Maternal-to-Zygotic Transition (eBook)

Howard Lipshitz (Herausgeber)

eBook Download: PDF | EPUB

2015 | 1. Auflage
430 Seiten
Elsevier Science (Verlag)
978-0-12-416612-7 (ISBN)

Infos

The Maternal-to-Zygotic Transition provides users with an expert accounting of the mechanisms and functions of this transition in a range of animal and plant models. The book provides critical information on how maternal gene products program the initial development of all animal and plant embryos, then undergoing a series of events, termed the maternal-to-zygotic transition, during which maternal products are cleared and zygotic genome activation takes over the developmental control. - Maternal gene products program the initial development of all animal and plant embryos - These then undergo a series of events, termed the maternal-to-zygotic transition, during which maternal products are cleared and zygotic genome activation takes over developmental control - In this book, experts provide their insights into the mechanisms and functions of this transition in a range of animal and plant models.

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Chapter One

The Maternal-to-Zygotic Transition in C. elegans

Scott Robertson1; Rueyling Lin    Department of Molecular Biology, UT Southwestern Medical Center, Dallas, Texas, USA
1 Corresponding author: email address: [e-mail]

Abstract

In Caenorhabditis elegans, the first zygotic transcription can be detected in the 4-cell stage C. elegans embryo, a little over 2 h after fertilization. However, early development until the onset of gastrulation at approximately the 28-cell stage takes place normally even in the absence of zygotic transcription. Therefore, posttranslational and posttranscriptional regulation of the maternal proteins and mRNAs, respectively, that are loaded into the developing oocytes is sufficient to direct development prior to gastrulation. Protein phosphorylation is extensively used throughout the C. elegans maternal-to-zygotic transition (MZT): (1) for maternal protein activation, (2) for coordination of the meiotic and mitotic cell cycle, (3) to mark specific proteins for degradation, and/or (4) to switch the biochemical activity of specific proteins. Maternally loaded mRNAs are regulated primarily by a set of maternal RNA-binding proteins (RBPs), each of which binds to sometimes overlapping target sequences within the mRNA 3′UTRs and either promotes or inhibits translation. Most maternal transcripts are uniformly distributed throughout the embryo but specific transcripts are translated only in certain blastomeres. This control is achieved by the asymmetric distribution of the maternal RBPs, such that the blastomere-specific constellation of RBPs present, and their relative levels, determines the translational readout for their target transcripts. In certain well-studied cases, such as the specification of the sole endodermal precursor in the 8-cell embryo, the maternal transcripts and proteins along with their directly targeted zygotic genes have been identified.

Keywords

C. elegans

OMA-1

MBK-2

Oocyte maturation

MZT

OET

ZGA

Translational repression

Transcriptional repression

RNA-binding proteins

Protein degradation

mRNA clearance

Abbreviations

APC anaphase-promoting complex

GPCR G protein-coupled receptor

MSP major sperm protein

MZT maternal-to-zygotic transition

NEBD nuclear envelope breakdown

OET oocyte-to-embryo transition

ZGA zygotic genome activation

1 Introduction

In mammalian embryos, primary oocytes initiate meiosis, then arrest at prophase of meiosis I, and remain so until puberty. Cyclical hormone surges lead to a small group of oocytes resuming meiosis and arresting a second time at metaphase of meiosis II. Following ovulation, meiosis completes if the egg is fertilized (Fig. 1A). This cycle continues in mammals over a period of months, years, or even decades (reviewed in Von Stetina & Orr-Weaver, 2011). The Drosophila oocyte differentiates as one member of an interconnected 16-cell cyst, with the other 15 cells forming polyploid nurse cells that support oocyte growth (Von Stetina & Orr-Weaver, 2011). The oocyte arrests at prophase I and then is induced to undergo meiotic maturation by an unknown extrinsic signal, although prostaglandin hormones or ecdysone are likely candidates. On meiotic maturation, the Drosophila oocyte arrests for a second time at metaphase I (Fig. 1A). The signal to resume meiosis in Drosophila is, surprisingly, independent of fertilization, requiring instead the mechanical stress associated with passage through the oviduct (Mahowald, Goralski, & Caulton, 1983). It is thought that this represents a holdover from an ancestral form that reproduced asexually, as some extant Drosophila species, such as Drosophila mercatorum, are capable of parthenogenic development (Eisman & Kaufman, 2007). However, it can lead to the seemingly wasteful situation where eggs can be laid that have not been fertilized.

