Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

Kristina Tarsis, Tsvia Gildor, Miri Morgulis, Smadar Ben-Tabou de-Leon

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Understanding how gene regulatory networks (GRNs) control developmental progression is a key to the mechanistic understanding of morphogenesis. The sea urchin larval skeletogenesis provides an excellent platform to tackle this question. In the early stages of sea urchin skeletogenesis, skeletogenic genes are uniformly expressed in the skeletogenic lineage. Yet, during skeletal elongation, skeletogenic genes are expressed in distinct spatial sub-domains. The regulation of differential gene expression during late skeletogenesis is not well understood. Results: Here we reveal the dynamic expression of the skeletogenic regulatory genes that define a specific regulatory state for each pair of skeletal rods, in the sea urchin Paracentrotus lividus. The vascular endothelial growth factor (VEGF) signaling, essential for skeleton formation, specifically controls the migration of cells that form the postoral and distal anterolateral skeletogenic rods. VEGF signaling also controls the expression of regulatory genes in cells at the tips of the postoral rods, including the transcription factors Pitx1 and MyoD1. Pitx1 activity is required for normal skeletal elongation and for the expression of some of VEGF target genes. Conclusions: Our study illuminates the fine-tuning of the regulatory system during the transition from early to late skeletogenesis that gives rise to rod-specific regulatory states.

Original languageEnglish
JournalDevelopmental Dynamics
DOIs
StateAccepted/In press - 2022

Bibliographical note

Funding Information:
We thank David Ben‐Ezra and Michael Kantorovitz for their help with sea urchin handling. We thank Majed Layous for insightful discussions and for his help with the imaging. We thank Charles Ettensohn for the gift of the 6a9 antibody produced in his lab. This study is supported by Israel Science Foundation grant #211/20 to Smadar Ben‐Tabou de‐Leon and Israeli Scholarship Education Foundation (ISEF) to Miri Morgulis.

Publisher Copyright:
© 2022 The Authors. Developmental Dynamics published by Wiley Periodicals LLC on behalf of American Association for Anatomy.

Keywords

  • biomineralization
  • gene regulatory networks
  • MyoD
  • Pitx
  • sea urchin
  • skeletogenesis
  • vascular endothelial growth factor

ASJC Scopus subject areas

  • Developmental Biology

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