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

Yi Xie,J Todd Blankenship,Claude Desplan

doi:10.1371/journal.pgen.1007174

Abstract

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.

Highlights

We show that a combination of higher ingression rates and longer duration phases drive changes in furrow dimensions through the introduction of a new ingression phase
Furrow ingression is an obligatory step in animal cells during cell division, and is a critical mechanism that underlies the ability of animal cells to divide and provide new cells for tissue homeostasis and development
We find that a new ingression phase (Ingression II) follows the stabilization phase of cycles 12 and 13 and helps to drive the four-fold lengthening of furrows that occurs between cycles 10 to 13

Summary

Introduction

Furrow ingression is an obligatory step in animal cells during cell division, and is a critical mechanism that underlies the ability of animal cells to divide and provide new cells for tissue homeostasis and development. The first nine rounds of nuclear divisions occur deep in the yolk, with nuclei migrating to the periphery of the embryo at cycle 10. At this point, the density of nuclei and their arrangement in a common cortical plane requires four cycles of transient plasma membrane furrow formation (syncytial division cycles 10–13) to adequately partition mitotic figures and ensure genomic stability [3,4,5]. At cycle 14 (cellularization), plasma membrane furrows permanently encapsulate individual nuclei, resulting in a monolayered epithelium [6,7,8]. It is in these early furrow-forming processes that rapid, morphogenetic changes occur in furrow structure and dimensions. As cycles 10–14 proceed, the furrows are sequentially narrower and more regular, and furrows extend deeper basally, generating greater nuclear separation

Methods

Results

Discussion

Conclusion