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Drosophila Pseudoobscura Copyright 0 1993 by the Genetics Society of America Structural Changes in the Antennapedia Complex of Drosophila pseudoobscura Filippo M. Randazzo,’ Mark A. Seeger,*Catherine A. HUSS,Margaret A. Sweeney, Jeffrey K. Cecil and Thomas C. Kaufman’ Howard Hughes Medical Institute, Institutefor Cellular and Molecular Biology, and Programs in Genetics and Cellular, Molecular and Developmental Biology, Department of Biology, Indiana University, Bloomington, Indiana 47405 Manuscript received October 16, 1992 Accepted for publication January 27, 1993 ABSTRACT The discovery of the striking positional conservation between the Antennapedia and Bithorax homeotic gene complexes (ANT-C and BX-C) in Drosophila melanogaster and the murine Hox and human HOX clusters has had a substantial impact on our understanding of the evolution of development and its genetic regulation. Structural differences do exist among the mammalian Hox complexes and the ANT-C in D. melanogaster. To gain further insight into the evolutionary changes among these complexes, the ANT-C was cloned in the closely related species, Drosophila pseudoobscura. The overall structure of the ANT-C in D. pseudoobscura is highlysimilar to its D. melanogaster counterpart; however, two differences in the organization of the ANT-C have been identified. First, the 22 gene, a member of the ANT-C in D. melanogaster, is not present in the D. pseudoobscura ANT- C and is possibly absent from the D.pseudoobscura genome. Second, the orientation of the Deformed gene is inverted in D. pseudoobscura, providing it with a 5’to 3‘ direction of transcription identical to the remaining ANT-C homeobox genes with the exception of fushitarazu. These differences demonstrate that subtle changes can occur in ANT-C structure during relatively short periods of evolutionary divergence, although the fundamental organization of the complex is conserved. These - - v observations and others suggest that the complex is not absolutely rigid but that selective pressures have maintained this organization of genes for some Functional reason that remains elusive. HE discoveries of the Antennapedia Complex PANGand EICHELE 1989; IZPISUA-BELMONTEet al. T (ANT-C) and the Bithorax Complex (BX-C) in 199 l), and the German cockroachBlattella germanica Drosophila melanogaster (KAUFMAN,LEWIS and WAKI- (Ross and TANAKA1988) and the red flour beetle MOTO 1980; LEWIS1978) and the subsequentisolation Triboliumcastaneum (STUARTet al. 1991).Genetic of cognate Hox complexes in mammals(DUBOULE and analysis ofTribolium has uncovered a combined DOLLE 1989;GRAHAM, PAPLOPULUand KRUMLAUF ANT-C/BX-C-like gene complex referred to as the 1989; BONCINELLIet al. 1988) have contributed sig- HOM-C (BEEMANet al. 1989). Its member genes are nificantly to an understandingof the evolution of the functionally homologous and similarly aligned to the developmental process and its genetic control. It has ANT-C and BX-C homeotic genes of Drosophila(BEE- become increasingly clear that not onlyare genes that MAN et al. 1989). Furthermore, four duplicated sets encode metabolically important products conserved of genes with high sequence similarity to theANT-C/ across phyla, but alsoloci that encode developmentally BX-C genes has been found in the mouse (Hox) and importantgene products. Among the develop- in humans (HOX)(see AKAM1989 forreview). These mentally important genes, homeobox genes have been observations taken together indicate that the homeo- isolated from a large array of eucaryotic species (see box must have been present early on in the evolution SCOTT, TAMKUN,and HARTZELL1989 for a review). of eucaryotes, and a combinedANT-C/BX- C-like Perhaps more significantly, clustered sets of homeo- complex must have been present before protostomes box genes have been discovered in humans (BONCI- and deuterostomes diverged over 500 million years NELLI et al. 1988), mice (DUBOULEand DOLLE 1989; ago. GRAHAM,PAPLOPULU and KRUMLAUF 1989;KAPPEN, The structure of the ANT-C and the BX-C in SCHUGHARTand RUDDLE1989), chickens (WEDDEN, D. melanogaster is characterized by the unusual proximity ’ Present address: Mount SinaiHospital Research Institute, 600 University of a significant number of developmentally important Avenue, Toronto, Ontario M5G 1x5, Canada. * Present address: Programin Molecular and Cell Biology, Oklahoma genes and by the collinearity between homeotic gene Medical Research Foundation, 825 Northeast 13th Street, Oklahoma City, position on the chromosome and their respective func- Oklahoma 73104. ’Present address: Howard Hughes Medical Institute, Department of tional domains along the anterior-posterioraxis ofthe Biology, Indiana University, Bloomington, Indiana 47405. animal. The numerous homeobox-containing genes Genetics 133: 319-330 (May, 1993) 320 F. M. Randazzo et al. of both these complexes presumably arose through a the murine HOX complexes and the human HOX series of duplication and divergence events (LEWIS complex. 