Evidence map›Paper›PMID 27135810›Full record

ArticlePLoS genetics2016

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

Enric Ureña, Silvia Chafino, Cristina Manjón, Xavier Franch-Marro, David Martín

Open access · goldAbstract read
In one paragraph

Article in PLoS genetics, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 57 papers.

0numbers the graph read from it
0cells of the map it votes in
57citing papers in PubMed
10.8field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

57 citing papers in PubMed, 121 citations in OpenAlex.

  1. Article
  2. Evolutionary dynamics of the arthropod molting machinery.Molecular biology and evolution · 2026
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  10. 20E-inducedProceedings of the National Academy of Sciences of the United States of America · 2025
    Article
  11. Article
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  14. Article
  15. E93 controls adult differentiation by repressingProceedings of the National Academy of Sciences of the United States of America · 2024
    Article
  16. Chronologically inappropriate morphogenesis (Proceedings of the National Academy of Sciences of the United States of America · 2024
    Article
  17. Article
  18. Article
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

5 authors at 2 institutions in 1 country.

Enric UreñaInstitute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
Silvia ChafinoInstitute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
Cristina ManjónInstitute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
Xavier Franch-MarroInstitute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
David MartínInstitute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
Pompeu Fabra University · ESInstitut de Biologia Evolutiva · ES

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

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.

Indexed as

Evolution, MolecularPhylogenyAnimalsBlattellidaeBTB-POZ DomainDrosophila ProteinsGene Expression Regulation, DevelopmentalKruppel-Like Transcription FactorsLarvaMetamorphosis, BiologicalPupaRNA InterferenceTranscription FactorsTriboliumDrosophila ProteinsEip93F protein, DrosophilaKr-h1 protein, DrosophilaKruppel-Like Transcription FactorsTranscription Factors

Identifiers

PMID27135810
PMCPMC4852927
OpenAlexW2347184359

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.