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Maternal AP determinants in the Drosophila oocyte and embryo

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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 This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Gene Expression and Transcriptional Hierarchies > Quantitative Methods and Models Early Embryonic Development > Development to the Basic Body Plan
Gene expression patterns in the Drosophila blastoderm embryo. The expression of different genes along the anterior–posterior and dorsal–ventral axes is shown in different colors. These patterns represent the fatemap of the embryo, with an illustrative 2D map generated from the 3D embryo. The genes shown are: pair‐rule genes even‐skipped (eve) and fushi tarazu (ftz), gap genes hunchback (hb) and tailless (tll), and the ventral‐specific gene snail (sna). (Reprinted with permission from Ref . Copyright 2009 IEEE)
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Distinct scaling mechanisms of Bcd in contrast with bcd gene dosage perturbation. Shown are schematic diagrams of two scaling mechanisms of Bcd (a and b) in contrast with the effect of genetic perturbation of bcd gene dosage in the mother. In panels (a) and (b), the Bcd concentration profiles are from large (red) or small (blue) embryos and are shown as a function of relative anterior–posterior (AP) position ξ. Panel (a) represents an amplitude‐based Bcd scaling mechanism, while panel (b) represents length‐scale‐based scaling mechanism (see text). For reference, panel (c) shows the effect of genetically altering maternal bcd gene dosage on the Bcd gradient profile (red and blue denote high and low bcd dosages, respectively). Bcd concentration is expressed on log scale. In panel (a), the critical position ξC is also shown (see text).
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Dynamic movements of gap gene expression boundaries in the embryo. Shown are the mean expression profiles of different gap genes along the anterior–posterior (AP) length of a group of embryos at a time during nc14 when their mRNA products reach peak levels (a). The colors for the genes shown are: red, hb; magenta, giant (gt); green, Kr; cyan, knirps (kni); blue, otd; black, tll. Panel (b) shows how these boundaries move as a function of time. The times shown are nc13 and 9 time classes (T1–T9) of nc14. Here, the anterior and posterior boundaries of an expression domain are denoted by left‐ and right‐pointing arrows, respectively. (Reprinted with permission from Ref . Copyright 2015 Nature Publishing Group)
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Patterns of gene expression in proportion to embryo length. Shown are scatter plots of the anterior–posterior (AP) positions of expression boundaries of the pair‐rule gene eve (colored) and the gap gene hb (black) against embryo length (a and b). ‘Large’ and ‘small’ refer to embryos from two inbred lines that lay large or small eggs, respectively. In panel (a), the boundary positions (x) and embryo lengths (L) are expressed as absolute values (µm). In panel (b), they are expressed as normalized values ξ and L/〈L〉, respectively. The fitted slope in panel (b) for each boundary represents its scaling coefficient S. S = 0 denotes perfect scaling, whereas S > 0 or < 0 denotes over‐ and under‐scaling, respectively. Panel (c) shows the scaling coefficient S for each of the measured boundaries along the AP axis. (Reprinted with permission from Ref . Copyright 2015 Nature Publishing Group)
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Cascade of gene expression regulation along the anterior–posterior (AP) axis of the embryo. Shown are schematic illustrations of maternal protein gradients (top panel) and patterns of zygotic gene expression in the embryo. The zygotic genes include gap, pair‐rule, and segment polarity genes as shown. Here, the process of forming these parasegments is depicted as distinct steps with initial inputs from maternal determinants. Parasegments are based on gene expression patterns in embryos and they correspond to the adult segments (with an offset in registration). (Reprinted with permission from Ref . Copyright 2005 Nature Publishing Group)
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Key events and development stages of oogenesis. Shown are a Drosophila ovariole (a) and the durations for individual stages of oogenesis (b). In panel (a), a germarium (G) and progressively older egg chambers are shown. The numbers shown refer to oogenesis stages. Within the germarium (shown at the top), germline stem cells (GSCs; green) are juxtaposed to cap cells, the major cellular component of the somatic niche (yellow), and a subset of escort cells (gray). GSCs divide to form daughter cells, which divide four more times to form 16‐cell germline cysts (green), each being composed of 15 nurse cells (nc) and an oocyte (oo). Follicle cells (fc, red) encapsulate each cyst, forming a follicle (or egg chamber) that pinches off from the germarium and progresses through 14 morphologically distinct stages. In panel (b), the stages of oogenesis and their durations are shown at the top. The three different cell cycle regimens for follicle cells correspond to early, middle, and late oogenesis, respectively (see text). Nurse cell endoreplication and vitellogenesis are also shown in this panel. (Panel a: Reprinted from permission from Ref . Copyright 2015 Elsevier)
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Localization of maternal mRNA in the developing oocyte. Shown are movements of gurken (grk) and bcd mRNAs within the nurse cells (a), microtubule‐dependent transport of grk, bcd, and oskar (osk) mRNAs within the oocyte during mid‐oogenesis (b), and localization of bcd and nos mRNAs during late oogenesis (c). Different mRNAs and the relevant cellular components are color coded as indicated by the key shown at the bottom. In panel (a), straight arrows indicate directed movements of grk and bcd mRNAs on microtubules, whereas squiggly arrows indicate movements of grk mRNA with cytoplasmic flows. In panel (b), the oocyte nucleus is shown in light blue; colored arrows show the directions of mRNA movements. In panel (c), the contraction of nurse cells for dumping is indicated by gray arrows pointing inward, and the entry of bcd and nos mRNAs into the oocyte is indicated by the heavy straight arrows. Small green arrows depict transport of bcd mRNA on anterior microtubules, and curved dark green arrows depict diffusion of nos mRNA facilitated by ooplasmic streaming. (Reprinted with permission from Ref . Copyright 2009 The Company of Biologists Ltd.)
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Gene Expression and Transcriptional Hierarchies > Quantitative Methods and Models
Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing
Early Embryonic Development > Development to the Basic Body Plan