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Trichothecene Biosynthesis in Fusarium Species: Chemistry, Genetics, and Significance

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Trichothecene Biosynthesis in Fusarium Species: Chemistry, Genetics, and Significance Supplied by U.S. Dept. of Agriculture 7049 MICROBIOLOGICAL REVIEWS, Sept. 1993, p. 595-604 Vol. 57, No.3 0146-0749/93/030595-10$02.00/0 National Center for Agricultural Copyright © 1993, American Society for Microbiology Utilization Research, Peoria, Illinois Trichothecene Biosynthesis in Fusarium Species: Chemistry, Genetics, and Significance ANNE E. DESJARDINS,* TIIOMAS M. HOHN, AND SUSAN P. McCORMICK Mycotoxin Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U. S. Department ofAgriculture, Peoria, Illinois 61604 INTRODUCTION 595 TRlCHOTHECENE BIOSYNTHESIS IN FUSARIUM SPECIES 596 Pathway Intermediates 596 Trichodiene Synthase 597 Other Pathway Enzymes 598 SIGNIFICANCE OF TRICHOTHECENES IN PLANT PATHOGENESIS 600 APPLICATIONS 601 ACKNOWLEDGMENTS 602 REFERENCES 602 INTRODUCTION various plant products. Subsequent investigations of moldy­ grain toxicoses led to the isolation and identification of many Trichothecenes are sesquiterpene epoxides that inhibit new trichothecenes, including T-2 toxin, diacetoxyscirpenol, eukaryotic protein synthesis and thereby impair human and and deoxynivalenol (Fig. 1) (74). These three closely related animal health. Several fungal species of the genus Fusarium compounds are the trichothecenes most commonly found in and related genera can produce trichothecenes in agricul­ agricultural commodities infected with Fusarium species. tural crops and commodities. Interest in these toxins is due The complex taxonomy of the genus Fusarium has led to primarily to the discovery that trichothecene contamination considerable confusion and misidentification of tricho­ of human foods and animal feeds is a continuing worldwide thecene-producing species. The publications of Nelson and problem. The most effective control strategy for tricho­ coworkers (55, 64) present the most comprehensive and thecene toxins is prevention of fungal infection and toxin widely used system for the identification of toxigenic Fusar­ production in the field and in storage. In the long term, ium species. According to the taxonomic system of these understanding the molecular biology of trichothecene pro­ authors and other authorities, six Fusarium species have duction should help the development of practical and spe­ been well documented worldwide to produce trichothecenes cific controls. In recent years, rapid advances in the molec­ (51,55). Two species, F. sporotrichioides and F. poae, of the ular genetics of filamentous fungi have opened the way for section Sporotrichiella produce mainly T-2 toxin and diace­ detailed genetic analysis of trichothecene biosynthesis in toxyscirpeno!. Four species, F. crookwellense, F. culmo­ Fusarium species. This review will describe recent progress rum, F. graminearum, and F. sambucinum, of section in understanding the biochemistry and genetics of the tricho­ Discolor produce mainly diacetoxyscirpenol and deoxyni­ thecene biosynthetic pathway and in evaluating the signifi­ valeno!. A wide variety of other trichothecenes and struc­ cance of trichothecenes in plant diseases caused by Fusar­ turally related compounds can be produced by individual ium species. strains of these species under specific growth conditions. The chemistry and toxicology of trichothecenes were All trichothecene-producing Fusarium species are de­ established by early studies, which have been thoroughly structive pathogens that can attack a wide range of plant reviewed (2, 55, 74). All trichothecenes share a tricyclic species. The main sources of trichothecenes in the food nucleus named trichothecene (Fig. 1) and usually contain an supply are contaminated cereal grains, namely maize, epoxide at C-12 and C-13, which is essential for toxicity. The wheat, rye, barley, and rice. Multiyear surveys in the United total number of naturally occurring trichothecenes known States and Canada indicate that maize and wheat are often today exceeds 60. Their chemical structures vary in both the contaminated with trichothecenes but that the levels are position and the number of hydroxylations, as well as in the generally below 2 ppm, a recommended tolerance level (66). position, number and complexity of esterifications. The The severity of Fusarium infection and of trichothecene Fusarium trichothecenes, which will be the major focus of contamination increases with wet weather at harvest and this review, are relatively simple alcohols and short-chain with storage under conditions of relatively high moisture. esters, whereas trichothecenes of Myrothecium, Verrucaria, There are few effective, economical methods for decontam­ and other genera can be complex macrocyclic esters. Tri­ ination of trichothecenes in grains. Contaminated grains can chothecenes are named after the fungus Trichothecium ro­ be diverted to nonfood uses such as fuel ethanol production, seum, from which the first trichothecene was isolated in or their toxicity can be reduced by dilution with clean grain. 