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MAPPING OF ELECTROPHORETIC SITES IN DROSOPHILA MELANOGASTER : FIDELITY O F INFORMATION TRANSFER BY GENE CONVERSION 1

A convenient method is described for the intracistronic mapping of genetic sites responsible for electrophoretic variation of a specific protein in Drosophih mezanogaster. A number of wild-type isoalleles of the rosy locus have been isolated which are associated with the production of electrophoretically distinguishable xanthine dehydrogenases. Large-scale recombination experiments were carried out involving null enzyme mutants induced on electrophoretically distinct wild-type isoalleles, the genetic basis for which is followed as a nonselective marker in the cross. Additionally, a large-scale recombination experiment was carried out involving null enzyme rosy mutants induced on the same wild-type isoallele. Examination of the electrophoretic character of crossover and convertant products recovered from the latter experiment revealed that all exhibited the same parental electrophoretic character. In addition to documenting the stability of the xanthine dehydrogenase electrophoretic character, this observation argues against a special mutagenesis hypothesis to explain conversions resulting from allele recombination studies. ALLELE recombination studies in Drosophila have been restricted heretofore to experiments utilizing mutants associated with visible phenotypic effects and/or enzyme inactivation. The present report describes a convenient method for the intracistronic mapping of genetic sites responsible for electrophoretic variation of a specific protein in Drosophila melanogaster which may be useful for several areas of investigation. The use of electrophoretic variants as markers facilitates investigation of two kinds of questions bearing upon the fidelity of the conversion process. The first question relates specifically to the two sites of heterozygosity in an individual heterozygous for two different mutant alleles. One point that has not been established questions whether, for those sites of heterozygosity, the conversion process in Drosophila is a conservative one, utilizing the preexisting genetic input, or whether conversion generates novel information at those sites. This question may be approached by searching for isoallelic differences among the wild-type exceptions produced in large-scale intracistronic recombination experiments. If the mutants used in this experiment were induced on the same isoallelic background, This investigation was supported by a research grant, GM-09886, from the Public Health Service Genetm 76: 289-299 February, 1974. 290 M. MCCARRON, W. GELBART A N D A. CHOVNICK wild-type exceptions of new isoallelic classes would indicate a lack of fidelity in the conversion process. A search of this nature simultaneously questions fidelity of information transfer involving a segment of DNA far greater than the two sites of heterozygosity discussed above, possibly involving most of the DNA sequence that codes for the polypeptide under investigation. With the development of suitable genetic systems for detailed analysis of conversion in Drosophila, a compelling case can be made that relates conversioll to the process of linked exchange (CHOVNICK, BALLANTYNE and HOLM 1971). An alternative interpretation relates conversion to the enigmatic case of the “mutable” reddish-alpha allele in DrosophiZa uirilis (DEMEREC 1928). This viewpoint suggests that conversion, as seen in Drosophila, really is a special mutagenesis that only occurs in heterozygous females (HEXTER 1963). By attempting to uncover differences in the wild-type alleles generated by conversion as compared to crossover products recovered from females heterozygous for two mutant alleles of a given cistron, some limit may be placed on the special mutagenesis hypothesis. Traditionally, the crossovers are inferred to represent exchanges of separable parts of the cistron, thereby restoring the original wild-type allele. If convertants arise by a mutation-like event, then one might anticipate that this class would include an array of wild-type isoalleles which would be distinguished from the original wild-type allele through an examination and comparison of the function of their respective gene products. Just such investigations have failed repeatedly to uncover differences between crossover and convertant products involving the garnet ( CHOVNICK 1958) , maroon-like (FINNERTY, DUCK and CHOVNICK 1970) and rosy (CHOVNICK et aZl970) loci. However, in all of these studies, the power of the methods used to distinguish between slight differences in wild-type isoalleles remained as a serious question. The present report describes an experiment which explores this point through electrophoretic characterization of crossover and convertant products. MATERIALS AND METHODS The genetic system: The msy cistron in Drosophila melanogaster (ry:3-52.00) is a solitary unit concerned with the enzyme xanthine dehydrogenase (XDH), located within an intensely mapped short region of the right arm of chromosome 3 (salivary section 87D). Strong genetic and biochemical evidence argues that rosy is a structural gene for XDH (GRELL 1962; YEN and GLASSMAN 1965). Mutations restricted to the rosy cistron are homozygous viable, and fall into two groups: (1) a class of “wild-type isoalleles” which produce electrophoretic variants of the enzyme (YEN and GLASSMAN 1965) ; and (2) a large group of mutants which are enzymatically inactive and exhibit a brownish mutant eye color phenotype resulting from a reduction in the red (drosopterin) pigments (CHOVNICK et al. 1964). Study of the latter class of mutants failed to find any evidence of allele complementation (SCHALET, KERNAGHAN and CHOVNICK 1964), and investigation of allele recombination heretofore has been restricted to this class of mutants. Figure 1 presents a map of the centromere-proximal region of the right arm of chromosome 3 of Drosophila melunogaster indicating the location of rosy, the centromere, and other markers used in the study (LINDSLEY and GRELL 1968). In addition, Figure 1 presents a summary map of separable sites within the rosy cistron obtained from prior experiments of enzymatically inactive mutants (CHOVNICK 1966; CHOVNICK, BALLANTYNE and HOLM 1971). Several sites responsible for electrophoretic variation of XDH have been localized within the existing map, and their distributim argues strongly that most, if not all, of this map includes genetic information coding CONVERSION IN DROSOPHILA 29 1 M(3 )s34 r i Cfd cu kar ry &(3)26 Sb UbX