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Embryonic Development

Embryonic Development

All embryonic structures are derived from a single cell formed by the union of two gametes. Every individual organism began as a single cell, which divided and differentiated into various types of cells that make up the diverse tissues and complex structures found in the adult. Ontogeny, or the development of an organism from fertilization to adult, begins with the fusion of two cells, the sperm and egg. The sperm and egg are haploid cells formed through the process of meiosis. The haploid cells have no function outside of their involvement in reproduction.

Many invertebrates have isolecithal eggs (yolk is evenly distributed throughout the egg). These eggs have relatively little yolk and various patterns of holoblastic cleavage (the cells divide completely and evenly). The arthropod egg has a moderate amount of yolk, concentrated in the egg's center. The eggs of amphibians and cartilaginous fishes have a moderate amount of yolk, mostly in the lower half of the egg (the vegetal hemisphere). Birds have extremely telolecithal eggs (yolk is concentrated in the vegetal pole, opposite the nucleus) that have a large amount of yolk.

A shell membrane surrounds the embryo, yolk, and albumin, or egg white. It offers mechanical protection and provides a surface for diffusion of oxygen and other gases. Within the egg the allantois acts as a compartment for the storage of nitrogenous excretory products such as uric acid, and may remain after birth or hatching as the urinary bladder. The amnion is filled with amniotic fluid to cushion the embryo that it surrounds. The chorion surrounds the amnion and yolk sac. Mammalian eggs contain some yolk but not nearly as much as found in bird eggs. The typical mammalian egg contains little yolk which is evenly distributed throughout the egg (it is microlecithal and isolecithal).

Stages of Development

In deuterostomes (one of two major groups of coelomate animals that includes echinoderms and chordates), early cleavage divisions are radial. In contrast, protostomes typically display spiral cleavage. Early cleavage divisions in most embryos are reductive, which means that they divide the original contents of the egg without an increase in the total cellular volume of the embryo. The average diameter of a cell decreases as cleavage continues so that the surface area increases relative to cellular volume.

Gastrulation occurs after several cycles of cleavage events. Several important events occur during gastrulation in multicellular animals:

  • The three primary germ layers, ectoderm, mesoderm, and endoderm, are established.
  • The basic body plan is established, including the physical construction of the primary body axes.
  • Cells are brought into new positions, allowing them to interact with cells that were initially not near them. These cellular interactions alter the fate of individual cells, which begin to look and behave differently. This phenomenon is known as induction (cell-cell interactions which lead to cellular differentiation) and is a critical step in the formation of tissue layers.

During invagination, a sheet of epithelial cells (cells that are in close contact with each other and adhere to a basement membrane) bends inward to form a "pocket." During ingression, cells leave an epithelial sheet by transforming into freely migrating mesenchyme cells. During involution, a sheet of tissue spreads inward from the lip of the newly formed cavity. As material moves in from the external portion of the sheet, material that was originally at the lip spreads further into the cavity, eventually forming a sheet of tissue that lines the invagination below the exterior tissue layers.

Intercalation is an expansion process during which cells from different layers lose contact with their neighbors and rearrange into a single layer, which increases in surface area and expands laterally. Intercalation is an important morphogenetic movement involved in the construction of the primary body axis in amphibians. A specialized form of intercalation is convergent extension. An epithelial sheet converges toward a central site, followed by its extension along a single axis through intercalation of the cells of the epithelium (picture a pile of poker chips arranging themselves into a stack). This rearrangement of epithelial cells is an important event during both gastrulation and subsequent neurulation. Convergent extension of the marginal zone (the region of intermediate pigmentation between the pigmented animal hemisphere and the unpigmented vegetal hemisphere) creates the anterior-posterior, or forward-backward axis. During neurulation, convergent extension of the central region of the neural plate (the region of embryonic ectodermal cells that lie directly above the notochord) occurs as the neural axis elongates and the neural tube closes. Also, during intercalation two or more rows of cells move between one another, creating an array of cells that is longer (in one or more dimensions) but thinner than the cell rows from which it formed. The overall change in shape of the tissue results from this cell rearrangement.

