Literature DB >> 21504568

Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait.

Suzanne V Saenko1, Marta Sp Marialva, Patrícia Beldade.   

Abstract

BACKGROUND: Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns. Changes in embryonic expression and activity of Hox genes were crucial in the evolution of animal body plans, but their role in the post-embryonic development of lineage-specific traits remains largely unexplored. Here, we focus on the insect Hox genes Ultrabithorax (Ubx) and Antennapedia (Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns.
RESULTS: First, we describe a conserved pattern of Ubx expression and a novel pattern of Antp expression in wing discs of Bicyclus anynana butterflies. The discrete, reiterated domains of Antp contrast with the typical expression of Hox genes in single continuous regions in arthropod embryos. Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots. Antp upregulation is the earliest event in organizer development described to date, and in contrast to all genes implicated in eyespot formation, is exclusive to those centres. Third, our comparative analysis of gene expression across nymphalids reveals unexpected differences in organizer determination.
CONCLUSIONS: We show that the Antp's recruitment for the formation of novel traits in butterfly wing discs involved the evolution of new expression domains, and is restricted to a particular lineage. This study contributes novel insights into the evolution of Antp expression, as well as into the genetic mechanisms underlying morphological diversification. Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

Entities:  

Year:  2011        PMID: 21504568      PMCID: PMC3108338          DOI: 10.1186/2041-9139-2-9

Source DB:  PubMed          Journal:  Evodevo        ISSN: 2041-9139            Impact factor:   2.250


  57 in total

1.  The generation and diversification of butterfly eyespot color patterns.

Authors:  C R Brunetti; J E Selegue; A Monteiro; V French; P M Brakefield; S B Carroll
Journal:  Curr Biol       Date:  2001-10-16       Impact factor: 10.834

Review 2.  The genetics and evo-devo of butterfly wing patterns.

Authors:  Patrícia Beldade; Paul M Brakefield
Journal:  Nat Rev Genet       Date:  2002-06       Impact factor: 53.242

Review 3.  Hox genes and the evolution of the arthropod body plan.

Authors:  Cynthia L Hughes; Thomas C Kaufman
Journal:  Evol Dev       Date:  2002 Nov-Dec       Impact factor: 1.930

Review 4.  Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings.

Authors:  Suzanne V Saenko; Vernon French; Paul M Brakefield; Patrícia Beldade
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2008-04-27       Impact factor: 6.237

5.  Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila.

Authors:  R G Fehon; P J Kooh; I Rebay; C L Regan; T Xu; M A Muskavitch; S Artavanis-Tsakonas
Journal:  Cell       Date:  1990-05-04       Impact factor: 41.582

6.  The development of crustacean limbs and the evolution of arthropods.

Authors:  G Panganiban; A Sebring; L Nagy; S Carroll
Journal:  Science       Date:  1995-11-24       Impact factor: 47.728

7.  Pattern formation on lepidopteran wings: determination of an eyespot.

Authors:  H F Nijhout
Journal:  Dev Biol       Date:  1980-12       Impact factor: 3.582

8.  Homeotic gene expression in the wild-type and a homeotic mutant of the moth Manduca sexta.

Authors:  Z Zheng; A Khoo; D Fambrough; L Garza; R Booker
Journal:  Dev Genes Evol       Date:  1999-08       Impact factor: 0.900

9.  Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution.

Authors:  D N Keys; D L Lewis; J E Selegue; B J Pearson; L V Goodrich; R L Johnson; J Gates; M P Scott; S B Carroll
Journal:  Science       Date:  1999-01-22       Impact factor: 47.728

10.  Evolution of a novel appendage ground plan in water striders is driven by changes in the Hox gene Ultrabithorax.

Authors:  Abderrahman Khila; Ehab Abouheif; Locke Rowe
Journal:  PLoS Genet       Date:  2009-07-31       Impact factor: 5.917

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  30 in total

1.  Genetic basis of stage-specific melanism: a putative role for a cysteine sulfinic acid decarboxylase in insect pigmentation.

Authors:  S V Saenko; M A Jerónimo; P Beldade
Journal:  Heredity (Edinb)       Date:  2012-01-11       Impact factor: 3.821

2.  Nymphalid eyespot serial homologues originate as a few individualized modules.

Authors:  Jeffrey C Oliver; Jeremy M Beaulieu; Lawrence F Gall; William H Piel; Antónia Monteiro
Journal:  Proc Biol Sci       Date:  2014-07-22       Impact factor: 5.349

3.  Multiple Loci Control Eyespot Number Variation on the Hindwings of Bicyclus anynana Butterflies.

Authors:  Angel G Rivera-Colón; Erica L Westerman; Steven M Van Belleghem; Antónia Monteiro; Riccardo Papa
Journal:  Genetics       Date:  2020-02-04       Impact factor: 4.562

4.  Hox genes are essential for the development of eyespots in Bicyclus anynana butterflies.

Authors:  Yuji Matsuoka; Antónia Monteiro
Journal:  Genetics       Date:  2021-03-03       Impact factor: 4.562

5.  Stage- and sex-specific transcriptome analyses reveal distinctive sensory gene expression patterns in a butterfly.

Authors:  David A Ernst; Erica L Westerman
Journal:  BMC Genomics       Date:  2021-08-02       Impact factor: 3.969

6.  Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles.

Authors:  Yonggang Hu; Armin P Moczek
Journal:  Proc Biol Sci       Date:  2021-01-20       Impact factor: 5.349

7.  Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation.

Authors:  Heather M Hines; Riccardo Papa; Mayte Ruiz; Alexie Papanicolaou; Charles Wang; H Frederik Nijhout; W Owen McMillan; Robert D Reed
Journal:  BMC Genomics       Date:  2012-06-29       Impact factor: 3.969

8.  Isolation of Hox cluster genes from insects reveals an accelerated sequence evolution rate.

Authors:  Heike Hadrys; Sabrina Simon; Barbara Kaune; Oliver Schmitt; Anja Schöner; Wolfgang Jakob; Bernd Schierwater
Journal:  PLoS One       Date:  2012-06-07       Impact factor: 3.240

9.  A cis-Acting Mutation in the PxABCG1 Promoter Is Associated with Cry1Ac Resistance in Plutella xylostella (L.).

Authors:  Jianying Qin; Fan Ye; Linzheng Xu; Xuguo Zhou; Neil Crickmore; Xiaomao Zhou; Youjun Zhang; Zhaojiang Guo
Journal:  Int J Mol Sci       Date:  2021-06-05       Impact factor: 5.923

10.  A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression.

Authors:  Jeffrey C Oliver; Xiao-Ling Tong; Lawrence F Gall; William H Piel; Antónia Monteiro
Journal:  PLoS Genet       Date:  2012-08-16       Impact factor: 5.917

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