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MARKERS and CENTROMERE DISTANCES in NEUROSPORA Tetraspermal

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MARKERS and CENTROMERE DISTANCES in NEUROSPORA Tetraspermal MARKERS AND CENTROMERE DISTANCES IN NEUROSPORA TETRASPERMAl H. BRANCH HOWE, JR. Department of Bacteriology, University of Georgia, Athens, Georgia Received September 24, 1962 ENETIC studies with Neurospora tetrasperma were begun by the late B. 0. GD~~~~( 1928) soon after the genus Neurospora was described (SHEARand DODGE1927). DODGE(1927) showed that the linear ascus of N. tetrasperm contains four binucleate ascospores and that events during ascus formation usually provide that the two nuclei in each ascospore will differ in mating type. The four ascospores from a single ascus, therefore, usually yield four self-fertile mycelia, a phenomenon variously known as facultative, secondary, or pseudo- homothallism. Genetic differences studied include mating type (DODGE1928; LINDEGREN 1932) ; conidial variation (DODGE1930,1935) ;lethals ( UBERand GODDARD1934; DODGE1934, 1935; SEAVER1937; DODGE,SINGLETON and ROLNICK1950); substrate color (TAI1936); dwarfism (DODGE,SCHMIDT and APPEL1945); and other morphological traits ( GOODSPEED1942; MALLOCH1942). Until recently (HOWE1961) mainly visible differences were employed. Genetic work in N. tetrasperma clearly lags behind that in N. crmsa both in numbers of mutants produced and in linkage analysis. Linkage analysis in N. tetrmperma is compli- cated by nuclear passing during ascus formation (DODGE1927) and by the di- caryotic condition of the ascospores. Single ascospore isolation does not neces- sarily insure homokaryosis for every allele, as in N.crassa. The present investigation involves the recovery of both morphological and nutritional mutants as well as a preliminary determination of gene-centromere distances using both tetrads and random ascospores. The genetic analyses are based upon current understanding of ascus formation and the relationship be- tween crossing over and nuclear content of the ascospores. These concepts are briefly traced below and outlined in Figures 1 and 2. DODGE(1 927) was the first to describe nuclear events in the developing ascus. His description may be summarized as follows. First meiotic division spindle orientation is longitudinal (with respect to the long axis of the ascus), and the two daughter nuclei come to rest one somewhat above the other. Second meiotic division spindle orientations occur in two ways, but both produce the same result. In one the two spindles are oriented longitudinally, with a spindle near each end of the ascus. In the other the two spindles are oriented obliquely and lie nearly parallel to each other near the center of the 1 Work supported by National Science Foundation Grant G-13267. Genetics 48: 121-131 January 1963. 1 22 H. B. HOWE, JR. MV DIV DIV FIGURE1.-Diagrammatic representation of ascus development in Neurospora tetraperma with respect to an allelic pair. Based upon several authors (see text). First division segregation results if a crossover does not occur between locus and centromere; second division segregation, if a single crossover does occur in this interval. Multiple exchanges are not considered. Nuclear passing (denoted by curved lines) occurs at both the second and third divisions. Sister nuclei shown by heavy and light circles, respectively. Upper Row: First division segregation resulting in heterokaryotic ascospores (Type I ascus). Middle Row: Second division segregation. Tetrad nuclei with nonidentical alleles at both ends of the ascus resulting in heterokaryotic ascospores (Type I ascus). Bottom Row: Second division segregation. Tetrad nuclei with identical alleles at both ends of the ascus resulting in homokaryotic ascospores (Type I1 ascus). ascus. Both, however, result in a pair of nonsister nuclei becoming situated near each end of the ascus. The four spindles in the third (mitotic) division are obliquely or nearly trans- versely oriented. The resulting eight nuclei assume nonsister pairwise arrange- ments, after which a pair of nonsister nuclei is cut off in each ascospore. COLSON ( 1934) verified DODGE’Scytological findings. Clearly, nuclear passing normally occws at both the second and third divisions. This is quite different from ascus development in N. crassa, where nuclear Neurospora tetrasperma MARKERS 123 TYPE I ASCUS TYPE U ASCUS ASCOSPORES ASCOSPORES HETEROKARYOTIC HOMOKARYOTIC ORIGIN: 1ST. DIV. SEC. ORIGIN: IR ZND. DIV. YG. + IR 2ND. DIV. SEC. FIGURE2.