Differentially-dimensioned furrow formation by zygotic gene expression and the MBT

• Published in: PLoS genetics 2018-01, Vol.14 (1), p.e1007174-e1007174
• Main Authors: Xie, Yi, Blankenship, J Todd
• Format: Article
• Language: English
• Subjects: Animals; Animals, Genetically Modified; Biology; Biology and Life Sciences; Blastula - cytology; Blastula - embryology; Cell cycle; Cell division; Cell Division - genetics; Cell Membrane - genetics; Cell Membrane - metabolism; Cell membranes; Chromosomes; Drosophila; Drosophila melanogaster; Drosophila melanogaster - embryology; Drosophila melanogaster - genetics; Embryo, Nonmammalian; Embryonic Development - physiology; Female; Gene expression; Gene Expression Regulation, Developmental; Genetics; Genomes; Giant Cells - cytology; Giant Cells - metabolism; Giant Cells - ultrastructure; Insects; Male; Morphogenesis; Morphogenesis - genetics; Observations; Physiological aspects; Plasma; Research and Analysis Methods; Transcription; Zygote - metabolism; Zygote - physiology
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1007174

Despite extensive work on the mechanisms that generate plasma membrane furrows, understanding how cells are able to dynamically regulate furrow dimensions is an unresolved question. Here, we present an in-depth characterization of furrow behaviors and their regulation in vivo during early Drosophila morphogenesis. We show that the deepening in furrow dimensions with successive nuclear cycles is largely due to the introduction of a new, rapid ingression phase (Ingression II). Blocking the midblastula transition (MBT) by suppressing zygotic transcription through pharmacological or genetic means causes the absence of Ingression II, and consequently reduces furrow dimensions. The analysis of compound chromosomes that produce chromosomal aneuploidies suggests that multiple loci on the X, II, and III chromosomes contribute to the production of differentially-dimensioned furrows, and we track the X-chromosomal contribution to furrow lengthening to the nullo gene product. We further show that checkpoint proteins are required for furrow lengthening; however, mitotic phases of the cell cycle are not strictly deterministic for furrow dimensions, as a decoupling of mitotic phases with periods of active ingression occurs as syncytial furrow cycles progress. Finally, we examined the turnover of maternal gene products and find that this is a minor contributor to the developmental regulation of furrow morphologies. Our results suggest that cellularization dynamics during cycle 14 are a continuation of dynamics established during the syncytial cycles and provide a more nuanced view of developmental- and MBT-driven morphogenesis.