Making stripes in the Drosophila embryo

doi:10.1016/0168-9525(90)90234-W

Trends in Genetics

Volume 6, 1990, Pages 287-292

https://doi.org/10.1016/0168-9525(90)90234-W Get rights and content

Abstract

The striped pattern of expression of the Drosophila primary pair rule genes is controlled by independent regulatory units that give rise to individual stripes. The different stripes seem to respond in a concentration-dependent manner to the different combinations of maternal and gap protein gradients found along the anterior-posterior axis of the early embryo. Thus, the initial periodicity appears to be generated by putting together a series of nonperiodic events.

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Drosophila melanogaster displays the complete metamorphosis process and the life cycle includes an egg, larval form, pupa, and adult fly. During the early development, different cascades of genes are activated which establish the anterior-posterior (A-P) and dorsal-ventral (D-V) patterning in the fly embryo. Maternal effect genes and zygotic genes play an essential role in this. The A-P patterning is established by maternal effect genes and zygotic genes which include gap genes, pair rule genes, segment polarity genes, and homeotic selector genes. The nuclear gradient of dorsal protein plays an important role in the D-V patterning and determining the cell fate to form the three germ layers.
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Future studies need to evaluate how the type I Bmprs differentially regulate the ability of the R-Smads to turn on the specific genes involved the assumption of specific dorsal cell fates. A curious, and mechanistically unresolved, feature of patterning along the dorsal spinal cord is the apparently discontinuous specification of dorsal IN identity, akin the expression of pair rule genes in the specification of segments in the Drosophila embryo (Pankratz & Jäckle, 1990). This finding was first reported by Elisa Martí and co-workers when they reported that BMP7 signaling is required for the generation of dI1, dI3 and dI5 subpopulations (Le Dreau et al., 2012).
Distinct classes of neurons arise at different positions along the dorsal-ventral axis of the spinal cord leading to spinal neurons being segregated along this axis according to their physiological properties and functions. Thus, the neurons associated with motor control are generally located in, or adjacent to, the ventral horn whereas the interneurons (INs) that mediate sensory activities are present within the dorsal horn. Here, we review classic and recent studies examining the developmental mechanisms that establish the dorsal-ventral axis in the embryonic spinal cord. Intriguingly, while the cellular organization of the dorsal and ventral halves of the spinal cord looks superficially similar during early development, the underlying molecular mechanisms that establish dorsal vs ventral patterning are markedly distinct. For example, the ventral spinal cord is patterned by the actions of a single growth factor, sonic hedgehog (Shh) acting as a morphogen, i.e., concentration-dependent signal. Recent studies have shed light on the mechanisms by which the spatial and temporal gradient of Shh is transduced by cells to elicit the generation of different classes of ventral INs, and motor neurons (MNs). In contrast, the dorsal spinal cord is patterned by the action of multiple factors, most notably by members of the bone morphogenetic protein (BMP) and Wnt families. While less is known about dorsal patterning, recent studies have suggested that the BMPs do not act as morphogens to specify dorsal IN identities as previously proposed, rather each BMP has signal-specific activities. Finally, we consider the promise that elucidation of these mechanisms holds for neural repair.
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A pair-rule oscillator could co-opt different transcription factors in evolution; perhaps an ancestral pair-rule oscillator could be driven by a different triad of pair-rule genes. In Drosophila, the primary pair-rule genes are eve, hairy and runt (Pankratz and Jäckle, 1990). Hairy is also a target of Notch signaling later in development and in other species (reviewed in Andersson et al., 2011).
Virtually all arthropods all arthropods add their body segments sequentially, one by one in an anterior to posterior progression. That process requires not only segment specification but typically growth and elongation. Here we review the functions of some of the key genes that regulate segmentation: Wnt, caudal, Notch pathway, and pair-rule genes, and discuss what can be inferred about their evolution. We focus on how these regulatory factors are integrated with growth and elongation and discuss the importance and challenges of baseline measures of growth and elongation. We emphasize a perspective that integrates the genetic regulation of segment patterning with the cellular mechanisms of growth and elongation.
The boundary paradox in the Bithorax complex
2015, Mechanisms of Development
The parasegment-specific expression of the three Drosophila Bithorax complex homeotic genes is orchestrated by nine functionally autonomous regulatory domains. Functional autonomy depends upon special elements called boundaries or insulators that are located between each domain. The boundaries ensure the independent activity of each domain by blocking adventitious interactions with initiators, enhancers and silencers in the neighboring domains. However, this blocking activity poses a regulatory paradox — the Bithorax boundaries are also able to insulate promoters from regulatory interactions with enhancers and silencers and six of the nine Bithorax regulatory domains are separated from their target genes by at least one boundary element. Here we consider several mechanisms that have been suggested for how the Bithorax regulatory domains are able to bypass intervening boundary elements and direct the appropriate parasegment-specific temporal and spatial expression of their target gene.
