Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis

Development ◽  
1988 ◽  
Vol 104 (4) ◽  
pp. 713-720 ◽  
Author(s):  
A. Busturia ◽  
G. Morata

The morphological patterns in the adult cuticle of Drosophila are determined principally by the homeotic genes of the bithorax and Antennapedia complexes. We find that many of these genes become indiscriminately active in the adult epidermis when the Pc gene is eliminated. By using the Pc3 mutation and various BX-C mutant combinations, we have generated clones of imaginal cells possessing different combinations of active homeotic genes. We find that, in the absence of BX-C genes, Pc- clones develop prothoracic patterns; this is probably due to the activity of Sex combs reduced which overrules Antennapedia. Adding contributions of Ultrabithorax, abdominal-A and Abdominal-B results in thoracic or abdominal patterns. We have established a hierarchical order among these genes: Antp less than Scr less than Ubx less than abd-A less than Abd-B. In addition, we show that the engrailed gene is ectopically active in Pc- imaginal cells.

Development ◽  
1993 ◽  
Vol 118 (2) ◽  
pp. 339-352 ◽  
Author(s):  
W. Zeng ◽  
D.J. Andrew ◽  
L.D. Mathies ◽  
M.A. Horner ◽  
M.P. Scott

The transcription factors encoded by homeotic genes determine cell fates during development. Each homeotic protein causes cells to follow a distinct pathway, presumably by differentially regulating downstream ‘target’ genes. The homeodomain, the DNA-binding part of homeotic proteins, is necessary for conferring the specificity of each homeotic protein's action. The two Drosophila homeotic proteins encoded by Antennapedia and Sex combs reduced determine cell fates in the epidermis and internal tissues of the posterior head and thorax. Genes encoding chimeric Antp/Scr proteins were introduced into flies and their effects on morphology and target gene regulation observed. We find that the N terminus of the homeodomain is critical for determining the specific effects of these homeotic proteins in vivo, but other parts of the proteins have some influence as well. The N-terminal part of the homeodomain has been observed, in crystal structures and in NMR studies in solution, to contact the minor groove of the DNA. The different effects of Antennapedia and Sex combs reduced proteins in vivo may depend on differences in DNA binding, protein-protein interactions, or both.


Development ◽  
1994 ◽  
Vol 120 (8) ◽  
pp. 2287-2296 ◽  
Author(s):  
P. de Zulueta ◽  
E. Alexandre ◽  
B. Jacq ◽  
S. Kerridge

Homeotic genes determine the identities of metameres in Drosophila. We have examined functional aspects of the homeotic gene teashirt by ectopically expressing its product under the control of a heat-shock promoter during embryogenesis. Our results confirm that the gene is critical for segmental identity of the larva. Under mild heat-shock conditions, the Teashirt protein induces an almost complete transformation of the labial to prothoracic segmental identity, when expressed before 8 hours of development. Positive autoregulation of the endogenous teashirt gene and the presence of Sex combs reduced protein in the labium explain this homeosis. Patterns in the maxillary and a more anterior head segment are partly replaced with trunk ones. Additional Teashirt protein has no effect on the identity of the trunk segments where the gene is normally expressed; teashirt function is overridden by some homeotic complex acting in the posterior trunk. Strong heat-shock regimes provoke novel defects: ectopic sense organs differentiate in posterior abdominal segments and trunk pattern elements differentiate in the ninth abdominal segment. Teashirt acts in a partially redundant way with certain homeotic complex proteins but co-operates with them for the establishment of specific segment types. We suggest that Teashirt and HOM-C proteins regulate common sets of downstream target genes.


Development ◽  
1989 ◽  
Vol 105 (1) ◽  
pp. 167-174 ◽  
Author(s):  
J.W. Mahaffey ◽  
R.J. Diederich ◽  
T.C. Kaufman

Antibodies that specifically recognize proteins encoded by the homeotic genes: Sex combs reduced, Deformed, labial and proboscipedia, were used to follow the distribution of these gene products during embryogenesis. The position of engrailed-expressing cells was used as a reference and staining conditions were established that could distinguish, among cells expressing engrailed, one of the homeotic proteins or both. Our observations demonstrate two important facts about establishing identity in the head segments. First, in contrast to the overlapping pattern of homeotic gene expression in the trunk segments, we observe a non-overlapping pattern in the head for those homeotic proteins required during embryogenesis. In contrast, the spatial accumulation of the protein product of the non-vital proboscipedia locus overlaps partially with the distribution of the Deformed and Sex combs reduced proteins in the maxillary and labial segments, respectively. Second, two of the proteins, Sex combs reduced and Deformed, have different dorsal and ventral patterns of accumulation. Dorsally, these proteins are expressed in segmental domains while, within the ventral region, a parasegmental register is observed. The boundary where this change in pattern occurs coincides with the junction between the ventral neurogenic region and the dorsal epidermis. After contraction of the germ band, when the nerve cord has completely separated from the epidermis, the parasegmental pattern is observed only within the ventral nerve cord while a segmental register is maintained throughout the epidermis.


Genetics ◽  
1998 ◽  
Vol 149 (4) ◽  
pp. 1823-1838 ◽  
Author(s):  
Olivier Saget ◽  
Françoise Forquignon ◽  
Pedro Santamaria ◽  
Neel B Randsholt

Abstract We have analyzed the requirements for the multi sex combs (mxc) gene during development to gain further insight into the mechanisms and developmental processes that depend on the important trans-regulators forming the Polycomb group (PcG) in Drosophila melanogaster. mxc is allelic with the tumor suppressor locus lethal (1) malignant blood neoplasm (l(1)mbn). We show that the mxc product is dramatically needed in most tissues because its loss leads to cell death after a few divisions. mxc has also a strong maternal effect. We find that hypomorphic mxc mutations enhance other PcG gene mutant phenotypes and cause ectopic expression of homeotic genes, confirming that PcG products are cooperatively involved in repression of selector genes outside their normal expression domains. We also demonstrate that the mxc product is needed for imaginal head specification, through regulation of the ANT-C gene Deformed. Our analysis reveals that mxc is involved in the maternal control of early zygotic gap gene expression previously reported for some PcG genes and suggests that the mechanism of this early PcG function could be different from the PcG-mediated regulation of homeotic selector genes later in development. We discuss these data in view of the numerous functions of PcG genes during development.


Development ◽  
1992 ◽  
Vol 115 (1) ◽  
pp. 35-47 ◽  
Author(s):  
J.G. Heuer ◽  
T.C. Kaufman

The Drosophila embryonic peripheral nervous system (PNS) contains segment-specific spatial patterns of sensory organs which derive from the ectoderm. Many studies have established that the homeotic genes of Drosophila control segment specific characteristics of the epidermis, and more recently these genes have also been shown to control gut morphogenesis through their expression in the visceral mesoderm (Tremml, G. and Bienz, M. (1989), EMBO J. 8, 2677–2685). We report here the roles of homeotic genes in establishing the spatial patterns of sensory organs in the embryonic PNS. The PNS was examined in embryos homozygous for mutations in the homeotic genes Sex combs reduced (Scr), Antennapedia (Antp), Ultrabithorax (Ubx), abdominal-A (abd-A) and Abdominal-B (Abd-B) with antibodies that label specific subsets of sensory organs. Our results suggest that the homeotic genes have specific roles in establishing the correct spatial patterns of sensory organs in their normal domains of expression. In addition, we also report the effects of ectopic expression of the homeotic genes labial (lab), Deformed (Dfd), Scr, Antp or Ubx on the normal development of sensory organs in the embryonic PNS. Interestingly, while previous studies have concluded that ectopic expression of the homeotic genes Dfd, Scr and Antp has no effect on the segmental identity of the abdominal segments, our results demonstrate that this is not true. We show that ectopic expression of these genes does result in the disruption of the developing PNS in the abdomen. Our results are suggestive of a role for the homeotic gene products in regulating genes which are necessary for generating sensory progenitor cells in the developing PNS.


Development ◽  
1997 ◽  
Vol 124 (1) ◽  
pp. 149-157 ◽  
Author(s):  
B.T. Rogers ◽  
M.D. Peterson ◽  
T.C. Kaufman

The products of the HOM/Hox homeotic genes form a set of evolutionarily conserved transcription factors that control elaborate developmental processes and specify cell fates in many metazoans. We examined the expression of the ortholog of the homeotic gene Sex combs reduced (Scr) of Drosophila melanogaster in insects of three divergent orders: Hemiptera, Orthoptera and Thysanura. Our data reflect how the conservation and variation of Scr expression has affected the morphological evolution of insects. Whereas the anterior epidermal expression of Scr, in a small part of the posterior maxillary and all of the labial segment, is found to be in common among all four insect orders, the posterior (thoracic) expression domains vary. Unlike what is observed in flies, the Scr orthologs of other insects are not expressed broadly over the first thoracic segment, but are restricted to small patches. We show here that Scr is required for suppression of wings on the prothorax of Drosophila. Moreover, Scr expression at the dorsal base of the prothoracic limb in two other winged insects, crickets (Orthoptera) and milkweed bugs (Hemiptera), is consistent with Scr acting as a suppressor of prothoracic wings in these insects. Scr is also expressed in a small patch of cells near the basitarsal-tibial junction of milkweed bugs, precisely where a leg comb develops, suggesting that Scr promotes comb formation, as it does in Drosophila. Surprisingly, the dorsal prothoracic expression of Scr is also present in the primitively wingless firebrat (Thysanura) and the leg patch is seen in crickets, which have no comb. Mapping both gene expression patterns and morphological characters onto the insect phylogenetic tree demonstrates that in the cases of wing suppression and comb formation the appearance of expression of Scr in the prothorax apparently precedes these specific functions.


Development ◽  
1988 ◽  
Vol 103 (4) ◽  
pp. 733-741 ◽  
Author(s):  
J.M. Dura ◽  
P. Ingham

The distributions of the products of the homeotic genes Sex combs reduced (Scr) and Ultrabithorax (Ubx) and of the segmentation genes, fushi tarazu (ftz), even skipped (eve) and engrailed (en) have been monitored in polyhomeotic (ph) mutant embryos. None of the genes monitored show abnormal expression at the blastoderm stage in the absence of zygotic ph expression. Both Scr and Ubx are ectopically expressed in the epidermis of ph embryos, confirming the earlier proposal, based on genetic analysis, that ph+ acts as a negative regulator of Antennapedia (ANT-C) and bithorax (BX-C) complex genes. At the shortened germ band stage, en is also ectopically expressed, mainly in the anterior region of each segment. In contrast to these effects in the epidermis, the expression of en, Ubx, Scr and ftz is largely or completely suppressed in the central nervous system, whereas eve becomes ectopically expressed in most neurones.


Development ◽  
1999 ◽  
Vol 126 (6) ◽  
pp. 1121-1128 ◽  
Author(s):  
A. Abzhanov ◽  
T.C. Kaufman

Homeotic genes are known to be involved in patterning morphological structures along the antero-posterior axis of insects and vertebrates. Because of their important roles in development, changes in the function and expression patterns of homeotic genes may have played a major role in the evolution of different body plans. For example, it has been proposed that during the evolution of several crustacean lineages, changes in the expression patterns of the homeotic genes Ultrabithorax and abdominal-A have played a role in transformation of the anterior thoracic appendages into mouthparts termed maxillipeds. This homeotic-like transformation is recapitulated at the late stages of the direct embryonic development of the crustacean Porcellio scaber (Oniscidea, Isopoda). Interestingly, this morphological change is associated with apparent novelties both in the transcriptional and post-transcriptional regulation of the Porcellio scaber ortholog of the Drosophila homeotic gene, Sex combs reduced (Scr). Specifically, we find that Scr mRNA is present in the second maxillary segment and the first pair of thoracic legs (T1) in early embryos, whereas protein accumulates only in the second maxillae. In later stages, however, high levels of SCR appear in the T1 legs, which correlates temporally with the transformation of these appendages into maxillipeds. Our observations provide further insight into the process of the homeotic leg-to-maxilliped transformation in the evolution of crustaceans and suggest a novel regulatory mechanism for this process in this group of arthropods.


Development ◽  
1983 ◽  
Vol 76 (1) ◽  
pp. 297-331
Author(s):  
Gary Struhl

The product of the extra sex combs+ (esc+) gene is required during embryogenesis for the correct determination of segments in Drosophila. If this product is absent, most segments develop like the normal eighth abdominal segment. Here, I extend previous results (Struhl, 1981a) showing that this phenotype results in large part from indiscriminate expression of the bithorax-complex genes which are normally active only in particular segments of the thorax and abdomen. In addition, I test whether the esc+ gene product is required for the correct expression of other homeotic genes. First, I have examined two genes of the Antennapedia-complex (Sex combs reduced+ and Antennapedia+): I find that both genes are normally required in only some of the body segments, but that in the absence of the esc+ gene product, both appear to function adventitiously in other segments. Second, comparing esc+ and esc− embryos lacking both these genes as well as the bithorax-complex, I find that additional homeotic genes (possibly those normally involved in specifying head segments) appear to be expressed indiscriminately when the esc+ gene product is absent. Finally, I present evidence that the products of the esc+ gene and the Polycomb+ gene (a second gene required for the correct regulation of the bithorax-complex) act independently. On the basis of these results, I propose a tentative outline of the roles and realms of action of all of these genes.


Development ◽  
1999 ◽  
Vol 126 (6) ◽  
pp. 1175-1187 ◽  
Author(s):  
G. Daubresse ◽  
R. Deuring ◽  
L. Moore ◽  
O. Papoulas ◽  
I. Zakrajsek ◽  
...  

The Drosophila kismet gene was identified in a screen for dominant suppressors of Polycomb, a repressor of homeotic genes. Here we show that kismet mutations suppress the Polycomb mutant phenotype by blocking the ectopic transcription of homeotic genes. Loss of zygotic kismet function causes homeotic transformations similar to those associated with loss-of-function mutations in the homeotic genes Sex combs reduced and Abdominal-B. kismet is also required for proper larval body segmentation. Loss of maternal kismet function causes segmentation defects similar to those caused by mutations in the pair-rule gene even-skipped. The kismet gene encodes several large nuclear proteins that are ubiquitously expressed along the anterior-posterior axis. The Kismet proteins contain a domain conserved in the trithorax group protein Brahma and related chromatin-remodeling factors, providing further evidence that alterations in chromatin structure are required to maintain the spatially restricted patterns of homeotic gene transcription.


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