-Determination of gene-centromere distance in N. tetrasperma. Based upon several authors (see text). A. Tetrad analysis: Percent 2nd. div. seg. = 2 x percent Type I1 asci. percent 2nd. div. seg. Centromere distance = =percent Type I1 asci. B. Random, binucleate 2 ascospore analysis: Percent Type I1 asci = 2 x percent homokaryotic-mutant ascospores. Cen- tromere distance = 2 x percent homokaryotic-mutant ascospores. Centromere distance for mating type = percent self-sterile ascospores. passing is very rare, requiring special techniques for detection ( MCCLINTOCK 1945; HOWE1956), and ascospores are initially uninucleate. LINDEGREN(1933) showed that second division segregation of a marker in the N. crassa ascus manifests crossing over between marker and centromere. COLSON (1934) suggested from her cytological studies that homokaryosis for a marker in the N. tetrasperma ascus manifests crossing over between marker and centro- mere. Homokaryosis for mating type had already been observed in N. tetra- sperma by DODGE(1927) and LINDEGREN(1932) and mentioned in a review by KNIEP ( 1929). More recently SANSOME( 1946) and CATCHESIDE( 195 1 ) again discussed the role of homokaryotic ascospores in linkage studies in this species. MATERIALS AND METHODS Stocks were derived from the DODGEN. tetrasperma wild type strain 87 (Columbia University stock Number 163) obtained from DR.L. S. OLIVE.Strain 87 is a typical secondarily homothallic strain, but reference to it has not yet been found in DODGE’Spapers. Strain 87 was inbred to increase isogenicity by twelve successive generations of single dicaryotic-ascospore isolations, a procedure equivalent to repetitive 124 H. B. HOWE, JR. intra-ascus crossing. Following inbreeding the heterothallic A and a mating type components were extracted by conidial plating and used in all subsequent work. These inbreds are referred to as 85A and 85a to distinguish them from the original strain 87. Prior to completion of inbreeding, however, some mutants were induced in strain 87. Standard N. crassa media were found satisfactory for growth of N. tetrasperma. WESTERGAARD-MITCHELL( 1947) crossing medium, however, was used almost exclusively as the routine culture medium so that heterokaryosis for mating type could be more easily detected. VOGEL’SMedium N (1956) was used when en- hancement of conidiation was desired. All mutants were of ultraviolet origin and were obtained by means of the filtration-concentration technique (WOODWARD,DEZEEUW and SRB 1954). Be- cause the heterothallic A and a components of N. tetrasperma usually conidiate poorly as homokaryons, 85A and 85a were grown in mixed culture (85A i- 85a) to increase conidial yield for irradiation purposes. Formation of unwanted peri- thecia in the mixed cultures was avoided by incubation at 35°C. Use of the mixed cultures actually aided in screening isolates from the post-irradiation sorbose plates, since isolates which fruited could not have originated from uni- nucleate conidia and therefore would probably not be homokaryotic for a mutation. Mutant strains were crossed to wild type. Both ascus (unordered) and random- ascospore isolations were made directly from dissection plates to slants, followed by heat shocking in a 60°C water bath for 4.0 minutes to induce germination. Sorbose colonizing medium ( NEWMEYER1954) was not employed in the original ascospore isolations. First division segregations and half of second division segregations both produce asci having ascospores heterokaryotic with respect to a marker-gene (Type I ascus). Asci having homokaryotic ascospores (Type I1 ascus), however, uniquely represent the other half of the second division segregations (Figure 1) . Second division segregations, therefore, are detected by observing Type I1 asci. Second division segregation of a marker results from crossing over between the marker and the centromere. Following second division segregation, the tetrad nuclei assume by chance either one of two kinds of arrangements (Figure 1) . One arrangement results in Type I asci; the other in Type I1 asci. Since these two ascus types should be equally frequent, second division segregation fre- quency is found by doubling the observed frequency of Type I1 asci (Figure 2). The centromere distance in standard map units, being half the percentage of second division segregation (LINDEGREN1933), is therefore simply the observed percentage frequency of Type I1 asci. Random ascospore analysis utilizes the fact that half the ascospores which originate in Type I1 asci are homokaryotic for the mutant allele. Doubling the observed percentage of random mutant ascospores, therefore, gives the percent- age of Type I1 asci that produce them and hence the centromere distance (Figure 2). Neurospora tetrasperna MARKERS 125 Occasionally only one nucleus is cut out in a N. tetrasperma ascospore (DODGE 1927). Such ascospores are usually dwarf and were purposely avoided in these studies. Even in normal-sized, binucleate ascospores, however, only one nucleus may survive and produce homokaryosis interpreted as crossing over. This anomaly was minimized in these studies by scoring all isolates for self-fertility and hence for the presence of two initially viable
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