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Incomplete Y Chromosomes Promote Magnification in Male and Female Drosophila (Ribosomal Genes/Ribosomal Gene Amplification) DONALD J

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Incomplete Y Chromosomes Promote Magnification in Male and Female Drosophila (Ribosomal Genes/Ribosomal Gene Amplification) DONALD J Proc. Nati. Acad. Sci. USA Vol. 84, pp. 2382-2386, April 1987 Genetics Incomplete Y chromosomes promote magnification in male and female Drosophila (ribosomal genes/ribosomal gene amplification) DONALD J. KOMMA AND SHARYN A. ENDOW* Department of Microbiology and Immunology, Duke University Medical Center, Durham, NC 27710 Communicated by D. Bernard Amos, December 12, 1986 ABSTRACT We have recently shown that magnification, on the Y that might encode a gene whose product initiates an increase in the number of ribosomal RNA genes (rDNA) in breaks in the rDNA or results in unequal pairing. Alterna- gametes produced by rDNA-deficient flies, can occur in female tively, the involvement of a limited region of the Y chromo- Drosophila if they have a Y chromosome. We now have tested some might imply a chromosomal pairing function analogous several X-Y translocation and recombinant chromosomes to to that of the collochores described by Cooper (8). determine which parts of the Y chromosome are necessary for The Ybb- chromosome, discovered by Schultz in 1933 (9), magnification to occur in females. Our data indicate that the has been described as being particularly effective in promot- required region is the distal part of the long arm of the Y ing magnification (1, 10, 11). In addition to promoting a high chromosome, yL. We have also used X-Y translocation chro- frequency of magnification in males carrying an Xbb chro- mosomes to study magnification of rDNA-deficient X chromo- mosome (1), it brings about the production of new bb alleles somes in males. Our data show that the region of the Y in males carrying an Xbb+ chromosome (2, 11, 12), and its chromosome from the distal end of the nucleolus organizer derivatives can bring about magnification of an Xbb chro- through the centromere is not required for magnfication in mosome in males of a bb+ phenotype (13), suggesting that it males. The frequency of magnification in males with rDNA- is in some sense "constitutive" for magnification. No other deficient Y fragments is comparable to that produced by Ybb-, Ybb- chromosomes have been discovered. However, among a chromosome that has often been used to produce magnifica- the reciprocal X-Y translocations produced by Kennison tion in males. These results demonstrate that the Ybb- (14), there are two Y fragments that together contain all ofthe chromosome is not uniquely effective in causing magnification Y fertility factors but have no additive effect in males with an to occur in males. The results of these studies imply that Xbb chromosome, indicating that they are completely or sequences present on yL are required for magnification to almost completely lacking in rDNA. By putting both ofthese occur in females; these sequences are probably also required fragments into males with an Xbb chromosome, we can for magnification in males. Since unequal sister chromatid produce the equivalent of a new Ybb- chromosome. This exchange has been implicated as the major mechanism of procedure can be used to learn whether or not any unique ribosomal gene increase during magnification, the yL se- feature of Ybb- is required for magnification. The procedure quences required for magnification may be involved in encod- also can provide at least some information as to which parts ing or regulating products needed for sister chromatid recom- of the Y chromosome are needed for magnification in males. bination in germ-line cells. Inasmuch as both arms ofthe Y chromosome contain factors necessary for male fertility, it would be very difficult to learn Magnification is an increase in the amount of rRNA genes anything about magnification in males completely lacking a Y (rDNA) in gametes produced by severely rDNA-deficient or chromosome, but this method allows us to examine males bobbed (bb) Drosophila melanogaster, resulting in a marked lacking a significant part of the Y. reversion toward wild type in the offspring (1). The major mechanism by which this increase occurs is most probably MATERIALS AND METHODS unequal sister chromatid exchange (2, 3), but other mecha- nisms are also possible (4). We have reported (5) that Drosophila Stocks. Descriptions of all mutants used in this magnification, hitherto known only to occur in males, can work can be found in Lindsley and Grell (9). The b19 occur in severely bobbed females if the females have a Y chromosome was obtained from R. S. Hawley in March, chromosome. The