Transcriptional regulation of cytoskeletal functions and segmentation by a novel maternal pair-rule gene, lilliputian

Transcriptional control during early Drosophila development is governed by maternal and zygotic factors. We have identified a novel maternal transcriptional regulator gene, lilliputian (lilli), which contains an HMG1 (AT-hook) motif and a domain with similarity to the human fragile X mental retardation FMR2 protein and the AF4 proto-oncoprotein. Embryos lacking maternal lilli expression show specific defects in the establishment of a functional cytoskeleton during cellularization, and exhibit a pair-rule segmentation phenotype. These mutant phenotypes correlate with markedly reduced expression of the early zygotic genes serendipity alpha, fushi tarazu and huckebein, which are essential for cellularization and embryonic patterning. In addition, loss of lilli in adult photoreceptor and bristle cells results in a significant decrease in cell size. Our results indicate that lilli represents a novel pair-rule gene that acts in cytoskeleton regulation, segmentation and morphogenesis.

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The HMG-box protein Lilliputian is required for Runt-dependent activation of the pair-rule gene fushi–tarazu

Developmental Biology ◽

10.1016/j.ydbio.2006.10.027 ◽

2007 ◽

Vol 301 (2) ◽

pp. 350-360 ◽

Cited By ~ 5

Author(s):

Christine J. VanderZwan-Butler ◽

Lisa M. Prazak ◽

J. Peter Gergen

Keyword(s):

Fushi Tarazu ◽

Hmg Box ◽

Pair Rule Gene ◽

Pair Rule

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Drosophila hairy pair-rule gene regulates embryonic patterning outside its apparent stripe domains

Development ◽

10.1242/dev.118.1.255 ◽

1993 ◽

Vol 118 (1) ◽

pp. 255-266 ◽

Cited By ~ 3

Author(s):

M. Lardelli ◽

D. Ish-Horowicz

Keyword(s):

Transcription Initiation ◽

Transcriptional Regulators ◽

Early Embryo ◽

Embryonic Patterning ◽

Gene Deletions ◽

Head Development ◽

Pair Rule Gene ◽

Blastoderm Stage ◽

Embryonic Viability ◽

Pair Rule

The hairy (h) segmentation gene of Drosophila regulates segmental patterning of the early embryo, and is expressed in a set of anteroposterior stripes during the blastoderm stage. We have used a set of h gene deletions to study the h promoter and the developmental requirements for individual h stripes. The results confirm upstream regulation of h striping but indicate that expression in the anterodorsal head domain depends on sequences downstream of the two transcription initiation sites. Surprisingly, the two anterior-most h domains appear to be dispensable for head development and embryonic viability. One partial promoter deletion expresses ectopic h, leading to misexpression of other segmentation genes and embryonic pattern defects. We demonstrate that h affects patterning outside its apparent stripe domains, supporting a model in which primary pair-rule genes act as concentration-dependent transcriptional regulators, i.e. as local morphogens.

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Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation

Development ◽

10.1242/dev.128.18.3459 ◽

2001 ◽

Vol 128 (18) ◽

pp. 3459-3472 ◽

Cited By ~ 5

Author(s):

Nipam H. Patel ◽

David C. Hayward ◽

Sabbi Lall ◽

Nicole R. Pirkl ◽

Daniel DiPietro ◽

...

Keyword(s):

Expression Patterns ◽

Axis Formation ◽

Embryonic Cells ◽

Embryonic Patterning ◽

Axial Patterning ◽

Gap Gene ◽

Segment Polarity ◽

Pair Rule Gene ◽

Set Up ◽

Pair Rule

While the expression patterns of segment polarity genes such as engrailed have been shown to be similar in Drosophila melanogaster and Schistocerca americana (grasshopper), the expression patterns of pair-rule genes such as even-skipped are not conserved between these species. This might suggest that the factors upstream of pair-rule gene expression are not conserved across insect species. We find that, despite this, many aspects of the expression of the Drosophila gap gene hunchback are shared with its orthologs in the grasshoppers S. americana and L. migratoria. We have analyzed both mRNA and protein expression during development, and find that the grasshopper hunchback orthologs appear to have a conserved role in early axial patterning of the germ anlagen and in the specification of gnathal and thoracic primordia. In addition, distinct stepped expression levels of hunchback in the gnathal/thoracic domains suggest that grasshopper hunchback may act in a concentration-dependent fashion (as in Drosophila), although morphogenetic activity is not set up by diffusion to form a smooth gradient. Axial patterning functions appear to be performed entirely by zygotic hunchback, a fundamental difference from Drosophila in which maternal and zygotic hunchback play redundant roles. In grasshoppers, maternal hunchback activity is provided uniformly to the embryo as protein and, we suggest, serves a distinct role in distinguishing embryonic from extra-embryonic cells along the anteroposterior axis from the outset of development – a distinction made in Drosophila along the dorsoventral axis later in development. Later hunchback expression in the abdominal segments is conserved, as are patterns in the nervous system, and in both Drosophila and grasshopper, hunchback is expressed in a subset of extra-embryonic cells. Thus, while the expected domains of hunchback expression are conserved in Schistocerca, we have found surprising and fundamental differences in axial patterning, and have identified a previously unreported domain of expression in Drosophila that suggests conservation of a function in extra-embryonic patterning.

