even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect

AbstractThe discovery of pair-rule genes (PRGs) in Drosophila revealed the existence of an underlying two-segment-wide prepattern directing embryogenesis. The milkweed bug Oncopeltus, a hemimetabolous insect, is a more representative arthropod: most of its segments form sequentially after gastrulation. Here we report the expression and function of orthologs of the complete set of nine Drosophila PRGs in Oncopeltus. Seven Of-PRG-orthologs are expressed in stripes in the primordia of every segment, rather than every-other segment, Of-runt is PR-like, and several are also expressed in the segment addition zone. RNAi-mediated knockdown of Of-odd-skipped, paired and sloppy-paired impacted all segments, with no indication of PR-like register. We confirm that Of-E75A is expressed in PR-like stripes, although it is not PR in Drosophila, demonstrating the existence of an underlying PR-like prepattern in Oncopeltus. These findings reveal that a switch occurred in regulatory circuits leading to segment formation: while several holometabolous insects are “Drosophila-like,” utilizing PRG-orthologs for PR-patterning, most Of-PRGs are expressed segmentally in Oncopeltus, a more basally-branching insect. Thus, an evolutionarily stable phenotype – segment formation – is directed by alternate regulatory pathways in diverse species.Summary StatementDespite the broad of conservation of segmentation in insects, the regulatory genes underlying this process in Drosophila have different roles in the hemipteran, Oncopeltus fasciatus.

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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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Tc-knirps plays different roles in the specification of antennal and mandibular parasegment boundaries and is regulated by a pair-rule gene in the beetle Tribolium castaneum

BMC Developmental Biology ◽

10.1186/1471-213x-13-25 ◽

2013 ◽

Vol 13 (1) ◽

pp. 25 ◽

Cited By ~ 7

Author(s):

Andrew D Peel ◽

Julia Schanda ◽

Daniela Grossmann ◽

Frank Ruge ◽

Georg Oberhofer ◽

...

Keyword(s):

Tribolium Castaneum ◽

Pair Rule Gene ◽

Pair Rule

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Unipolar distributions of junctional Myosin II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension

eLife ◽

10.7554/elife.12094 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 55

Author(s):

Robert J Tetley ◽

Guy B Blanchard ◽

Alexander G Fletcher ◽

Richard J Adams ◽

Bénédicte Sanson

Keyword(s):

Myosin Ii ◽

Interaction Model ◽

Cell Interaction ◽

Cell Number ◽

Cell Polarization ◽

Convergence And Extension ◽

Pair Rule Gene ◽

Cell Intercalation ◽

Pair Rule ◽

Cell Cell

Convergence and extension movements elongate tissues during development. Drosophila germ-band extension (GBE) is one example, which requires active cell rearrangements driven by Myosin II planar polarisation. Here, we develop novel computational methods to analyse the spatiotemporal dynamics of Myosin II during GBE, at the scale of the tissue. We show that initial Myosin II bipolar cell polarization gives way to unipolar enrichment at parasegmental boundaries and two further boundaries within each parasegment, concomitant with a doubling of cell number as the tissue elongates. These boundaries are the primary sites of cell intercalation, behaving as mechanical barriers and providing a mechanism for how cells remain ordered during GBE. Enrichment at parasegment boundaries during GBE is independent of Wingless signaling, suggesting pair-rule gene control. Our results are consistent with recent work showing that a combinatorial code of Toll-like receptors downstream of pair-rule genes contributes to Myosin II polarization via local cell-cell interactions. We propose an updated cell-cell interaction model for Myosin II polarization that we tested in a vertex-based simulation.

