Sex-specific gene interactions in the patterning of insect genitalia

Aspiras, Ariel C.; Smith, F. W.; Angelini, David R.

doi:10.1016/j.ydbio.2011.09.026

Cited by 50 publications

(76 citation statements)

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“…Although comparative data are limited, other data are consistent with the suggestion that appendage identity is more labile at metamorphosis in holometabolous species than it is in hemimetabolous species. In particular, Dll RNAi has homeotic effects on appendage identity at metamorphosis in T. castaneum (Smith et al, 2014b;Suzuki et al, 2009), but not in post-embryonic development of multiple species of Hemiptera (Aspiras et al, 2011;Khila et al, 2012;Lin et al, 2014). This pattern raises the question of how the identity specification processes active during metamorphosis of ventral appendages in holometabolous insects relate to processes active in hemimetabolous insects.…”

Section: Discussionmentioning

confidence: 99%

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Hox genes require homothorax and extradenticle for body wall identity specification but not for appendage identity specification during metamorphosis of Tribolium castaneum

Smith

Jockusch

2014

Developmental Biology

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The establishment of segment identity is a key developmental process that allows for divergence along the anteroposterior body axis in arthropods. In Drosophila, the identity of a segment is determined by the complement of Hox genes it expresses. In many contexts, Hox transcription factors require the protein products of extradenticle (exd) and homothorax (hth) as cofactors to perform their identity specification functions. In holometabolous insects, segment identity may be specified twice, during embryogenesis and metamorphosis. To glean insight into the relationship between embryonic and metamorphic segmental identity specification, we have compared these processes in the flour beetle Tribolium castaneum, which develops ventral appendages during embryogenesis that later metamorphose into adult appendages with distinct morphologies. At metamorphosis, comparisons of RNAi phenotypes indicate that Hox genes function jointly with Tc-hth and Tc-exd to specify several region-specific aspects of the adult body wall. On the other hand, Hox genes specify appendage identities along the anteroposterior axis independently of Tc-hth/Tc-exd and Tc-hth/Tc-exd specify proximal vs. distal identity within appendages independently of Hox genes during this stage. During embryogenesis, Tc-hth and Tc-exd play a broad role in the segmentation process and are required for specification of body wall identities in the thorax; however, contrasting with results from other species, we did not obtain homeotic transformations of embryonic appendages in response to Tc-hth or Tc-exd RNAi. In general, the homeotic effects of interference with the function of Hox genes and Tc-hth/Tc-exd during metamorphosis did not match predictions based on embryonic roles of these genes. Comparing metamorphic patterning in T. castaneum to embryonic and post-embryonic development in hemimetabolous insects suggests that holometabolous metamorphosis combines patterning processes of both late embryogenesis and metamorphosis of the hemimetabolous life cycle.

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Section: Discussionmentioning

confidence: 99%

“…A8-A10 are membranous and normally pulled within the abdomen, but are telescoped out during mating (Sokoloff, 1972). The male aedeagus articulates with A8, and the female ovipositor is composed of parts of A8-A10 (Aspiras et al, 2011).…”

Section: Abdominal Segmentsmentioning

confidence: 99%

Hox genes require homothorax and extradenticle for body wall identity specification but not for appendage identity specification during metamorphosis of Tribolium castaneum

Smith

Jockusch

2014

Developmental Biology

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“…In the thysanuran Thermobia domestica , Abd-B is expressed in the eight through the tenth abdominal segments [48]. In the milkweed bug Oncopeltus fasciatus , Abd-B also has a genital-specifying role [49]. In crustaceans, Abd-B is also expressed in the genital segments [50-52] and extends throughout all five segments of the posterior tagma (the pleon) of the isopod Porcellio scaber [51], but remains in the genital region of Artemia franciscana [50] .…”

Section: Discussionmentioning

confidence: 99%

Posterior Hox gene reduction in an arthropod: Ultrabithorax and Abdominal-B are expressed in a single segment in the mite Archegozetes longisetosus

