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Genetic Analysis of Chromosomal Region 67A-D of Drosophila Melanogaster

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Genetic Analysis of Chromosomal Region 67A-D of Drosophila Melanogaster Copyright 0 1988 by the Genetics Society of America Genetic Analysis of Chromosomal Region 67A-D of Drosophila melanogaster Brenda G. Leicht' and J. JosC Bonner2 Department of Biology, Indiana UniversiCy, Bloomington, Indiana 47405 Manuscript received December 17, 1987 Accepted March 3, 1988 ABSTRACT Inan effort to (1) characterize the 67 interval of chromosome 3 of Drosophila melanogaster genetically and(2) isolate mutations of the 67B1 small heat shock protein (hsp) gene cluster specifically, we undertook a mutational analysis of the 67A-D subinterval. Using a deficiency of the 67A2 to 67D11-13 region, Df(3L)ACI, we screened 8700 diepoxybutane-treated chromosomes and 7800 ethyl methanesulfonate-treated chromosomes for visible and lethal mutations throughout this interval and recovered 74 independent recessive lethal mutations, but no visible mutations. One of the lethal mutations, d29A6, was identified as an overlapping deficiency extending from 66F3 to 67B1. An additional 6000 diepoxybutane-treated chromosomes were screened for lethality over d29A6, yielding anotherfour lethal mutations within the 67A2-Bl subinterval. These 78 lethal mutations, along with two others isolated in other laboratories, define 23 essential loci-6 within the 67A2-Bl subinterval and 17 within the 67A2 to Dl 1-13 subinterval. Many of these loci appear to be required for imaginal development only, exhibiting late larval to pharate adult lethal phases. Examination of the 67A2-Bl lethal complementation groupsfor (1) earlier onset of lethality following a heat shock, (2) missing or altered small hsps on two-dimensional protein gels, and (3) restoration of viability by transformed wild-type copies of the small hsp genes indicates that none of these mutations affect the small hsps. On the basis of this analysis and the known homology of the genes, we conclude that the small hsps are functionally equivalent. HE availability of sophisticated genetic, cytolog- (SHEARNet al. 1971; SHEARN,HERSPERGER, and HER- T ical, and, more recently, molecular techniques SPERGER 1978). The recessive wing mutation curooid has allowed characterization of a considerable portion [cur] had also been mapped to approximately 67C of the Drosophila melanogaster genome (for example; (30.0 map units), but subsequent investigation has seeGAUSZ et al. 1981, 1986;HILLIKER et al. 1980; called this map position into question (LEICHT1987). HOCHMAN1976; JUDD, SHEN, and KAUFMAN 1972; In an effort to characterize the 67 region of D. KAUFMAN,LEWIS, and WAKIMOTO1980; KOTARSKI, melanogaster further, we have carried out screens for PICKERT,and MACINTYRE 1983;LEFEVRE 1981; ROB- diexpoxybutane (DEB)- and ethyl methanesulfonate ERTS et al. 1985; WOODRUFFand ASHBURNER 1979). (EMS)-induced recessive visible and lethal mutations Nonetheless, many regions of the Drosophila genome throughout the 67A2 to 67D11-13 subinterval. As a still remain largely uncharacterized, both genetically second goal of this analysis, we have attempted and molecularly. Among the regions for which little specifically to isolate mutations of the small heat characterization has been reported is the 67 interval shock protein (hsp) genes. These four genes, along of chromosome 3. Although this region contains 56 with three closely related genes (gene 1, 2, and 3), chromosome bands (BRIDGES 1941),very few known are tightly clustered in a 15-kb region at polytene genetic loci have beenmapped to this region (see chromosome band 67B1 (CORCESet al. 1980; CRAIG Figure 1). Among the few genes reported to map and MCCARTHY1980; VOELLMYet al. 1981;AYME within the 67 intervalare thesmall heat shock protein and TISSI~RES1985). In addition to their induction genes at 67B (hp28,hsp26, hp23, and hp22; PETER- by heat and other environmental stresses (reviewed SON, MOLLERand MITCHELL1979; CORCESet al. 1980; in ASHBURNER and BONNER1979), these seven genes CRAIG andMCCARTHY 1980; VOELLMYet al. 1981), a are developmentally regulated (SIROTKIN and DAV- maternallyexpressed a-tubulin gene at 67C (KAL- IDSON 1982; IRELANDet al. 1982; CHENEY and SHEARN FAYAN and WENSINK198 1; K. MATTHEWS,personal 1983; ZIMMERMAN,PETRI and MESELSON 1983; communication), Minute(3)i [M(3)i]at 67C (Moscoso MASON,HALL and GAUSZ1984; AYMEand TISSI~RES DELPRADO and RIPOLL1983), andthe vital locus 1985). While it is thought that the small heat shock 1(3)67Fa (also known as polycombeotic [pco]) at67F proteinsperform some vital function duringheat shock, and possibly during normal development as ' Presentaddress: Department of Molecular Genetics, 484 W. 12th Avenue, The Ohio State University, Columbus, Ohio 43210. well, the specific function(s) of theseproteins has * To whom correspondence should be addressed. remained elusive. Thus, we reasoned that the isola- Genetics 119: 579-593 uulv, 1988) 580 G. B. Leicht and J. J. Bonner tion of mutations in the genes encoding these proteinsassociated with this class. If this