma and their GenBank numbers for sequences of translation-elongation factor EF-1α and internal transcribed spacer rDNA is provided. The Trichoderma chronology. Identification of Trichoderma species is notoriously difficult. The few morphological characters available are variable to some degree, leading to overlap among species; this could explain why so few species have been described over most of the life of the genus. An unfortunate result of the failure of taxonomists, until recently, to provide the basics for species identification is that strains reported in the literature may have been misidentified. Kullnig et al. (63) reidentified several strains as Trichoderma harzianum that had been reported in the literature under different names. How have we come to this state of species recognition, and what are we doing to improve the situation? To understand this, it is essential to review how the taxonomy of Trichoderma has developed. The appreciation of what constitutes a species of Trichoderma, or even of what constitutes the genus, has been incremental and free of a plethora of names that cannot be pinned down, or competing taxonomic systems, both of which have plagued taxonomy of other economically important genera such as Fusarium. Following is a summary of the highlights in this development. Trichoderma was first proposed as a genus by Persoon in 1794 (77) on the basis of material collected in Germany. Persoon included four species and evidently had difficulty recognizing his own genus because, of the four species originally included in the genus, only one—T. viride—remains in Trichoderma. In 1865, the Tulasne brothers (99), in France, elegantly illustrated a link between T. viride and a sexual stage, Hypocrea rufa. Their illustrations are the standard of identification for this holomorph. Prior to 1969, few species were added to Trichoderma. Over time a few genera, each including one or a few species, were synonymized with Trichoderma thereby expanding the concept of the genus to include species that produced hairs and colorless (white in mass) conidia as well as characteristic species with green conidia. With this expansion in generic concept one might think that the flood gates for description of new species would have been opened, but that was not the case. In 1927, Abbott (1) only recognized four well-defined groups among the intergrading Trichoderma isolates from soil but distinguished only three species in a key; two of them are now considered to be synonyms of T. viride. In 1939, Bisby (8) expressed what probably most people feel even today: they all look the same! He was not able to distinguish between H. rufa, a species with colorless ascospores, and H. gelatinosa, a species with green ascospores. One would not think it difficult to distinguish between these two species because of the difference in ascospore colors, and the anamorph of H. gelatinosa, T. gelatinosum, is easily distinguished from that of true H. rufa, T. viride. For whatever reason, Bisby could not see the differences and the practical result was a taxonomy that reduced most of Trichoderma to a single species, T. viride. This system was in place until 1969. Needless to say, this single-species system was very popular; certainly no special skills were required to reach an identification, and only few species were added until 1969. In 1957, Dingley (31), characterizing the Trichoderma anamorphs of several species of Hypocrea in New Zealand, identified all of the anamorphs as typical of T. viride. Bisby’s one-species system prompted John Webster and student Mein Rifai to review taxonomy of Trichoderma and Hypocrea by examining life cycles of identified Hypocrea species (81,82,102, Corresponding author: G. J. Samuels; E-mail address: [email protected] DOI: 10.1094 / PHYTO-96-0195 This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological