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

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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Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo

Development ◽

10.1242/dev.104.supplement.51 ◽

1988 ◽

Vol 104 (Supplement) ◽

pp. 51-60 ◽

Cited By ~ 13

Author(s):

Philip Ingham ◽

Peter Gergen

Keyword(s):

Double Mutant ◽

Early Embryo ◽

Drosophila Embryo ◽

Periodic Pattern ◽

Fushi Tarazu ◽

Blastoderm Stage ◽

Pair Rule

The pair-rule genes of Drosophila play a fundamental role in the generation of periodicity in the early embryo. We have analysed the transcript distributions of runt, hairy, even-skipped and fushi tarazu in single and double mutant ernbryos. The results indicate a complex set of interactions between the genes during the blastoderm stage of embryogenesis.

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

Development ◽

10.1242/dev.128.5.801 ◽

2001 ◽

Vol 128 (5) ◽

pp. 801-813 ◽

Cited By ~ 8

Author(s):

A.H. Tang ◽

T.P. Neufeld ◽

G.M. Rubin ◽

H.A. Muller

Keyword(s):

Transcriptional Control ◽

Fragile X ◽

Transcriptional Regulator ◽

Regulator Gene ◽

Embryonic Patterning ◽

Fushi Tarazu ◽

Fragile X Mental Retardation ◽

Pair Rule Gene ◽

Mutant Phenotypes ◽

Pair Rule

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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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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buttonhead does not contribute to a combinatorial code proposed for Drosophila head development

Development ◽

10.1242/dev.124.8.1509 ◽

1997 ◽

Vol 124 (8) ◽

pp. 1509-1517 ◽

Cited By ~ 2

Author(s):

E.A. Wimmer ◽

S.M. Cohen ◽

H. Jackle ◽

C. Desplan

Keyword(s):

Ectopic Expression ◽

Early Embryo ◽

Proximal Promoter ◽

Head Region ◽

Head Development ◽

Stage Embryo ◽

Overlapping Domains ◽

Targeted Gene Expression ◽

Blastoderm Stage ◽

Combinatorial Code

The Drosophila gap-like segmentation genes orthodenticle, empty spiracles and buttonhead (btd) are expressed and required in overlapping domains in the head region of the blastoderm stage embryo. Their expression domains correspond to two or three segment anlagen that fail to develop in each mutant. It has been proposed that these overlapping expression domains mediate head metamerization and could generate a combinatorial code to specify segment identity. To test this model, we developed a system for targeted gene expression in the early embryo, based on region specific promoters and the flp-out system. Misexpression of btd in the anterior half of the blastoderm embryo directed by the hunchback proximal promoter rescues the btd mutant head phenotype to wild-type. This indicates that, while btd activity is required for the formation of specific head segments, its ectopic expression does not disturb head development. We conclude that the spatial limits of btd expression are not instructive for metamerization of the head region and that btd activity does not contribute to a combinatorial code for specification of segment identity.

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Two distinct mechanisms for differential positioning of gene expression borders involving the Drosophila gap protein giant

Development ◽

10.1242/dev.125.19.3765 ◽

1998 ◽

Vol 125 (19) ◽

pp. 3765-3774 ◽

Cited By ~ 6

Author(s):

X. Wu ◽

R. Vakani ◽

S. Small

Keyword(s):

Target Genes ◽

Early Embryo ◽

Drosophila Embryo ◽

Anterior Border ◽

Gap Gene ◽

Gap Genes ◽

Pair Rule Gene ◽

Differential Positioning ◽

Pair Rule

We have combined genetic experiments and a targeted misexpression approach to examine the role of the gap gene giant (gt) in patterning anterior regions of the Drosophila embryo. Our results suggest that gt functions in the repression of three target genes, the gap genes Kruppel (Kr) and hunchback (hb), and the pair-rule gene even-skipped (eve). The anterior border of Kr, which lies 4–5 nucleus diameters posterior to nuclei that express gt mRNA, is set by a threshold repression mechanism involving very low levels of gt protein. In contrast, gt activity is required, but not sufficient for formation of the anterior border of eve stripe 2, which lies adjacent to nuclei that express gt mRNA. We propose that gt's role in forming this border is to potentiate repressive interaction(s) mediated by other factor(s) that are also localized to anterior regions of the early embryo. Finally, gt is required for repression of zygotic hb expression in more anterior regions of the embryo. The differential responses of these target genes to gt repression are critical for the correct positioning and maintenance of segmentation stripes, and normal anterior development.

