Hexapoda: A Drosophila’s View of Development

Hartenstein, Volker; Chipman, Ariel D.

doi:10.1007/978-3-7091-1868-9_1

Cited by 12 publications

(28 citation statements)

References 257 publications

(224 reference statements)

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“…The early development of the visceral muscle of the insect model system Drosophila has been analyzed in considerable detail (Bate, 1993; Azpiazu and Frasch, 1993; Maggert et al, 1995; Lee et al, 2003; reviewed in Hartenstein and Chipman, 2016). Visceral muscle is derived from the lateral part of the mesoderm, the so-called visceral mesoderm, which attaches to the developing gut tube during mid stages of embryogenesis, very similar to the formation of the splanchnopleura that gives rise to the visceral muscle in vertebrates (Tribioli et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

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Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

Aghajanian

Takashima

Paul

et al. 2016

Developmental Biology

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The visceral musculature of the Drosophila intestine plays important roles in digestion as well as development. Detailed studies investigating the embryonic development of the visceral muscle exist; comparatively little is known about postembryonic development and metamorphosis of this tissue. In this study we have combined the use of specific markers with electron microscopy to follow the formation of the adult visceral musculature and its involvement in gut development during metamorphosis. Unlike the adult somatic musculature, which is derived from a pool of undifferentiated myoblasts, the visceral musculature of the adult is a direct descendant of the larval fibers, as shown by activating a lineage tracing construct in the larval muscle and obtaining labeled visceral fibers in the adult. However, visceral muscles undergo a phase of remodeling that coincides with the metamorphosis of the intestinal epithelium. During the first day following puparium formation, both circular and longitudinal syncytial fibers dedifferentiate, losing their myofibrils and extracellular matrix, and dissociating into mononuclear cells (“secondary myoblasts”). Towards the end of the second day, this process is reversed, and between 48 and 72h after puparium formation, a structurally fully differentiated adult muscle layer has formed. We could not obtain evidence that cells apart from the dedifferentiated larval visceral muscle contributed to the adult muscle, nor does it appear that the number of adult fibers (or nuclei per fiber) is increased over that of the larva by proliferation. In contrast to the musculature, the intestinal epithelium is completely renewed during metamorphosis. The adult midgut epithelium rapidly expands over the larval layer during the first few hours after puparium formation; in case of the hindgut, replacement takes longer, and proceeds by the gradual caudad extension of a proliferating growth zone, the hindgut proliferation zone (HPZ). The subsequent elongation of the hindgut and midgut, as well as the establishment of a population of intestinal stem cells active in the adult midgut and hindgut, requires the presence of the visceral muscle layer, based on the finding that ablation of this layer causes a severe disruption of both processes.

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Section: Introductionmentioning

confidence: 99%

“…During metamorphosis, the larval gut is replaced by an adult gut. The epithelium of the foregut, midgut, ureter and hindgut forms from undifferentiated, proliferatory progenitor cells (reviewed in Hartenstein and Chipman, 2016; Fig. 1A).…”

Section: Introductionmentioning

confidence: 99%

Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

Aghajanian

Takashima

Paul

et al. 2016

Developmental Biology

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“…In D. melanogaster, forkhead ( fkh), wingless (wg) and hedgehog (hh) are expressed during stomodeum and proctodeum formation (Figure , reviewed in Hartenstein & Chipman, ), therefore, we cloned and analyzed the expression of their respective orthologs in the spider P. tepidariorum .…”

Section: Resultsmentioning

confidence: 99%

Molecular control of gut formation in the spider Parasteatoda tepidariorum

Feitosa

Pechmann

Schwager

et al. 2017

Genesis

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The development of a digestive system is an essential feature of bilaterians. Studies of the molecular control of gut formation in arthropods have been studied in detail in the fruit fly Drosophila melanogaster. However, little is known in other arthropods, especially in noninsect arthropods. To better understand the evolution of arthropod alimentary system, we investigate the molecular control of gut development in the spider Parasteatoda tepidariorum (Pt), the primary chelicerate model species for developmental studies. Orthologs of the ectodermal genes Pt-wingless (Pt-wg) and Pt-hedgehog (Pt-hh), of the endodermal genes, Pt-serpent (Pt-srp) and Pt-hepatocyte-nuclear factor-4 (Pt-hnf4) and of the mesodermal gene Pt-twist (Pt-twi) are expressed in the same germ layers during spider gut development as in D. melanogaster. Thus, our expression data suggest that the downstream molecular components involved in gut development in arthropods are conserved. However, Pt-forkhead (Pt-fkh) expression and function in spiders is considerably different from its D. melanogaster ortholog. Pt-fkh is expressed before gastrulation in a cell population that gives rise to endodermal and mesodermal precursors, suggesting a possible role for this factor in specification of both germ layers. To test this hypothesis, we knocked down Pt-fkh via RNA interference. Pt-fkh RNAi embryos not only fail to develop a proper gut, but also lack the mesodermal Pt-twi expressing cells. Thus, in spiders Pt-fkh specifies endodermal and mesodermal germ layers. We discuss the implications of these findings for the evolution and development of gut formation in Ecdysozoans.

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“…Axis determination in insects has been extensively studied in one of main models in biology, the fruit fly Drosophila melanogaster (Hartenstein and Chipman, ). However, work on other insects and arthropods indicates many developmental properties of Drosophila are not representative (Peel et al, ), and this is especially true for early processes such as axis formation.…”

Section: Introductionmentioning

confidence: 99%

“…For example, the morphogen bicoid , an important anterior maternal determinant in Drosophila , apparently has no orthologs outside the cyclorhaphan flies (Stauber et al, ). Notably, the A‐P and D‐V axes in Drosophila are distinct and are determined through different pathways (Hartenstein and Chipman, ). There is evidence to suggest that this distinction is not so clear in other insects (Berni et al, ; da Fonseca et al, ; Sachs et al, ; Wilson and Dearden, ).…”

Section: Introductionmentioning

confidence: 99%

Factors involved in early polarization of the anterior‐posterior axis in the milkweed bug Oncopeltus fasciatus

Ginzburg

Cohen

Chipman

2017

Genesis

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The axes of insect embryos are defined early in the blastoderm stage. Genes involved in this polarization are well known in Drosophila, but less so in other insects, such as the milkweed bug Oncopeltus fasciatus. Using quantitative PCR, we looked at differential expression of several candidate genes for early anterior-posterior patterning and found that none of them are expressed asymmetrically in the early blastoderm. We then used an RNA-Seq approach to identify novel candidate genes that might be involved in early polarization in Oncopeltus. We focused on transcription factors (TFs) as these are likely to be central players in developmental processes. Using both homology and domain based identification approaches, we were unable to find any TF encoding transcripts that are expressed asymmetrically along the anterior-posterior axis at early stages. Using a GO-term analysis of all asymmetrically expressed mRNAs, we found an enrichment of genes relating to mitochondrial function in the posterior at the earliest studied time-point. We also found a gradual enrichment of transcription related activities, giving us a putative time frame for the maternal to zygotic transition. Our dataset provides us with a list of new candidate genes in early development, which can be followed up experimentally.

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Hexapoda: A Drosophila’s View of Development

Cited by 12 publications

References 257 publications

Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

Molecular control of gut formation in the spider Parasteatoda tepidariorum

Factors involved in early polarization of the anterior‐posterior axis in the milkweed bug Oncopeltus fasciatus

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