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The Nucleolar Organizer* (Genetic Interaction/Interspecific Hybridization/Genetic Divergence/Suppressed Loci) HERMIONE E

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The Nucleolar Organizer* (Genetic Interaction/Interspecific Hybridization/Genetic Divergence/Suppressed Loci) HERMIONE E Proc. NatI. Acad. Sci. USA Vol. 74, No. 8, pp. 3498-3502, August 1977 Genetics Gene regulation in Drosophila mulleri, D. arizonensis, and their hybrids: The nucleolar organizer* (genetic interaction/interspecific hybridization/genetic divergence/suppressed loci) HERMIONE E. M. C. BIcUDOt AND R. H. RICHARDSON*§ t Instituto de Biociencias, Letras e Ciencias Escatas de Sio Jose do Rio Preto, Sao Paulo, Brazil; and * Department of Zoology, University of Texas at Austin, Austin, Texas 78712 Communicated by Verne Grant, May 16, 1977 ABSTRACT Typically, Dwsophila have nucleolar organizer the various ways for having additional rDNA when needed in regions (NORs) confined to the sex chromosomes. Salivary gland abnormal circumstances that have been observed in several cells of hybrids between Drosophila mulleri females and D. for a single species.- Which arizonensis males exhibit features in nucleolar organizer reg- species may be options available ulation that differentiate the species on one hand, and which particular option is activated depends upon the response of a show an interplay between the X and the microchromosome on regulation system to the circumstances. the other hand. In the hybrid females only the X chromosome from D. ari- zonensis appears to be attached to the nucleolus. In the hybrid MATERIALS AND METHODS males the X chromosome, from D. mulleri, also does not seem lines from to contain a functional NOR. However, in hybrid males the The stock of D. mulleri is a pool of twenty isofemale microchromosome from D. arizonensis increases greatly in size Guayalejo, Mexico, and the stock of D. arizonensis is a pool of and appears to be associated with the nucleolus. The increase 25 isofemale lines from the same area. The hybrids were ob- in size of the microchromosome involves a 4-fold increase in tained in crosses between D. mullei females and D. arizonensis DNA content. In D. anizonensis and in hybrid females the NOR males. This cross yields fertile females and sterile males, while of the microchromosome appears to be suppressed. In the ab- the reciprocal cross is incompatible (22). sence of an arizonensis X chromosome, the NOR of the micro- brains were chromosome typically is active, while the NOR on the mulleri The squashes of salivary glands and prepared X chromosome remains suppressed. Therefore, the ribosomal using two stain techniques: lacto aceto-orcein (8) and Feulgen cistrons and interchromosomal regulator element appears to (9). About 60 hybrid larvae of both sexes and more than 200 be duplicated on both the X chromosome and microchromo- larvae of each parental species were analyzed. some of D. arizonensis, but with epistatic suppression of the The relative width in a salivary gland preparations of chro- microchromosomal NOR by the arizonensis X-linked NOR. mosome 6 (microchromosome) was measured in photographic Either arizonensis NOR, X linked or microchromosomal, sup- prints, taking the ratio of the major width of this chromosome presses the mulleri NOR. to the width of a dark condensed band considered to be repre- The vital role played by ribosomes in the physiological economy sentative of the general width of another autosome. Synapsed of a cell is clearly illustrated in the systems that have evolved chromosomes were measured in the parental species and to ensure an adequate supply of 18S and 28S rRNA. Not only asynapsed single chromosomes were measured in the hybrids. are the ribosomal cistrons amplified and transcribed in a special In the hybrids, the same autosomal band was used for com- organelle, the nucleolus, but a variety of "backup" strategies parison of both microchromosomes in a cell. have been observed in a range of eukaryotes. These alternative For DNA content estimates, the area of chromosome 6 was or compensatory abilities are activated when unusual conditions measured in black-and-white transparency enlargements of the arise. For example, oocytes of vertebrates and invertebrates same magnification, and the average percent absorbance of synthesize prodigious amounts of polypeptides, and some Fuelgen-stained chromosomes was obtained from scans with species have high degrees of nuclear extra-chromosomal rep- a Gilford 250 spectrophotometer (narrow slit, 500 \nm). Care lication of DNA (1-3). Compensatory replication of the rRNA was taken to make all exposures in the linear range of the genes of Drosophila melanogaster also occurs when one nu- emulsion and transparancies were developed together. Mea- cleolar organizer chromosome is completely or partially defi- surements taken from several chromosomes were averaged. cient in its nucleolar organizer region (NOR). In some of these Using a parental species as a reference, the relative amount of cases the additional copies of