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Aspergillus Nidulans DETECTION AND IDENTIFICATION OF TRANSLOCATIONS BY INCREASED SPECIFIC NONDISJUNCTION IN ASPERGILLUS NIDULANS ALAN UPs€3.ALL1p2AND ETTA Department of Biology, McGill University, Montreal, Canada Manuscript received June 28, 1973 Revised copy received September 24,1973 ABSTRACT A meiotic technique for visual detection of translocations has been applied to ten mitotically identified interchanges, and three new translocations were discovered using this method. Testcrosses between “standard” strains and potential translocation strains-e.g. strains with newly induced mutants or descendants from translocation crosse+are inspected for the frequency of abnormal-looking colonies. In all heterozygous translocation crosses “abnor- mals” are increased at least tenfold compared to the average control level of 0.15%. Most of these are rjisomics, and can be recognized by their character- istic phenotypes. Each translocation produces a few specific types, since nondisjunction is increased mainly in the linkage groups involved in the translocation (5GIOO-fold over control values). Therefore, translocations were not only detected but often tentatively assigned to linkage groups from the analysis of the disomic progeny in crosses. In addition, this technique allows reciprocal and nonreciprocal translocations to be distinguished, since only the latter produce one-third phenotypically abnormal duplication progeny. While results are clearcut in most cases, occasionally problems are encountered, e.g. when morphological mutants segregate in crosses, or when other genetic factors which increase or reduce the frequency of nondisjunction are present in certain strains. IN many organisms chromosomal translocations produce specific patterns of genetic segregation, such as unusual linkages and reduced meiotic recombi- nation (e.g., in Drosophila, ROBERTS1970), reduced viability of a fraction of the offspring (e.g., in maize, BURNHAM1948), familial patterns of trisomy (in man, LEJEUNE,GAUTIER and TURPIN1959), etc. These can lead to the detection and mapping of translocations in genetically well-known organisms, but generally, in higher plants and animals, cytological investigations are used for identification or confirmation, when either characteristic meiotic metaphase configurations or rearranged banding patterns in mitotic chromosomes can be observed. In fungi, cytological identification is not practicable as a routine procedure, although it has been successful in Neurospora (e.g., BARRY1967). A genetic method for detection is available in Neurospora where heterozygous translocations produce character- istic ascus-patterns, since inviable meiotic products form unpigmented ascospores Supported by operating grant A2564 (to E.K.) from the National Researh Council of Canada. a On sabbatical leave from the Department of Biological Sciences, Lancaster University, Lancaster, England. Genetics 76: 19-31 January, 1974. 20 A. UPSHALL AND E. GFER which can be observed in ordered or even unordered tetrads (PERKINS1967). In this fungus, a large number of reciprocal and insertional translocations have been analyzed and genetically mapped in this way (PERKINS1974). In Aspergillus nidulans, techniques for the detection and identification of trans- locations are also of a genetic type. The system in general use relies upon the detection of complete mitotic linkage between all markers known to be located on two different chromosomes, when haploid segregants from translocation heter- ozygotes are tested (UFER1962)-analogous to the inversion technique used in Drosophila. This method does not differentiate between reciprocal and insertional translocations. It has been successfully employed in identifying and tracing the pedigrees of eight translocations, most of which were radiation-induced simul- taneously with the induction of new markers (=FER 1965). However, while such information is obtained automatically when new markers are mapped into their mitotic linkage groups (%FER 1958) this method is somewhat laborious for pedigree analysis; also it is not always easy to obtain translocation-free tester strains with suitable combinations of markers for every strain to be tested. A second method, which is the topic of this report, depends on the observation that in many organisms meiotic nondisjunction is significantly increased in trans- location heterozygotes, especially for the two homologs involved in the rearrange- ment (e.g., in Drosophila, GRELL1959). This was also found in Aspergillus nidulans, where crosses heterozygous for the reciprocal translocation TI (VI;VIZ) produced increased frequencies of nondisjunctionals, mainly disomic for VI or VII, and such increases could be detected visually in ascospore platings of moderate size (POLLARD,&FER and