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Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca

Development ◽

10.1242/dev.121.12.3989 ◽

1995 ◽

Vol 121 (12) ◽

pp. 3989-3996 ◽

Cited By ~ 4

Author(s):

J. Broadus ◽

C.Q. Doe

Keyword(s):

Gene Expression ◽

Central Nervous System ◽

Gene Function ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Key Features ◽

Insect Central Nervous System ◽

Or Gene ◽

Species Specific ◽

Pair Rule

In the Drosophila CNS, early neuroblast formation and fate are controlled by the pair-rule class of segmentation genes. The distantly related Schistocerca (grasshopper) embryo has a similar arrangement of neuroblasts, despite lack of known pair-rule gene function. Does divergent pair-rule gene function lead to different neuroblast identities, or can different patterning mechanisms produce homologous neuroblasts? We use four molecular markers to compare Drosophila and Schistocerca neuroblast identity: seven-up, prospero, engrailed, and fushi-tarazu/Dax. In both insects some early-forming neuroblasts share key features of neuroblast identity (position, time of formation, and temporally accurate gene expression); thus, different patterning mechanisms can generate similar neuroblast fates. In contrast, several later-forming neuroblasts show species-specific differences in position and/or gene expression; these neuroblast identities seem to have diverged, suggesting that evolution of the insect central nervous system can occur through changes in embryonic neuroblast identity.

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Ftz-F1 is a cofactor in Ftz activation of the Drosophila engrailed gene

Development ◽

10.1242/dev.124.4.839 ◽

1997 ◽

Vol 124 (4) ◽

pp. 839-847 ◽

Cited By ~ 6

Author(s):

B. Florence ◽

A. Guichet ◽

A. Ephrussi ◽

A. Laughon

Keyword(s):

Transcriptional Activation ◽

Binding Sites ◽

Direct Contact ◽

Regulatory Element ◽

Drosophila Embryo ◽

Homeodomain Protein ◽

Reporter Expression ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Pair Rule

The fushi tarazu pair-rule gene is required for the formation of alternating parasegmental boundaries in the Drosophila embryo. fushi tarazu encodes a homeodomain protein necessary for transcription of the engrailed gene in even-numbered parasegments. Here we report that, within an engrailed enhancer, adjacent and conserved binding sites for the Fushi tarazu protein and a cofactor are each necessary, and together sufficient, for transcriptional activation. Footprinting shows that the cofactor site can be bound specifically by Ftz-F1, a member of the nuclear receptor superfamily. Ftz-F1 and the Fushi tarazu homeodomain bind the sites with 4- to 8-fold cooperativity, suggesting that direct contact between the two proteins may contribute to target recognition. Even parasegmental reporter expression is dependent on Fushi tarazu and maternal Ftz-F1, suggesting that these two proteins are indeed the factors that act upon the two sites in embryos. The two adjacent binding sites are also required for continued activity of the engrailed enhancer after Fushi tarazu protein is no longer detectable, including the period when engrailed, and the enhancer, become dependent upon wingless. We also report the existence of a separate negative regulatory element that apparently responds to odd-skipped.

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Pair-rule expression of the Drosophila fushi tarazu gene: a nuclear receptor response element mediates the opposing regulatory effects of runt and hairy

Development ◽

10.1242/dev.121.2.453 ◽

1995 ◽

Vol 121 (2) ◽

pp. 453-462 ◽

Cited By ~ 2

Author(s):

C. Tsai ◽

P. Gergen

Keyword(s):

Nuclear Receptor ◽

Transcriptional Activation ◽

Reporter Genes ◽

Orphan Nuclear Receptor ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Dna Elements ◽

Regulatory Effects ◽

Opposing Effects ◽

Pair Rule

The segmentation genes runt and hairy are required for the proper transcriptional regulation of the pair-rule gene fushi tarazu during the blastoderm stage of Drosophila embryogenesis. The expression of different fushi tarazu reporter genes was examined in runt and hairy mutant embryos, as well as in runt over-expressing embryos in order to identify DNA elements responsible for mediating these regulatory effects. The results indicated that runt and hairy act through a common 32 base-pair element. This element, designated as fDE1, contains a binding site for a small family of orphan nuclear receptor proteins that are uniformly expressed in blastoderm embryos. The pair-rule expression of reporter gene constructs containing multimerized fDE1 elements depends on activation by runt and repression by hairy. Examination of reporter genes with mutated fDE1 elements provided further evidence that this element mediates both transcriptional activation and repression. Genetic experiments indicated that the opposing effects of runt and hairy were not due solely to cross-regulatory interactions between these two genes and that fDE1-dependent expression is regulated by factors in addition to runt and hairy.

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Dosage-Sensitive Maternal Modifiers of the Drosophila Segmentation Gene runt

Genetics ◽

10.1093/genetics/142.3.839 ◽

1996 ◽

Vol 142 (3) ◽

pp. 839-852

Author(s):

Joseph B Duffy ◽

James Wells ◽

J Peter Gergen

Keyword(s):

Transcriptional Regulation ◽

Transcriptional Regulator ◽

Drosophila Embryo ◽

Over Expression ◽

Spatial Regulation ◽

Gap Genes ◽

Pair Rule Gene ◽

Pair Rule ◽

Anterior Posterior

Abstract The protein encoded by the pair-rule gene runt functions as a transcriptional regulator during anterior-posterior patterning of the Drosophila embryo. Results of over-expression experiments as well as parallels drawn from the recent characterization of vertebrate homologues indicate that interactions with other proteins are likely to be central to the function of the Runt protein. To identify factors important for runt activity, we took advantage of an adult visible phenotype observed in animals heterozygous for runt mutations. Using a set of 126 different deficiency chromosomes we screened ~65% of the genome for genes that act as dose-sensitive maternal modifiers of runt. Eighteen deficiencies representing 12 putative loci were identified as maternally acting enhancers of runt haplo-insufficiency. Further characterization of two of these regions led to the identification of the interacting loci. Both of these loci affect the spatial regulation of runt transcription and appear genetically complex. Furthermore, the effects of one of these loci, M(1)1B, is indirect and mediated through effects on the transcriptional regulation of posterior gap genes.

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