Intercalation can be a powerful means of expanding a tissue sheet. During convergent extension, two or more rows of cells intercalate. Cells converge by intercalating perpendicular to the axis of extension, resulting in the overall extension of the tissue in a preferred direction. Primary mesenchyme cells undergo ingression at the onset of gastrulation. During epiboly, a sheet of cells spreads by thinning which is accomplished by changes in the shape or position of cells.

In deuterostomes, the vegetal plate (a thin sheet of epithelial cells) undergoes invagination to produce the archenteron (the cavity formed by the endoderm during gastrulation). The blastopore (the external opening of the archenteron) forms the anus of the larva later in development. Secondary invagination involves the elongation of the archenteron across the blastocoel (the fluid-filled cavity of the blastula, as the embryo is known at this stage), where it attaches to the ectoderm near the animal pole (the pole nearest the nucleus) of the embryo. The onset of secondary invagination correlates with the appearance of long, thin filopodia extended by secondary mesenchyme cells at the tip of the archenteron.

One characteristic found in vertebrates is neural crest cells, derived from ectodermal cells. They develop along the top of the neural tube. As the neural folds close, most neural crest cells change into mesenchyme, an embryonic tissue that consists of star-shaped cells from all three germ layers. Mesechymal derivatives eventually give rise to the visceral skeleton (gill arches, some of which will develop into jaws), pigment cells, sensory and postganglionic neurons (the dentine-producing cells of teeth), Schwann cells that help protect neurons, and bony scales. Differentiation and derivation of tissues and organs during development is called organogenesis. After the production of the neural tube, differentiation of the germ layers occurs rapidly, and organogenesis begins, in which the primary tissues differentiate into specific organs and tissues.

Neurulation creates three important structures in the embryos of higher vertebrates:

  • The neural tube, which gives rise the central nervous system;
  • The neural crest, which gives rise to a diverse set of cell types; and
  • A true epidermis, which covers over the neural tube.

Examples of Development

Four examples illustrate some aspects of embryonic development. All four are metazoans : Platyhelminthes (a nematode), Echinodermata (a sea urchin), and Chordata (represented by a frog, a bird, and a mammal).

A worm.

Caenorhabditis elegans (C. elegans ) is a free-living nematode with two sexes: a self-fertilizing hermaphrodite and a male. The general body plan of this worm is in the form of two concentric tubes separated by a space called the pseudocoelom. The intestine forms the inner tube and the outer tube consists of cuticle, hypodermis, musculature, and nerve cells. In the adult, the pseudocoelomic space also contains the tubular gonad. The shape of the worm is maintained by internal hydrostatic pressure, controlled by an osmoregulatory system.

C. elegans is a primitive organism yet it shares many embryological characteristics with members of higher phyla. The worm is conceived as a single cell that undergoes a complex process of development, starting with embryonic cleavage, proceeding through morphogenesis and growth to the adult worm-like animal.

Shortly after fertilization, the maternal pronucleus (the sperm nucleus and egg nucleus within the fertilized egg before their fusion to form the diploid zygote nucleus) migrates from the anterior to the posterior through the pseudocleavage furrow. It meets the paternal pronucleus in the rear, and they migrate forward before fusing and entering mitosis. Eggs are laid at about the time of gastrulation and hatch into first-stage juveniles. At hatching there are 558 cells in the hermaphrodite and 560 in the male. The animal matures through four larval stages, punctuated by molts and characterized by additional divisions of a few cells. These result primarily in elaboration of the nervous system and development of the secondary sexual characteristics.

Gonadogenesis, the formation of reproductive organs, begins in the first larval stage and ends in the fourth larval stage.

Sea urchins.