JOHNSTON1968). Assuming that other translocations would produce similar effects, we postulated that meiotic analysis could provide a convenient way (1) to detect such aberrations by observing an increased frequency of disomic, phenotypically abnormal progeny, and (2) in favorable cases, to identify the heterozygous translocations by characterizing the nondisjunctional progeny genetically and visually. The latter is possible in A. nidulans since disomics, as well as trisomics, for each of the eight linkage groups show specific phenotypes (KAFER 1961) and the last of the eight disomic types, n '+ 1 for group VI11 which has very poor viability, has recently been recovered and identified by segregation of genetic markers (UFERand UPSHALL 1973). Our investigations show that this meiotic method of detection and identification of translocations is applicable to all previously known cases as well as to those which were newly discovered in the course of this work. In heterozygous crosses all translocations yielded a significantly higher frequency of visually abnormal progeny than control crosses, and most of this increase was due to a very high specific increase of nondisjunctionals for one or both of the chromosomes involved in the rearrangement. MATERIALS AND METHODS Strains: All strains employed are descendants of the original wild-type strain of Aspergillus niduZans used by PONTECORVOand coworkers (1953). Details of the origin of the mutants used here are given by DORN(1967). The new gene symbols of the mutants used have been described DETECTION OF TRANSLOCATIONS 21 and current information on mapping and recent terminology changes have been summarized by CLUTTERBUCKand COVE(1974). Most of the translocations were found in strains with W- induced mutants and many of these are also in the Glasgow stock collection (several translocations detected by mitotic analysis have been reported previously-KXFm 1965). Most of the mitotic tester strains, i.e. translocation-free strains with markers in all or most linkage groups, are the same as used in the earlier work and many are available from the Fungal Genetics Stock Center (Humbolt College, Arcata, California; BAFIRAZT,JOHNSON and OGATA1965). “Meiotic tester” and control strains with the standard chromosome complement and a few suitable markers were isolated from crosses between the following strains: biA (1) (biotinless), induced by X-rays in the original wild type and used as “standard“ in Glasgow; the Montreal standard, which is an eighth-generation backcross strain containing the conidial color mutants yA(2) (=yellow), and WA(3) (=white), and the p-aminobenzoic-acid-requiringmutant pabd (1); two translocation-free strains with mutants induced by UV-treatment of biA, namely riboA (1) biA (1) and biA (1) ; pyroA (4) requiring riboflavine or pyridoxine respectively. The most frequently used meiotic testers were pdaA yA, riboA biA and pabaA yA; wA. One other meiotic tester AcrA; 1ysB; C~QAhad been obtained after five generations of backcrossing of the resistance mutant AcrA (1) (=acriflavine), the color mutant chaA (1) (=chartreuse) and the mutant lysB(5) requiring lysine (details of above backcrosses are given in BARRA~et al. 19%). All these strains are expected to be almost isogenic. Media and general techniques: Standard media and established methods were used with respect to incubating temperature, “perithecium analysis”, production of heterokaryons and diploids, etc. (PONTECORVOet al. 1953; for details of media see BARRATTet al. 1965). Experimental procedures a) Measurement of meiotic nondisjunction The frequency of meiotic nondisjunction is regarded as being represented by the frequency of disomic colonies recovered among the ascospore progeny. We observed no clones of premeiotically produced disomics, nor were any found previously among larger samples of disomics (then called “unstable mutants”; UPSHALL1966). This is, in fact, a minimum estimate, since even under optimal conditions aneuploid types are occasionally overgrown by normal colonies and in some translocation crosses certain expected disomic types have not been recovered and appear to be inviable. Controls: For measurements of the influence of structural nonhomology on meiotic nondis- junction, crosses between completely isogenic strains provide the theoretical control from which base-values of nondisjunction frequencies should be obtained. Aspergillus nidulans, being homothallic, provides such an isogenic system with the production of selfed cleistothecia. In our experiments (Table 1) such controls were obtained from platings of selfed ascospores from two prototrophic standard strains (descendants of the meiotic tester pubaA TA and the translocation- free biA; pyroA strain). Similarly, platings of selfed ascospores from
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