Early <i>Distal‐less</i> expression in a developing crustacean limb bud becomes restricted to setal‐forming cells

Williams, Terri A.

doi:10.1111/j.1525-142x.2007.00218.x

Cited by 6 publications

(3 citation statements)

References 32 publications

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“…Thus, regulation of sclerotization, in particular the sclerotization associated with forming points of articulation and bending, may have been the evolutionarily earlier function of dac in the leg allowing it then to be co-opted for patterning. This is similar to Dll, another leg gap gene, since it has a late role in patterning sensory and setal structures (Panganiban 2000;Williams et al 2002;Williams 2008), which ancestrally would occur naturally on outgrowths from the body wall.…”

Section: Late Dac Expressionmentioning

confidence: 92%

Evidence for a novel role for dachshund in patterning the proximal arthropod leg

et al. 2008

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The branchiopod crustacean Triops longicaudatus has paddlelike thoracic appendages with few joints and multiple marginal lobes. Here, we explore the degree to which the Triops limb is patterned by the same network of genes known to pattern the uniramous, multi-jointed insect appendage. Insect leg patterning proceeds through a process of subdividing the leg into proximal, intermediate, and distal regions by the activity of the transcription factors hth/exd, dac, and Dll. The immature Triops limb is subdivided into large, discrete regional domains (proximal and distal) as defined by nuclear-EXD and DLL. We show that HTH expression in Triops overlaps cell-to-cell with n-EXD expression. In addition, dac is expressed in two domains: (1) adjacent to and partially overlapping the distal Dll domain and (2) along the medial margin of the developing leg. The DAC domain adjacent to the distal Dll domain supports the early establishment of the expected intermediate domain of DAC expression. The medial expression domain resolves over time into a series of reiterated stripes located on the lower side of each medial lobe. Later, this expression pattern correlates with the sclerotized regions associated with limb flexion. We propose that these stripes of DAC expression play a role in forming reiterated medial lobes. Unlike Drosophila, where the proximal distal patterning of the leg is coincident with patterning of reiterated structures (segments), we hypothesize that the patterning in Triops may reflect an ancestral state where the patterning of reiterated medial structures was not coincident with proximodistal limb patterning.

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Section: Late Dac Expressionmentioning

confidence: 92%

Evidence for a novel role for dachshund in patterning the proximal arthropod leg

et al. 2008

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“…It is also possible that the legs of the anterior three trunk segments exhibit only proximal identity. In arthropods, even on the proximalmost podomeres of developing ventral appendages, Dll plays a role in regulating the position of sensory outgrowths after PD axes have been established [78,79]. Therefore, broad expression of He-Dll in H. exemplaris legs is not necessarily indicative of distal identity.…”

Section: (C) the Evolution Of Proximodistal Axes In Tardigradamentioning

confidence: 99%

Loss of intermediate regions of perpendicular body axes contributed to miniaturization of tardigrades

Game

Smith

2020

Proc. R. Soc. B.

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Tardigrades have a miniaturized body plan. Miniaturization in tardigrades is associated with the loss of several organ systems and an intermediate region of their anteroposterior (AP) axis. However, how miniaturization has affected tardigrade legs is unclear. In arthropods and in onychophorans, the leg gap genes are expressed in regionalized proximodistal (PD) patterns in the legs. Functional studies indicate that these genes regulate growth in their respective expression domains and establish PD identities, partly through mutually antagonistic regulatory interactions. Here, we investigated the expression patterns of tardigrade orthologs of the leg gap genes. Rather than being restricted to a proximal leg region, as in arthropods and onychophorans, we detected coexpression of orthologues of homothorax and extradenticle broadly across the legs of the first three trunk segments in the tardigrade Hypsibius exemplaris . We could not identify a dachshund orthologue in tardigrade genomes, a gene that is expressed in an intermediate region of developing legs in arthropods and onychophorans, suggesting that this gene was lost in the tardigrade lineage. We detected Distal-less expression broadly across all developing leg buds in H. exemplaris embryos, unlike in arthropods and onychophorans, in which it exhibits a distally restricted expression domain. The broad expression patterns of the remaining leg gap genes in H. exemplaris legs may reflect the loss of dachshund and the accompanying loss of an intermediate region of the legs in the tardigrade lineage. We propose that the loss of intermediate regions of both the AP and PD body axes contributed to miniaturization of Tardigrada.

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“…The recent move towards integrating the fields of evolutionary and developmental biology (e.g. Averof and Akam 1995 ; Gilbert et al 1996 ; Akam 1998a ; Hughes and Kaufman 2000 ; Harzsch and Hafner 2006 ; Harzsch 2007 ) has fostered a surge of studies on Crustacean limb development which examined the expression and function of genes such as Distal-less (Panganiban et al 1995 ; Popadic et al 1996 , 1998 ; Scholtz et al 1998 ; Williams 1998 , 2008 ; Williams et al 2002 ), Ultrabithorax and AbdominalA (Averof and Akam 1995 ; Averof and Patel 1997 ), Extradenticle (Gonzáles-Crespo and Morata 1996 ; Abzhanov and Kaufmann 2000 ), Pdm and Apterous (Averof and Cohen 1997 ), Sex combs reduced (Abzhanov and Kaufman 1999 ), and Wingless (Nulsen and Nagy 1999 ) in various Crustacean taxa with uniramous, biramous or phyllopodous branched limbs. Interestingly, some of these studies failed to establish homologies between the function of these genes during development of the complex Crustacean limbs as compared to the uniramous limbs of Insecta (Williams and Nagy 1995 , 1996 ; Averof and Patel 1997 ; Williams et al 2002 ; Williams 2004 ) but instead established new hypotheses on the evolution of hox gene function (Averof et al 1996 ; Akam 1998b ).…”

Section: Introductionmentioning

confidence: 99%

Muscle precursor cells in the developing limbs of two isopods (Crustacea, Peracarida): an immunohistochemical study using a novel monoclonal antibody against myosin heavy chain

2008

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In the hot debate on arthropod relationships, Crustaceans and the morphology of their appendages play a pivotal role. To gain new insights into how arthropod appendages evolved, developmental biologists recently have begun to examine the expression and function of Drosophila appendage genes in Crustaceans. However, cellular aspects of Crustacean limb development such as myogenesis are poorly understood in Crustaceans so that the interpretative context in which to analyse gene functions is still fragmentary. The goal of the present project was to analyse muscle development in Crustacean appendages, and to that end, monoclonal antibodies against arthropod muscle proteins were generated. One of these antibodies recognises certain isoforms of myosin heavy chain and strongly binds to muscle precursor cells in malacostracan Crustacea. We used this antibody to study myogenesis in two isopods, Porcellio scaber and Idotea balthica (Crustacea, Malacostraca, Peracarida), by immunohistochemistry. In these animals, muscles in the limbs originate from single muscle precursor cells, which subsequently grow to form multinucleated muscle precursors. The pattern of primordial muscles in the thoracic limbs was mapped, and results compared to muscle development in other Crustaceans and in insects.

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Early Distal‐less expression in a developing crustacean limb bud becomes restricted to setal‐forming cells

Cited by 6 publications

References 32 publications

Evidence for a novel role for dachshund in patterning the proximal arthropod leg

Evidence for a novel role for dachshund in patterning the proximal arthropod leg

Loss of intermediate regions of perpendicular body axes contributed to miniaturization of tardigrades

Muscle precursor cells in the developing limbs of two isopods (Crustacea, Peracarida): an immunohistochemical study using a novel monoclonal antibody against myosin heavy chain

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