1948. The discovery of the carcinogenic aflatoxins in the All animal species that have been tested appear to be 1960s greatly increased interest in mycotoxins (i.e., fungal sensitive to trichothecene toxins. Disease symptoms vary toxins that affect animals) and stimulated the development of widely with the species of animal, the particular tricho­ sensitive analytical methods for mycotoxin detection in thecenes present, their levels and routes of exposure, and other factors. Experiments with chemically pure tricho­ thecenes at low dosage levels have reproduced many of the * Corresponding author. features observed in moldy-grain toxicoses in animals, in- 595 596 DESJARDINS ET AL. MICROBIOL. REV. 16 kia that occurred in the former Soviet Union in the 1940s have been associated with consumption of overwintered grains infected with F. sporotrichioides, which is a T-2 toxin-producing species (55). In Japan, outbreaks of a similar 14 disease called akakabi-byo or red mold disease have been Trichothecene T-2 toxin associated with grains infected with F. graminearum, which is a deoxynivalenol-producing species (55). There is, how­ ever, no direct evidence that either T-2 toxin or deoxyni­ valenol was responsible for these human disease epidemics. _O O""OH On the other hand, symptoms similar to those of alimentary o~:: toxic aleukia and akakabi-byo were produced by pure diace­ HO : ,,~ toxyscirpenol in clinical trials conducted with terminally ill HO" cancer patients (1). The most controversial aspect of human Diacetoxyscirpenol Deoxynivalenol exposure to trichothecene toxins has been the charge that FIG. 1. Structure of trichothecene, T-2 toxin, diacetoxyscirpe­ they were used as chemical-warfare agents in Southeast Asia nol, and deoxynivalenol. in the early 1980s. Most recent assessments of this contro­ versy have concluded that the evidence is not sufficient to warrant such claims (53). cluding anemia and immunosuppression, hemorrhage, eme­ sis, and feed refusal in cattle, pigs, and poultry (55). Animal­ feeding experiments have also demonstrated that TRICHOTHECENE BIOSYNTHESIS IN FUSARIUM trichothecenes are teratogenic but have provided no evi­ SPECIES dence that they are carcinogenic (1). Historical and epide­ miological data obtained with humans indicate an associa­ Pathway Intermediates tion between certain disease epidemics and consumption of grain infected with Fusarium species that produce tricho­ The biosynthesis of trichothecenes proceeds from tri­ thecenes. In particular, outbreaks of alimentary toxic aleu- chodiene (Fig. 2), a natural product first isolated from T. ~.~""O~~"'O~~"'~OH ~"'OHOH · h d' 2 H d t . h d' 12,13-Epoxy- Isotrichodiol Isotrichotriol "'OH Tr IC 0 lene - y roxy nc 0 lene 9,1 O-trichoene-2-ol , HO" ""-': 0 ~ :: II.. 0H \' OAe IsovaIO" :: ""~--l"",.. OAe . 1C\3Trichotriol ""OH AeO\'\(' 3-Acetyl T-2 toxin T-2 toxin , \'(~""OH ~""OH ~ HO"\'" Isotrichodermol OAe Deoxynivalenol 3-Acetylneosolaniol ~ , y!°~""OH ~ ~~OAe YJO~""OH Y'(~''''OAC o ~ AeO' YJu~""OAC 4,15-Diacetoxyscirpenol ~ ~ ~OAe 3 15-Didecalonectrin Isotrichodermin AeO' , 3,4,15-Triacetoxyscirpenol " o ""OAe ~O""OAe ~O0 ""OAe O. 0 ~ : : ~ ~; ~,~ OH ,,\" HO AeO" AeO, 15-Decalonectrln 3,15-Diacetoxyscirpenol Calonectnn FIG. 2. Trichothecene biosynthetic pathway in Fusarium species. VOL. 57, 1993 TRICHOTHECE E BIOSYNTHESIS IN FUSARIUM SPP. 597 roseum (52). Feeding tritiated trichodiene to T. roseum oxygenations, at C-2, C-ll, and C-12/13. One possible pre­ resulted in low-level incorporation of tritium into trichothe­ cursor, lla-hydroxytrichodiene, has been shown in feeding colone, which suggested that trichodiene is a precursor of T. experiments with UV-induced mutants and ToxS- transfor­ roseum trichothecenes (52). Treatment of trichothecene­ mants to be a precursor of apotrichothecenes rather than producing strains of F. sporotrichioides, Gibberella pulicaris trichothecenes (57a, 59). Pulse-labeling experiments have (anamorph, F. sambucinum), and F. culmorum with oxyge­ identified a dioxygenated compound, 12,13-epoxy-9,10-tri­ nase inhibitors such as ancymidol and xanthotoxin resulted choene-2-ol (Fig. 2) as an efficient precursor of 3-acetylde­ in the inhibition of trichothecene production and the accu­ oxynivalenol in F. culmorum. mulation of trichodiene, which suggested that trichodiene is In summary, F. culmorum, F. sporotrichioides, and G. a precursor of Fusarium trichothecenes (25, 26, 33, 79). pulicaris share most of the initial scheme of oxygenations Further evidence was obtained by UV irradiation of F. and cyclizations in trichothecene
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