Drosophila embryogenesis, the process by which Drosophila (fruit fly) embryos form, is a favorite model system for geneticists and developmental biologists studying embryogenesis. The small size, short generation time, and large brood size make it ideal for genetic studies. Transparent embryos facilitate developmental studies. Drosophila melanogaster was introduced into the field of genetic experiments by Thomas Hunt Morgan in 1909.
Drosophila display a holometabolous method of development, meaning that they have three distinct stages of their post-embryonic life cycle, each with radically different body plans: larva, pupa and finally, adult. The machinery necessary for the function and smooth transition between these three phases develops during embryogenesis. During embryogenesis, the larval stage fly will develop and hatch at a stage of its life known as the first larval instar. Cells that will produce adult structures are put aside in imaginal discs. During the pupal stage, the larval body breaks down as the imaginal disks grow and produce the adult body. This process is called complete metamorphosis.
The mother fly produces oocytes that already have anterior-posterior and dorsal-ventral axes defined by maternal activities.
Embryogenesis in Drosophila is unique among model organisms in that cleavage occurs in a syncytium. About 5,000 nuclei accumulate in the unseparated cytoplasm of the oocyte before they migrate to the surface and are encompassed by plasma membranes to form cells surrounding the yolk sac. Early on, the germ line segregates from the somatic cells through the formation of pole cells at the posterior end of the embryo.
Like other triploblastic metazoa, gastrulation leads to the formation of three germ layers: the endoderm, mesoderm, and ectoderm. The mesoderm invaginates from the ventral furrow (VF), as do the ectoderm that will give rise to the midgut. The pole cells are internalized by a different route.
Germ band elongation involves many rearrangements of cells, and the appearance of distinct differences in the cells of the three germ bands and various regions of the embryo. The posterior region (including the hindgut) expands and extends towards the anterior pole along the dorsal side of the embryo. The earliest signs of segmentation appear during this phase with the formation of parasegmental furrows. This is also when the tracheal pits form, the first signs of structures for breathing.
Germ band retraction returns the hindgut to the dorsal side of the posterior pole and coincides with overt segmentation. The remaining stages involve the internalization of the nervous system (ectoderm) and the formation of internal organs (mainly mesoderm).
Anterior-posterior axis patterning in Drosophila
One of the best understood examples of pattern formation is the patterning along the future head to tail (antero-posterior) axis of the fruit fly Drosophila melanogaster. The development of Drosophila is particularly well studied, and it is representative of a major class of animals, the insects or insecta. Other multicellular organisms sometimes use similar mechanisms for axis formation, although the relative importance of signal transfer between the earliest cells of many developing organisms is greater than in the example described here.
Maternal effect genes
The building-blocks of anterior-posterior axis patterning in Drosophila are laid out during egg formation (oogenesis), well before the egg is fertilized and deposited. The developing egg (oocyte) is polarized by differentially localized mRNA molecules.
The genes that code for these mRNAs, called maternal effect genes, encode for proteins that get translated upon fertilization to establish concentration gradients that span the egg. Bicoid and hunchback are the maternal effect genes that are most important for patterning of anterior parts (head and thorax) of the Drosophila embryo. Nanos and Caudal are maternal effect genes that are important in the formation of more posterior abdominal segments of the Drosophila embryo.
Cytoskeletal elements such as microtubules are polarized within the oocyte and can be used to allow the localization of mRNA molecules to specific parts of the cell. Maternally synthesized bicoid mRNAs attach to microtubules and are concentrated at the anterior ends of forming Drosophila eggs. In unfertilized eggs, transcripts are still strictly localized at the tip, but immediately after fertilization, a small mRNA gradient is formed in the anterior 20% of the eggs. nanos mRNA also attaches to a Drosophila egg's cytoskeleton but is concentrated at the posterior end of the egg. hunchback and caudal mRNAs lack special location control systems and are fairly evenly spread throughout the entire interior of the egg cells.
When the mRNAs from the maternal effect genes are translated into proteins, a Bicoid protein gradient forms at the anterior end of the egg. Nanos protein forms a gradient at the posterior end. The Bicoid protein blocks translation of caudal mRNA so Caudal protein is made only in the posterior part of the cell. Nanos protein binds to the hunchback mRNA and blocks its translation in the posterior end of Drosophila embryos.
The Bicoid, Hunchback, and Caudal proteins are transcription factors. Bicoid has a DNA-binding homeodomain that binds both DNA and the nanos mRNA. Bicoid binds a specific RNA sequence in the 3' untranslated region, called the Bicoid 3'-UTR regulatory element, of caudal mRNA and blocks translation.
Hunchback protein levels in the early embryo are significantly augmented by new hunchback gene transcription and translation of the resulting zygotically produced mRNA. During early Drosophila embryogenesis there are nuclear divisions without cell division. The many nuclei that are produced distribute themselves around the periphery of the cell cytoplasm. Gene expression in these nuclei is regulated by the Bicoid, Hunchback, and Caudal proteins. For example, Bicoid acts as a transcriptional activator of hunchback gene transcription.
