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Journal articles on the topic 'Segment polarity genes'

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Published: 4 June 2021

Last updated: 14 February 2022

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van den Heuvel, Marcel, John Klingensmith, Norbert Perrimon, and Roel Nusse. "Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos." Development 119, Supplement (1993): 105–14. http://dx.doi.org/10.1242/dev.119.supplement.105.

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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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Ingham, Philip W., and Yoshiro Nakano. "Cell Patterning and Segment Polarity Genes in Drosophila. (pattern formation/Drosophila/Cell interacton/Signal transduction/Segment polarity genes)." Development, Growth and Differentiation 32, no. 6 (1990): 563–74. http://dx.doi.org/10.1111/j.1440-169x.1990.00563.x.

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Ingham, Philip W. "Segment polarity genes and cell patterning within the Drosophila body segment." Current Opinion in Genetics & Development 1, no. 2 (1991): 261–67. http://dx.doi.org/10.1016/s0959-437x(05)80080-2.

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Perrimon, Norbert, and Anthony P. Mahowald. "Multiple functions of segment polarity genes in Drosophila." Developmental Biology 119, no. 2 (1987): 587–600. http://dx.doi.org/10.1016/0012-1606(87)90061-3.

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Gubb, David. "Genes controlling cellular polarity in Drosophila." Development 119, Supplement (1993): 269–77. http://dx.doi.org/10.1242/dev.119.supplement.269.

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The control of cellular polarity is one of the least understood aspects of development. Genes have been identified in Drosophila that affect the polarity of embryonic cells in all three axes, apical-hasal, proximodistal and dorsoventral. Mutations that affect adult polarity are also known and mutant flies show several types of pattern alteration, including rotations and mirror-image duplications. Imaginal discs are much greater in size, however, than the embryo, and adult structures contain very large numbers of cells, many of which are not visibly differentiated with respect to their immediate neighbours. In regions where neighbouring cells are similar to each other, the imaginal polarity mutants alter the orientation of bristles and hairs but do not change cellular fate. Other regions, such as the tarsal segments of the legs, the ommatidia of the eye and the bracted bristle sockets on the tibia, behave as discrete fields. Within these fields, fine-scale mirror-image reversals and pattern duplications are observed, analogous to those caused by the embryonic segment polarity mutants. Thus, the polarised transmission of information can affect either orientation or fate depending on whether cells are differentiated from their immediate neighbours. Cellular polarity will be critically dependent on both the internal cytoskeletal architecture and the spatial organisation of signal transduction molecules within the cell membrane.

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Martinez Arias, A., N. E. Baker, and P. W. Ingham. "Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo." Development 103, no. 1 (1988): 157–70. http://dx.doi.org/10.1242/dev.103.1.157.

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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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Crozatier, M., D. Valle, L. Dubois, S. Ibnsouda, and A. Vincent. "Head versus trunk patterning in the Drosophila embryo; collier requirement for formation of the intercalary segment." Development 126, no. 19 (1999): 4385–94. http://dx.doi.org/10.1242/dev.126.19.4385.

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Whereas the segmental nature of the insect head is well established, relatively little is known about the genetic and molecular mechanisms governing this process. In this paper, we report the phenotypic analysis of mutations in collier (col), which encodes the Drosophila member of the COE family of HLH transcription factors and is activated at the blastoderm stage in a region overlapping a parasegment (PS0: posterior intercalary and anterior mandibular segments) and a mitotic domain, MD2. col mutant embryos specifically lack intercalary ectodermal structures. col activity is required for intercalary-segment expression both of the segment polarity genes hedgehog, engrailed, and wingless, and of the segment identity gene cap and collar. The parasegmental register of col activation is controlled by the combined activities of the head-gap genes buttonhead and empty spiracles and the pair-rule gene even skipped; it therefore integrates inputs from both the head and trunk segmentation systems, which were previously considered as being essentially independent. After gastrulation, positive autoregulation of col is limited to cells of anterior PS0. Conversely, heat-pulse induced ubiquitous expression of Col leads to disruption of the head skeleton. Together, these results indicate that col is required for establishment of the PS(−1)/PS0 parasegmental border and formation of the intercalary segment. Our data support neither a simple combinatorial model for segmental patterning of the head nor a direct activation of segment polarity gene expression by head-gap genes, but rather argue for the existence of parasegment-specific second order regulators acting in the head, at a level similar to that of pair-rule genes in the trunk.

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Patel, N. H., B. Schafer, C. S. Goodman, and R. Holmgren. "The role of segment polarity genes during Drosophila neurogenesis." Genes & Development 3, no. 6 (1989): 890–904. http://dx.doi.org/10.1101/gad.3.6.890.

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Noordermeer, Jasprien, John Klingensmith, and Roel Nusse. "Differential requirements for segment polarity genes in wingless signaling." Mechanisms of Development 51, no. 2-3 (1995): 145–55. http://dx.doi.org/10.1016/0925-4773(95)00348-7.

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Gutjahr, T., N. H. Patel, X. Li, C. S. Goodman, and M. Noll. "Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro." Development 118, no. 1 (1993): 21–31. http://dx.doi.org/10.1242/dev.118.1.21.

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The segment-polarity class of segmentation genes in Drosophila are primarily involved in the specification of sub-segmental units. In addition, some of the segment-polarity genes have been shown to specify cell fates within the central nervous system. One of these loci, gooseberry, consists of two divergently transcribed genes, gooseberry and gooseberry neuro, which share a paired box as well as a paired-type homebox. Here, the expression patterns of the two gooseberry gene products are described in detail. The gooseberry protein appears in a characteristic segment-polarity pattern of stripes at gastrulation and persists until head involution. It is initially restricted to the ectodermal and neuroectodermal germ layer, but is later detected in mesodermal and neuronal cells as well. The gooseberry neuro protein first appears during germ band extension in cells of the central nervous system and also, much later, in epidermal stripes and in a small number of muscle cells. P-element-mediated transformation with the gooseberry gene has been used to demonstrate that gooseberry transactivates gooseberry neuro and is sufficient to rescue the gooseberry cuticular phenotype in the absence of gooseberry neuro.

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Hidalgo, A., and P. Ingham. "Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched." Development 110, no. 1 (1990): 291–301. http://dx.doi.org/10.1242/dev.110.1.291.

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Intrasegmental patterning in the Drosophila embryo requires the activity of the segment polarity genes. The acquisition of positional information by cells during embryogenesis is reflected in the dynamic patterns of expression of several of these genes. In the case of patched, early ubiquitous expression is followed by its repression in the anterior portion of each parasegment; subsequently each broad band of expression splits into two narrow stripes. In this study we analyse the contribution of other segment polarity gene functions to the evolution of this pattern; we find that the first step in patched regulation is under the control of engrailed whereas the second requires the activity of both cubitus interruptusD and patched itself. Furthermore, the products of engrailed, wingless and hedgehog are essential for maintaining the normal pattern of expression of patched.

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Mohler, J., and K. Vani. "Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila." Development 115, no. 4 (1992): 957–71. http://dx.doi.org/10.1242/dev.115.4.957.

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hedgehog is a segment polarity gene necessary to maintain the proper organization of each segment of the Drosophila embryo. We have identified the physical location of a number of rearrangement breakpoints associated with hedgehog mutations. The corresponding hh RNA is expressed in a series of segmental stripes starting at cellular blastoderm in the posterior portion of each segment. This RNA is localized predominantly within nuclei until stage 10, when the localization becomes primarily cytoplasmic. Expression of hh RNA in the posterior compartment is independent of most other segment polarity genes, including en, until the late extended germ-band stage (stage 11). Sequence analysis of the hedgehog locus suggests the protein product is a transmembrane protein, which may, therefore, be directly involved in cell-cell communication.

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Howard, Ken. "The generation of periodic pattern during early Drosophila embryogenesis." Development 104, Supplement (1988): 35–50. http://dx.doi.org/10.1242/dev.104.supplement.35.

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The first indication of the formation of segment primordia in Drosophila is expression of the segment-polarity genes in particular parts of each primordium. These patterns are controlled by another class of genes, the pair-rule genes, which show characteristic two-segment periodic expression. Each pair-rule gene has a unique domain of activity and in one view different combinations of pair-rule gene products directly control the expression of the segment-polarity genes. There is a hierarchy within the pair-rule class revealed by pair-rule gene interactions. It is unlikely that these interactions generate the periodicity de novo. Instead, pair-rule genes respond to positional information generated by a system involving zygotic gap and maternal coordinate genes. In this paper, I will concentrate on the problem of the mechanism that generates these pair-rule patterns, the first periodic ones seen during segmentation. I will review and discuss some of the relevant literature, illustrating certain points with data from my recent work.

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Forbes, A. J., Y. Nakano, A. M. Taylor, and P. W. Ingham. "Genetic analysis of hedgehog signalling in the Drosophila embryo." Development 119, Supplement (1993): 115–24. http://dx.doi.org/10.1242/dev.119.supplement.115.

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The segment polarity genes play a fundamental role in the patterning of cells within individual body segments of the Drosophila embryo. Two of these genes wingless (wg) and hedgehog (hh) encode proteins that enter the secretory pathway and both are thought to act by instructing the fates of cells neighbouring those in which they are expressed. Genetic analysis bas identified the transcriptional activation of wg as one of the targets of hh activity: here we present evidence that transduction of the hh-encoded signal is mediated by the activity of four other segment polarity genes, patched, fused, costal-2 and cubitus interruptus. The results of our genetic epistatsis analysis together with the molecular structures of the products of these genes where known, suggest a pathway of interactions leading from reception of the hh-encoded signal at the cell membrane to transcriptional activation in the cell nucleus. We have also found that transcription of patched is regulated by the same pathway and describe the identification of cis-acting upstream elements of the ptc transcription unit that mediate this regulation.

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Schmidt-Ott, U., and G. M. Technau. "Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants." Development 116, no. 1 (1992): 111–25. http://dx.doi.org/10.1242/dev.116.1.111.

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Based on the expression pattern of the segment polarity genes engrailed and wingless during the embryonic development of the larval head, we found evidence that the head of Drosophila consists of remnants of seven segments (4 pregnathal and 3 gnathal) all of which contribute cells to neuromeres in the central nervous system. Until completion of germ band retraction, the four pregnathal segment remnants and their corresponding neuromeres become arranged in an S-shape. We discuss published evidence for seven head segments and morphogenetic movements during head formation in various insects (and crustaceans).

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Limbourg-Bouchon, B., D. Busson, and C. Lamour-Isnard. "Interactions between fused, a segment-polarity gene in Drosophila, and other segmentation genes." Development 112, no. 2 (1991): 417–29. http://dx.doi.org/10.1242/dev.112.2.417.

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Fused (fu) is a segment polarity gene whose product is maternally required in the posterior part of each segment. To define further the role of fused and determine how it interacts with other segmentation genes, we examined the phenotypes obtained by combining fused with mutations of pair rule, homeotic and other segment polarity loci. When it was possible, we also looked at the distribution of corresponding proteins in fused mutant embryos. We observed that fused-naked (fu;nkd) double mutant embryos display a phenotypic suppression of simple mutant phenotypes: both naked cuticle and denticle belts, which would normally have been deleted by one of the two mutants alone, were restored. In fused mutant embryos, engrailed (en) and wingless (wg) expression was normal until germ band extension, but partially and completely disappeared respectively during germ band retraction. In the fu;nkd double mutant embryo, en was expressed as in nkd mutant at germ band extension, but later this expression was restricted and became normal at germ band retraction. On the contrary, wg expression disappeared as in fu simple mutant embryos. We conclude that the requirements for fused, naked and wingless activities for normal segmental patterning are not absolute, and propose mechanisms by which these genes interact to specify anterior and posterior cell fates.

