Maternal AP determinants in the Drosophila oocyte and embryo

Abstract

An animal embryo cannot initiate its journey of forming a new life on its own. It must rely on maternally provided resources and inputs to kick-start its developmental process. In Drosophila, the initial polarities of the embryo along both the anterior-posterior (AP) and dorsal-ventral (DV) axes are also specified by maternal determinants. Over the past several decades, genetic and molecular studies have identified and characterized such determinants, as well as the zygotic genetic regulatory networks that control patterning in the early embryo. Extensive studies of oogenesis have also led to a detailed knowledge of the cellular and molecular interactions that control the formation of a mature egg. Despite these efforts, oogenesis and embryogenesis have been studied largely as separate problems, except for qualitative aspects with regard to maternal regulation of the asymmetric localization of maternal determinants. Can oogenesis and embryogenesis be viewed from a unified perspective at a quantitative level, and can that improve our understanding of how robust embryonic patterning is achieved? Here, we discuss the basic knowledge of the regulatory mechanisms controlling oogenesis and embryonic patterning along the AP axis. We explore properties of the maternal Bicoid gradient in relation to embryo size in search for a unified framework for robust AP patterning. WIREs Dev Biol 2016, 5:562-581. doi: 10.1002/wdev.235 For further resources related to this article, please visit the WIREs website.

Independence of 3D chromatin conformation and gene regulation during Drosophila dorsoventral patterning

“…We and others have previously shown that chromatin organisation in Drosophila is established at nc14, coincident with ZGA (Hug et al, 2017;Ogiyama et al, 2018). While a small number of genes are zygotically expressed prior to the major wave of ZGA (Lott et al, 2011), maternally provided cues are responsible for establishing the major anterior-posterior and dorsoventral axes (Ma et al, 2016;Stein and Stevens, 2014). Therefore, by ZGA, cells in different regions of the embryo contain different developmental transcription factors, have different patterns of chromatin accessibility (Cusanovich et al, 2018), and are primed to express different genes.…”

Time to move on: Modeling transcription dynamics during an embryonic transition away from maternal control

“…21,32,33 The quick shutdown of hb transcription (<3 min into the nc14 interphase as estimated in our model; Table 1) provides a mechanism for hb P2 promoter to respond to the Bcd gradient as its primary input in forming an expression boundary in a Bcd concentration-dependent manner. 3 This relatively reliable input-output relationship between Bcd and hb transcription has been suggested to be important for AP pattern formation in a manner that is robust to embryo size variations. 3,[34][35][36][37][38] The estimated parameters in our current study are consistent with existing estimates and yield new insights into transcription regulatory mechanism during embryonic development.…”

“…3 This relatively reliable input-output relationship between Bcd and hb transcription has been suggested to be important for AP pattern formation in a manner that is robust to embryo size variations. 3,[34][35][36][37][38] The estimated parameters in our current study are consistent with existing estimates and yield new insights into transcription regulatory mechanism during embryonic development. For example, our estimated k on (prior to shutdown) and k off are both fast, as those at earlier nuclear cycles reported by Xu et al, 15 despite the significant differences in our experimental and modeling approaches.…”

“…[1][2][3][4] In Drosophila, a landmark of this transition period is the mid-blastula transition (MBT) at nuclear cycle (nc) 14, during which numerous molecular and cellular events take place concurrently. For example, many zygotically expressed genes become transcriptionally active for the first time at nc14, whereas other genes that became transcriptionally active prior to this time now experience a shutdown phase.…”

“…[5][6][7][8] Our own analysis of published datasets 9 identified over 190 zygotically active genes that exhibit characteristics of becoming shut down during nc14. 1 The hunchback (hb) gene, which is required for thoracic development and activated by the maternal morphogenetic protein Bicoid (Bcd), 3,4,10 , is among these genes. 1 The shutdown of hb transcription during nc14 is a property that is associated with the MBT, and postponing the MBT to nc15 in haploid embryos leads to a corresponding postponement of hb shutdown.…”