Barnett

Thomas

2013

EvoDevo

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BackgroundHox genes encode transcription factors that have an ancestral role in all bilaterian animals in specifying regions along the antero-posterior axis. In arthropods (insects, crustaceans, myriapods and chelicerates), Hox genes function to specify segmental identity, and changes in Hox gene expression domains in different segments have been causal to the evolution of novel arthropod morphologies. Despite this, the roles of Hox genes in arthropods that have secondarily lost or reduced their segmental composition have been relatively unexplored. Recent data suggest that acariform mites have a reduced segmental component of their posterior body tagma, the opisthosoma, in that only two segments are patterned during embryogenesis. This is in contrast to the observation that in many extinct and extant chelicerates (that is, horseshoe crabs, scorpions, spiders and harvestmen) the opisthosoma is comprised of ten or more segments. To explore the role of Hox genes in this reduced body region, we followed the expression of the posterior-patterning Hox genes Ultrabithorax (Ubx) and Abdominal-B (Abd-B), as well as the segment polarity genes patched (ptc) and engrailed (en), in the oribatid mite Archegozetes longisetosus.ResultsWe find that the expression patterns of ptc are in agreement with previous reports of a reduced mite opisthosoma. In comparison to the ptc and en expression patterns, we find that Ubx and Abd-B are expressed in a single segment in A. longisetosus, the second opisthosomal segment. Abd-B is initially expressed more posteriorly than Ubx, that is, into the unsegmented telson; however, this domain clears in subsequent stages where it remains in the second opisthosomal segment.ConclusionsOur findings suggest that Ubx and Abd-B are expressed in a single segment in the opisthosoma. This is a novel observation, in that these genes are expressed in several segments in all studied arthropods. These data imply that a reduction in opisthosomal segmentation may be tied to a dramatically reduced Hox gene input in the opisthosoma.

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“…Because of the potential for functional redundancy of some genes studied here, we also included some treatments in which multiple genes were targeted by injecting multiple dsRNAs (Table 2). Validation of RNAi knockdown was performed by real-time PCR comparison of target gene expression in control ( GFP ) dsRNA and gene-specific dsRNA treatments (Table 2), as described in an accompanying article in Genetics, Angelini et al (2012; see also Aspiras et al 2011). …”

Section: Methodsmentioning

confidence: 99%

Extent With Modification: Leg Patterning in the BeetleTribolium castaneumand the Evolution of Serial Homologs

Angelini

Smith

Jockusch

2012

G3 Genes|Genomes|Genetics

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Serial homologs are similar structures that develop at different positions within a body plan. These structures share some, but not all, aspects of developmental patterning, and their evolution is thought to be constrained by shared, pleiotropic gene functions. Here we describe the functions of 17 developmental genes during metamorphic development of the legs in the red flour beetle, Tribolium castaneum. This study provides informative comparisons between appendage development in Drosophila melanogaster and T. castaneum, between embryonic and adult development in T. castaneum, and between the development of serially homologous appendages. The leg gap genes Distal-less and dachshund are conserved in function. Notch signaling, the zinc-finger transcription factors related to odd-skipped, and bric-à-brac have conserved functions in promoting joint development. homothorax knockdown alters the identity of proximal leg segments but does not reduce growth. Lim1 is required for intermediate leg development but not distal tarsus and pretarsus development as in D. melanogaster. Development of the tarsus requires decapentaplegic, rotund, spineless, abrupt, and bric-à-brac and the EGF ligand encoded by Keren. Metathoracic legs of T. castaneum have four tarsomeres, whereas other legs have five. Patterns of gene activity in the tarsus suggest that patterning in the middle of the tarsal region, not the proximal- or distal-most areas, is responsible for this difference in segment number. Through comparisons with other recent studies of T. castaneum appendage development, we test hypotheses for the modularity or interdependence of development during evolution of serial homologs.

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Sex-specific gene interactions in the patterning of insect genitalia

Cited by 50 publications

References 50 publications

Hox genes require homothorax and extradenticle for body wall identity specification but not for appendage identity specification during metamorphosis of Tribolium castaneum

Hox genes require homothorax and extradenticle for body wall identity specification but not for appendage identity specification during metamorphosis of Tribolium castaneum

Posterior Hox gene reduction in an arthropod: Ultrabithorax and Abdominal-B are expressed in a single segment in the mite Archegozetes longisetosus

Extent With Modification: Leg Patterning in the BeetleTribolium castaneumand the Evolution of Serial Homologs

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