The BTB transcription factor, Abrupt, acts cooperatively with Chronologically inappropriate morphogenesis (Chinmo) to repress metamorphosis and promotes leg regeneration
Open accessAbstract
Many insects undergo the process of metamorphosis when larval precursor cells begin to differentiate to create the adult body. The larval precursor cells retain stem cell-like properties and contribute to the regenerative ability of larval appendages. Here we demonstrate that two Broad-complex/Tramtrack/Bric-à-brac Zinc-finger (BTB) domain transcription factors, Chronologically inappropriate morphogenesis (Chinmo) and Abrupt (Ab), act cooperatively to repress metamorphosis in the flour beetle, Tribolium castaneum. Knockdown of chinmo led to precocious development of pupal legs and antennae. We show that although topical application of juvenile hormone (JH) prevents the decrease in chinmo expression in the final instar, chinmo and JH act in distinct pathways. Another gene encoding the BTB domain transcription factor, Ab, was also necessary for the suppression of broad (br) expression in T. castaneum in a chinmo RNAi background, and simultaneous knockdown of ab and chinmo led to the precocious onset of metamorphosis. Furthermore, knockdown of ab led to the loss of regenerative potential of larval legs independently of br. In contrast, chinmo knockdown larvae exhibited pupal leg regeneration when a larval leg was ablated. Taken together, our results show that both ab and chinmo are necessary for the maintenance of the larval tissue identity and, apart from its role in repressing br, ab acts as a crucial regulator of larval leg regeneration. Our findings indicate that BTB domain…
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In holometabolous insects, the larval, pupal, and adult stages are determined by three metamorphic genes: chinmo, broad, and E93, respectively.
“In holometabolous insects, the larval, pupal, and adult stages are determined by three metamorphic genes: chinmo, broad , and E93 , respectively.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
Chinmo is anti-metamorphic and suppresses the expression of broad and E93.
“Chinmo is anti-metamorphic and suppresses the expression of broad and E93 .”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
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 [30]
In Tribolium, treatment of last-stage larvae with JH mimics extended larval molting.
“In Tribolium , by contrast, treatment of last-stage larvae with JH mimics extended larval molting.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
The extent of pupal development was enhanced by simultaneous knockdown of abrupt.
“The extent of pupal development was enhanced by the simultaneous knockdown of abrupt , another BTB Zinc finger protein [30].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
Knockdown of abrupt alone did not induce precocious metamorphosis nor alter levels of broad, E93, or Kr-h1.
“The knockdown of abrupt alone, though, did not induce precocious metamorphosis nor did it alter levels of broad , E93 , or Kr-h1.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
Chinmo knockdown can cause premature E93 expression and metamorphosis despite Kr-h1 levels remaining elevated.
“Importantly, chinmo knockdown can cause premature E93 expression and metamorphosis despite Kr-h1 levels remaining elevated [30].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
Chinmo maintains the larval state in both Drosophila and Tribolium, and it inhibits both broad and E93 expression.
“Chinmo maintains the larval state in both Drosophila [59,7] and Tribolium [30], and it inhibits both broad and E93 expression .”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
The main way that JH, through Kr-h1, maintains the nymphal stage is by maintaining chinmo expression.
“Thus, the main way that JH, through Kr-h1 , maintains the nymphal stage is by maintaining chinmo expression.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [30]
Cites
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
Chafino, S., Giannios, P., Casanova, J., Martín, D., & Franch-Marro, X. (2023) · eLife · doi:10.7554/elife.84648 · Cited by 30 · see citing works
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Regulation 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
- Khong, H., Hattley, K. B., & Suzuki, Y.
- Affiliations
- Wellesley College (US)
- Corresponding author
- Suzuki, Yuichiro
- ORCID
- Suzuki, Yuichiro
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2024-05
- Volume
- 509
- Pages
- 70-84
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W4391899874
- Cited by
- 15
- References
- 2
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 4
- FWCI
- 2.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- SSRN Electronic Journal (acceptedVersion)
- PubMed (publishedVersion)
- Funders
- Wellesley College
- National Science Foundation (IOS-2002354)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- Chinmo, metamorphosis, Tribolium castaneum, juvenile hormone, Broad-Complex, Tramtrack, bric-a-brac, tissue homeostasis, precocious development, antennal development
- MeSH terms
- Animals, Coleoptera, Juvenile Hormones, Larva, Metamorphosis, Biological, Morphogenesis, Pupa, Regeneration, Transcription Factors, Tribolium, Gene Expression Regulation, Developmental, Insect Proteins
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