Unexpected mutual regulation underlies paralogue functional diversification and promotes epithelial tissue maturation in Tribolium

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Abstract

Insect Hox3/zen genes represent an evolutionary hotspot for changes in function and copy number. Single orthologues are required either for early specification or late morphogenesis of the extraembryonic tissues, which protect the embryo. The tandemly duplicated zen paralogues of the beetle Tribolium castaneum present a unique opportunity to investigate both functions in a single species. We dissect the paralogues' expression dynamics (transcript and protein) and transcriptional targets (RNA-seq after RNAi) throughout embryogenesis. We identify an unexpected role of Tc-Zen2 in repression of Tc-zen1, generating a negative feedback loop that promotes developmental progression. Tc-Zen2 regulation is dynamic, including within co-expressed multigene loci. We also show that extraembryonic development is the major event within the transcriptional landscape of late embryogenesis and provide a global molecular characterization of the extraembryonic serosal tissue. Altogether, we propose that paralogue mutual regulation arose through multiple instances of zen subfunctionalization, leading to their complementary extant roles.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
SWORD Depositor: Library Publications Router
Library of Congress Subject Headings (LCSH): Evolutionary genetics, Red flour beetle -- Genetics, Macroevolution
Journal or Publication Title: Communications Biology
Publisher: Nature Publishing Group
ISSN: 2399-3642
Official Date: 5 October 2020
Dates:
Date
Event
5 October 2020
Published
21 August 2020
Accepted
Volume: 3
Number: 1
Article Number: 552
DOI: 10.1038/s42003-020-01250-3
Status: Peer Reviewed
Publication Status: Published
Re-use Statement: ** From PubMed via Jisc Publications Router ** History: received 19-09-2019; accepted 21-08-2020.
Access rights to Published version: Open Access (Creative Commons open licence)
Date of first compliant deposit: 26 October 2020
Date of first compliant Open Access: 26 October 2020
RIOXX Funder/Project Grant:
Project/Grant ID
RIOXX Funder Name
Funder ID
SFB 680 project A12
Deutsche Forschungsgemeinschaft
PA 2044/1-1
Deutsche Forschungsgemeinschaft
URI: https://wrap.warwick.ac.uk/143249/

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