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The Neurospora Revolution Copyright 0 1991 by the Genetics Society of America Perspectives Anecdotal, Historical and Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove Fifty Years Ago: The Neurospora Revolution Norman H. Horowitz Biology Division, Calijornia Institute of Technology, Pasadena, Calgornia 91 125 HIS year marks the fiftieth anniversary of the microorganisms, but it should be pointed out that the T publication of one of the pivotal works ofmod- Neurospora discoveriesfirst described in the 1941 ern biology, the first Neurospora paper of BEADLE paper werecrucial for making bacteria genetically and TATUM(1941). This brief paper, revolutionary useful. in both its methods and its findings, changed the BEADLE hadlearned of Neurospora at a lecture by genetic landscape for all time. Where previously there B. 0. DODGEgiven at Cornel1University in 1930, existed only scattered observations (albeit with some when the former was a graduate student. DODGE,a acute insights) on the relation between genetics and mycologist at the New York Botanical Garden, was a biochemistry, this paper established biochemical ge- strong advocate of Neurospora as a genetic organism. netics as an experimental science, one in which pro- It was he who found that theascospores-the products gresswould no longer belimited by the rarity of of meiosis-requiredheat shock to induce germination. mutants with biochemically knowablephenotypes, but (He had made this discovery originally in Ascobolus, where such mutants would be generated at will and by accident, after setting down some plates of asco- where findingscould be repeated and hypotheses spores ina sterilizing oventhat he thought was turned explored, as in other experimental sciences. This pa- off.) This finding made Neurospora available for ge- per was the first in a series of fundamental advances netic studies, and DODGE worked out the basic ge- in chemical geneticsthat by 1953 had bridged the gap netics of the organism. Among other things, he inves- between geneticsand biochemistry and ushered in the tigated the inheritance of mating type, albinism, and age of molecular biology. other monogenic characters. He showed that the eight I have explained in a recent memoir of BEADLE ascospores of an ascus display a perfect Mendelian (HOROWITZ1990) how the Neurospora investigation ratio (4:4). By isolating and culturing the ascospores arose from his earlier study of the genetics of eye- in the linear order in which they occur in the ascus, color synthesis inDrosophila with BORISEPHRUSSI, he discovered the patternsof first-and second-division and I will not repeat this history here. segregations. DODGE alsounderstood the benefits that The methodological innovations of the BEADLE- haploidy offered for genetic studies. When combined TATUMpaper were twofold. First, the authors intro- with the other features of Neurospora, it convinced duced what was for most geneticists a new kind of him that this ascomycete was the ideal genetic orga- experimental organism-amicroorganism that was nism. He frequently pointed this out to his friend T. ideally suited for classical genetic studies but which H. MORGAN,arguing that it was actually superior to differed from the classical organisms in that it grew Drosophila (ROBBINS1962). readily ona medium ofdefined chemical composition. As its second methodological innovation, the BEA- It was actually superior in some ways to the usual DLE-TATUMpaper introduced a procedure for re- experimental species becausethe entiremeiotic tetrad covering an important classof lethal mutations, could be recovered and cultured. Thisnovel creature namely those blocking the synthesis of essential bio- was the filamentousascomycete Neurospora crassa. logical substances.These were expressed in the orga- (Neurospora sitophila was also used inthe early studies, nism as new nutritional requirements. These muta- but was abandoned before long in favor of N. crassa.) tions were crucialfor understanding the biochemistry It is well known that the investigations that led to the of gene action. They displayed in a most convincing development of molecular genetics largely employed manner the central importance of genes in biochem- Genetics 147: 631-635 (April, 1991) 632 N. H. Horowitz Aside from its revolutionary methods, the BEADLE- TATUMpaper was remarkable for the results it re- ported. Itdescribed three X-ray-induced mutants that grew on “complete medium” (a complex, undefined mixture containing yeast extract), but that failed to grow on “minimal medium” (a mixture consisting of the minimal nutrients capable of supporting the growth of wild-type Neurospora). The presumption was that the mutations expressed in these cultures affected genes needed for the production of growth- essential compounds present in complete, but not minimal, medium. A systematic search revealed that each of the mutants required a different substance. The three substances were pyridoxine, thiamine and p-aminobenzoic acid, and the inability to synthesize them was eventually shown,in every case, to be inher- ited as a single-gene defect. (The 194 1 paper reported on the genetics of only the “pyridoxineless” mutant.) FIGURE I.