Transcription factor E93 specifies adult metamorphosis in hemimetabolous and holometabolous insects
Open accessAbstract
All immature animals undergo remarkable morphological and physiological changes to become mature adults. In winged insects, metamorphic changes either are limited to a few tissues (hemimetaboly) or involve a complete reorganization of most tissues and organs (holometaboly). Despite the differences, the genetic switch between immature and adult forms in both types of insects relies on the disappearance of the antimetamorphic juvenile hormone (JH) and the transcription factors Krüppel-homolog 1 (Kr-h1) and Broad-Complex (BR-C) during the last juvenile instar. Here, we show that the transcription factor E93 is the key determinant that promotes adult metamorphosis in both hemimetabolous and holometabolous insects, thus acting as the universal adult specifier. In the hemimetabolous insect Blattella germanica, BgE93 is highly expressed in metamorphic tissues, and RNA interference (RNAi)-mediated knockdown of BgE93 in the nymphal stage prevented the nymphal-adult transition, inducing endless reiteration of nymphal development, even in the absence of JH. We also find that BgE93 down-regulated BgKr-h1 and BgBR-C expression during the last nymphal instar of B. germanica, a key step necessary for proper adult differentiation. This essential role of E93 is conserved in holometabolous insects as TcE93 RNAi in Tribolium castaneum prevented pupal-adult transition and produced a supernumerary second pupa. In this beetle, TcE93 also represses expression of TcKr-h1 and TcBR-C during the pupal…
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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 [65]
Based on whether JH is needed to maintain the larva, either E93 (Tribolium) or broad (Drosophila) serves as the entry to metamorphosis.
“Based on whether JH is needed to maintain the larva, either E93 ( Tribolium ) or broad ( Drosophila ) serves as the entry to metamorphosis.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [65]
E93 expression is required for adult differentiation.
“E93 expression is required for adult differentiation.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [65]
The arrested phenotypes of null mutants of broad and E93 in Drosophila indicate that the gateway to metamorphosis shifts from E93 to broad in higher flies.
“The arrested phenotypes of null mutants of broad [27] and E93 [65,35] in Drosophila indicate that the gateway to metamorphosis shifts from E93 to broad in higher flies.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [65]
As in Holometabola, E93 functions in hemimetabolous species to mediate the entry into metamorphosis, and its suppression results in permanent nymphs.
“As in the Holometabola, E93 functions in these species to mediate the entry into metamorphosis, and its suppression results in permanent nymphs [65,43].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [65]
Cites
The pupal specifier <i>broad</i> directs progressive morphogenesis in a direct-developing insect
Erezyilmaz, D. F., Riddiford, L. M., & Truman, J. W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509983103 · Cited by 122 · see citing works
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Truman, J. W., & Riddiford, L. M. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201071119 · Cited by 53 · see citing works
He, L. L., Shin, S. H., Wang, Z., Yuan, I., Weschler, R., Chiou, A., Koyama, T., Nijhout, H. F., & Suzuki, Y. (2020) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2020.103452 · Cited by 53 · see citing works
Chafino, S., Giannios, P., Casanova, J., Martín, D., & Franch-Marro, X. (2023) · eLife · doi:10.7554/elife.84648 · Cited by 30 · see citing works
Self-citationRegulation of metamorphosis in holometabolous insects
Truman, J. W., & Riddiford, L. M. (2026) · Current Opinion in Insect Science · doi:10.1016/j.cois.2026.101508 · Cited by 6 · see citing works
- Authors
- Ureña, E., Manjón, C., Franch-Marro, X., & Martín, D.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Institute of Evolutionary Biology, Consejo Superior de Investigaciones Cientificas–Universitat Pompeu Fabra, 08003 Barcelona, Spain
- ORCID
- Ureña, Enric
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-04-28
- Volume
- 111
- Issue
- 19
- Pages
- 7024-7029
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4024875
- OpenAlex
- W1986231903
- Cited by
- 188
- References
- 1
- Citations by year
- 2026: 24 · 2025: 17 · 2024: 19 · 2023: 14 · 2022: 15 · 2021: 17 · 2020: 22 · 2019: 18 · 2018: 10 · 2017: 14 · 2016: 7 · 2015: 9 · 2014: 2
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- 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
- hemimetabolism, holometabolism, Blattella germanica, Tribolium castaneum, Drosophila melanogaster, juvenile hormone, Krüppel homolog 1, Broad-Complex, insect development, transcriptional regulation
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Drosophila melanogaster, Biological Evolution, Juvenile Hormones, Larva, Metamorphosis, Biological, Methoprene, Molecular Sequence Data, Species Specificity, Transcription Factors, Tribolium, Gene Expression Regulation, Developmental, Insect Proteins, Blattellidae, Drosophila Proteins, Kruppel-Like Transcription Factors
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