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Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network

eLife ◽

10.7554/elife.18215 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 31

Author(s):

Erik Clark ◽

Michael Akam

Keyword(s):

Gene Expression ◽

Gene Regulatory Network ◽

Regulatory Network ◽

Frequency Doubling ◽

Drosophila Embryo ◽

Anteroposterior Patterning ◽

Regulatory Interactions ◽

Pair Rule Gene ◽

Gene Regulatory ◽

Pair Rule

The Drosophila embryo transiently exhibits a double-segment periodicity, defined by the expression of seven 'pair-rule' genes, each in a pattern of seven stripes. At gastrulation, interactions between the pair-rule genes lead to frequency doubling and the patterning of 14 parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of pair-rule gene expression, we demonstrate that frequency-doubling is precipitated by multiple coordinated changes to the network of regulatory interactions between the pair-rule genes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa/Zic), as the cause of these changes, and show that the patterning of the even-numbered parasegment boundaries relies on Opa-dependent regulatory interactions. Our findings indicate that the pair-rule gene regulatory network has a temporally modulated topology, permitting the pair-rule genes to play stage-specific patterning roles.

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The zygotic control of Drosophila pair-rule gene expression. I. A search for new pair-rule regulatory loci

Development ◽

10.1242/dev.107.3.663 ◽

1989 ◽

Vol 107 (3) ◽

pp. 663-672 ◽

Cited By ~ 2

Author(s):

S.H. Vavra ◽

S.B. Carroll

Keyword(s):

Gene Expression ◽

Regulatory System ◽

Wild Type ◽

Periodic Patterns ◽

Pair Rule Gene ◽

New Type ◽

Regulatory Loci ◽

Direct Inspection ◽

Pair Rule ◽

Zygotic Control

The examination of pair-rule gene expression in wild-type and segmentation mutant embryos has identified many, but not necessarily all, of the elements of the regulatory system that establish their periodic patterns. Here we have conducted a new type of search for previously unknown regulators of these genes by examining pair-rule gene expression in blastoderm embryos lacking parts of or entire chromosomes. This method has the advantage of direct inspection of abnormal pair-rule gene patterns without relying upon mutagenesis or interpretation of larval phenotypes for the identification of segmentation genes. From these experiments we conclude that: (i) most zygotically required regulators of the fushi tarazu (ftz), even-skipped (eve) and hairy (h) pair-rule genes have been identified, except for one or more loci we have uncovered on chromosome arm 2L; (ii) the repression of the ftz and eve genes in the anterior third of the embryo is under maternal, not zygotic control; and (iii) there are no general zygotically required activators of pair-rule gene expression. The results suggest that the molecular basis of pair-rule gene regulation can be pursued with greater confidence now that most key trans-acting factors are already in hand.

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Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity

Development ◽

10.1242/dev.110.3.759 ◽

1990 ◽

Vol 110 (3) ◽

pp. 759-767 ◽

Cited By ~ 4

Author(s):

R. Warrior ◽

M. Levine

Keyword(s):

Expression Patterns ◽

Gene Products ◽

Embryonic Cells ◽

Periodic Patterns ◽

Threshold Response ◽

Gap Gene ◽

Relative Placement ◽

Segment Polarity ◽

Pair Rule Gene ◽

Pair Rule

A key step in Drosophila segmentation is the establishment of periodic patterns of pair-rule gene expression in response to gap gene products. From an examination of the distribution of gap and pair-rule proteins in various mutants, we conclude that the on/off periodicity of pair-rule stripes depends on both the exact concentrations and combinations of gap proteins expressed in different embryonic cells. It has been suggested that the distribution of gap gene products depends on cross-regulatory interactions among these genes. Here we provide evidence that autoregulation also plays an important role in this process since there is a reduction in the levels of Kruppel (Kr) RNA and protein in a Kr null mutant. Once initiated by the gap genes each pair-rule stripe is bell shaped and has ill-defined margins. By the end of the fourteenth nuclear division cycle, the stripes of the pair-rule gene even-skipped (eve) sharpen and polarize, a process that is essential for the precisely localized expression of segment polarity genes. This sharpening process appears to depend on a threshold response of the eve promoter to the combinatorial action of eve and a second pair-rule gene hairy. The eve and hairy expression patterns overlap but are out of register and the cells of maximal overlap form the anterior margin of the polarized eve stripe. We propose that the relative placement of the eve and hairy stripes may be an important factor in the initiation of segment polarity.

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