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Cited by 129Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationInsect and Arachnid Ecology and Behavior

The Occurrence of the Holometabolous Pupal Stage Requires the Interaction between E93, Krüppel-Homolog 1 and Broad-Complex

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Ureña, Enric, Chafino, Silvia, Manjón, Cristina, Franch-Marro, Xavier, Martín, David·2016·PLOS Genetics
DOI 10.1371/journal.pgen.1006020PMC PMC4852927
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Abstract

Complete metamorphosis (Holometaboly) is a key innovation that underlies the spectacular success of holometabolous insects. Phylogenetic analyses indicate that Holometabola form a monophyletic group that evolved from ancestors exhibiting hemimetabolous development (Hemimetaboly). However, the nature of the changes underlying this crucial transition, including the occurrence of the holometabolan-specific pupal stage, is poorly understood. Using the holometabolous beetle Tribolium castaneum as a model insect, here we show that the transient up-regulation of the anti-metamorphic Krüppel-homolog 1 (TcKr-h1) gene at the end of the last larval instar is critical in the formation of the pupa. We find that depletion of this specific TcKr-h1 peak leads to the precocious up-regulation of the adult-specifier factor TcE93 and, hence, to a direct transformation of the larva into the adult form, bypassing the pupal stage. Moreover, we also find that the TcKr-h1-dependent repression of TcE93 is critical to allow the strong up-regulation of Broad-complex (TcBr-C), a key transcription factor that regulates the correct formation of the pupa in holometabolous insects. Notably, we show that the genetic interaction between Kr-h1 and E93 is also present in the penultimate nymphal instar of the hemimetabolous insect Blattella germanica, suggesting that the evolution of the pupa has been facilitated by the co-option of regulatory mechanisms present in hemimetabolan metamorphosis. Our findings, therefore, contribute to the molecular understanding of insect metamorphosis, and indicate the evolutionary conservation of the genetic circuitry that controls hemimetabolan and holometabolan metamorphosis, thereby shedding light on the evolution of complete metamorphosis.

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  • In Tribolium, JH, working through Kr-h1, represses E93 expression, but it has no effect on broad.

    “In Tribolium, JH, working through Kr-h1, represses E93 expression, but it has no effect on broad [64].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [64]

    The Results section confirms that TcKr-h1 represses TcE93 at the larval–pupal transition. But the Discussion says JH represses Broad-Complex (Br-C) in young holometabolous larvae and that Kr-h1 also affects Br-C expression in a stage-specific way, contrary to the claim that JH has no effect on broad. (LLM, conf=0.88)

    Checked by a reasoning model — may be wrong.

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  • Both Tribolium and Drosophila need JH and Kr-h1 to make the pupa.

    “Although Tribolium and Drosophila differ in their need for JH to maintain their larval stage, both need JH and Kr-h1 to make the pupa (Figure 3b).”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [64]

    The Introduction reports that a prepupal Kr-h1 peak is critical for pupal formation in Tribolium and Drosophila. The Discussion does not establish that either species needs juvenile hormone (JH) to form a pupa: it calls JH control of the Tribolium peak plausible, notes that Drosophila Kr-h1 is also induced by 20E, and says the controlling factors remain unclear. Page numbers are not available in our copy. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • Kr-h1 is needed for pupa formation in Drosophila.

    “Kr-h1 is also needed for pupa formation in Drosophila [64].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [64]

    The Introduction says a late Kr-h1 pulse is critical for the occurrence of the pupa and identifies Drosophila as one of the insects studied. But the Drosophila Results report disrupted gene expression and degeneration of Kr-h1-depleted wings during the pupal stage; they do not show that Kr-h1 is needed for formation of the pupa as a whole. No page numbers are available in our copy. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • The decline in JH can stimulate E93.

    “and the decline in JH can stimulate E93.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [64]

  • Proper broad induction in Drosophila wing discs at pupariation requires Kr-h1, which prevents precocious expression of E93 and suppression of broad expression.

    “For example, proper broad induction in Drosophila wing discs at pupariation requires Kr-h1, which prevents precocious expression of E93 and suppression of broad expression [64].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [64]

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Authors
Ureña, E., Chafino, S., Manjón, C., Franch-Marro, X., & Martín, D.
Affiliations
Universitat Pompeu Fabra (ES)
ORCID
Ureña, Enric
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2016-05-02
Volume
12
Issue
5
Pages
e1006020
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1006020
PMC
PMC4852927
OpenAlex
W2347184359
Cited by
129
References
1
Citations by year
2026: 18 · 2025: 14 · 2024: 13 · 2023: 9 · 2022: 12 · 2021: 12 · 2020: 16 · 2019: 13 · 2018: 13 · 2017: 8 · 2016: 1
FWCI
6.56
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
Ministerio de Economía y Competitividad (BFU2009-10571, BFU2009-08748, CGL2014-55786-P)
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
holometabolism, pupal stage, insect metamorphosis, Krüppel homolog 1, E93, Broad-Complex, Tribolium castaneum, Blattella germanica, hemimetabolism, larval to adult transition, transcription factor repression
MeSH terms
BTB-POZ Domain, Animals, Larva, Metamorphosis, Biological, Phylogeny, Pupa, Transcription Factors, Tribolium, Gene Expression Regulation, Developmental, Evolution, Molecular, Blattellidae, Drosophila Proteins, RNA Interference, Kruppel-Like Transcription Factors

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