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Hidalgo, Alicia. "Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila." Mechanisms of Development 35, no. 2 (1991): 77–87. http://dx.doi.org/10.1016/0925-4773(91)90059-f.

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Forbes, A. J., A. C. Spradling, P. W. Ingham, and H. Lin. "The role of segment polarity genes during early oogenesis in Drosophila." Development 122, no. 10 (1996): 3283–94. http://dx.doi.org/10.1242/dev.122.10.3283.

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In the Drosophila ovary, hedgehog (hh) signaling from cells near the apical tip of the germarium stimulates the proliferation and specification of somatic cells in region 2 of the germarium, 2–5 cells away from the hh-expressing cells (A. J. Forbes, H. Lin, P. Ingham and A. Spradling (1996) Development 122, 1125–1135). This report examines the role during early oogenesis of several genes that are known to function in hh-mediated signaling during embryonic and larval development (P. Ingham (1995) Current Opin. Genetics Dev. 5, 528–534). As in imaginal discs, engrailed (en) is co-expressed with hh in the germarium, while patched (ptc) and cubitus interruptus (ci) are expressed in somatic cells throughout the germarium and in developing egg chambers, with ptc expression being elevated within 10 cell diameters of the source of the hh signal. Moreover, the somatic cell overproliferation caused by ectopic hh expression is accompanied by elevated levels of ptc and is phenocopied in ptc- somatic clones. These analyses suggest that ptc and ci are components of the hh signaling pathway in the germarium. However, unlike embryos and imaginal discs, neither wingless (wg) nor decapentaplegic (dpp) appear to mediate the ovarian hh signal. wg is expressed in ‘cap cells,’ a subset of hh-expressing cells located adjacent to germ-line stem cells, but is unaffected by ectopic hh expression. Nor does the ectopic expression of wg or dpp mimic the effect of ectopic hh expression. We propose that Hh diffuses from apical cells, including cap cells, and regulates the proliferation of nearby ovarian somatic cells by antagonizing the negative effects of ptc on ci activity in these cells, thereby allowing the transcription of ci-dependent genes, including ptc itself.

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Ingham, P. W., and A. Hidalgo. "Regulation of wingless transcription in the Drosophila embryo." Development 117, no. 1 (1993): 283–91. http://dx.doi.org/10.1242/dev.117.1.283.

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The segment polarity gene wingless (wg) is expressed in a complex pattern during embryogenesis suggesting that it plays multiple roles in the development of the embryo. The best characterized of these is its role in cell pattening in each parasegment, a process that requires the activity of other segment polarity genes including patched (ptc) and hedgehog (hh). Here we present further evidence that ptc and hh encode components of a signal transduction pathway that regulate the expression of wg transcription following its activation by pair-rule genes. We also show that most other aspects of wg expression are independent of this regulatory network.

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Lehmann, Ruth, and Hans Georg Frohnhöfer. "Segmental polarity and identity in the abdomen of Drosophila is controlled by the relative position of gap gene expression." Development 107, Supplement (1989): 21–29. http://dx.doi.org/10.1242/dev.107.supplement.21.

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The establishment of the segmental pattern in the Drosophila embryo is directed by three sets of maternal genes: the anterior, the terminal and the posterior group of genes. Embryos derived from females mutant for one of the posterior group genes lack abdominal segmentation. This phenotype can be rescued by transplantation of posterior pole plasm into the abdominal region of mutant embryos. We transplanted posterior pole plasm into the middle of embryos mutant either for the posterior, the anterior and posterior, or all three maternal systems and monitored the segmentation pattern as well as the expression of the zygotic gap gene Krüppel in control and injected embryos. We conclude that polarity and identity of the abdominal segments do not depend on the relative concentration of posterior activity but rather on the position of gap gene expression. By changing the pattern of gap gene expression, the orientation of the abdomen can be reversed. These experiments suggest that maternal gene products act in a strictly hierarchical manner. The function of the maternal gene products becomes dispensable once the position of the zygotically expressed gap genes is determined. Subsequently the gap genes will control the pattern of the pair-rule and segment polarity genes.

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Eldon, E., S. Kooyer, D. D'Evelyn, et al. "The Drosophila 18 wheeler is required for morphogenesis and has striking similarities to Toll." Development 120, no. 4 (1994): 885–99. http://dx.doi.org/10.1242/dev.120.4.885.

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We have isolated and characterized a novel gene, named 18 wheeler (18w) for its unique segmental expression pattern in Drosophila embryos and expression in cells that migrate extensively. 18 wheeler transcripts accumulate in embryos in a pattern reminiscent of segment polarity genes. Mutations in 18w cause death during larval development and early adulthood. Escaping mutant adults often display leg, antenna, and wing deformities, presumably resulting from improper eversion of imaginal discs. Sequence analysis indicates that 18w encodes a transmembrane protein with an extracellular moiety containing many leucine rich repeats and cysteine motifs, and an intracellular domain bearing homology to the cytoplasmic portion of the interleukin-1-receptor. Expression of 18W protein in non-adhesive Schneider 2 cells promotes rapid and robust aggregation of cells. Analysis of the expression of 18w in different mutant backgrounds shows that it is under control of segment polarity and homeotic genes. The data suggest that the 18W protein participates in the developmental program specified by segmentation and homeotic genes as a cell adhesion or receptor molecule that facilitates cell movements.

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Bejsovec, A., and E. Wieschaus. "Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos." Development 119, no. 2 (1993): 501–17. http://dx.doi.org/10.1242/dev.119.2.501.

