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Cited by 12Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationInsect and Arachnid Ecology and Behavior

Chinmo function in cockroaches provides new insights into the regulation and evolution of insect metamorphosis

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Escudero, Jorge, Gonzalvo, Judit, Piulachs, Maria-Dolors, Belles, Xavier·2025·PLOS Genetics
DOI 10.1371/journal.pgen.1011993PMC PMC12758806
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Abstract

Insect metamorphosis occurs in two main forms, hemimetaboly (simple) and holometaboly (complete), both regulated by hormonal and genetic pathways involving the transcription factors Krüppel homolog 1 (Kr-h1), Broad-Complex (BR-C), and Ecdysone-induced protein 93F (E93). The BTB–zinc finger protein Chronologically inappropriate morphogenesis (Chinmo), recently identified in the fruit fly Drosophila melanogaster , an holometabolan, as a larval state maintainer, was studied here in the German cockroach, Blattella germanica , an hemimetabolan. We also examined another BTB transcription factor, Abrupt (Ab), based on findings in another holometabolan, the red flour beetle, Tribolium castaneum , suggesting a cooperative role. We characterized chinmo expression in B. germanica and found sustained transcript levels during the N4 and N5 nymphal instars, followed by a marked decline at the final N6 instar. RNA interference (RNAi) knockdown of chinmo at N4 induced precocious metamorphosis two molts later, accompanied by reduced Kr-h1 and elevated E93 expression. Combined knockdown of chinmo and E93 revealed that Chinmo primarily represses E93 . Similarly, ab knockdown also triggered precocious metamorphosis, decreasing Kr-h1 and increasing E93 expression; double knockdown of ab and E93 indicated that Ab primarily promotes Kr-h1 expression. These results expand the MEKRE93 pathway by identifying Chinmo and Ab as additional regulators that help maintain the juvenile state in both hemimetabolan and holometabolan insects. Holometaboly likely evolved from hemimetabolan ancestors through the embryonic internalization of wing primordia into imaginal cells, which enabled the emergence of distinct larval forms. Key regulatory factors like Kr-h1, Chinmo, Ab, BR-C, and E93, already present in hemimetabolan lineages, were conserved and rewired in holometabolans. Crucial shifts in this evolutionary transition include Chinmo-mediated inhibition of BR-C and an inversion in the juvenile hormone effect on BR-C , from activation to repression.

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  • In hemimetabolous insects, Chinmo and JH, via Kr-h1, maintain the nymphal stage and suppress E93 and adult differentiation.

    “In hemimetabolous insects, Chinmo and JH, via Kr-h1 , maintain the nymphal stage and suppress E93 and adult differentiation.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [17]

    The Introduction says JH induces Kr-h1, which represses E93 and maintains the nymphal state. The Discussion says Chinmo also maintains the nymphal state by repressing E93, but acts alongside Kr-h1 through a distinct mechanism; it does not support the implication that Chinmo acts via Kr-h1. (LLM, conf=0.84)

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Cited by

Sorted by citations

Authors
Escudero, J., Gonzalvo, J., Piulachs, M.-D., & Belles, X.
Affiliations
Universitat Pompeu Fabra (ES)
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2025-12-26
Volume
21
Issue
12
Pages
e1011993
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1011993
PMC
PMC12758806
OpenAlex
W7117303688
Cited by
12
References
2
Citations by year
2026: 12
FWCI
4.71
Type
journal article
Language
en
Update notices
new_version (2026-01-02)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Ministerio de Ciencia, Innovación y Universidades (TED2021-130489B-I00, PID2021-122316OB-I00)
  • Department of Universities, Research and Information Society of the Catalan Government (2021 SGR 00419)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
Keywords
Chinmo, Blattella germanica, insect metamorphosis, Krüppel homolog 1, Broad-Complex, E93, juvenile hormone, nymphal instars, precocious metamorphosis, Tribolium castaneum
MeSH terms
Animals, Cockroaches, Drosophila melanogaster, Biological Evolution, Larva, Metamorphosis, Biological, Transcription Factors, Tribolium, Gene Expression Regulation, Developmental, Insect Proteins, Blattellidae, Drosophila Proteins, RNA Interference, Kruppel-Like Transcription Factors

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