Deciphering the onychophoran 'segmentation gene cascade': Gene expression reveals limited involvement of pair rule gene orthologs in segmentation, but a highly conserved segment polarity gene network
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The accumulated data suggest, however, a high degree of conservation on the level of SPGs (and associated factors) in arthropods. Comprehensive data on PRG expression are available from insects, myriapods and chelicerates (Pankratz and Jäckle, 1990; Chipman et al., 2004; Damen et al., 2000, 2005; Choe et al., 2006; Chipman and Akam, 2008; Choe and Brown, 2007, 2009; Janssen et al., 2011, 2012), but again data on crustaceans are scarce (Copf et al., 2003; Davis et al., 2005). These data suggest that at least some of the PRGs are involved in segmentation in these species, and thus that PRGs are generally involved in arthropod segmentation.
The hallmark of the arthropods is their segmented body, although origin of segmentation, however, is unresolved. In order to shed light on the origin of segmentation we investigated orthologs of pair rule genes (PRGs) and segment polarity genes (SPGs) in a member of the closest related sister-group to the arthropods, the onychophorans. Our gene expression data analysis suggests that most of the onychophoran PRGs do not play a role in segmentation. One possible exception is the even-skipped (eve) gene that is expressed in the posterior end of the onychophoran where new segments are likely patterned, and is also expressed in segmentation-gene typical transverse stripes in at least a number of newly formed segments. Other onychophoran PRGs such as runt (run), hairy/Hes (h/Hes) and odd-skipped (odd) do not appear to have a function in segmentation at all. Onychophoran PRGs that act low in the segmentation gene cascade in insects, however, are potentially involved in segment-patterning. Most obvious is that from the expression of the pairberry (pby) gene ortholog that is expressed in a typical SPG-pattern. Since this result suggested possible conservation of the SPG-network we further investigated SPGs (and associated factors) such as Notum in the onychophoran. We find that the expression patterns of SPGs in arthropods and the onychophoran are highly conserved, suggesting a conserved SPG-network in these two clades, and indeed also in an annelid. This may suggest that the common ancestor of lophotrochozoans and ecdysozoans was already segmented utilising the same SPG-network, or that the SPG-network was recruited independently in annelids and onychophorans/arthropods.
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Also in Oncopeltus the knockdown of the ortholog of the pair rule gene even-skipped affects gnathal and trunk segments in a similar way although not by pair rule function (Liu and Kaufman, 2005). Hox genes are required for gnathal identity specification the same way as in the trunk, as shown by functional work in Drosophila, Tribolium, Oncopeltus and the cockroach Periplaneta americana (Angelini et al., 2005; Brown et al., 2000, 2002; Chesebro et al., 2009; DeCamillis and ffrench-Constant, 2003; DeCamillis et al., 2001; Hrycaj et al., 2010; Hughes and Kaufman, 2000; Pankratz and Jackle, 1990; Rogers et al., 2002; Shippy et al., 2006). Based on differences seen in the expression of developmental genes it becomes obvious that patterning of the procephalon must differ from trunk patterning.
Many questions regarding evolution and ontogeny of the insect head remain open. Likewise, the genetic basis of insect head development is poorly understood. Recently, the investigation of gene expression data and the analysis of patterning gene function have revived interest in insect head development. Here, we argue that the red flour beetle Tribolium castaneum is a well suited model organism to spearhead research with respect to the genetic control of insect head development. We review recent molecular data and discuss its bearing on early development and morphogenesis of the head. We present a novel hypothesis on the ontogenetic origin of insect head sutures and review recent insights into the question on the origin of the labrum. Further, we argue that the study of developmental genes may identify the elusive anterior non-segmental region and present some evidence in favor of its existence. With respect to the question of evolution of patterning we show that the head Anlagen of the fruit fly Drosophila melanogaster and Tribolium differ considerably and we review profound differences of their genetic regulation. Finally, we discuss which insect model species might help us to answer the open questions concerning the genetic regulation of head development and its evolution.

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Trends in Genetics

ReviewMaking stripes in the Drosophila embryo

Abstract

Cell

Trends Genet.

Cell

Cell

Cell

Cell

Cell

Cell

Am. Zool.

Nature

Roux's Arch. Dev. Biol.

Roux's Arch. Dev. Biol.

Roux's Arch. Dev. Biol.

Verb. Dtsch. Zool. Ges.

Development

Nature

Development

Review
Making stripes in the Drosophila embryo