frequency of magnified gametes produced 1984, and cloned in June, 1984. The y bb2 chromosome was by such females is about 1-2%. recovered after recombination in a b19/y car bb+ female. A single y bb recombinant chromosome was cloned in Novem- X-Y translocation and recombinant chromosomes can be ber, 1985. The uco3 bb chromosome was found by K. C. used to learn which parts of the Y chromosome are required Atwood (15). The y mutation was placed on the chromosome for magnification to occur in females. Such tests cannot by D.J.K. in 1974 by recombination in a bb/y car bb+ female. easily be performed in males because both arms of the Y The stock was cloned in October, 1984. chromosome are required for male fertility. Therefore, the The In(l)sc4LscSR, sc4sc8 chromosome is an inverted X fact that the Y chromosome is needed for magnification in chromosome with the nucleolus organizer deleted. It is females provides an opportunity to learn whether all of the Y referred to as X-NO in this report. The C(1)DX chromosome is required or only a small part ofit. Requirement for an entire is a compound double-X chromosome with both nucleolus Y chromosome, iffound, would imply an effect similarto that organizers deleted and is denoted A-NO. Both of these of suppression-of-position effect variegation by the Y chro- variant chromosomes are described in Lindsley and Grell (9). mosome (6, 7). The requirement for a limited region of the Y The XYbb- chromosome was made by D.J.K. and is chromosome would suggest the involvement of a single locus described in Komma and Endow (5). It consists of an X chromosome deficient for bb but normal in sequence and The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviation: rDNA, 18S and 28S rRNA genes. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 2382 Downloaded by guest on September 27, 2021 Genetics: Komma and Endow Proc. Natl. Acad. Sci. USA 84 (1987) 2383 kl-5 kl-3 kl-2 kl-l NIt, ks-l ks-2 -v+ w19 ---o vi y+ 82 w28 BS v31 BS P7 Bs v24 Bs FIG. 1. Schematic diagram of the Y chromosome fragments used in this work. The top line shows a BsYy+ chromosome; the w19, w28, v31, P7, and v24 X-Y translocation chromosomes were derived from this Y chromosome. The approximate positions of the male fertility factors on the long and short arms of the Y chromosome are indicated. The X-Y translocation chromosomes are shown with solid lines indicating Y chromosome sequences and dashed lines representing regions from the X chromosome. The open and filled circles represent centromeres from the X and Y chromosomes, respectively. It is not certain whether the centromere and bb locus in scvl.Ys are from the X or Y chromosome. All Y fragments shown are either bb0 or bb- except for the scvl.Ys chromosome, of which a severely bobbed variant was used. attached to the long arm of Ybb-. It contains all of the Y contains kl-S, is marked with Bs, and has no additive effect chromosome male fertility factors. when combined with an Xbb chromosome. X-Y Translocation Chromosomes. The translocation chro- Two other Y-fragment chromosomes were obtained from mosomes furnished to us by D. L. Lindsley were made by the Bowling Green stock center in November, 1985 (Fig. 1). Kennison (14) and further characterized and described by The scvl.Ys chromosome (18) is the result of a recombination Hardy and co-workers (16, 17). They are maintained as between the Y chromosome and the centromeric heterochro, reciprocal X-Y translocations in balanced stocks. The Y- matin of the scvl chromosome. It contains all of the Ys fragment translocations are diagrammed in Fig. 1 and are fertility factors, but it is not certain whether the centromere briefly described as follows. and bobbed locus are from the X or Y chromosome. After the T(J;Y)w19. The short arm of the Y chromosome, Ys, is stock was obtained, males were mated to C(J)DX y w brokenjust distal to the nucleolus organizer and the tip of Ys, females, and a severely bobbed LNO/Ys female carrying marked with y', is attached to the X centromere. The Ys tip the scvl.Y chromosome was selected. This chromosome was contains all of the Ys fertility factors and has no additive cloned in January, 1986, and is called scvl.Ysbb in this report. effect when combined with an Xbb chromosome, suggesting The YL y+B2 chromosome (19) is the result of a recombina- that it is completely or almost completely deficient for rDNA. tion between Ys and the distal heterochromatin of In(1)sc8L, T(J;Y)w28. yL is broken just distal to the centromere and ENR. It contains all of yL and the Y centromere, but not the attached to the X centromere. The yL fragment contains all nucleolus organizer. It is marked with y'. of the yL fertility factors, is marked with Bs, and has no Magnifying Crosses.
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