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Each segment of a Drosophila larva shows a precisely organized pattern of cuticular structures, indicating diverse cellular identities in the underlying epidermis. Mutations in the segment polarity genes alter the cuticle pattern secreted by the epidermal cells; these mutant patterns provide clues about the role that each gene product plays in the development of wild-type epidermal pattern. We have analyzed embryos that are multiply mutant for five key patterning genes: wingless, patched, engrailed, naked and hedgehog. Our results indicate that wild-type activity of these five segment polarity genes can account for most of the ventral pattern elements and that their gene products interact extensively to specify the diverse cellular identities within the epidermis. Two pattern elements can be correlated with individual gene action: wingless is required for formation of naked cuticle and engrailed is required for formation of the first row of denticles in each abdominal denticle belt. The remaining cell types can be produced by different combinations of the five gene activities. wingless activity generates the diversity of cell types within the segment, but each specific cell identity depends on the activity of patched, engrailed, naked and hedgehog. These molecules modulate the distribution and interpretation of wingless signalling activity in the ventral epidermal cells and, in addition, each can contribute to pattern through a pathway independent of the wingless signalling pathway.

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Jäckle, Herbert, Eveline Seifert, Anette Preiss, and Urs B. Rosenberg. "Probing gene activity in Drosophila embryos." Development 97, Supplement (1986): 157–68. http://dx.doi.org/10.1242/dev.97.supplement.157.

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The segmentation pattern of the Drosophila wild-type embryo is characterized by a number of easily identifiable cuticular structures. They include skeletal elements of the involuted head and ventral denticle belts that define by size, pattern and orientation the anterior part of the three thoracic and eight abdominal segments. Further landmarks such as sensory organs and the posterior tracheal endings (‘Filzkörper’), in combination with the denticle belts, allow one to unequivocally determine the polarity and quality of each segment in preparations of the larval cuticle (see Fig. 1D). The segmentation pattern of Drosophila is established at about blastoderm stage and it requires both maternally and zygotically active genes. Genetic analysis has identified a number of genes with zygotic activity that regulate key steps during pattern formation. Mutations in these genes cause specific defects in the segmental pattern of the embryo that allow the definition of classes of segmentation genes required for the subdivision of the embryo into segmental units (Nüsslein-Volhard & Wieschaus, 1980).

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Mohler, J., J. W. Mahaffey, E. Deutsch, and K. Vani. "Control of Drosophila head segment identity by the bZIP homeotic gene cnc." Development 121, no. 1 (1995): 237–47. http://dx.doi.org/10.1242/dev.121.1.237.

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Mutational analysis of cap'n'collar (cnc), a bZIP transcription factor closely related to the mammalian erythroid factor NF-E2 (p45), indicates that it acts as a segment-specific selector gene controlling the identity of two cephalic segments. In the mandibular segment, cnc has a classical homeotic effect: mandibular structures are missing in cnc mutant larvae and replaced with duplicate maxillary structures. We propose that cnc functions in combination with the homeotic gene Deformed to specify mandibular development. Labral structures are also missing in cnc mutant larvae, where a distinct labral primordia is not properly maintained in the developing foregut, as observed by the failure to maintain and elaborate patterns of labral-specific segment polarity gene expression. Instead, the labral primordium fuses with the esophageal primordium to contribute to formation of the esophagus. The role of cnc in labral development is reciprocal to the role of homeotic gene forkhead, which has an identical function in the maintenance of the esophageal primordium. This role of homeotic selector genes for the segment-specific maintenance of segment polarity gene expression is a unique feature of segmentation in the preoral head region of Drosophila.

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Bhat, Krishna Moorthi. "Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis." BioEssays 21, no. 6 (1999): 472–85. http://dx.doi.org/10.1002/(sici)1521-1878(199906)21:6<472::aid-bies4>3.0.co;2-w.

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Davis, Gregory K., Carlos A. Jaramillo, and Nipam H. Patel. "Pax group III genes and the evolution of insect pair-rule patterning." Development 128, no. 18 (2001): 3445–58. http://dx.doi.org/10.1242/dev.128.18.3445.

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Pair-rule genes were identified and named for their role in segmentation in embryos of the long germ insect Drosophila. Among short germ insects these genes exhibit variable expression patterns during segmentation and thus are likely to play divergent roles in this process. Understanding the details of this variation should shed light on the evolution of the genetic hierarchy responsible for segmentation in Drosophila and other insects. We have investigated the expression of homologs of the Drosophila Pax group III genes paired, gooseberry and gooseberry-neuro in short germ flour beetles and grasshoppers. During Drosophila embryogenesis, paired acts as one of several pair-rule genes that define the boundaries of future parasegments and segments, via the regulation of segment polarity genes such as gooseberry, which in turn regulates gooseberry-neuro, a gene expressed later in the developing nervous system. Using a crossreactive antibody, we show that the embryonic expression of Pax group III genes in both the flour beetle Tribolium and the grasshopper Schistocerca is remarkably similar to the pattern in Drosophila. We also show that two Pax group III genes, pairberry1 and pairberry2, are responsible for the observed protein pattern in grasshopper embryos. Both pairberry1 and pairberry2 are expressed in coincident stripes of a one-segment periodicity, in a manner reminiscent of Drosophila gooseberry and gooseberry-neuro. pairberry1, however, is also expressed in stripes of a two-segment periodicity before maturing into its segmental pattern. This early expression of pairberry1 is reminiscent of Drosophila paired and represents the first evidence for pair-rule patterning in short germ grasshoppers or any hemimetabolous insect.

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Saulier-Le Drean, B., A. Nasiadka, J. Dong, and H. M. Krause. "Dynamic changes in the functions of Odd-skipped during early Drosophila embryogenesis." Development 125, no. 23 (1998): 4851–61. http://dx.doi.org/10.1242/dev.125.23.4851.

