Abstract
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.
Highlights
Subcellular organelles are transferred to the developing oocyte from surrounding sister germ cells in vertebrates such as mouse and invertebrates such as Drosophila and are important for their differentiation
Mitochondria were present in cortical regions of the blastoderm embryo (Fig. 1B,D,G) and they distributed around nuclei on arrival at the cortex in NC10 of the syncytial blastoderm (Fig. 1E)
This increase in the depth of enrichment of mitochondria across syncytial cycles correlates with previous observations of increase in metaphase furrow lengths[27] and increased tubulin spread in depth from the cortex across syncytial division cycles suggesting that the distribution is likely to be regulated by cytoskeletal organization and transport differences across cycles and may be important for local supply of ATP
Summary
Subcellular organelles are transferred to the developing oocyte from surrounding sister germ cells in vertebrates such as mouse and invertebrates such as Drosophila and are important for their differentiation. Mitochondria occur in a small, globular state and in limited numbers in stem cells and early embryos. They are transformed from a nascent immature structure in stem cells to a more tubular, higher ATP generating architecture during differentiation[4]. Mutations in the mitochondrial Kinesin linker protein, Miro lead to increased accumulation of mitochondria in cell body and motor neuron diseases[22]. We find that mitochondria do not move between neighbouring syncytial cells and are distributed to daughter syncytial cells Their density along the apico-basal axis in the syncytial Drosophila embryo depends upon appropriate microtubule based transport and their functionality is important for generation of local ATP, which drives the syncytial division cycles of the blastoderm embryo
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