rRNA genes (rDNA) are DNA per chromosome was calculated from the product of area structurally integrated into the genome (4), while in other cases and average absorbance. In the parental species, measurements they are not (4, 5). In maize, there appears to be a reserve of were of synapsed chromosomes, so the DNA values were di- ribosomal cistrons that may be activated (6). Also, when NORs vided by two. are totally absent, nucleolar material (which probably contains some rRNA) is synthesized by alternative loci (7). RESULTS These examples illustrate two alternative strategies of X chromosomes are ho- achieving rDNA synthesis, extra-chromosomal and chromo- The D. mulleri and D. arizonensis available mosequential. However, they can be recognized in salivary somal, as well as the possibility of latent cistrons being gland cells by some consistent morphological differences. For for emergency use. The experiments reported here suggest that example, there is a distinct difference in the thickness of a single The costs of publication of this article were defrayed in part by the payment of page charges from funds made available to support the Abbreviations: NOR, nucleolar organizer region; rDNA, genes for research which is the subject of the article. This article must therefore rRNA. be hereby marked "advertisement" in accordance with 18 U. S. C. * This is part I of a series. §1734 solely to indicate this fact. § To whom reprint requests should be addressed. 3498 Downloaded by guest on September 30, 2021 Genetics: Bicudo and Richardson Proc. Natl. Acad. Sci. USA 74 (1977) 3499- A Cv FIG.1.Proximal part of the X4 chromosomesa , . in hybrid females. -. 4 - to wo ferecei th shp o th poimalf en.Thadigpatr iw.;:~ a t; of~th~~rxi 0 (ma setoseF-5tFI)othX cho /~~~~~ portinof thi reio ma beosevd N I N the en sh owcinpoximlThe and of owusheXcrmsomasa morp frqen'al is attahe FIG. 2. Association between the X chromosome and the nucleolus (N) in D. mulleri and D. arizonensis. (A) D. arizonensis male; (B) D. arizonensis female; (C) D. mulleri male; (D) D. mulleri female. Note strands which connect nucleolus to separate X chromosomes phowionsg th isan (regonw bsed obseamrved. ia m rerfr in the females and males. The magnifications in A-D are the same. tIncthe gln=elsoD.mulleniD. arizonensis,.Tesae nti n FIG.X1.hProximal partcofdthe Xhchromosomes inthybridafemales to the nucleolus. Although no clear connection between the X and the nucleolus was observed, the possibility of a frneithshpoftheproximalend.ohcrmsmfreqentlydisg pattacedn connection dIst Profhisma chromosomeisnparentas i foralse not the ( could be excluded in some cases (Fig. 4D). tof tionnuclolus,(Mhe D. mulle(apscommonschr izoonensi)locationofthefofscaleithe th israndinro The banding pattern of chromosome 6 is not as distinct as in the other chromosomes. It shows variable degrees of banding 4fereuncesin,Band(Fi.)soctadinshaperThethf th tprxmledTheuoo~fhowversomapincrebandingl1)adasophatendif- disorganization not associated with the larval developmental dithenulei80 fthesncleolu lighter,omsapperdn malen.Syassfrom stages. These phenomena are observed in D. mulleri and D. widMostibothn of speciesthes e io hybaddoob s mvemoalesdfte.acell t ha isp lae de arizonensis, but are more striking in D. mulleK. In both species, aretunusuallwidery thand thelatoomsof thler same azorthns one to three heterochromatic dark granules are visible at the theth XpcroxmosoesdDevari ne aromsnoeof the malesoinsthein vole (Fbis.parequntalyinso seies ofa(Fig.het proximal end of the polytene chromosome 6 (Fig. 5 A and 4tA Be andlC).usTheydstainlghterhomoweersoaton theiNcRes in B). The morphology of the polytene chromosome 6 found in the withe Doe notnecesisarlmladoewsnovd(itina aotheseIn o parental species is preserved in the hybrid females. They are asynapsed, as are the other chromosomes. However, the mi- crochromosomes frequently appear joined to each other hyrdthe X chromosomeoth smaetime isepositinedl adjaient(ig by the proximal regions, directly or through strands (Fig. 5 C and D). In the hybrid males, one of the microchromosomes increases Table IC Distribution of average width of the microchromosomes relative to autosomes in males and females of D. mulleri, D. arizonensis, and the interspecific hybrids Microchrom- osome No. of chromosomes with the indicated ratio to reference bandt No. Aver- mea- 1.0- 1.6- 2.1- 2.6- ... 3.6- 4.1- 4.6- 5.1- ... 6.6- ... 7.5- age Source Sex Type* sured 1.5 2.0 2.5 3.0 4.0 4.5 5.0 5.5 7.0 8.0 ratio D. arizon- ensis 9 A 22 13 9 1.47 a A 22 10 9 2 1 - 1.68 D. mulleri 9 M 20 8 10 2 - 1.67 d M 22 7 11 4 1.70 Hybrid 9 A 20 7 9h 3 1 1.76 M 20 3 11 4 2 2.04 d A 19 - 1 3 7 2 2 2 1 1 4.25 M 21 1 7 9 4 - 2.26 * A = D. arizonensis; M = D. mulleri. t See text for procedure. Downloaded by guest on September 30, 2021 3500 Genetics: Bicudo and Richardson Proc. Natl. Acad. Sci. USA 74 (1977) .$*40~ ~ JL A) a:*% '; %- low~ ~ ~ ~ A Jr-, X < f~t~s^:} N *t; Gil ,\4, 3., FIG. 3. Hybrid female cells showing only the D. arizonensis X attached to the nucleolus.
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