Like all echinoderms, the purple sea urchin (Strongylocentrotus purpuratus ) undergoes radial cleavage, as do typical deuterostomes, such as chordates, ascidians, and other echinoderms. As in embryonic cleavages in other metazoans, sea urchin cleavage divisions are reductive, that is, the cleavages result in more cells but without an increase in the total cellular volume of the embryo. The first two cleavages are meridional, meaning that the cleavage furrow passes through the animal and vegetal poles. The next cleavage is equatorial, that is, it passes through the embryo's midsection. The fourth cleavage is unequal. In deuterostome development, early cleavage divisions are radial. Protostomes typically display spiral cleavage. Early cleavage divisions in most embryos are reductive, dividing the original contents of the egg without increasing the total cellular volume of the embryo. The average diameter of a cell decreases as cleavage continues, and there is an increase in surface area relative to cellular volume. The embryo at this stage (known as the morula) is shaped like a blackberry made up of small, homogeneous cells. During the third cleavage, the surface area roughly doubles. The embryo then enters the blastula stage.

The blastula is a hollow ball of cells organized into an epithelial mono-layer. The vegetal pole epithelium thickens to form the vegetal plate, which will give rise to primary mesenchyme cells and the archenteron during gastrulation. The epithelium is lined on its outer, or apical, surface by two extracellular matrice, an inner apical lamina and a hyaline layer outside it. Both are attached to the apices ("tips") of the cells in the wall of the blastula, which extend microvilli into these extracellular matrix layers.

Sea urchin gastrulae (as the embryo is called at this stage) elongate their archenterons via convergent extension during gastrulation. The epithelial cells of the archenteron rearrange as it elongates. Secondary invagination involves autonomous extension of the archenteron in the early phase of elongation, followed by mesenchyme-dependent pulling in the second phase. The sea urchin embryo possesses extracellular matrix layers lining the inside and outside of the embryo. The outer layer is divided into two layers, an apical lamina directly attached to the apical ends of the cells, and a hya-line layer on top of the first layer.

A frog.

Xenopus laevis is a frog commonly used in embryological studies. The egg of this species is a huge cell, with a volume that is over one million times larger than a normal somatic frog cell. During embryonic development, the egg is converted into a tadpole containing millions of cells but with the same volume of material.

After fertilization, the cortical reaction (a wave of chemicals is released from the egg plasma membrane after fusion of the sperm and egg) results in loss of contact between the surface of the egg and the vitelline envelope (an extracellular membrane that encloses the embryo), permitting the re-orientation of the egg via gravity. The varying densities of yolk in the egg result in a consistent orientation. The upper hemisphere of the egg, the animal pole, is dark. The lower hemisphere, the vegetal pole, is light. When it is deposited in the water and ready for fertilization, the haploid egg is at metaphase of meiosis II (the chromosomes are aligned at separate poles during second phase of reductive division).

Entrance of the sperm initiates a sequence of fertilization events. After meiosis II is completed, the cytoplasm (the contents of the cell outside the nucleus and within the plasma membrane) of the egg rotates about 30 degrees relative to the poles, which is revealed by the appearance of a light-colored band, the gray crescent. This crescent forms opposite the point where the sperm entered. The crescent establishes the future pattern of the animal: its dorsal and ventral surfaces; its anterior and posterior; and its left and right sides.

The haploid sperm and egg nuclei fuse to form the diploid nucleus of the zygote. The zygote nucleus undergoes several cycles of mitosis (the nuclear division that follows duplication of the chromosomes, resulting in daughter nuclei with the same chromosome content as the parent nucleus). During cytokinesis, a belt of actin filaments forms around the perimeter of the cell, midway between the poles. As the belt tightens, the cell is pinched into two daughter cells. The first cleavage occurs shortly after the zygote nucleus forms and begins with the appearance of a furrow that runs longitudinally through the poles of the egg, passing through the point of sperm entry and bisecting the gray crescent. This divides the egg into two halves, forming the two-cell stage. During the second cleavage, the cleavage furrow again runs through the poles but at right angles to the first furrow, forming the four-cell stage. The third cleavage furrow runs horizontally but in a plane closer to the animal than to the vegetal pole. It produces the eight-cell stage.

The next few cleavages proceed in a similar fashion, producing a sixteen-cell and then a thirty-two-cell embryo. As cleavage continues, the cells in the animal pole begin dividing more rapidly than those in the vegetal pole and thus become smaller and more numerous. Subsequent cleavages produce a hollow ball comprised of thousands of cells called the blastula, which contains a fluid-filled cavity, the blastocoel.