The other important function of the gradients of Bicoid, Hunchback, and Caudal proteins is in the transcriptional regulation of other zygotically expressed proteins. Many of these are the protein products derived from members of the "gap" family of developmental control genes. giant, huckebein, hunchback, knirps, Krüppel and tailless are all gap genes. Their expression patterns in the early embryo are determined by the maternal effect gene products and shown in the diagrams on the right side of this page. The gap genes are part of a larger family called the segmentation genes. These genes establish the segmented body plan of the embryo along the anterior-posterior axis. The segmentation genes specify 14 parasegments that are closely related to the final anatomical segments. The gap genes are the first layer of a hierarchical cascade of the segmentation control genes.
Additional segmentation genes
Two additional classes of segmentation genes are expressed after the gap gene products. The pair-rule genes are expressed in striped patterns of seven bands perpendicular to the anterior-posterior axis (see Figure 6, even-skipped). These patterns of expression are established within the syncytial blastoderm. After these initial patterning events, cell membranes form around the nuclei of the syncytial blastoderm converting it to a cellular blastoderm.
The expression patterns of the final class of segmentation genes, the segment polarity genes, are then fine-tuned by interactions between the cells of adjacent parasegments (see the example, engrailed, Figure 7). The Engrailed protein is a transcription factor (yellow in Figure 7) that is expressed in one row of cells at the edge of each parasegment. This expression pattern is initiated by the pair-rule genes (like even-skipped) that code for transcription factors that regulate the engrailed gene's transcription in the syncytial blastoderm.
Cells that make Engrailed can make the cell-to-cell signaling protein Hedgehog (green in Figure 7). The motion of Hedgehog is limited by its lipid modification, and so Hedgehog activates a thin stripe of cells anterior to the Engrailed-expressing cells. Only cells to one side of the Engrailed-expressing cells are competent to respond to Hedgehog because they express the receptor protein Patched (blue in Figure 7). Cells with activated Patched receptor make the Wingless protein (red in Figure 7). Wingless is a secreted protein that acts on the adjacent rows of cells by activating its cell surface receptor, Frizzled.
Wingless acts on Engrailed-expressing cells to stabilize Engrailed expression after the cellular blastoderm forms. The Naked cuticle protein is induced by Wingless to limit the number of rows of cells that express Engrailed. The short-range, reciprocal signaling by Hedgehog and Wingless, held in check by the Patched and Naked proteins, stabilizes the boundary between each segment. The Wingless protein is called "wingless" because of the phenotype of some wingless mutants. Wingless and Hedgehog also function in multiple tissues later in embryogenesis and also during metamorphosis.
The transcription factors that are coded for by segmentation genes regulate yet another family of developmental control genes, the homeotic selector genes. These genes exist in two ordered groups on Drosophila chromosome 3. The order of the genes on the chromosome reflects the order that they are expressed along the anterior-posterior axis of the developing embryo. The Antennapedia group of homeotic selector genes includes labial, antennapedia, sex combs reduced, deformed, and proboscipedia. Labial and Deformed proteins are expressed in head segments where they activate the genes that define head features. Sex-combs-reduced and Antennapedia specify the properties of thoracic segments. The bithorax group of homeotic selector genes control the specializations of the third thoracic segment and the abdominal segments.
In 1995, the Nobel Prize for Physiology or Medicine was awarded for studies concerning the genetic control of early embryonic development to Christiane Nüsslein-Volhard, Edward B. Lewis and Eric Wieschaus. Their research on genetic screening for embryo patterning mutants revealed the role played in early embryologic development by Homeobox genes like bicoid. An example of a homeotic mutation is the so-called antennapedia mutation. In Drosophila, antennae and legs are created by the same basic "program", they only differ in a single transcription factor. If this transcription factor is damaged, the fly grows legs on its head instead of antennae. See images of this "antennapedia" mutant and others, at FlyBase.
Formation of the Dorsal-Ventral Axis is dependent on a maternally synthesized transcription factor known as dorsal protein. The production of dorsal protein is stimulated by the localization of the embryonic nuclei. The nuclei secretes a protein called Gurken. Gurken inhibits the production of PIPE protein by interacting with Torpedo receptor on flanking oocyte follicle cells. PIPE positive cells are able to secrete dorsal protein and form the ventral side of the egg, while PIPE negative cells do not secrete dorsal protein and form the dorsal side of the egg.
Dorsal induces the transcription of two genes twist & snail while repressing zerknüllt & decapentaplegic.
Intra-membranous dorsal receptor proteins, known as Toll receptors are responsible for transporting dorsal protein into the embryonic nuclei. These Toll receptors are the product of Toll gene, and are uniformly spaced across the embryoinic plasma-membrane.
Since dorsal protein is secreted by PIPE positive-ventral follicular cells of an egg, dorsal protein enters the embryo to the ventral side. Once transported into the nuclei, dorsal protein is most concentrated at the ventral side of the embryo.
This process sets up a gradient differential between the ventral and dorsal side of an immature embryo, the repression or induction of these four genes are differentially regulated. For example;
- At the ventral end of the embryo, blastoderm nuclei exposed to high concentrations of dorsal protein induce the transcription of twist and snail while repressing zerknüllt & decapentaplegic.
- In the middle of the embryo, blastoderm nuclei exposed to mild concentrations of dorsal protein don't express any genes.
- At the dorsal end of the embryo, blastoderm nuclei exposed to little or no dorsal protein express only zerknüllt & decapentaplegic.
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