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The Zygotic Control of Drosophila Pair-Rule Gene Expression II

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The Zygotic Control of Drosophila Pair-Rule Gene Expression II Development 107, 673-683 (1989) 673 Printed in Great Britain © The Company of Biologists Limited 1989 The zygotic control of Drosophila pair-rule gene expression II. Spatial repression by gap and pair-rule gene products SEAN B. CARROLL and STEPHANIE H. VAVRA Laboratory of Molecular Biology and Department of Genetics, University of Wisconsin-Madison, 1525 Linden Drive, Madison, WI 53706, USA Summary We examined gene expression patterns in certain single (hb), Krtippel (Kr), and knirps (Icnf) have been removed, and double pair-rule mutant embryos to determine indicating that these gap genes are not essential to which of the largely repressive pair-rule gene interac- activate the pair-rule genes. In fact, we show that in the tions are most likely to be direct and which interactions absence of either hb+ or kni+, or both gap genes, the Kr+ are probably indirect. From these studies we conclude product represses hairy expression. These results suggest that: (i) hairy+ and even-skipped (eve+) regulate the fushi that gap genes repress hairy expression in the interstripe tarazu (ftz) gene; (ii) eve+ and runt+ regulate the hairy regions, rather than activate hairy expression in the gene; (iii) runt+ regulates the eve gene; but, (iv) runt does stripes. The molecular basis of pair-rule gene regulation not regulate the ftz gene pattern, and hairy does not by gap genes must involve some dual control mechan- regulate the eve gene pattern. These pair-rule interac- isms such that combinations of gap genes affect pair-rule tions are not sufficient, however, to explain the period- transcription in a different manner than a single gap icity of the hairy and eve patterns, so we examined gene. specific gap gene mutant combinations to uncover their regulatory effects on these two genes. Our surprising observation is that the hairy and eve genes are expressed Key words: gap genes, pair-rule genes, blastoderm, in embryos where the three key gap genes hunchback Drosophila embryogenesis. Introduction proteins (Ish-Horowicz and Pinchin, 1987), analyses of cis-acting elements that control pair-rule gene ex- Analyses of terminal phenotypes and of segmentation pression (Hiromi et al. 1985; Fliromi and Gehring, 1987; gene expression patterns in various mutant embryos has Howard, 1988), studies on the effects of inhibiting defined the overall regulatory hierarchy of the segmen- segmentation protein synthesis (Edgar et al. 1986, tation genes. Generally, each class of segmentation 1989), and in vitro biochemical experiments (Hoey and genes interacts to specify the finer expression pattern of Levine, 1988). This combination of approaches is the next group of genes. Thus, the maternal coordinate expected to resolve the complex problem of how a genes affect each other (Frohnhofer and Niisslein- crude pattern in the unfertilized egg is translated into a Volhard, 1987; Driever and Nusslein-Volhard, 1988) periodic pattern of segments. and the gap genes (Gaul and Jackie, 1987), which In the accompanying paper, we showed that most interact (Jackie et al. 1986) to control pair-rule gene zygotically required regulators of the pair-rule genes patterns (Carroll and Scott, 1986; Ingham et al. 1986; have apparently been identified and that the initial Frasch and Levine, 1987), which interact to specify the activation of the pair-rule genes does not depend upon patterns of the segment polarity genes (DiNardo and other zygotic genes (Vavra and Carroll, accompanying O'FarreH, 1987; Martinez-Arias and White, 1988). paper). However, even with most of the key genes Given the extent of these fundamental pattern-regulat- identified, it is difficult to demonstrate whether remov- ing gene interactions, it is a large task to determine the ing one gene from the system directly or indirectly nature of the regulatory circuitry that operates between perturbs the expression of others or if an observed segmentation genes and to identify the trans- and cis- interaction reflects positive or negative control. To acting factors that are responsible for the pattern of address these difficulties we have analyzed pair-rule gene expression. gene expression in selected single, double, and triple The present approaches aimed at elucidating these mutant embryos to uncover which zygotic genes are factors include formal genetic analyses, studies on the likely to act directly upon the hairy, eve and ftz genes. effect of ectopic expression of putative regulatory Our results, combined with other recent studies on pair- 674 5. B. Carroll and S. H. Vavra rule gene interactions (Ingham and Gergen, 1988) and regulation of other genes in the pathway. The obser- protein synthesis inhibition experiments (Edgar et al. vations presented here on pair-rule protein patterns 1989), support the view that certain pair-rule genes are