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Although many of the genes that pattern the segmented body plan of the Drosophila embryo are known, there remains much to learn in terms of how these genes and their products interact with one another. Like many of these gene products, the protein encoded by the pair-rule gene odd-skipped (Odd) is a DNA-binding transcription factor. Genetic experiments have suggested several candidate target genes for Odd, all of which appear to be negatively regulated. Here we use pulses of ectopic Odd expression to test the response of these and other segmentation genes. The results are complex, indicating that Odd is capable of repressing some genes wherever and whenever Odd is expressed, while the ability to repress others is temporally or spatially restricted. Moreover, one target gene, fushi tarazu, is both repressed and activated by Odd, the outcome depending upon the stage of development. These results indicate that the activity of Odd is highly dependent upon the presence of cofactors and/or overriding inhibitors. Based on these results, and the segmental phenotypes generated by ectopic Odd, we suggest a number of new roles for Odd in the patterning of embryonic segments. These include gap-, pair-rule- and segment polarity-type functions.

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Lawrence, P. A., J. Casal, and G. Struhl. "hedgehog and engrailed: pattern formation and polarity in the Drosophila abdomen." Development 126, no. 11 (1999): 2431–39. http://dx.doi.org/10.1242/dev.126.11.2431.

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Like the Drosophila embryo, the abdomen of the adult consists of alternating anterior (A) and posterior (P) compartments. However the wing is made by only part of one A and part of one P compartment. The abdomen therefore offers an opportunity to compare two compartment borders (A/P is within the segment and P/A intervenes between two segments), and ask if they act differently in pattern formation. In the embryo, abdomen and wing P compartment cells express the selector gene engrailed and secrete Hedgehog protein whilst A compartment cells need the patched and smoothened genes in order to respond to Hedgehog. We made clones of cells with altered activities of the engrailed, patched and smoothened genes. Our results confirm (1) that the state of engrailed, whether ‘off’ or ‘on’, determines whether a cell is of A or P type and (2) that Hedgehog signalling, coming from the adjacent P compartments across both A/P and P/A boundaries, organises the pattern of all the A cells. We have uncovered four new aspects of compartments and engrailed in the abdomen. First, we show that engrailed acts in the A compartment: Hedgehog leaves the P cells and crosses the A/P boundary where it induces engrailed in a narrow band of A cells. engrailed causes these cells to form a special type of cuticle. No similar effect occurs when Hedgehog crosses the P/A border. Second, we look at the polarity changes induced by the clones, and build a working hypothesis that polarity is organised, in both compartments, by molecule(s) emanating from the A/P but not the P/A boundaries. Third, we show that both the A and P compartments are each divided into anterior and posterior subdomains. This additional stratification makes the A/P and the P/A boundaries fundamentally distinct from each other. Finally, we find that when engrailed is removed from P cells (of, say, segment A5) they transform not into A cells of the same segment, but into A cells of the same parasegment (segment A6).

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Miller, Sherry, Teresa D. Shippy, Prashant S. Hosmani, et al. "Annotation of segmentation pathway genes in the Asian citrus psyllid, Diaphorina citri." Gigabyte 2021 (July 8, 2021): 1–13. http://dx.doi.org/10.46471/gigabyte.26.

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Insects have a segmented body plan that is established during embryogenesis when the anterior–posterior (A–P) axis is divided into repeated units by a cascade of gene expression. The cascade is initiated by protein gradients created by translation of maternally provided mRNAs, localized at the anterior and posterior poles of the embryo. Combinations of these proteins activate specific gap genes to divide the embryo into distinct regions along the anterior–posterior axis. Gap genes then activate pair-rule genes, which are usually expressed in parts of every other segment. The pair-rule genes, in turn, activate expression of segment polarity genes in a portion of each segment. The segmentation genes are generally conserved among insects, although there is considerable variation in how they are deployed. We annotated 25 segmentation gene homologs in the Asian citrus psyllid, Diaphorina citri. Most of the genes expected to be present in D. citri based on their phylogenetic distribution in other insects were identified and annotated. Two exceptions were eagle and invected, which are present in at least some hemipterans, but were not found in D. citri. Many of the segmentation pathway genes are likely to be essential for D. citri development, and thus they may be useful targets for gene-based pest control methods.

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Buescher, Marita, Murni Tio, Guy Tear, Paul M. Overton, William J. Brook, and William Chia. "Functions of the segment polarity genes midline and H15 in Drosophila melanogaster neurogenesis." Developmental Biology 292, no. 2 (2006): 418–29. http://dx.doi.org/10.1016/j.ydbio.2006.01.016.

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Mukherjee, Ashim, S. C. Lakhotia, and J. K. Roy. "1 (2)gl gene regulates late expression of segment polarity genes in Drosophila." Mechanisms of Development 51, no. 2-3 (1995): 227–34. http://dx.doi.org/10.1016/0925-4773(95)00367-3.

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Warrior, R., and M. Levine. "Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity." Development 110, no. 3 (1990): 759–67. http://dx.doi.org/10.1242/dev.110.3.759.

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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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Epps, Janet L., Jessa B. Jones, and Soichi Tanda. "oroshigane, a New Segment Polarity Gene of Drosophila melanogaster, Functions in Hedgehog Signal Transduction." Genetics 145, no. 4 (1997): 1041–52. http://dx.doi.org/10.1093/genetics/145.4.1041.