Gastrulation begins with the invagination of cells in the region of the embryo once occupied by the middle of the gray crescent. This produces an opening, the blastopore, that will be the future anus and a cluster of cells that develops into the Spemann organizer (a cluster of cells which act as powerful inducer of surrounding cells). As gastrulation continues, three distinct germ layers are formed: ectoderm, mesoderm, and endoderm.

The ectoderm eventually forms the skin, brain, spinal cord, and other neurons. The mesoderm forms the notocord, muscles, blood, bone, and sex organs. The endoderm eventually forms the linings of the gut, lungs, and bladder, as well as of the liver and pancreas.

The Spemann organizer, which is mostly mesoderm, develops into the notochord, the precursor of the vertebral column, and induces the ectoderm lying above it to begin to form neural tissue instead of skin. This ectoderm will develop into two longitudinal folds, forming the neural folds stage. Eventually, the lips of the folds fuse to form the neural tubewhich later develops into the brain and spinal cordand the embryo elongates, forming an anterior-posterior, or front-rear, axis.

Each of the various layers of cells in the frog gastrula has a definite and different fate. Embryonic cells form many of the specialized structures in the tadpole, including neurons, blood cells, muscle cells, and epithelial cells.

Neurulation in Xenopus involves neural fold elevation and invagination of the neural plate to form the neural tube. The neural axis elongates as neurulation proceeds. The induction of convergence and extension behavior in cells of the neural tube is associated with neural induction, also known as primary embryonic induction.

The chicken (Gallus gallus).

The chicken ovum consists of the yellow yolk and a small yolk-free area called the blastoderm (blastodisc or germinal disc). The nucleus of the ovum is in the blastodisc. The blastodisc appears as a small whitish area on the upper surface of the yolk. Albumin is added to the ovum as it moves down the hen's oviduct. Eventually, two shell membranes and a calcareous shell are added to form the complete egg.

Because of the large amount of yolk present in the chicken egg, cleavage, morphogenesis, and differentiation are confined to the blastoderm. Initially, the blastoderm becomes several cell layers thick and a cavity, called the subgerminal cavity, is formed under these layers. This stage of the embryo is comparable to the sea urchin morula. As cleavage continues and more cells are formed, the blastoderm splits to form two layers, a dorsal epiblast (ectoderm) and ventral hypoblast (endoderm). This embryonic stage corresponds to the sea urchin blastula and the cavity separating these two layers is called the blastocoel. Development to this stage takes place while the egg is still in the oviduct of the hen.

Gastrulation occurs by a process of involution. Involution is the curling inward and in-growth of a group of cells. Cells of the blastoderm surface migrate backward and medially (toward the middle of the embryo) and involute, or turn in, along a line called the primitive streak. These involuted cells will form the mesoderm germ layer. As gastrulation progresses, the anterior end of the streak moves backward so that the anterior region of the embryo is formed first. The primitive streak is functionally the same as the blastopore of the sea urchin gastrula.

The three germ layers, ectoderm, endoderm, and mesoderm, are created by involution following gastrulation. The coelom results from a separation of the lateral mesoderm. The involuted cells form the notochord anterior to the primitive streak and the lateral mesoderm (somites) laterally. After gastrulation, the process of neurulation, or formation of the neural tube and associated structures, takes place.

Neurulation occurs at or near the end of gastrulation and transforms the gastrula into a neurula by establishing the central nervous system. The ectoderm gives rise to neural folds flanking a neural groove along an axis from the blastopore toward the future head. These folds sink into the dorsum (back) of the embryo and meet mid-dorsally, forming a neural tube of which the anterior part becomes the brain and the rest the spinal cord. A population of mesodermal cells called the chordamesoderm aggregates, or gathers, to form the notochord. The chordamesoderm is required for the formation of the neural tube. During neurulation the portion of chordamesoderm that will form the notochord induces neural plate formation, which is the first stage in the formation of the neural tube. This process is characterized in most vertebrates by three stages. During the neural plate stage, the ectoderm on the dorsal side of the embryo overlying the noto-chord thickens to form the neural plate. During the neural fold stage, the thickened ectoderm curves inward, leaving an elevated area along the neural groove. The neural fold is wider in the anterior portion of the vertebrate embryo, which is the region where the brain will be formed. During the neural tube stage, the neural folds move closer together and fuse. The neural groove becomes the cavity within the neural tube, which will later contain cerebrospinal fluid that aids in the function of the central nervous system.

