Mitochondria in Embryogenesis: An Organellogenesis Perspective.

Yoan Arribat,Philipp Gut,Mélanie Gachet,Dogan Grepper,Francesca Amati,Joy Richard,Sylviane Lagarrigue

doi:10.3389/fcell.2019.00282

Yoan Arribat, Philipp Gut + Show 5 more

Open Access

https://doi.org/10.3389/fcell.2019.00282

Copy DOI

Abstract

Organogenesis is well characterized in vertebrates. However, the anatomical and functional development of intracellular compartments during this phase of development remains unknown. Taking an organellogenesis point of view, we characterize the spatiotemporal adaptations of the mitochondrial network during zebrafish embryogenesis. Using state of the art microscopy approaches, we find that mitochondrial network follows three distinct distribution patterns during embryonic development. Despite of this constant morphological change of the mitochondrial network, electron transport chain supercomplexes occur at early stages of embryonic development and conserve a stable organization throughout development. The remodeling of the mitochondrial network and the conservation of its structural components go hand-in-hand with somite maturation; for example, genetic disruption of myoblast fusion impairs mitochondrial network maturation. Reciprocally, mitochondria quality represents a key factor to determine embryonic progression. Alteration of mitochondrial polarization and electron transport chain halts embryonic development in a reversible manner suggesting developmental checkpoints that depend on mitochondrial integrity. Our findings establish the subtle dialogue and co-dependence between organogenesis and mitochondria in early vertebrate development. They also suggest the importance of adopting subcellular perspectives to understand organelle-organ communications during embryogenesis.

Highlights

Embryogenesis follows an evolutionary conserved stereotypical sequence of events leading to the formation of functional tissues and organs
We expressed a GFP-tagged transgene of zebrafish tomm20, which encodes an outer mitochondrial membrane protein, under the control of muscle specific α actin promotor (Figure 1A). This model allows the observation of the mitochondrial network reorganization between the beginning of somitogenesis (11 h post-fertilization; hpf) and the end of embryogenesis (48 hpf), which is concomitant with the maturation of muscle fibers (Figure 1B and Supplementary Figure S1)
Our findings reveal the existence of three distinct mitochondrial patterns of distribution during somitogenesis

Summary

Introduction

Embryogenesis follows an evolutionary conserved stereotypical sequence of events leading to the formation of functional tissues and organs. Signaling pathways involved in these processes have been extensively characterized, and include the morphogenes Sonic Hedgehog (Shh) and Bone Morphogenic Protein (BMP), among many others (Maurya et al, 2011). Invertebrate development shares commonalities with vertebrates, neuromuscular structuration in the latter follows a unique patterning during early developmental stages (Lewis et al, 1999; Lewis, 2006). Mitochondria in Embryogenesis common steps in embryonic and adult myogenesis, including myoblasts proliferation, fusion in multinucleated cells and final maturation into myofibers (Paululat et al, 1999). The mechanisms conducting cell fate upon embryogenesis have been extensively described, but one of the major challenges facing the field is to understand embryogenesis from the organelles point of view, and regarding mitochondria

Methods

Results

Conclusion