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Here we describe a new segment polarity gene of Drosophila melanogaster, oroshigane (oro). Identified as a dominant enhancer of Bar (B), oro is also recessive embryonic lethal, and homozygous oro embryos show variable substitution of naked cuticle with denticles. These patterns are distinctly similar to those of hedgehog (hh) and wingless (wg) embryos, which indicates that oro functions in determining embryonic segment polarity. Evidence that oro function is involved in Hh signal transduction during embryogenesis is provided by its genetic interactions with the segment polarity genes patched (ptc) and fused (fu). Furthermore, ptcIN is a dominant suppressor of the oro embryonic lethal phenotype, suggesting a close and dose-dependent relationship between oro and ptc in Hh signal transduction. oro function is also required in imaginal development. The oro1 allele significantly reduces decapentaplegic (dpp), but not hh, expression in the eye imaginal disc. Furthermore, oro enhances the fu1 wing phenotype in a dominant manner. Based upon the interactions of oro with hh, ptc, and fu, we propose that the oro gene plays important roles in Hh signal transduction.

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Peifer, M., C. Rauskolb, M. Williams, B. Riggleman, and E. Wieschaus. "The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation." Development 111, no. 4 (1991): 1029–43. http://dx.doi.org/10.1242/dev.111.4.1029.

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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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Hou, Xitan, Maokai Wei, Qi Li, et al. "Transcriptome Analysis of Larval Segment Formation and Secondary Loss in the Echiuran Worm Urechis unicinctus." International Journal of Molecular Sciences 20, no. 8 (2019): 1806. http://dx.doi.org/10.3390/ijms20081806.

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The larval segment formation and secondary loss in echiurans is a special phenomenon, which is considered to be one of the important characteristics in the evolutionary relationship between the Echiura and Annelida. To better understand the molecular mechanism of this phenomenon, we revealed the larval transcriptome profile of the echiuran worm Urechis unicinctus using RNA-Seq technology. Twelve cDNA libraries of U. unicinctus larvae, late-trochophore (LT), early-segmentation larva (ES), segmentation larva (SL), and worm-shaped larva (WL) were constructed. Totally 243,381 unigenes were assembled with an average length of 1125 bp and N50 of 1836 bp, and 149,488 unigenes (61.42%) were annotated. We obtained 70,517 differentially expressed genes (DEGs) by pairwise comparison of the larval transcriptome data at different developmental stages and clustered them into 20 gene expression profiles using STEM software. Based on the typical profiles during the larval segment formation and secondary loss, eight signaling pathways were enriched, and five of which, mTOR, PI3K-AKT, TGF-β, MAPK, and Dorso-ventral axis formation signaling pathway, were proposed for the first time to be involved in the segment formation. Furthermore, we identified 119 unigenes related to the segment formation of annelids, arthropods, and chordates, in which 101 genes were identified in Drosophila and annelids. The function of most segment polarity gene homologs (hedgehog, wingless, engrailed, etc.) was conserved in echiurans, annelids, and arthropods based on their expression profiles, while the gap and pair-rule gene homologs were not. Finally, we verified that strong positive signals of Hedgehog were indeed located on the boundary of larval segments using immunofluorescence. Data in this study provide molecular evidence for the understanding of larval segment development in echiurans and may serve as a blueprint for segmented ancestors in future research.

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Akam, M. "The molecular basis for metameric pattern in the Drosophila embryo." Development 101, no. 1 (1987): 1–22. http://dx.doi.org/10.1242/dev.101.1.1.

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The metameric organization of the Drosophila embryo is generated in the first 5 h after fertilization. An initially rather simple pattern provides the foundation for subsequent development and diversification of the segmented part of the body. Many of the genes that control the formation of this pattern have been identified and at least twenty have been cloned. By combining the techniques of genetics, molecular biology and experimental embryology, it is becoming possible to unravel the role played by each of these genes. The repeating segment pattern is defined by the persistent expression of engrailed and of other genes of the ‘segment polarity’ class. The establishment of this pattern is directed by a transient molecular prepattern that is generated in the blastoderm by the activity of the ‘pair-rule’ genes. Maternal determinants at the poles of the egg coordinate this prepattern and define the anteroposterior sequence of pattern elements. The primary effect of these determinants is not known, but genes required for their production have been identified and the product of one of these, bicoid is known to be localized at the anterior of the egg. One early consequence of their activity is to define domains along the A-P axis within which a series of ‘cardinal’ genes are transcribed. The activity of the cardinal genes is required both to coordinate the process of segmentation and to define the early domains of homeotic gene expression. Further interactions between the homeotic genes and other classes of segmentation genes refine the initial establishment of segment identities.

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McNamara, Kenneth J., and Megan E. Tuura. "Evidence for segment polarity during regeneration in the Devonian asteropygine trilobite Greenops widderensis." Journal of Paleontology 85, no. 1 (2011): 106–10. http://dx.doi.org/10.1666/10-049.1.

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A complete molted exoskeleton of the asteropygine phacopid trilobite Greenops widderensis Lieberman and Kloc, 1997 from the Middle Devonian (Givetian) Widder Formation in southwestern Ontario, Canada that has suffered predatory trauma provides insights into the sequence of regeneration of segments. The molt configuration is such that it is possible to interpret the molting technique used by the trilobite. Predatory trauma affected four areas of the exoskeleton. The pygidium shows loss of the spinose margin on one side and damage to a single spine on the other; one genal spine has been broken and partially regrown; and the posterior of the glabella has been removed. It is thought that the first three traumas occurred during life, as these areas affected show signs of exoskeletal regeneration. The fourth trauma probably occurred to the exuvium. Analysis of the degree of regeneration of the pygidial pleurae indicates that there was an anteroposterior polarity to the regeneration. Other examples in the literature suggest that this regeneration polarity pattern may have been widespread in trilobites. It is suggested that, as in modern arthropods and annelids, this sequential regeneration was under the control of segmentation polarity genes.

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Fietz, Michael J., Jean-Paul Concordet, Robert Barbosa, et al. "The hedgehog gene family in Drosophila and vertebrate development." Development 1994, Supplement (1994): 43–51. http://dx.doi.org/10.1242/dev.1994.supplement.43.