-BEADLE’S lantern slide explaining the procedure for isolating biochemical mutants of Neurospora. The thiamine-requiring mutant was found to respond to the thiazole moiety of thiamine by itself, implying istry and ended forever the idea that the role of the that the mutant could synthesize the pyrimidine half genes in metabolism was somehow a subordinate one. of the molecule and showing that genes were limited Genetics,which before the Neurospora revolution in the range of their individual chemical effects. had been notably isolated from the physical sciences, The fact thatthe first three mutants found by now found itself in the mainstream of biochemistry. BEADLEand TATUMwere vitaminauxotrophs reflects, Or, more correctly, genetics and biochemistry were at least in part, the relatively high frequency of such now seen to be different aspects of the same thing. mutants recovered by their method of mutant selec- A diagram of the BEADLE-TATUMprocedure is tion. [See BEADLEand TATUM(1945), Table 5, for a shown in Figure 1. This figure is reproduced from a listing of all Neurospora mutants identified and cited lantern slide drawn and lettered by BEADLE,one of a in the literature up to that time.] In this method, set that he used in lectures in the 1940s. As the slide ascospore descendants of irradiated conidia were iso- suggests, BEADLEfavored the word “sex” rather than lated and cultured separately (see Figure l), a proce- “mating type” in his writing and speaking about Neu- dure that recovers even mutants with trace require- rospora. It should be noted that the test tube labeled ments. The mass selection procedures that came later “vitamins” alsocontained nucleic acid components. are biasedagainst such mutants becauseof cross- The essential character of the substanceswhose feeding. syntheses were affected in the Neurospora mutants- The pyridoxineless mutant, No. 299, is of special amino acids, purines, pyrimidines, vitamins-suggested interest. This was the first mutant found by BEADLE that similar mutations should occur in other microbial and TATUM,and it was one of the few that were species. This proved to be the case. In thefirst impor- recovered in N. sitophila. It was, so to speak, the tant extension of the Neurospora findings, GRAY and breakthrough mutant, the one that vindicated their TATUM(1 944) showed that “biochemical mutations” ideas about a new kind of genetics. But itsimportance could be induced in bacteria. This result solved a did not end there. Soon after the 1941 paper was fundamental difficulty that had long prevented pro- published, BEADLEreceived a letterfrom an acquaint- gress toward a genetics of bacteria-that is, the lack of ance at the Merck Research Laboratory requesting a suitable markers-and led directly to the demonstra- culture of No. 299 for the purpose of developing an tion of genetic recombination in Escherichia coli by assay method for pyridoxine. BEADLEsent a transfer, TATUM’Sstudent JOSHUA LEDERBERG.Biochemical as he invariably did once a mutant had been referred mutations were induced later in yeast and other mi- to in print. BEADLE firmly believed that this policy croorganisms. Modern microbial geneticsis to a large was in the best interest of science, a belief that was extent based on mutations of the type first described certainly confirmed in this case because,in the course by BEADLEand TATUMin their 1941 paper and on of their investigation, the Merck group discovered temperature-sensitive alleles of theseand otheressen- that No. 299 would grow without pyridoxine if the tial genes.The discovery of temperature-sensitive mu- pH of minimal mediumwas raised to 6 from its normal tants followed directly from the 1941 paper, as will value of 5 (STOKES, FOSTERand WOODWARD1943). be shown later. I recall first hearing of this unexpected result at an Perspectives 633 GEORGEBEADLE afternoon tea-break in the BEADLElab at Stanford who has written a perceptive essay on the rediscovery University. In the ensuing discussion, it was decided (EDGAR1966). to learn if other environmental variables-tempera- In another, and different, early application, a tem- ture, in particular-might also affect the phenotype of perature-sensitive mutant of E. coli was used to dem- mutants in a specific way. The mutant hunt that ran onstrate that genes determine the molecular proper- more or less continuously
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