overlap with the results of Ingham and Gergen (1988) extensively negatively regulated, i.e. specific maternal, on pair-rule RNA patterns. Because these interactions gap and pair-rule proteins repress pair-rule genes. It and the patterns of certain mutant combinations are appears that, at least for the ftz and hairy genes, their critical to the subsequent discussion of gap gene con- striped patterns are more the result of repression of trol, we will present all of our results dealing with the gene expression in the interstripe regions than a re- regulation of h, eve and ftz protein expression and gional activation of individual stripes. emphasize those details and mutant combinations that may differ from the previous observations of RNA patterns. We generally agree with the conclusions of Materials and methods Ingham and Gergen (1988) as to the nature of individual pair-rule regulatory interactions. Antibodies We have examined pair-rule gene expression in whole-mount Gene expression in single pair-rule mutants cellular blastoderm embryos by filtered fluorescence imaging The wild-type hairy, ftz and eve protein patterns at the (Karr and Kornberg, 1989; Carroll et al. 1988) after immuno- peroxidase staining with polyclonal antibodies specific for the cellular blastoderm stage of embryogenesis consist of ftz (Carroll and Scott, 1985), eve (Frasch etal. 1987; antibody seven transverse stripes encircling the embryo and, in gift of M. Frasch and M. Levine) hairy (Carroll et al. 1988), the case of the hairy gene, an additional dorsal anterior and KrUppel (Gaul and Jackie, 1987; antibody gift from patch of expression (Fig. 1A-C). The ftz and eve stripes U. Gaul). This technique gives sharp images of protein are in alternating domains while the hairy stripes are localization and was used to double-label embryos to examine offset such that the six posterior ones transiently relative expression patterns or to unambiguously identify the overlap the ftz stripes by about one cell and all seven genotype of an individual embryo derived from crosses that hairy stripes overlap with each eve stripe (Carroll et al. yield a variety of mutant progeny. 1988). Loss of runt+ activity changes h, eve and ftz expression (Fig. 1D-F). The hairy pattern partly Stocks and Crosses expands with the first hairy stripe spreading posteriorly, The null allele stocks used to generate the pair-rule double B57 V ma1102 while the interband between stripes 3 and 4 accumu- mutant embryos were: Df(l) rw«r /FM6y Y (kindly provided by Peter Gergen), Df(2R) eve 1.27 en bw sp/SM6a, lates some protein, and stripes 6 and 7 are stronger and 7h94 s nearly fused (Fig. ID). Note that the hairy pattern is and/i e /TM3. + Runt; eve and runt; hairy double mutant embryos were still fairly periodic, so although loss of runt de- generated by mating runt males to heterozygous eve or hairy represses hairy expression, runt is only one of probably virgin females. The double heterozygous Fj females were several negative regulators of hairy. We will symbolize then mated to either heterozygous eve or hairy males, yielding these gene interactions with an arrow indicating posi- one-sixteenth double mutant embryos. tive regulation and a cross-hatch indicating negative Stocks used in gap mutant analysis were Kr1 en bw/CyO (a UE>4 m4S 5 control, i.e. null allele), and the double mutant fcm W cu sr e runt 1 hairy ca/TM3 Sb Ser, generously provided by R. Lehmann and C. Niisslein-Volhard. The triple gap mutant embryos were pro- duced at a frequency of one-sixteenth from heterozygous hb, ftz expression is reduced in runt~ embryos with the kni; Kr parents. first, third, fifth, and sixth stripes narrowing or almost disappearing (Fig. IE). The ftz protein pattern comp- lements the hairy protein pattern and is likely to result Results from the initial effect of runt~ on the hairy pattern and the subsequent effect of hairy on ftz (Howard and Interactions between pair-rule genes Ingham, 1986; Carroll and Scott, 1986; and see Fig. IN Several previous studies have analyzed the effect of below), i.e.: individual pair-rule mutations on the expression of runt 1 hairy 1 ftz other pair-rule genes (Howard and Ingham, 1986; Carroll and Scott, 1986; Frasch and Levine, 1987; eve expression is only slightly affected during the Ingham and Gergen, 1988). From these experiments, a cellular blastoderm stage in runt~ embryos, the princi- general picture emerged of the pair-rule gene hierarchy pal early defects are a reduced fifth eve stripe with a that placed hairy, runt and eve at the top, with other slight spreading of the other stripes (Fig. IF; see also pair-rule genes (e.g. ftz) being downstream from them. Frasch and Levine, 1987). During early gastrulation, For example, ftz expression is altered by mutations in h, the eve pattern spreads more dramatically but we are runt or eve, but ftz mutants have no impact on primarily concerned here with the initial periodic expression of h, runt or eve. blastoderm pattern.
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