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Cited by 11Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationInvertebrate Immune Response Mechanisms

TGFß/activin-dependent activation of Torso controls the timing of the metamorphic transition in the red flour beetle Tribolium castaneum

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Chafino, Sílvia, Salvia, Roser, Cruz, Josefa, Martín, David, Franch-Marro, Xavier·2023·PLOS Genetics
DOI 10.1371/journal.pgen.1010897PMC PMC10703416
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Abstract

Understanding the mechanisms governing body size attainment during animal development is of paramount importance in biology. In insects, a crucial phase in determining body size occurs at the larva-pupa transition, marking the end of the larval growth period. Central to this process is the attainment of the threshold size (TS), a critical developmental checkpoint that must be reached before the larva can undergo metamorphosis. However, the intricate molecular mechanisms by which the TS orchestrates this transition remain poor understood. In this study, we investigate the role of the interaction between the Torso and TGFß/activin signaling pathways in regulating metamorphic timing in the red flour beetle, Tribolium castaneum . Our results show that Torso signaling is required specifically during the last larval instar and that its activation is mediated not only by the prothoracicotropic hormone (Tc-Ptth) but also by Trunk (Tc-Trk), another ligand of the Tc-Torso receptor. Interestingly, we show that while Tc-Torso activation by Tc-Ptth determines the onset of metamorphosis, Tc-Trk promotes growth during the last larval stage. In addition, we found that the expression of Tc-torso correlates with the attainment of the TS and the decay of juvenile hormone (JH) levels, at the onset of the last larval instar. Notably, our data reveal that activation of TGFß/activin signaling pathway at the TS is responsible for repressing the JH synthesis and inducing Tc-torso expression, initiating metamorphosis. Altogether, these findings shed light on the pivotal involvement of the Ptth/Trunk/Torso and TGFß/activin signaling pathways as critical regulatory components orchestrating the TS-driven metamorphic initiation, offering valuable insights into the mechanisms underlying body size determination in insects.

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  • Elevated myoglianin levels seen when juveniles surpass their threshold weight act on both the corpora allata and the prothoracic glands.

    “The elevated myoglianin levels seen when juveniles surpass their threshold weight act on both the corpora allata [25,8,22] and the prothoracic glands (e.g. [25]).”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [8]

    The Discussion sections on JH biosynthesis and PG function report that myoglianin-dependent signaling reduces juvenile hormone production and also affects ecdysone production in last-stage Tribolium larvae. They suggest that myoglianin rises with muscle growth toward a threshold, but do not establish that elevated myoglianin acts directly on both glands; the paper says the PG-specific effects require further study. Page numbers were not available in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • The JH decline evoked by crossing the threshold weight is sufficient to induce E93, but some other signal is needed for broad induction.

    “Apparently, the JH decline evoked by crossing the threshold weight is sufficient to induce E93, but some other signal is needed for broad induction.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [8]

    The Discussion (‘Up-regulation of Tc-torso depends on the TS checkpoint’; page unavailable) says that the JH decline at threshold size enables Tc-E93 up-regulation. The Results (‘The TGFß/Activin signaling pathway facilitates the metamorphic transition by regulating ecdysone levels’; page unavailable) show that suppressing JH alone did not promote metamorphosis and identify ecdysone as additionally required for the developmental transition. They do not establish that another signal is specifically needed for broad E93 induction. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • The best candidates for the signal needed for broad induction are myoglianin and/or ecdysteroids.

    “The best candidates are myoglianin and/or ecdysteroids [9,8].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [8]

    The Discussion (‘TGFβ/Activin signaling regulates JH biosynthesis’; ‘Up-regulation of Tc-torso depends on the TS checkpoint’; pages not supplied) links myoglianin signaling to declining juvenile hormone and says that decline enables up-regulation of Tc-Br-C (Broad-Complex). The paper also links myoglianin to ecdysone production, but it does not identify ecdysteroids as a signal needed for Broad induction or call these the ‘best candidates.’ (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • Myoglianin and/or ecdysteroids cause broad expression.

    “Myoglianin and/or ecdysteroids cause broad expression, and the decline in JH can stimulate E93.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [8]

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Cited by

Sorted by citations

Authors
Chafino, S., Salvia, R., Cruz, J., Martín, D., & Franch-Marro, X.
Affiliations
Universitat Pompeu Fabra (ES)
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2023-11-27
Volume
19
Issue
11
Pages
e1010897
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1010897
PMC
PMC10703416
OpenAlex
W4389042278
Cited by
11
References
1
Citations by year
2026: 4 · 2025: 4 · 2024: 3
FWCI
1.33
Type
journal article
Language
en
Update notices
new_version (2023-12-07)
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)
Funders
  • Ministerio de Ciencia e Innovación (PGC2018-098427-B-I00, PID2021-125661NB-100, FJC2019-041549-I)
  • Direcció General de Recerca, Generalitat de Catalunya (2017-SGR 1030, 2021-SGR 0417)
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 › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
Keywords
TGF-beta/activin signaling, metamorphosis timing, threshold size, Tribolium castaneum, prothoracicotropic hormone, juvenile hormone, last instar larva, insect development
MeSH terms
Animals, Coleoptera, Juvenile Hormones, Larva, Metamorphosis, Biological, Tribolium, Gene Expression Regulation, Developmental, Insect Proteins, Receptor Protein-Tyrosine Kinases, Torso

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