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Chromatin dynamics during plant sexual reproduction.

She W, Baroux C - Front Plant Sci (2014)

Bottom Line: This ability is exemplified during sexual reproduction in flowering plants where novel cell types are generated in floral tissues of the adult plant during sporogenesis, gametogenesis, and embryogenesis.While the molecular and genetic basis of cell specification during sexual reproduction is being studied for a long time, recent works disclosed an unsuspected role of global chromatin organization and its dynamics.In this review, we describe the events of chromatin dynamics during the different phases of sexual reproduction and discuss their possible significance particularly in cell fate establishment.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Biology - Zürich-Basel Plant Science Center, University of Zürich Zürich, Switzerland.

ABSTRACT
Plants have the remarkable ability to establish new cell fates throughout their life cycle, in contrast to most animals that define all cell lineages during embryogenesis. This ability is exemplified during sexual reproduction in flowering plants where novel cell types are generated in floral tissues of the adult plant during sporogenesis, gametogenesis, and embryogenesis. While the molecular and genetic basis of cell specification during sexual reproduction is being studied for a long time, recent works disclosed an unsuspected role of global chromatin organization and its dynamics. In this review, we describe the events of chromatin dynamics during the different phases of sexual reproduction and discuss their possible significance particularly in cell fate establishment.

No MeSH data available.


Related in: MedlinePlus

Sexual reproduction in flowering plants. The process of sexual reproduction begins with sporogenesis where spore mother cells (SMCs) differentiate in the floral organs of adult plants. The female SMC, also called megaspore mother cell (MMC) differentiates from a subepidermal nucellar cell within the ovule primordium, the MMC then undergoes meiosis to produce four haploid spores while only one survives to form the functional megaspore (FM). In the stamen primordium, one subepidermal cell enlarges to from the archesporial cell (AC). The archesporial cell then divides to form one primary sporogenous cell (PS) on the inner side and one primary parietal cell (PP) toward the outside. The primary parietal cell divides periclinally and anticlinally to generate the anther wall that is composed of epidermis (E), endothecium (En), the middle layer (ML), and the tapetum (T), while the primary sporogenous cell divides to give rise to the male SMCs, also called the pollen mother cells (PMCs). Each PMC then undergoes meiosis to form four haploid microspores (MS). During gametogenesis, the FM undergoes three rounds of mitosis and cellularization to generate the female gametophyte that harbors two gametes: the egg cell and the central cell, accompanied with three antipodals and two synergids. While for the male side, each microspore undergoes an asymmetric division to give rise to a larger vegetative cell and a smaller generative cell within the bicellular pollen grain. The generative cell divides further to produce the gametes: two sperm cells. During double fertilization, the egg cell is fertilized by one sperm to form the zygote that will give rise to the embryo, while the central cell fuses with the other sperm to generate the triploid endosperm. Original drawings were made after microscopy pictures (female sporogenesis) or inspired from Zhang et al. (2011) (male sporogenesis).
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Figure 1: Sexual reproduction in flowering plants. The process of sexual reproduction begins with sporogenesis where spore mother cells (SMCs) differentiate in the floral organs of adult plants. The female SMC, also called megaspore mother cell (MMC) differentiates from a subepidermal nucellar cell within the ovule primordium, the MMC then undergoes meiosis to produce four haploid spores while only one survives to form the functional megaspore (FM). In the stamen primordium, one subepidermal cell enlarges to from the archesporial cell (AC). The archesporial cell then divides to form one primary sporogenous cell (PS) on the inner side and one primary parietal cell (PP) toward the outside. The primary parietal cell divides periclinally and anticlinally to generate the anther wall that is composed of epidermis (E), endothecium (En), the middle layer (ML), and the tapetum (T), while the primary sporogenous cell divides to give rise to the male SMCs, also called the pollen mother cells (PMCs). Each PMC then undergoes meiosis to form four haploid microspores (MS). During gametogenesis, the FM undergoes three rounds of mitosis and cellularization to generate the female gametophyte that harbors two gametes: the egg cell and the central cell, accompanied with three antipodals and two synergids. While for the male side, each microspore undergoes an asymmetric division to give rise to a larger vegetative cell and a smaller generative cell within the bicellular pollen grain. The generative cell divides further to produce the gametes: two sperm cells. During double fertilization, the egg cell is fertilized by one sperm to form the zygote that will give rise to the embryo, while the central cell fuses with the other sperm to generate the triploid endosperm. Original drawings were made after microscopy pictures (female sporogenesis) or inspired from Zhang et al. (2011) (male sporogenesis).