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Spatial control of hairy protein expression during embryogenesis

Development ◽

10.1242/dev.107.3.489 ◽

1989 ◽

Vol 107 (3) ◽

pp. 489-504 ◽

Cited By ~ 12

Author(s):

K.L. Hooper ◽

S.M. Parkhurst ◽

D. Ish-Horowicz

Keyword(s):

Hierarchical Models ◽

Polyclonal Antiserum ◽

Wild Type ◽

Spatial Cues ◽

Protein Patterns ◽

Pair Rule Gene ◽

H Protein ◽

Blastoderm Stage ◽

Pair Rule ◽

Phase Relationships

We have used a polyclonal antiserum specific for the Drosophila segmentation gene, hairy (h), to analyse its expression during embryogenesis. The pattern of wild-type expression resembles that of h transcription, being expressed in stripes at the blastoderm stage. h is also expressed later in the stomodaeum, proctodaeum, tracheal pits and mesoderm. We demonstrate that h protein stripes show consistent phase relationships to those of the even-skipped (eve) pair-rule gene. We examine h protein patterns in embryos mutant for other segmentation genes, including h itself. We show that lack of h activity appears not to affect h striping, arguing that h expression is not under autoregulatory control. We also show that h activity is not needed for tracheal invagination. Mutations that are rearranged upstream of the h gene cause the loss of specific stripes, indicating that the h promoter includes activating elements that respond to specific spatial cues. Our observations suggest that pair-rule striping may be under redundant control, and we discuss possible implications for hierarchical models of pair-rule gene action.

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Faculty Opinions recommendation of Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.726638482.793522390 ◽

2016 ◽

Author(s):

Siegfried Roth

Keyword(s):

Gene Regulatory Network ◽

Regulatory Network ◽

Frequency Doubling ◽

Pair Rule Gene ◽

Gene Regulatory ◽

Pair Rule

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odd Oz: A novel Drosophila pair rule gene

Cell ◽

10.1016/0092-8674(94)90220-8 ◽

1994 ◽

Vol 77 (4) ◽

pp. 587-598 ◽

Cited By ~ 105

Author(s):

Anna Levine ◽

Ayelet Bashan-Ahrend ◽

Ofra Budai-Hadrian ◽

Devorah Gartenberg ◽

Sophia Menasherow ◽

...

Keyword(s):

Pair Rule Gene ◽

Pair Rule

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Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain

Journal of Cell Science ◽

10.1242/jcs.112.12.2019 ◽

1999 ◽

Vol 112 (12) ◽

pp. 2019-2032 ◽

Cited By ~ 7

Author(s):

A.D. Minet ◽

B.P. Rubin ◽

R.P. Tucker ◽

S. Baumgartner ◽

R. Chiquet-Ehrismann

Keyword(s):

Sequence Motifs ◽

Heparin Binding ◽

Terminal Part ◽

Phylogenetic Conservation ◽

Neuronal Protein ◽

Repeat Proteins ◽

Heparin Binding Domain ◽

Pair Rule Gene ◽

Pair Rule

The Drosophila gene ten-m is the first pair-rule gene not encoding a transcription factor, but an extracellular protein. We have characterized a highly conserved chicken homologue that we call teneurin-1. The C-terminal part harbors 26 repetitive sequence motifs termed YD-repeats. The YD-repeats are most similar to the core of the rhs elements of Escherichia coli. Related repeats in toxin A of Clostridium difficile are known to bind specific carbohydrates. We show that recombinantly expressed proteins containing the YD-repeats of teneurin-1 bind to heparin. Furthermore, heparin lyase treatment of extracts of cells expressing recombinant YD-repeat protein releases this protein from high molecular mass aggregates. In situ hybridization and immunostaining reveals teneurin-1 expression in neurons of the developing visual system of chicken and Drosophila. This phylogenetic conservation of neuronal expression from flies to birds implies fundamental roles for teneurin-1 in neurogenesis. This is supported by the neurite outgrowth occurring on substrates made of recombinant YD-repeat proteins, which can be inhibited by heparin. Database searches resulted in the identification of ESTs encoding at least three further members of the teneurin family of proteins. Furthermore, the human teneurin-1 gene could be identified on chromosome Xq24/25, a region implied in an X-linked mental retardation syndrome.

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