The role of the pupal determinant broad during embryonic development of a direct-developing insect
- 1 December 2009
- journal article
- research article
- Published by Springer Science and Business Media LLC in Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen
- Vol. 219 (11-12), 535-544
- https://doi.org/10.1007/s00427-009-0315-7
Abstract
Metamorphosis is one of the most common, yet dramatic of life history strategies. In insects, complete metamorphosis with morphologically distinct larval stages arose from hemimetabolous ancestors that were more direct developing. Over the past century, several ideas have emerged that suggest the holometabolous pupa is developmentally homologous to the embryonic stages of the hemimetabolous ancestor. Other theories consider the pupal stage to be a modification of a hemimetabolous nymph. To address this question, we have isolated an ortholog of the pupal determinant, broad (br), from the hemimetabolous milkweed bug and examined its role during embryonic development. We show that Oncopeltus fasciatus br (Of’br) is expressed in two phases. The first occurs during germ band invagination and segmentation when Of’br is expressed ubiquitously in the embryonic tissues. The second phase of Of’br expression appears during the pronymphal phase of embryogenesis and persists through nymphal differentiation to decline just before hatching. Knock-down of Of’br transcripts results in defects that range from posterior truncations in the least-affected phenotypes to completely fragmented embryonic tissues in the most severe cases. Analysis of the patterning genes engrailed and hunchback reveal loss of segments and a failure in neural differentiation after Of’br depletion. Finally, we show that br is constitutively expressed during embyrogenesis of the ametabolous firebrat, Thermobia domestica. This suggests that br expression is prominent during embryonic development of ametabolous and hemimetabolous insects but was lost with the emergence of the completely metamorphosing insects.Keywords
This publication has 36 references indexed in Scilit:
- Temporal patterns of broad isoform expression during the development of neuronal lineages in DrosophilaNeural Development, 2009
- The nuclear receptor E75A has a novel pair-rule-like function in patterning the milkweed bug, Oncopeltus fasciatusDevelopmental Biology, 2009
- Transcription factor broad suppresses precocious development of adult structures during larval–pupal metamorphosis in the red flour beetle, Tribolium castaneumMechanisms of Development, 2008
- The morphostatic actions of juvenile hormoneInsect Biochemistry and Molecular Biology, 2007
- Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosisIntegrative and Comparative Biology, 2006
- The pupal specifier broad directs progressive morphogenesis in a direct-developing insectProceedings of the National Academy of Sciences of the United States of America, 2006
- even-skippedis not a pair-rule gene but has segmental and gap-like functions inOncopeltus fasciatus, an intermediate germband insectDevelopment, 2005
- Ultrastructure, development, and homology of insect embryonic cuticlesJournal of Morphology, 2005
- Exogenous makisterone A accelerates early embryonic development in the milkweed bugOncopeltus fasciatusCellular and Molecular Life Sciences, 1982
- Ultrastructure of embryonic envelopes and integument ofOncopeltus fasciatus Dallas (Insecta, Heteroptera)Zoomorphology, 1976