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Perspectives Copyright 0 1992 by the Genetics Society of America Perspectives Anecdotal, Historical and Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove Neurospora: The Organism Behind the Molecular Revolution David D. Perkins Department of Biological Sciences, Stanford University, Stanford, Calgornia 94305-5020 NDER the title “Fifty Years Ago: The Neuro- grown in the light quickly became brightorange. U spora Revolution,” HOROWITZ(1 991) has cele- Colonies grown in the dark,however, remained white brated an anniversary of the epochal 1941 paper of for more than8 days, but thewhite colonies developed BEADLEand TATUM,which reported the first mutants orange pigment within 2 hr when they were brought with biochemically defined nutritional requirements. into thelight. Thermal tolerance was also studied (see HOROWITZ’Saccount and others (HOROWITZ1973, PAYEN1848, 1859). These results were cited by PAS- 1985, 1990; LEDERBERC1990) have focused on the TEUR (1 862)in reporting his own experiments on the people who were involved, the genesis of their ideas, survival of mold spores, which helped to refute theo- and therole of the 1941 results in transforming ries of spontaneous generation. biology. The present essay will be concerned mainly The next experimental study of Neurospora began with the research organism that was so important to in Indonesia during Dutch colonial times. In market- the success of the initial experiments.Neurospora places of East Java, bright orangecakes are displayed. possesses a combination of features that made it an These consist of Neurospora grown on soybean or ideal choice not only for accomplishing the original peanut solids from whichoil and protein for curd objectives set by BEADLEand TATUMbut also for a have been pressed. The Javanese inoculate the solids continuing succession of contributions,including with conidia to create an appetizing and highly nutri- many in areas that transgress the boundsof biochem- tious food called oncham, which has a mushroom-like ical genetics and molecular biology. 1 shall begin by taste(WENT 1901a; SHURTLEFFand AOYACI1979; outlining the story of Neurospora prior to BEADLE Ho 1986). Producing oncham is a cottage industry and TATUMand then go on to sketch its subsequent which has probably gone on for centuries and which history. The previous accounts have stressed biochem- continues today. ical genetics and molecular biology. I shall consider A Dutch plant physiologist, F. A. F. C. WENT,was other aspects as well, focusing first on genetics, con- stationed at the famous Buitzenjorg (now Bogor) Bo- tinuing with a summary of research accomplishments tanic Gardens in Java at the turnof the century. WENT of all sorts, and concluding with a consideration of was attracted by theorange oncham fungus and the potential usefulness of Neurospora for population started experimenting with it. He was frustrated be- studies. cause humidity in Java is sa great that the organism The vegetative phase of Neurospora was described grew through the cotton plugs of his culture tubes. and used for experiments by French microbiologists WENT (1904) also foundNeurospora in Surinam, nearly 100 years before BEADLEand TATUM(PAYEN where he noted that the fungus was used to process 1843; MONTAGNE1843). In thewarm, humid summer cassava meal in preparation of an indigenousalcoholic of 1842, bread from bakeries in Paris was spoiled by beverage. Back home in Utrecht, he described the massive growth of an orangemold. A commission was onchamfungus and its culture (WENT 1901a) and set up by the minister of war to investigate the cause used it for a series of studies on the effects of various of the infestation and to make recommendations. The substrates on enzymes such as trehalase, invertase and commission’s report (PAYEN1843) includes a colored tyrosinase (WENT 1901b). WENT(1 904)also studied plate whichshows colonies, mycelia, conidiophores the effect of light on carotenoid production. With and conidia of the “champignons rougesdu pain.” An knowledge of WENT’Swork, PRINGSHEIM(1 909) in- experiment in photobiology is described. Colonies cluded Neurosporain a study of oxidases, and KUNKEL Genetics 130 687-701 (April, 1992) 688 D. D. Perkins (1 9 13, 19 14)used it in studies of chemical toxicity. About the time KITAZIMAwas examining his orange All these observations were made using the vegetative fungus in Japan, CHARLESTHOM, a colleague of phase of the organism and the asexually produced DODGE’Sat the Department of Agriculture mycology powdery conidia (vegetative spores). and pathology laboratory in Arlington, Virginia, was The association of Neurospora with heat and fire studying cultures of orange mold from sugar cane must have been known from the earliest times. We bagasse in