Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians

The Drosophila central nervous system derives from neural precursor cells, the neuroblasts (NBs), which are born from the neuroectoderm by the process of delamination. Each NB has a unique identity, which is revealed by the production of a characteristic cell lineage and a specific set of molecular markers it expresses. These NBs delaminate at different but reproducible time points during neurogenesis (S1-S5) and it has been shown for early delaminating NBs (S1/S2) that their identities depend on positional information conferred by segment polarity genes and dorsoventral patterning genes. We have studied mechanisms leading to the fate specification of a set of late delaminating neuroblasts, NB 6-4 and NB 7-3, both of which arise from the engrailed (en) expression domain, with NB 6-4 delaminating first. In contrast to former reports, we did not find any evidence for a direct role of hedgehog in the process of NB 7-3 specification. Instead, we present evidence to show that the interplay of the segmentation genes naked cuticle (nkd) and gooseberry (gsb), both of which are targets of wingless (wg) activity, leads to differential commitment to NB 6-4 and NB 7-3 cell fate. In the absence of either nkd or gsb, one NB fate is replaced by the other. However, the temporal sequence of delamination is maintained, suggesting that formation and specification of these two NBs are under independent control.

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The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation

Development ◽

10.1242/dev.111.4.1029 ◽

1991 ◽

Vol 111 (4) ◽

pp. 1029-1043 ◽

Cited By ~ 42

Author(s):

M. Peifer ◽

C. Rauskolb ◽

M. Williams ◽

B. Riggleman ◽

E. Wieschaus

Keyword(s):

Pattern Formation ◽

Imaginal Discs ◽

Protein Accumulation ◽

Segment Polarity Genes ◽

Adult Pattern ◽

Segment Polarity ◽

Lethal Allele ◽

Segment Polarity Gene ◽

Polarity Gene

The segment polarity genes of Drosophila were initially defined as genes required for pattern formation within each embryonic segment. Some of these genes also function to establish the pattern of the adult cuticle. We have examined the role of the armadillo (arm) gene in this latter process. We confirmed and extended earlier findings that arm and the segment polarity gene wingless are very similar in their effects on embryonic development. We next discuss the role of arm in pattern formation in the imaginal discs, as determined by using a pupal lethal allele, by analyzing clones of arm mutant tissue in imaginal discs, and by using a transposon carrying arm to produce adults with a reduced level of arm. Together, these experiments established that arm is required for the development of all imaginal discs. The requirement for arm varies along the dorsal-ventral and proximal-distal axes. Cells that require the highest levels of arm are those that express the wingless gene. Further, animals with reduced arm levels have phenotypes that resemble those of weak alleles of wingless. We present a description of the patterns of arm protein accumulation in imaginal discs. Finally, we discuss the implications of these results for the role of arm and wingless in pattern formation.

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Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos

Development ◽

10.1242/dev.119.supplement.105 ◽

1993 ◽

Vol 119 (Supplement) ◽

pp. 105-114 ◽

Cited By ~ 7

Author(s):

Marcel van den Heuvel ◽

John Klingensmith ◽

Norbert Perrimon ◽

Roel Nusse

Keyword(s):

Cell Communication ◽

Drosophila Embryo ◽

Current View ◽

Gene Products ◽

Cellular Interactions ◽

Protein Distribution ◽

Cubitus Interruptus ◽

Segment Polarity Genes ◽

Segment Polarity

By a complex and little understood mechanism, segment polarity genes control patterning in each segment of the Drosophila embryo. During this process, cell to cell communication plays a pivotal role and is under direct control of the products of segment polarity genes. Many of the cloned segment polarity genes have been found to be highly conserved in evolution, providing a model system for cellular interactions in other organisms. In Drosophila, two of these genes, engrailed and wingless, are expressed on either side of the parasegment border, wingless encodes a secreted molecule and engrailed a nuclear protein with a homeobox. Maintenance of engrailed expression is dependent on wingless and vice versa. To investigate the role of other segment polarity genes in the mutual control between these two genes, we have examined wingless and engrailed protein distribution in embryos mutant for each of the segment polarity genes. In embryos mutant for armadillo, dishevelled and porcupine, the changes in engrailed expression are identical to those in wingless mutant embryos, suggesting that their gene products act in the wingless pathway. In embryos mutant for hedgehog, fused, cubitus interruptus Dominant and gooseberry, expression of engrailed is affected to varying degrees. However wingless expression in the latter group decays in a similar way earlier than engrailed expression, indicating that these gene products might function in the maintenance of wingless expression. Using double mutant embryos, epistatic relationships between some segment polarity genes have been established. We present a model showing a current view of segment polarity gene interactions.