Mentions: Flowering plants have a life cycle alternating between a dominant, diploid sporophytic phase and a short haploid gametophytic phase. Sexual reproduction can be divided into three phases: sporogenesis, gametogenesis, embryo- and endosperm-genesis (Figure 1). Unlike animals, plants do not set aside a germline lineage during embryogenesis. Instead, the reproductive lineage is established late in development. Cells that will share a meiotic fate and hence initiate a “reproductive lineage” differentiate from and within a somatic tissue in dedicated floral organs of adult plants. Sporogenesis is initiated by the differentiation of spore mother cells (SMCs) that engage somatic cells into a meiotic fate entailing the development of haploid, multicellular gametophytes. The female SMC, also called megaspore mother cell (MMC) differentiates in a subepidermal position in an ovule primordium – composed of the L1-outer layer of cells and the nucellus –; the male SMC differentiates from a mitotic division of the archesporial cell within the sporangium of the anther locule (Figure 1, and see section Chromatin Dynamics During Sporogenesis). Gametogenesis is the process by which the gametes are formed within the gametophytes. The male and female gametophytes develop from one haploid spore through a limited number of mitosis and cellularization events that will give rise to highly distinct cell types. A vast majority of flowering plants share the seven-celled type of female gametophyte comprising two gametes – the egg cell and the central cell – and five accessory cells – two synergids and three antipodals. All cells are haploid except for the central cell that inherits two polar nuclei, which following fusion generate a di-haploid maternal genome in the central cell. In contrast, the mature male gametophyte contained in the pollen grain is highly reduced and is composed of one vegetative – accessory – cell and two gametes, the sperm cells (Maheshwari, 1950; Figure 1). During double fertilization, the egg cell fuses with one sperm to give rise to the diploid zygote, while the central cell is fertilized by the second sperm cell – from the same pollen – to produce the triploid endosperm (Figure 1). Strikingly, although genetically identical the two fertilization products share distinct developmental fates. The totipotent zygote engages into embryogenesis that establishes the basic body plan and the symmetries (axial and radial) of the future seedling; in contrast, the primary endosperm cell engages in a syncytial phase of proliferation, before cellularization, to form an extra-embryonic, nurturing tissue (Maheshwari, 1950).


Chromatin dynamics during plant sexual reproduction.

She W, Baroux C - Front Plant Sci (2014)

Sexual reproduction in flowering plants. The process of sexual reproduction begins with sporogenesis where spore mother cells (SMCs) differentiate in the floral organs of adult plants. The female SMC, also called megaspore mother cell (MMC) differentiates from a subepidermal nucellar cell within the ovule primordium, the MMC then undergoes meiosis to produce four haploid spores while only one survives to form the functional megaspore (FM). In the stamen primordium, one subepidermal cell enlarges to from the archesporial cell (AC). The archesporial cell then divides to form one primary sporogenous cell (PS) on the inner side and one primary parietal cell (PP) toward the outside. The primary parietal cell divides periclinally and anticlinally to generate the anther wall that is composed of epidermis (E), endothecium (En), the middle layer (ML), and the tapetum (T), while the primary sporogenous cell divides to give rise to the male SMCs, also called the pollen mother cells (PMCs). Each PMC then undergoes meiosis to form four haploid microspores (MS). During gametogenesis, the FM undergoes three rounds of mitosis and cellularization to generate the female gametophyte that harbors two gametes: the egg cell and the central cell, accompanied with three antipodals and two synergids. While for the male side, each microspore undergoes an asymmetric division to give rise to a larger vegetative cell and a smaller generative cell within the bicellular pollen grain. The generative cell divides further to produce the gametes: two sperm cells. During double fertilization, the egg cell is fertilized by one sperm to form the zygote that will give rise to the embryo, while the central cell fuses with the other sperm to generate the triploid endosperm. Original drawings were made after microscopy pictures (female sporogenesis) or inspired from Zhang et al. (2011) (male sporogenesis).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4109563&req=5