Louisiana. THOMwas of the opinion that now know that the sexually produced heat-tolerant theorange fungus, then called Moniliasitophila, ascospores remain dormant until exposed toheat. lacked a sexual stage. However, C. L. SHEAR, the head Heat activation of ascospores explains the occurrence of the laboratory, found perithecia in one of THOM’S of Neurosporaboth in bakery infestations and on plates. The material was given to DODGEfor analysis. burned vegetation. Numerousrecords going back The success of DODGE’Sexperimental crosses kindled over a century describe large orange areas following his enthusiasm, and Neurospora became hismain volcanic eruptions in tropical areas. In New Guinea, lifelong interest. tribesmen traditionally set hillsides on fire to flush DODGE’Sfirst Neurospora paper, with SHEARin game, and Neurospora bloomed fobowing the burns. 1927, goes far beyond the conventional taxonomic In Brazil, MOLLER(1 90 1) describedan orangefungus descriptions of genus and species. Cultures of the growing on burned vegetation (and on maize bread). orange fungus had been obtained frommany sources. A typically ascomycete sexual phase appeared in his Isolates were assigned to the new genus Neurospora cultures, and the sexual fruiting bodies (perithecia) on the basisof their grooved ascospores. (Prior to and ascospores were later identified as Neurospora. 1927, thevegetative stage hadsuccessively been called In Japan, Neurospora made a dramatic appearance Oidiumaurantiacum, Penicillium sitophilum and Mo- following thegreat Tokyo earthquake and fire of niliasitophila.) DODGEshowed that the cultures in- 1923. Within a few days, burned and scorched trees cluded three species which were set off fromone became festooned with orange. Mycologistsin two another by their crossing behavior. Hybrid perithecia laboratories cultured the organism. KITAZIMA(1 925) from crosses between different species developed observed perithecia in his cultures, and going back to slowly and were unproductive or poorly fertile. Al- the source, discovered that perithecia were present though a conventional morphologically based taxo- underthe bark of trees in theTemple of Shiba. nomic species description was provided for each spe- Orange progeny were obtainedfrom single asco- cies, crossing behavior was implicitly taken into con- spores. TOKUGAWAand EMOTO (1924) studied sur- sideration and used to assign strains to the designated vival of the fungus following exposure to moist and species. This innovation contrasted with the purely dryheat, and identified the orange pigment as a morphological criteria then used by mycologists and carotenoid. clearly anticipated the idea of biological species long Neurospora is commonly seen following agricul- before the concept was formalized. tural burning in warm, moist climates. Sugar cane Two species with eight-spored asci, Neurospora appears to be an ideal substrate. Ascospores are no crassa and Neurosporasitophila, were shown to be doubt activated by burning in the fields and by heating heterothallic: individual haploid cultures from single in the mill. Bales of bagasse (fiber from which the sap ascospores were unable to enter thesexual cycle. They has been pressed) become orange. In Australia,solids fell into two mating types, defined because crosses from refinery filters are spread on fields as fertilizer. could occur only between strains of opposite mating Largeorange colonies develop on this filtermud. tYPea Honey bees can be seen visiting the colonies and filling DODGEcarried out the first tetrad analysis with N. their pollen baskets with the brightly colored conidia crassa, showing that the mating types segregated 4:4 (SHAWand ROBERTSON1980). in individual asci. The asci were obtained as groups The modern history of Neurospora begins in the of eight ascospores thathad been spontaneously mid-1920s with materialfrom sugar cane bagasse. ejected from the perithecia. The Neurospora asco- The key person was BERNARDDODGE. Like BEADLE, spores were activated by heat, as inAscobolus. In DODGEhad grown upon a farm. He worked for years contrast to the eight-spored species, isolates of Neu- asa school teacher and managed to complete his rosporatetrasperma, with four-spored asci, appeared bachelor’s degree only at age 39. He published his to be homothallic. Culturesfrom single ascospores first paper at the age of 40 and was already past 50 were usually self-fertile. A few self-sterile progeny when he began to work with Neurospora (ROBBINS were produced, however, thatbehaved as though they 1962). Prior to the Neurospora work,DODGE was the were heterothallic. DODGE(1927) was shortly to de- first to discover heat activation of ascospores (1912) scribe the cytological basis ofthis “pseudohomothallic” and to describe mating
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