Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
09 2023
Historique:
received: 02 03 2023
accepted: 16 08 2023
revised: 20 09 2023
medline: 21 9 2023
pubmed: 8 9 2023
entrez: 8 9 2023
Statut: epublish

Résumé

TAIMAN (TAI), the only insect ortholog of mammalian Steroid Receptor Coactivators (SRCs), is a critical modulator of ecdysone and juvenile hormone (JH) signaling pathways, which govern insect development and reproduction. The modulatory effect is mediated by JH-dependent TAI's heterodimerization with JH receptor Methoprene-tolerant and association with the Ecdysone Receptor complex. Insect hormones regulate insect physiology and development in concert with abiotic cues, such as photo- and thermoperiod. Here we tested the effects of JH and ecdysone signaling on the circadian clock by a combination of microsurgical operations, application of hormones and hormone mimics, and gene knockdowns in the linden bug Pyrrhocoris apterus males. Silencing taiman by each of three non-overlapping double-strand RNA fragments dramatically slowed the free-running period (FRP) to 27-29 hours, contrasting to 24 hours in controls. To further corroborate TAIMAN's clock modulatory function in the insect circadian clock, we performed taiman knockdown in the cockroach Blattella germanica. Although Blattella and Pyrrhocoris lineages separated ~380 mya, B. germanica taiman silencing slowed the FRP by more than 2 hours, suggesting a conserved TAI clock function in (at least) some insect groups. Interestingly, the pace of the linden bug circadian clock was neither changed by blocking JH and ecdysone synthesis, by application of the hormones or their mimics nor by the knockdown of corresponding hormone receptors. Our results promote TAI as a new circadian clock modulator, a role described for the first time in insects. We speculate that TAI participation in the clock is congruent with the mammalian SRC-2 role in orchestrating metabolism and circadian rhythms, and that TAI/SRCs might be conserved components of the circadian clock in animals.

Identifiants

pubmed: 37683015
doi: 10.1371/journal.pgen.1010924
pii: PGENETICS-D-23-00239
pmc: PMC10511111
doi:

Substances chimiques

Ecdysone 3604-87-3
Juvenile Hormones 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010924

Informations de copyright

Copyright: © 2023 Smykal et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Vlastimil Smykal (V)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.

Lenka Chodakova (L)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic.

Marketa Hejnikova (M)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.

Kristina Briedikova (K)

Faculty of Science, Masaryk University, Brno, Czech Republic.

Bulah Chia-Hsiang Wu (BC)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic.

Hana Vaneckova (H)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.

Ping Chen (P)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic.

Anna Janovska (A)

Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences of the Czech Republic, Prague, Czech Republic.

Pavlina Kyjakova (P)

Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences of the Czech Republic, Prague, Czech Republic.

Martin Vacha (M)

Faculty of Science, Masaryk University, Brno, Czech Republic.

David Dolezel (D)

Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Entomology, Ceske Budejovice, Czech Republic.
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic.

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Classifications MeSH