classwas lethal or had might provide someinsight into their function(s). some visible mutant phenotype, a stock was established by However, given that the small hsp genes represent a crossing the ri pp*lTM3Ser or ri pp*/Dp(3;3)MS4male sibs to TM3SbITM6B females. Once established, all stocks were gene family (INGOLIAand CRAIG1982; SOUTHGATE, retested by backcrossing to Df(3L)ACI. AYMEand VOELLMY 1983;AYME and TISSIBRES1985), Although the vast majority of the mutagenized chro- we realized at the outset that mutations in any one mosomes were of the genotype ri pp, a group of approxi- of the genes might not confer a mutant phenotype matelB 300 EMS-treated chromosomes of thegenotype and that a deletion of the entiregene cluster may be Adhh "Zfm(3)7 were also screened for lethality or visible defects over Df(3L)ACI. Adhh6'" is an insertion of an to required do so. hp70-Adh fusion gene at cytological location 61C (BONNER This paper reports the results of our mutational et al. 1984); the presence of this insertion was irrelevant analysis of the 67A2 to D 11- 13 subinterval and pre- for the purposes of these screens. liminary characterization of the mutations obtained. Isolation of recessive lethal mutations in the 66F3-67B1 This analysis has revealed that (1) this region of the subinterval: Df(3L)29A6,a DEB-induced deletion of 66F3- 67B1 isolated in the above screens, was used to screen for chromosome contains a minimum of 24 essential loci, additional lethal mutations within the 67A2-B 1 subinterval. many of which are required for imaginal develop- These screens were essentially identical in design to those ment, and (2) the small heat shock protein genes are using Df(3L)ACI except that males of the genotype ri e functionally equivalent. were mutagenized (0.007 M DEB). In addition, the F2 generation was subjected to a 36" heat shock during the MATERIALS AND METHODS course of larval or pupal development. The heat shocks were administered in two ways: the first method involved Fly stocks and culture conditions: Df(3L)ACI is a dele- immersion of the vials into circulating waterbaths for 2 hr; tion extendingfrom 67A2 to 67D11-13 generated by the second involved placing trays of vials into an incubator ADELAIDET. C. CARPENTER (unpublished results).TM6B is for 5-6 hr. Putative lethals were backcrossed toDf(3L)29A6 a newer version of the TM6 balancer chromosome that and examined for lethality at both 22" and following a 36" carries the dominant marker Tb (CRAYMER1984). M(3)i55 heat shock. Balanced stocks were established for those is a mutant allele of the M(3)ilocus (MORATAand RIPOLL which retested positively (ie., died over the deletion). Each 1975).Hsp28""is an hp28 mutation resultingfrom insertion stock was subsequently crossed to Df(3L)ACI to identify of a defective P element into the 5' regulatory sequences those mutations which mapped in the region of overlap of the hp28 gene that disruptsits inducibility by heat shock between these two deletions. (EISSENBERGand ELGIN 1987). 9500.1 is a transformant Complementation analysis: Inter se complementation stock that carries wild-type copies of hsp28, hp23 and gene crosses were performed among all DEB- and EMS-induced 1 on the second chromosome (COHEN andMESELSON 1985). lethals obtained from the F2 screens over Df(3L)ACI and The 9500.1 insertion also carriesa nonfunctional hsp26 Df(3L)29A6. Crosses were done between mutations bal- gene (due to the insertion of bacteriophage A DNA se- anced over TM3Sb, and the progeny were scored for the quences into the middle of the coding sequence) and the presence of Sb' individuals. Typically, two virgin females alcohol dehydrogenase (Adh) gene as a selectable marker. were mated with two males in vials, and these were passed A2.1 is a transformant stock that carries wild type copies as needed. Initially, all crosses were done in both directions. of hsp22 and thexanthine dehydrogenase (rosy) gene Later crosses were done in only one direction. Generally, inserted on thesecond chromosome (KLEMENZand GEHRING on the order of 100 progeny were scored per cross, unless 1986). Other mutations, rearrangements,and balancer it was obvious that the two mutations complemented fully. chromosomes are described in LINDSLEYand GRELL (1968) Recombination mapping: To establish whether the lethal or LINDSLEY andZIMM (1985, 1987). mutations recovered over Df(3L)ACI mapped to the 67A- Unless indicated otherwise, all stocks and crosses were D subinterval or were interacting mutations that mapped maintained at either 22" or room temperature on media elsewhere, the recombination frequency between the mu- consisting of cornmeal, molasses, and agar onto which live tation and M(3)i55was measured. Each mutant stock was baker's yeast was sprinkled. For growing larvae for cytology, outcrossed to M(3)i55and rn~tIM(3)i~~females were col- flies were grown on yeast glucose media (10% yeast, 10% lected. Four to six such females were then mated to several glucose, 1.5% agar, 0.15% Tegasept). Df(3L)ACIITM3Sbmales in vials, and these were generally Isolation of recessive lethal mutations in the 67A-D sub- passed twice.
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