Mitochondria are inherited maternally as globular and immature organelles in metazoan embryos. We have used the Drosophila blastoderm embryo to characterize their morphology, distribution and functions in embryogenesis. We find that mitochondria are relatively small, dispersed and distinctly distributed along the apico-basal axis in proximity to microtubules by motor protein transport. Live imaging, photobleaching and photoactivation analyses of mitochondrially targeted GFP show that they are mobile in the apico-basal axis along microtubules and are immobile in the lateral plane thereby associating with one syncytial cell. Photoactivated mitochondria distribute equally to daughter cells across the division cycles. ATP depletion by pharmacological and genetic inhibition of the mitochondrial electron transport chain (ETC) activates AMPK and decreases syncytial metaphase furrow extension. In summary, we show that small and dispersed mitochondria of the Drosophila blastoderm embryo localize by microtubule transport and provide ATP locally for the fast syncytial division cycles. Our study opens the possibility of use of Drosophila embryogenesis as a model system to study the impact of maternal mutations in mitochondrial morphology and metabolism on embryo patterning and differentiation.

The dynamics, distribution and activity of subcellular organelles are integral to regulating cell shape changes during various physiological processes such as epithelial cell formation, cell migration and morphogenesis. Mitochondria are famously known as the powerhouse of the cell and play an important role in buffering calcium, releasing reactive oxygen species and key metabolites for various activities in a eukaryotic cell. Mitochondrial dynamics and morphology changes regulate these functions and their regulation is, in turn, crucial for various morphogenetic processes. In this review, we evaluate recent literature which highlights the role of mitochondrial morphology and activity during cell shape changes in epithelial cell formation, cell division, cell migration and tissue morphogenesis during organism development and in disease. In general, we find that mitochondrial shape is regulated for their distribution or translocation to the sites of active cell shape dynamics or morphogenesis. Often, key metabolites released locally and molecules buffered by mitochondria play crucial roles in regulating signaling pathways that motivate changes in cell shape, mitochondrial shape and mitochondrial activity. We conclude that mechanistic analysis of interactions between mitochondrial morphology, activity, signaling pathways and cell shape changes across the various cell and animal-based model systems holds the key to deciphering the common principles for this interaction.

Mitochondria are maternally inherited in many organisms. Mitochondrial morphology and activity regulation is essential for cell survival, differentiation and migration. An analysis of mitochondrial dynamics and function in morphogenetic events in early metazoan embryogenesis has not been carried out. In our study we find a crucial role of mitochondrial morphology regulation in cell formation in Drosophila embryogenesis. We find that mitochondria are small, fragmented and translocate apically on microtubules and distribute progressively along the cell length during cellularization. Embryos mutant for mitochondrial fission protein, Drp1, die in embryogenesis and show an accumulation of clustered mitochondria on the basal side in cellularization. Additionally, Drp1 mutant embryos contain lower levels of reactive oxygen species (ROS). ROS depletion has been previously shown to decrease Myosin II activity. Drp1 loss also leads to Myosin II depletion at the membrane furrow thereby resulting in decreased cell height and larger contractile ring area in cellularization similar to Myosin II mutants. The mitochondrial morphology and cellularization defects in Drp1 mutants are suppressed by reducing mitochondrial fusion and increasing cytoplasmic ROS in superoxide dismutase mutants. Our data show a key role for mitochondrial morphology and activity in supporting the morphogenetic events that drive cellularization in Drosophila embryos. [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text]

The blastocyst is a conserved stage and distinct milestone in the development of the mammalian embryo. Blastocyst stage embryos comprise three cell lineages which arise through two sequential binary cell fate specification steps. In the first, extra-embryonic trophectoderm (TE) cells segregate from inner cell mass (ICM) cells. Subsequently, ICM cells acquire a pluripotent epiblast (Epi) or extra-embryonic primitive endoderm (PrE, also referred to as hypoblast) identity. In the mouse, nascent Epi and PrE cells emerge in a salt-and-pepper distribution in the early blastocyst and are subsequently sorted into adjacent tissue layers by the late blastocyst stage. Epi cells cluster at the interior of the ICM, while PrE cells are positioned on its surface interfacing the blastocyst cavity, where they display apicobasal polarity. As the embryo implants into the maternal uterus, cells at the periphery of the PrE epithelium, at the intersection with the TE, break away and migrate along the TE as they mature into parietal endoderm (ParE). PrE cells remaining in association with the Epi mature into visceral endoderm. In this review, we discuss our current understanding of the PrE from its specification to its maturation. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.

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