Figure 1 (A) Oocyte development and fertilization. General schematic of oocyte maturation and fertilization, highlighting the meiotic arrest(s) (red text), inducers of oocyte maturation (orange arrow), and timing of fertilization (green arrows) for C. elegans, Drosophila, and mammals. MI, meiosis I; MII, meiosis II; NEBD, nuclear envelope breakdown; MSP, major sperm protein; LH, luteinizing hormone. (B) Schematic of C. elegans gonad. One arm of the adult C. elegans hermaphrodite gonad is represented. Specific mitotic/meiotic stages are indicated above the gonad by the bars. Below the gonad, bars and arrow indicate oocyte maturation, OET, ZGA, and MZT, respectively. Inset: Schematic of an adult hermaphrodite, highlighting the gonad (red fill) and developing embryos (red outline). DTCs, distal tip cells.

Free-living, solitary Caenorhabditis elegans are self-fertilizing hermaphrodites and offer several distinct advantages for the study of oocyte development, maturation, fertilization, and the maternal-to-zygotic transition (MZT). The adult body, including the germline, is transparent and the germline develops in a highly spatially ordered, linear manner. A C. elegans hermaphrodite generates sperm in the L3 larval stage, which are stored in the spermatheca, and then switches completely to the generation of oocytes in the L4 larval stage, continuing to do so for the remainder of its reproductive life (Hirsh, Oppenheim, & Klass, 1976; Schedl, 1997). Hermaphrodites contain two tube-like syncytial gonad arms (Fig. 1B). In each gonad, nuclei in the distal region divide mitotically to provide continuing supplies of new germ nuclei. As nuclei move away from the distal region, they initiate and progress through different stages of meiosis, cellularize, and grow in volume in an assembly line-like fashion. The fully grown oocytes undergo maturation, are ovulated through the spermatheca, and are fertilized. Meiosis is completed upon fertilization and embryonic development initiates within the uterus, where the embryos again line up in developmental order before expulsion through the vulva during gastrulation (Fig. 1B).

The MZT includes both initiation within the embryo of transcription of select genes (zygote genome activation, ZGA), as well as inactivation of many maternal mRNAs and proteins that functioned to regulate developmental events following fertilization. The actual timing of the onset of the MZT, as well as its duration, can vary considerably between species. For C. elegans, no zygotic transcription occurs in late oocytes or early embryos prior to the 4-cell stage. In fact, zygotic transcription is not needed for embryos to develop normally—including the stereotypic asymmetric early cleavages, orientation of cleavage planes, and lineage-specific timing of early divisions—until the time when gastrulation should occur, at the 28-cell stage. However, a number of processes are already underway in the developing and maturing oocytes that directly or indirectly affect the MZT. For the purpose of this review, we will describe C. elegans MZT as from late-stage oocytes to approximately 28-cell embryos. An overriding theme of C. elegans MZT regulation is that it is controlled primarily posttranscriptionally and posttranslationally. We aim to show how the combination of asymmetric partitioning of maternal factors, protein modification-mediated changes in function, protein degradation, and highly regulated translational repression ensures a smooth transition.

We will divide the MZT into four key components: (1) oocyte maturation, ovulation, and fertilization; (2) the transition from meiosis to mitosis; (3) the special case of the C. elegans 1-cell embryo; and (4) the transition from a single-cell embryo to a multicell embryo, including the initiation of zygotic transcription. We will review our current understanding of these processes and discuss how they are coordinated one to another and to the cell cycle. We will also highlight four important regulators/events that play key roles in coordinating this transition.

The MZT in C. elegans demonstrates nicely how genetics, cell biology, and biochemistry can be brought to bear upon a highly complex developmental process in a model organism. While genetic screens led to the isolation of mutations defective in individual processes and, thereby, key genes in each process, cell biological and biochemical analyses allowed us to determine how these separate events are precisely timed and coordinated.

2 Components of the MZT

2.1 Oocyte Maturation, Ovulation, and Fertilization

The details of oocyte maturation, ovulation, and fertilization have been reviewed recently elsewhere (Kim, Spike, & Greenstein, 2013; Marcello, Singaravelu, & Singson, 2013; Marcello & Singson, 2010), and we direct readers there for a more complete discussion on these topics.

The solitary worm has...

Produkt-Details

• Erscheint lt. Verlag: 14.9.2015
• Sprache: englisch
• Themenwelt: Medizin / Pharmazie ► Allgemeines / Lexika
• Themenwelt: Naturwissenschaften ► Biologie ► Genetik / Molekularbiologie
• Themenwelt: Naturwissenschaften ► Biologie ► Zellbiologie
• ISBN-10: 0-12-416612-1 / 0124166121
• ISBN-13: 978-0-12-416612-7 / 9780124166127