Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum

Suzuki, Yuichiro; Squires, Diego C.; Riddiford, Lynn M.

doi:10.1016/j.ydbio.2008.10.022

Cited by 36 publications

(52 citation statements)

References 33 publications

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“…The metamorphic expression of leg gap genes has been examined in the moth Manduca (Tanaka and Truman 2007 ), which develops its adult appendages from discrete primordia in the embryonic legs, and in the beetle Tribolium (Suzuki et al 2009 ), which has greater continuity between larval and adult appendages. Gene expression patterns refl ect these differences in metamorphic patterning.…”

Section: Leg Gap Genes At Metamorphosismentioning

confidence: 99%

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

Jockusch

Smith

2015

Evolutionary Developmental Biology of Invertebrates 5

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Section: Leg Gap Genes At Metamorphosismentioning

confidence: 99%

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

Jockusch

Smith

2015

Evolutionary Developmental Biology of Invertebrates 5

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“…The embryonic and metamorphic functions of Dll in T. castaneum are also similar: the gene is required for the development of distal structures at both stages, and during embryogenesis Dll is expressed throughout the developing palps (Beermann et al 2001). Interestingly, removal of T. castaneum Dll expression earlier during larval life led to delayed metamorphosis, as well as changes in appendage morphology (Suzuki et al 2009). Many insects delay molting after appendage loss to allow time for regeneration, and this dual role of Dll suggests a mechanism linking these processes (Suzuki et al 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, removal of T. castaneum Dll expression earlier during larval life led to delayed metamorphosis, as well as changes in appendage morphology (Suzuki et al 2009). Many insects delay molting after appendage loss to allow time for regeneration, and this dual role of Dll suggests a mechanism linking these processes (Suzuki et al 2009). …”

Section: Discussionmentioning

confidence: 99%

“…dachshund: dachshund is homologous to the human Ski/Sno transcription factor (Caubit et al 1999), and its expression intercalates between the hth and Dll domains where it is required for development of an intermediate leg region in T. castaneum (Suzuki et al 2009;Angelini et al 2012) and D. melanogaster (Lecuit and Cohen 1997; Abu-Shaar and Mann 1998). Although not expressed in the maxillary or labial primordia of D. melanogaster (Abzhanov et al 2001;Joulia et al 2006), dac is expressed in all three mouthparts in T. castaneum embryos (Prpic et al 2001).…”

Section: Maxillae and Labiummentioning

confidence: 99%

“…Distal-less: Distal-less is the third classical leg gap gene, required for development of distal regions of the leg in T. castaneum (Beermann et al 2001;Suzuki et al 2009;Angelini et al 2012) and D. melanogaster (Cohen and Jürgens 1989), as well as distal appendage regions of other species (reviewed by Angelini and Kaufman 2005b). In T. castaneum, depletion of Dll led to distal truncations of the palps, with only a small proximal nub remaining in the most severely affected labial palps, and a single, unjointed segment in the maxillary palps ( Figure 4F).…”

Section: Maxillae and Labiummentioning

confidence: 99%

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Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

et al. 2012

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Specialized insect mouthparts, such as those of Drosophila, are derived from an ancestral mandibulate state, but little is known about the developmental genetics of mandibulate mouthparts. Here, we study the metamorphic patterning of mandibulate mouthparts of the beetle Tribolium castaneum, using RNA interference to deplete the expression of 13 genes involved in mouthpart patterning. These data were used to test three hypotheses related to mouthpart development and evolution. First, we tested the prediction that maxillary and labial palps are patterned using conserved components of the leg-patterning network. This hypothesis was strongly supported: depletion of Distal-less and dachshund led to distal and intermediate deletions of these structures while depletion of homothorax led to homeotic transformation of the proximal maxilla and labium, joint formation required the action of Notch signaling components and odd-skipped paralogs, and distal growth and patterning required epidermal growth factor (EGF) signaling. Additionally, depletion of abrupt or pdm/nubbin caused fusions of palp segments. Second, we tested hypotheses for how adult endites, the inner branches of the maxillary and labial appendages, are formed at metamorphosis. Our data reveal that Distal-less, Notch signaling components, and odd-skipped paralogs, but not dachshund, are required for metamorphosis of the maxillary endites. Endite development thus requires components of the limb proximal-distal axis patterning and joint segmentation networks. Finally, adult mandible development is considered in light of the gnathobasic hypothesis. Interestingly, while EGF activity is required for distal, but not proximal, patterning of other appendages, it is required for normal metamorphic growth of the mandibles.

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Regeneration in Crustaceans and Insects

Khan

Schuster

Smith-Bolton

2016

Encyclopedia of Life Sciences

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Many animal species have the capability to regenerate lost body parts. How regeneration takes place and why animals have varying potentials for regeneration remain active questions for biologists. The field of regenerative biology has witnessed unprecedented advances in the last several years owing to the availability of molecular and genomics tools and the establishment of many animal models. Regeneration research in arthropods has a long history, with extensive insights achieved from using model organisms from the taxa Crustacea and Insecta. Studies in animals ranging from fiddler crabs to crickets have revealed much about the different stages of regeneration, such as wound healing, blastema formation, growth, proliferation and patterning, as well as how hormonal control and systemic signalling impact regenerative capacity. The molecular and genetic insights achieved from studying these simpler model organisms have the potential to impact the field of regenerative biology by identifying conserved mechanisms of regeneration. Key Concepts Regeneration studies use the fiddler crab, crayfish, sand hopper, red flour beetle, fruit fly, cockroach, cricket and silverfish. For amputated limbs, wounds heal by a combination of rapid closure of the wound with a scab or autotomy membrane, and migration of cells into the wound. Imaginal disc wound closure involves cytoskeletal‐driven cell shape changes and zippering together of the epithelium, without cell migration. A regeneration blastema, or zone of proliferating cells, forms after both external limb amputation and imaginal disc damage. Growth of the blastema requires similar signals in multiple model organisms, including growth factor signalling in response to FGFs and EGFR activity, Wg/WNT signalling and Hippo signalling. Many developmental patterning genes are also required for patterning during regeneration. However, knockdown of these patterning genes revealed additional roles in regeneration beyond those observed during normal development. Some plasticity in cell fate enables replacement of lost cell types. Signals at the wound can alter pattern and cell fate, generating ectopic eye spots in butterflies and requiring the activity of a protective factor that stabilises cell fate gene expression during regeneration in fruit flies. Hormonal signalling, which controls moulting and metamorphosis, limits regenerative capacity. In some model organisms, tissue damage can influence hormone production and the timing of moults and metamorphosis.

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Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum

Cited by 36 publications

References 33 publications

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

Regeneration in Crustaceans and Insects

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