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The segment polarity gene hedgehog plays a central role in cell patterning during embryonic and post-embryonic development of the dipteran, Drosophila melanogaster. Recent studies have identified a family of hedgehog related genes in vertebrates; one of these, Sonic hedgehog is implicated in positional signalling processes that show interesting similarities with those controlled by its Drosophila homologue.

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van den Heuvel, M., C. Harryman-Samos, J. Klingensmith, N. Perrimon, and R. Nusse. "Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein." EMBO Journal 12, no. 13 (1993): 5293–302. http://dx.doi.org/10.1002/j.1460-2075.1993.tb06225.x.

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Ingham, P. W., N. E. Baker, and A. Martinez-Arias. "Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped." Nature 331, no. 6151 (1988): 73–75. http://dx.doi.org/10.1038/331073a0.

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Orenic, Teresa, Jennifer Chidsey, and Robert Holmgren. "Cell and cubitus interruptus Dominant: Two segment polarity genes on the fourth chromosome in Drosophila." Developmental Biology 124, no. 1 (1987): 50–56. http://dx.doi.org/10.1016/0012-1606(87)90458-1.

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Gutjahr, T., E. Frei, and M. Noll. "Complex regulation of early paired expression: initial activation by gap genes and pattern modulation by pair-rule genes." Development 117, no. 2 (1993): 609–23. http://dx.doi.org/10.1242/dev.117.2.609.

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The paired gene is one of approximately 30 zygotic segmentation genes responsible for establishing the segmented body plan of Drosophila melanogaster. To gain insight into the mechanism by which the paired gene is expressed in a complex temporal and spatial pattern, we have examined paired protein expression in wild-type and mutant embryos. In wild-type embryos, paired protein is expressed in several phases. Initial expression in broad domains evolves into a pair-rule pattern of eight stripes during cellularization. Subsequently, a segment-polarity-like pattern of fourteen stripes emerges. Later, at mid-embryogenesis, paired is expressed in specific regions of the head and in specific cells of the central nervous system. Analysis of the initial paired expression in the primary pair-rule mutants even-skipped, runt and hairy, and in all gap mutants suggests that the products of the gap genes hunchback, Kruppel, knirps and giant activate paired expression in stripes. With the exception of stripe 1, which is activated by even-skipped, and stripe 8, which depends upon runt, the primary pair-rule proteins are required for subsequent modulation rather than activation of the paired stripes. The factors activating paired expression in the pair-rule mode appear to interact with those activating it along the dorsoventral axis.

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Heitzler, P., D. Coulson, M. T. Saenz-Robles, et al. "Genetic and cytogenetic analysis of the 43A-E region containing the segment polarity gene costa and the cellular polarity genes prickle and spiny-legs in Drosophila melanogaster." Genetics 135, no. 1 (1993): 105–15. http://dx.doi.org/10.1093/genetics/135.1.105.

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Abstract A cytogenetic analysis of the 43A-E region of chromosome 2 in Drosophila melanogaster is presented. Within this interval 27 complementation groups have been identified by extensive F2 screens and ordered by deletion mapping. The region includes the cellular polarity genes prickle and spiny-legs, the segmentation genes costa and torso, the morphogenetic locus sine oculis and is bounded on its distal side by the eye-color gene cinnabar. In addition 19 novel lethal complementation groups and two semi-lethal complementation groups with morphogenetic escaper phenotypes are described.

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Struhl, G., D. A. Barbash, and P. A. Lawrence. "Hedgehog organises the pattern and polarity of epidermal cells in the Drosophila abdomen." Development 124, no. 11 (1997): 2143–54. http://dx.doi.org/10.1242/dev.124.11.2143.

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The abdomen of adult Drosophila, like that of other insects, is formed by a continuous epithelium spanning several segments. Each segment is subdivided into an anterior (A) and posterior (P) compartment, distinguished by activity of the selector gene engrailed (en) in P but not A compartment cells. Here we provide evidence that Hedgehog (Hh), a protein secreted by P compartment cells, spreads into each A compartment across the anterior and the posterior boundaries to form opposing concentration gradients that organize cell pattern and polarity. We find that anteriorly and posteriorly situated cells within the A compartment respond in distinct ways to Hh: they express different combinations of genes and form different cell types. They also form polarised structures that, in the anterior part, point down the Hh gradient and, in the posterior part, point up the gradient - therefore all structures point posteriorly. Finally, we show that ectopic Hh can induce cells in the middle of each A compartment to activate en. Where this happens, A compartment cells are transformed into an ectopic P compartment and reorganise pattern and polarity both within and around the transformed tissue. Many of these results are unexpected and lead us to reassess the role of gradients and compartments in patterning insect segments.

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Hepker, J., Q. T. Wang, C. K. Motzny, R. Holmgren, and T. V. Orenic. "Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes." Development 124, no. 2 (1997): 549–58. http://dx.doi.org/10.1242/dev.124.2.549.

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The Drosophila segment polarity gene cubitus interruptus (ci) encodes a zinc finger protein that is required for the proper patterning of segments and imaginal discs. Epistasis analysis indicates that ci functions in the Hedgehog (Hh) signal transduction pathway and is required to maintain wingless expression in the embryo. In this paper, the role of the Ci protein in the Hh signaling pathway is examined in more detail. Our results show that ectopic expression of ci in imaginal discs and the embryo activates the expression of Hh target genes. One of these target genes, patched, forms a negative feedback loop with ci that is regulated by Hh signal transduction. Activation is also achieved using the Ci zinc finger domain fused to a heterologous transactivation domain. Conversely, repression of Hh target genes occurs in animals expressing the Ci zinc finger domain fused to a repression domain. To examine Ci function in more detail, regions of the Ci protein that are responsible for its ability to transactivate and its subcellular distribution have been identified.

