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- Title
TGFß/activin-dependent activation of Torso controls the timing of the metamorphic transition in the red flour beetle Tribolium castaneum.
- Authors
Chafino, Sílvia; Salvia, Roser; Cruz, Josefa; Martín, David; Franch-Marro, Xavier
- 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 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. Author summary: Understanding the mechanisms that determine an animal's final body size is a fundamental question in biology. In animals, the majority of growth takes place during the juvenile stage, with adult size being established as they transition into adulthood. Hormones play a pivotal role in orchestrating this complex process. In the case of insects, the metamorphic transition is induced by the interplay between the steroid hormone ecdysone and the sesquiterpenoid juvenile hormone (JH). Our research delved into the roles of the Torso and TGFß/Activin signaling pathways in regulating ecdysone and JH biosynthesis. Remarkably, we discovered that in contrast to other insects, the Torso pathway in Tribolium is activated by not one, but two ligands: the prothoracicotropic hormone that regulates ecdysone production and Trunk that promotes growth in the last larval stage. Additionally, our investigations unveiled the dual functionality of the TGFß/Activin signaling pathway in the initiation of metamorphosis. Firstly, it lowers JH levels, setting in motion the genetic changes required for the metamorphic transition, including the upregulation of Torso and, secondly, facilitating ecdysone production. In summary, our research sheds light on the intricate regulatory network governing metamorphic timing and body size in insects.
- Subjects
RED flour beetle; LARVAE; ANIMAL development; INSECT size; TORSO; JUVENILE hormones; PUPAE
- Publication
PLoS Genetics, 2023, Vol 19, Issue 11, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010897