1978). In contrast to the clustered configuration of To address the questions pertaining to the rigidity these genes, inversion events normally tend to rear- of the ANT-C organization and the unique presence range genesover evolutionary time (STURTEVANT and ofnonhomeotic genes withinits boundaries, the TAN1937; DOBZHANSKYand STURTEVANT 1937). ANT-C in Drosophila pseudoobscura was cloned. Pre- Thus, the extreme proximity of the homeobox genes viousstudies have documented numerous chromo- inferssome form of evolutionary constraint on somalchanges in D.pseudoobscura whencompared change.At least twohypotheses could explain the with D. melanogaster, indicatingthe potential for existence of the homeotic gene complexes: (A) these changes in the ANT-C (STURTEVANTand TAN1937; genescannot function or do notfunction as well DOBZHANSKYand STURTEVANT 1937; STEINEMANN, outside the domain of the complexes, e.g., because of PINSKERand SPERLICH1984). The cloning of ANT- possible chromatinstructure requirements; (B) the C from a secondDrosophilid species, estimated to juxtaposition of the member genes and their complex havediverged approximately 46 millionyears ago cis-regulatoryregions makes separation by random (BEVERLY andWILSON 1984), and the previous clon- genetic processes highly unlikely or even impossible, ing of homologous homeobox gene clusters in two thereby maintaining the ancient configuration. mammalian species (mouse and human), estimated to The uniquecharacteristics of the ANT-C in D. have diverged roughly 68 million years ago (BENTON melanogaster necessitate evolutionary analysis in more 1990), presents an opportunity to explore patternsin closely related species to determine the plasticity of the more recently evolutionary history of homeobox the ANT-C structure. The ANT-C containsfive hom- gene complexes. eotic genes that specify head and thoracic segmental identity, Antennapedia (Antp), Sexcombs reduced (Scr), MATERIALS AND METHODS Deformed (Dfd),proboscipedia (pb)and labial (lab) [see Cloning ANT-C The chromosome walk was performed MAHAFFEYand KAUFMAN 1987or KAUFMAN, SEEGER using techniques described in SCOTTet al. (1983). Both and OLSEN1990 forreview]. The ANT-C differs from lambda EMBL-4 (gift of C. LANGLEY,University of Califor- nia, Davis) and lambda DASH-2 (gift of T. HAZELRIGG, the BX-C [see DUNCAN 1987 and PEIFER,KARCH and Columbia University) D. pseudoobscura genomic libraries BENDER 1987 for review] and from the murine Hox were used. The Ayala strain was used to make the EMBL-4 (DUBOULEand DOLLE 1989;GRAHAM, PAPLOPULU library. All clones except for p191, p195, p474, p475 and and KRUMLAUF 1989;KAPPEN, SCHUCHART and RUD- p488 were obtained from the EMBL-4 library. Prehybridi- zation and hybridization were performed using either 4X DLE et 1989) and humanHOX (BONCINELLI al. 1988) SSC, 5X Dendhardt's solution, 0.1% (w/v) SDS and 0.1% complexes in that it carries some unique homeobox (w/v) carrier calf thymus DNA at 65" (interspecies and genesinvolved in establishingthe embryonic body intraspecies hybridizations) or 5X SSC, 5X Denhardts, 0.1 % plan, namely zen,ftr and bcd. The pair rule genefushi (w/v) SDS and 0.1 % (w/v) calf thymus DNA plus either 30% tarazu (ftz) acts to divide the embryo into segments (w/v) formamide (intraspecies) or 50% (w/v) formamide (interspecies) at 42". Intraspecies hybridizations were fol- (WAKIMOTO,TURNER and KAUFMAN 1984;WEINER, lowed by 0.1X SSC, 0.1 % (w/v) SDS, 0.1% (w/v) sodium SCOTTand KAUFMAN 1984), the maternal effect gene py.rophosphate washes (IX wash at room temperature for 4 bicoid (bcd) encodes a morphogen important in estab- mln followed by 2X washes for 40 min at 65'). The same lishinganterior-posterior polarity (FRIGERIO et al. conditions were used for Southern hybridizations. Probes were made by the nick translation method using Amersham 1986; BERLETHet al. 1988),and the zygotic gene kits (Arlington Heights, Illinois). All lambda genomic clones zerknullt(ren) specifies dorsal embryonic structures recovered in this study were mapped with five restriction (WAKIMOTO,TURNER and KAUFMAN 1984;RUSHLOW enzymes (BurnH1, EcoRI, HindIII, Sal1 and XbaI). Cuticle- et al. 1987). In addition, thez2 gene, which is located like genes were identified by Southern blot hybridization using a pIBI5 1 RX 1.5 (a known cuticle gene) subclones as justproximal to Zen, contains a zen-like homeobox probes (FECHTELet al. 1988; FECHTEL,FRISTROM and FRIS- (RUSHLOWet al. 1987; PULTZ et al. 1988). It is ex- TROM 1989) WITHTHE METHODS AND CONDITIONS AS DE- pressed in a pattern similar to that of zen, but has
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