Temperature sensitivity of Notch signaling underlies species-specific developmental plasticity and robustness in amniote brains

Tadashi Nomura,Katsuhiko Ono,Hitoshi Gotoh,Masato Umeda,Kohjiro Nagao,Ryo Shirai

doi:10.1038/s41467-021-27707-5

Abstract

Ambient temperature significantly affects developmental timing in animals. The temperature sensitivity of embryogenesis is generally believed to be a consequence of the thermal dependency of cellular metabolism. However, the adaptive molecular mechanisms that respond to variations in temperature remain unclear. Here, we report species-specific thermal sensitivity of Notch signaling in the developing amniote brain. Transient hypothermic conditions increase canonical Notch activity and reduce neurogenesis in chick neural progenitors. Increased biosynthesis of phosphatidylethanolamine, a major glycerophospholipid components of the plasma membrane, mediates hypothermia-induced Notch activation. Furthermore, the species-specific thermal dependency of Notch signaling is associated with developmental robustness to altered Notch signaling. Our results reveal unique regulatory mechanisms for temperature-dependent neurogenic potentials that underlie developmental and evolutionary adaptations to a range of ambient temperatures in amniotes.

Highlights

Ambient temperature significantly affects developmental timing in animals
We found that temperature-dependent changes in the biosynthesis and cell surface exposure of phosphatidylethanolamine (PE), a major membrane glycerophospholipid, contribute to the thermal responsiveness of Notch signaling in chick neural progenitors
We report temperature-dependent changes in neurogenesis in developing reptilian and avian brains, which are mediated by the thermal sensitivity of Notch signaling

Summary

Introduction

Ambient temperature significantly affects developmental timing in animals. The temperature sensitivity of embryogenesis is generally believed to be a consequence of the thermal dependency of cellular metabolism. We report species-specific thermal sensitivity of Notch signaling in the developing amniote brain. Our results reveal unique regulatory mechanisms for temperature-dependent neurogenic potentials that underlie developmental and evolutionary adaptations to a range of ambient temperatures in amniotes. We report species-specific thermal dependency of Notch signaling in the neural progenitors of developing amniote brains. Transient hypothermic incubation significantly increases canonical Notch activity in chick neural progenitors, which is mediated by ligand ubiquitylation and internalization. We found that temperature-dependent changes in the biosynthesis and cell surface exposure of phosphatidylethanolamine (PE), a major membrane glycerophospholipid, contribute to the thermal responsiveness of Notch signaling in chick neural progenitors. Our results revealed that the temperature-dependent regulation of Notch signaling is tightly coupled with species-specific neurogenic programs, which underlies multiple levels of developmental canalization in response to environmental changes during amniote evolution

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