The mouse (Mus musculus).

Embryos of the mouse develop in a very different environment than do those of the chicken. The relatively low yolk content in the typical, small mammalian egg requires that the embryo quickly implant, or adhere to the inner lining of the uterus, in order to obtain nutrients from the mother. Early cleavage in mammalian embryos is followed by the blastocyst stage. There are two groups of cells present at this stage. The outer layer of cells, called the trophoblast, and the inner mass of cells, called the blastocyst, will together go on to form the embryo.

During implantation of the fertilized ovum in the uterus the placenta is formed, which is a structure for physiological exchange between the fetus and the mother. The placenta consists of both a maternal contribution, the endometrium of the uterus, and a fetal contribution, the trophoblast. It is believed that the latter is used as an immunological barrier that prevents rejection of the fetus, and its paternal chromosomes, by the mother. The shape of the placenta varies, depending on the species. The inner cell mass of the blastocyst develops into the blastodisk, similar to that in chickens. Early stages of development of the mammalian embryo, such as the primitive streak stage, neurulation, and germ layer differentiation, are similar to those in birds and reptiles. The primary difference found in mammals is the development of the umbilical cord. The umbilical cord contains the allantois and yolk sac as well as circulatory system structures that connect the embryo to the placenta.

see also Embryology.

Andrew G. Gluesenkamp

Bibliography

Bruska, Richard G., and Gary J. Bruska. Invertebrates. Sunderland, MA: Sinauer Associates, 1990.

Butler, Harry, and B. H. Juurlink. An Atlas for Staging Mammalian and Chick Embryos. Boca Raton, FL: CRC Press Inc., 1987.

Gilbert, Scott F. Developmental Biology, 5th ed. Sunderland, MA: Sinauer Associates, Inc., 1997.

Gilbert, Scott F., and Anne M. Raunio, eds. Embryology, Constructing the Organism. Sunderland, MA: Sinauer Associates, Inc., 1997.

Johnson, Leland G. Johnson & Volpe's Patterns & Experiments in Developmental Biology, 2nd ed. New York: Wm. C. Brown Publishers, 1995.

Kalthoff, Klaus. Analysis of Biological Development, 2nd ed. New York: McGraw-Hill, Inc., 2001.

Mathews, Willis W., and Gary C. Schoenwolf. Atlas of Descriptive Embryology, 5th ed. Englewood, NJ: Prentice-Hall, Inc., 1998.

Raff, Rudolf A., and Thomas C. Kaufman. Embryos, Genes, and Evolution: The Developmental-Genetic Basis of Evolutionary Change. New York: Macmillan, 1983.

Schoenwolf, Gary C. Laboratory Studies of Vertebrate and Invertebrate Embryos, 8th ed. Englewood Cliffs, NJ: Prentice Hall, 2001.

Torrey, Theodore W., and Alan Feduccia. Morphogenesis of the Vertebrates. New York: John Wiley, 1991.

Wolpert, Lewis, R. Beddington, J. Brockes, T. Jessell, P. Lawrence, and E. Meyerowitz. Principles of Development. Oxford, U.K.: Current Biology Ltd., Oxford University Press, 1998.

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Embryogenesis

Embryogenesis

The development of the embryo, or embryogenesis, begins with the repeated divisions of the zygote to give rise to thousands of cells. These in turn form the various tissues and organs of the adult plant. In seed plants, embryogenesis occurs within the embryo sac of the ovule. Since the ovule is transformed into the seed, embryo development is intimately associated with seed formation.

Dicot and Monocot Embryos

The first division of the zygote is almost always asymmetric (uneven) and transverse to its long axis, producing a small apical cell and a large basal (bottom) cell. The apical cell then divides, forming a longitudinal wall, and then divides again, forming a second wall at right angles to the first, to generate a four-celled embryo; subsequent divisions give rise to a globular embryo of eight to thirty-two cells. By changes in shape, accompanied by tissue and organ formation, the globular embryo successively forms the heart-shaped, torpedo-shaped, walking-stick-shaped, and mature embryo.