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Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians

10.1101/029892 ◽

2016 ◽

Cited By ~ 1

Author(s):

Bruno C. Vellutini ◽

Andreas Hejnol

Keyword(s):

Marine Invertebrates ◽

Early Embryogenesis ◽

Anterior Region ◽

Segmentation Genes ◽

Segment Polarity Genes ◽

Developmental Mechanisms ◽

Segment Polarity ◽

Anterior Patterning

AbstractThe diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids—distantly related animals considered to be segmented. Far less is known about the role of “segmentation genes” in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods—marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects—except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis.

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Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo

Development ◽

10.1242/dev.103.1.157 ◽

1988 ◽

Vol 103 (1) ◽

pp. 157-170 ◽

Cited By ~ 60

Author(s):

A. Martinez Arias ◽

N.E. Baker ◽

P.W. Ingham

Keyword(s):

Positional Information ◽

Drosophila Embryo ◽

Gene Products ◽

Segment Polarity Genes ◽

Restricted Domains ◽

Segment Polarity ◽

Mutant Phenotypes ◽

Segment Polarity Gene ◽

Polarity Gene

Segment polarity genes are expressed and required in restricted domains within each metameric unit of the Drosophila embryo. We have used the expression of two segment polarity genes engrailed (en) and wingless (wg) to monitor the effects of segment polarity mutants on the basic metameric pattern. Absence of patched (ptc) or naked (nkd) functions triggers a novel sequence of en and wg patterns. In addition, although wg and en are not expressed on the same cells absence of either one has effects on the expression of the other. These observations, together with an analysis of mutant phenotypes during development, lead us to suggest that positional information is encoded in cell states defined and maintained by the activity of segment polarity gene products.

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The role of segment polarity genes during Drosophila neurogenesis.

Genes & Development ◽

10.1101/gad.3.6.890 ◽

1989 ◽

Vol 3 (6) ◽

pp. 890-904 ◽

Cited By ~ 128

Author(s):

N H Patel ◽

B Schafer ◽

C S Goodman ◽

R Holmgren

Keyword(s):

Segment Polarity Genes ◽

Segment Polarity

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1 (2)gl gene regulates late expression of segment polarity genes in Drosophila

Mechanisms of Development ◽

10.1016/0925-4773(95)00367-3 ◽

1995 ◽

Vol 51 (2-3) ◽

pp. 227-234 ◽

Cited By ~ 5

Author(s):

Ashim Mukherjee ◽

S.C. Lakhotia ◽

J.K. Roy

Keyword(s):

Segment Polarity Genes ◽

Segment Polarity ◽

Late Expression

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Studying the effect of cell division on expression patterns of the segment polarity genes

Journal of The Royal Society Interface ◽

10.1098/rsif.2007.1345.focus ◽

2008 ◽

Vol 5 (suppl_1) ◽

Cited By ~ 10

Author(s):

Madalena Chaves ◽

Réka Albert

Keyword(s):

Cell Division ◽

Expression Patterns ◽

Gene Expression Pattern ◽

Specific Gene ◽

Biological Processes ◽

Segment Polarity Genes ◽

Genes Expression ◽

Its Gene ◽

Segment Polarity ◽

Segment Polarity Gene

The segment polarity gene family, and its gene regulatory network, is at the basis of Drosophila embryonic development. The network's capacity for generating and robustly maintaining a specific gene expression pattern has been investigated through mathematical modelling. The models have provided several useful insights by suggesting essential network links, or uncovering the importance of the relative time scales of different biological processes in the formation of the segment polarity genes' expression patterns. But the developmental pattern formation process raises many other questions. Two of these questions are analysed here: the dependence of the signalling protein sloppy paired on the segment polarity genes and the effect of cell division on the segment polarity genes' expression patterns. This study suggests that cell division increases the robustness of the segment polarity network with respect to perturbations in biological processes.

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