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Eggleston, W. B., M. Alleman, and J. L. Kermicle. "Molecular organization and germinal instability of R-stippled maize." Genetics 141, no. 1 (1995): 347–60. http://dx.doi.org/10.1093/genetics/141.1.347.

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Abstract The spotted seed allele R-stippled (R-st) is comprised of the following genetic components: strong seed color (Sc), inhibitor-of-R (I-R) and near-colorless seed (Nc). I-R is a mobile element that represses (Sc) expression irregularly. Germinal I-R losses produce progeny with fully colored seed. Southern blot analysis revealed four r-hybridizing segments in R-st and three, two or one in two sets of unequal crossover deletion products. By comparison to published reports of r gene structure, we maintain that each segment contains at least one r gene. The proximal r gene, Sc, confers strong seed color; the three distal r genes together produce near-colorless seed. R-st's seed spotting phenotype is correlated with the presence of a 3.3-kb insert in Sc identified as I-R. The level of the near-colorless phenotype is inversely correlated with the number of r genes present, suggesting involvement of a multiple copy silencing mechanism in their regulation. Phenotypic changes in R-st occurred primarily by unequal exchange between r genes. The locations of exchange positions showed a strong polarity, nearly all occurring in the 3' portions of the identified r genes.

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Franke, Franziska Anni, and Georg Mayer. "Controversies Surrounding Segments and Parasegments in Onychophora: Insights from the Expression Patterns of Four “Segment Polarity Genes” in the Peripatopsid Euperipatoides rowelli." PLoS ONE 9, no. 12 (2014): e114383. http://dx.doi.org/10.1371/journal.pone.0114383.

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Ciechanska, Ewa, David A. Dansereau, Pia C. Svendsen, Tim R. Heslip, and William J. Brook. "dAP-2 and defective proventriculus regulate Serrate and Delta expression in the tarsus of Drosophila melanogaster." Genome 50, no. 8 (2007): 693–705. http://dx.doi.org/10.1139/g07-043.

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The segmentation of the proximal–distal axis of the Drosophila melanogaster leg depends on the localized activation of the Notch receptor. The expression of the Notch ligand genes Serrate and Delta in concentric, segmental rings results in the localized activation of Notch, which induces joint formation and is required for the growth of leg segments. We report here that the expression of Serrate and Delta in the leg is regulated by the transcription factor genes dAP-2 and defective proventriculus. Previous studies have shown that Notch activation induces dAP-2 in cells distal and adjacent to the Serrate/Delta domain of expression. We find that Serrate and Delta are ectopically expressed in dAP-2 mutant legs and that Serrate and Delta are repressed by ectopic expression of dAP-2. Furthermore, Serrate is induced cell-autonomously in dAP-2 mutant clones in many regions of the leg. We also find that the expression of a defective proventriculus reporter overlaps with dAP-2 expression and is complementary to Serrate expression in the tarsal segments. Ectopic expression of defective proventriculus is sufficient to block joint formation and Serrate and Delta expression. Loss of defective proventriculus results in localized, ectopic Serrate expression and the formation of ectopic joints with reversed polarity. Thus, in tarsal segments, dAP-2 and defective proventriculus are necessary for the correct proximal and distal boundaries of Serrate expression and repression of Serrate by defective proventriculus contributes to tarsal segment asymmetry. The repression of the Notch ligand genes Serrate and Delta by the Notch target gene dAP-2 may be a pattern-refining mechanism similar to those acting in embryonic segmentation and compartment boundary formation.

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Castelli-Gair, J. "The lines gene of Drosophila is required for specific functions of the Abdominal-B HOX protein." Development 125, no. 7 (1998): 1269–74. http://dx.doi.org/10.1242/dev.125.7.1269.

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The Hox genes encode homeobox transcription factors that control the formation of segment specific structures in the anterior-posterior axis. HOX proteins regulate the transcription of downstream targets acting both as repressors and as activators. Due to the similarity of their homeoboxes it is likely that much of the specificity of HOX proteins is determined by interaction with transcriptional cofactors, but few HOX cofactor proteins have yet been described. Here I present genetic evidence showing that lines, a segment polarity gene of Drosophila, is required for the function of the Abdominal-B protein. In lines mutant embryos Abdominal-B protein expression is normal but incapable of promoting its normal functions: formation of the posterior spiracles and specification of an eighth abdominal denticle belt. These defects arise because in lines mutant embryos the Abdominal-B protein cannot activate its direct target empty spiracles or other downstream genes while it can function as a repressor of Ultrabithorax and abdominal-A. The lines gene seems to be required exclusively for Abdominal-B but not for the function of other Hox genes.

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Simcox, A. A., I. J. H. Roberts, E. Hersperger, M. C. Gribbin, A. Shearn, and J. R. S. Whittle. "Imaginal discs can be recovered from cultured embryos mutant for the segment-polarity genes engrailed, naked and patched but not from wingless." Development 107, no. 4 (1989): 715–22. http://dx.doi.org/10.1242/dev.107.4.715.

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Drosophila embryos homozygous for strong mutations in each of the segment-polarity genes wingless (wg), engrailed (en), naked (nkd) and patched (ptc) form a larval cuticle in which there is a deletion in every segment. The mutant embryos normally fail to hatch but by in vivo culture we were able to show which could produce adult structures. Cultured wg- embryos did not produce any adult structures. Cultured en- embryos produced eye-antennal derivatives and rarely produced partial thoracic structures. nkd- and ptc- embryos produced eye-antennal and thoracic derivatives. The nkd- and ptc- thoracic imaginal discs developed with an abnormal morphology and abnormal pattern of en- expression. Our findings are consistent with the idea that the thoracic imaginal discs derive from two adjacent groups of cells that express wg and en respectively in the embryo.

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