The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis

To gain insights into how juvenile hormone (JH) came to regulate insect metamorphosis, we studied its function in the ametabolous firebrat, Thermobia domestica. Highest levels of JH occur during late embryogenesis, with only low levels thereafter. Loss-of-function and gain-of-function experiments sh...

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出版年:eLife
主要な著者: James W Truman, Lynn M Riddiford, Barbora Konopova, Marcela Nouzova, Fernando G Noriega, Michelle Herko
フォーマット: 論文
言語:英語
出版事項: eLife Sciences Publications Ltd 2024-04-01
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オンライン・アクセス:https://elifesciences.org/articles/92643
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author James W Truman
Lynn M Riddiford
Barbora Konopova
Marcela Nouzova
Fernando G Noriega
Michelle Herko
author_facet James W Truman
Lynn M Riddiford
Barbora Konopova
Marcela Nouzova
Fernando G Noriega
Michelle Herko
author_sort James W Truman
collection DOAJ
container_title eLife
description To gain insights into how juvenile hormone (JH) came to regulate insect metamorphosis, we studied its function in the ametabolous firebrat, Thermobia domestica. Highest levels of JH occur during late embryogenesis, with only low levels thereafter. Loss-of-function and gain-of-function experiments show that JH acts on embryonic tissues to suppress morphogenesis and cell determination and to promote their terminal differentiation. Similar embryonic actions of JH on hemimetabolous insects with short germ band embryos indicate that JH’s embryonic role preceded its derived function as the postembryonic regulator of metamorphosis. The postembryonic expansion of JH function likely followed the evolution of flight. Archaic flying insects were considered to lack metamorphosis because tiny, movable wings were evident on the thoraces of young juveniles and their positive allometric growth eventually allowed them to support flight in late juveniles. Like in Thermobia, we assume that these juveniles lacked JH. However, a postembryonic reappearance of JH during wing morphogenesis in the young juvenile likely redirected wing development to make a wing pad rather than a wing. Maintenance of JH then allowed wing pad growth and its disappearance in the mature juvenile then allowed wing differentiation. Subsequent modification of JH action for hemi- and holometabolous lifestyles are discussed.
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spelling doaj-art-62cfd1ef4ff24ef495dddf4a653656852025-08-19T23:24:39ZengeLife Sciences Publications LtdeLife2050-084X2024-04-011210.7554/eLife.92643The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosisJames W Truman0https://orcid.org/0000-0002-9209-5435Lynn M Riddiford1https://orcid.org/0000-0002-3026-7430Barbora Konopova2Marcela Nouzova3Fernando G Noriega4Michelle Herko5Friday Harbor Laboratories, University of Washington, Friday Harbor, United States; Department of Biology, University of Washington, Seattle, United StatesFriday Harbor Laboratories, University of Washington, Friday Harbor, United States; Department of Biology, University of Washington, Seattle, United StatesDepartment of Zoology, Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic; Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech RepublicInstitute of Parasitology, Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech RepublicDepartment of Biological Sciences and BSI, Florida International University, Miami, United States; Department of Parasitology, Faculty of Science, University of South Bohemia, Ceské Budejovice, Czech RepublicFriday Harbor Laboratories, University of Washington, Friday Harbor, United StatesTo gain insights into how juvenile hormone (JH) came to regulate insect metamorphosis, we studied its function in the ametabolous firebrat, Thermobia domestica. Highest levels of JH occur during late embryogenesis, with only low levels thereafter. Loss-of-function and gain-of-function experiments show that JH acts on embryonic tissues to suppress morphogenesis and cell determination and to promote their terminal differentiation. Similar embryonic actions of JH on hemimetabolous insects with short germ band embryos indicate that JH’s embryonic role preceded its derived function as the postembryonic regulator of metamorphosis. The postembryonic expansion of JH function likely followed the evolution of flight. Archaic flying insects were considered to lack metamorphosis because tiny, movable wings were evident on the thoraces of young juveniles and their positive allometric growth eventually allowed them to support flight in late juveniles. Like in Thermobia, we assume that these juveniles lacked JH. However, a postembryonic reappearance of JH during wing morphogenesis in the young juvenile likely redirected wing development to make a wing pad rather than a wing. Maintenance of JH then allowed wing pad growth and its disappearance in the mature juvenile then allowed wing differentiation. Subsequent modification of JH action for hemi- and holometabolous lifestyles are discussed.https://elifesciences.org/articles/92643juvenile hormoneecdysonemyoglianinmetamorphosisdifferentiationprecocene
spellingShingle James W Truman
Lynn M Riddiford
Barbora Konopova
Marcela Nouzova
Fernando G Noriega
Michelle Herko
The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
juvenile hormone
ecdysone
myoglianin
metamorphosis
differentiation
precocene
title The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
title_full The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
title_fullStr The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
title_full_unstemmed The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
title_short The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis
title_sort embryonic role of juvenile hormone in the firebrat thermobia domestica reveals its function before its involvement in metamorphosis
topic juvenile hormone
ecdysone
myoglianin
metamorphosis
differentiation
precocene
url https://elifesciences.org/articles/92643
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