In contrast, the basal cell divides by a series of transverse walls to form a filamentous structure known as the suspensor, which anchors the embryo to the embryo sac wall and aids in nutrient absorption from the surrounding tissues. Typically in dicots, the mature embryo consists of the shoot apex, the two cotyledons (seed leaves), the hypocotyl (primitive stem), and the root. Together, these occupy most of the volume of the mature seed. Although the early division sequences of embryos of mono-cots appear somewhat similar to those of dicots, several organs not found in dicot embryos assume prominence in monocot embryos, especially in embryos of cereal grains. In the latter, the single cotyledon (known as the scutellum) functions to absorb nutrients from the endosperm. Sheathlike structures, known as the coleorhiza and coleoptile, cover the root and shoot, respectively. Finally, a flaplike outgrowth called the epiblast is found at the origin of the coleorhiza. The mature embryo is confined to a small part of the cereal grain, which is filled with the nutritive tissue of the endosperm.

Tissue Formation in the Early Embryo

Although embryos lack most organs of the adult plant, the characteristic body plan of the adult is nonetheless established during early embryo-genesis. This involves the formation of an apico-basal (top-bottom) axis, constituting the body of the embryo, and a radial axis of differentiated tissues around the apico-basal axis. In dicots, the apico-basal axis is established as early as the four-celled stage of the embryo, when a transverse division gives rise to upper and lower tiers of four cells each. The shoot apical meristem and cotyledons are generated from the upper tier of cells, and the hypocotyl and root are generated from the lower tier. Thus, the primary meristems of the shoot and root come to occupy positions at opposite poles of the embryo axis. In Arabidopsis thaliana and Capsella bursa-pastoris, two model species to study embryogenesis in dicots, the uppermost cell of the suspensor (known as the hypophysis) functions as the founder cell that generates parts of the embryonic root such as the root cap, cortex, quiescent center, and epidermis .

After the apico-basal axis is established, the radial pattern elements of the primordial tissue layers are laid down in the eight-celled embryo by a new round of divisions. These create an outer layer of eight cells (forming the protoderm) and an inner core of eight cells (forming the ground meristem and procambium). The protoderm and procambium become the epidermal and vascular tissues, respectively, of the mature embryo, whereas the cells of the ground meristem differentiate into a cortex or into both cortex and pith. In cereals such as maize, the globular embryo of sixteen to thirty-two cells attains a club-shaped stage when the scutellum appears as a vague elevation at the apico-basal region. The shoot apex and leaf primordia are formed as lateral outgrowths opposite the scutellum. Finally, the appearance of the coleorhiza and the differentiation of the root in the central zone of the embryo complete the process of embryogenesis. In both dicot and monocot embryos, the active life of the suspensor is terminated when the embryonic organs are formed.

see also Cells, Specialized Types; Differentiation and Development; Genetic Mechanisms and Development; Germination; Reproduction, Fertilization and; Seeds; Tissues.

V. Raghavan

Bibliography

Raghavan, V. Molecular Embryology of Flowering Plants. New York: Cambridge University Press, 1997.

Raven, Peter H., Ray F. Evert, and Susan E. Eichhorn. Biology of Plants, 6th ed. New York: W. H. Freeman and Company, 1999.

Genetic and molecular studies of embryogenesis in Arabidopsis thaliana have shown that specific genes control the formation of both apico-basal and radial pattern elements in the embryo. Among the genes isolated and characterized are Gnom, Monopteros, and Shoot Meristemless, controlling the apico-basal pattern, and Knolle, controlling the radial pattern.

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embryogenesis

em·bry·o·gen·e·sis / ˌembrē-ōˈjenəsis/ • n. Biol. the formation and development of an embryo. DERIVATIVES: em·bry·o·ge·net·ic / -jəˈnetik/ adj. em·bry·o·gen·ic / -ˈjenik/ adj. em·bry·og·e·ny / ˌembrēˈäjənē/ n. .

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embryogenesis

embryogenesis See EMBRYOGENY.

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