Figure 1: Sexual reproduction in flowering plants. The process of sexual reproduction begins with sporogenesis where spore mother cells (SMCs) differentiate in the floral organs of adult plants. The female SMC, also called megaspore mother cell (MMC) differentiates from a subepidermal nucellar cell within the ovule primordium, the MMC then undergoes meiosis to produce four haploid spores while only one survives to form the functional megaspore (FM). In the stamen primordium, one subepidermal cell enlarges to from the archesporial cell (AC). The archesporial cell then divides to form one primary sporogenous cell (PS) on the inner side and one primary parietal cell (PP) toward the outside. The primary parietal cell divides periclinally and anticlinally to generate the anther wall that is composed of epidermis (E), endothecium (En), the middle layer (ML), and the tapetum (T), while the primary sporogenous cell divides to give rise to the male SMCs, also called the pollen mother cells (PMCs). Each PMC then undergoes meiosis to form four haploid microspores (MS). During gametogenesis, the FM undergoes three rounds of mitosis and cellularization to generate the female gametophyte that harbors two gametes: the egg cell and the central cell, accompanied with three antipodals and two synergids. While for the male side, each microspore undergoes an asymmetric division to give rise to a larger vegetative cell and a smaller generative cell within the bicellular pollen grain. The generative cell divides further to produce the gametes: two sperm cells. During double fertilization, the egg cell is fertilized by one sperm to form the zygote that will give rise to the embryo, while the central cell fuses with the other sperm to generate the triploid endosperm. Original drawings were made after microscopy pictures (female sporogenesis) or inspired from Zhang et al. (2011) (male sporogenesis).
Mentions: Flowering plants have a life cycle alternating between a dominant, diploid sporophytic phase and a short haploid gametophytic phase. Sexual reproduction can be divided into three phases: sporogenesis, gametogenesis, embryo- and endosperm-genesis (Figure 1). Unlike animals, plants do not set aside a germline lineage during embryogenesis. Instead, the reproductive lineage is established late in development. Cells that will share a meiotic fate and hence initiate a “reproductive lineage” differentiate from and within a somatic tissue in dedicated floral organs of adult plants. Sporogenesis is initiated by the differentiation of spore mother cells (SMCs) that engage somatic cells into a meiotic fate entailing the development of haploid, multicellular gametophytes. The female SMC, also called megaspore mother cell (MMC) differentiates in a subepidermal position in an ovule primordium – composed of the L1-outer layer of cells and the nucellus –; the male SMC differentiates from a mitotic division of the archesporial cell within the sporangium of the anther locule (Figure 1, and see section Chromatin Dynamics During Sporogenesis). Gametogenesis is the process by which the gametes are formed within the gametophytes. The male and female gametophytes develop from one haploid spore through a limited number of mitosis and cellularization events that will give rise to highly distinct cell types. A vast majority of flowering plants share the seven-celled type of female gametophyte comprising two gametes – the egg cell and the central cell – and five accessory cells – two synergids and three antipodals. All cells are haploid except for the central cell that inherits two polar nuclei, which following fusion generate a di-haploid maternal genome in the central cell. In contrast, the mature male gametophyte contained in the pollen grain is highly reduced and is composed of one vegetative – accessory – cell and two gametes, the sperm cells (Maheshwari, 1950; Figure 1). During double fertilization, the egg cell fuses with one sperm to give rise to the diploid zygote, while the central cell is fertilized by the second sperm cell – from the same pollen – to produce the triploid endosperm (Figure 1). Strikingly, although genetically identical the two fertilization products share distinct developmental fates. The totipotent zygote engages into embryogenesis that establishes the basic body plan and the symmetries (axial and radial) of the future seedling; in contrast, the primary endosperm cell engages in a syncytial phase of proliferation, before cellularization, to form an extra-embryonic, nurturing tissue (Maheshwari, 1950).

Bottom Line: This ability is exemplified during sexual reproduction in flowering plants where novel cell types are generated in floral tissues of the adult plant during sporogenesis, gametogenesis, and embryogenesis.While the molecular and genetic basis of cell specification during sexual reproduction is being studied for a long time, recent works disclosed an unsuspected role of global chromatin organization and its dynamics.In this review, we describe the events of chromatin dynamics during the different phases of sexual reproduction and discuss their possible significance particularly in cell fate establishment.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Biology - Zürich-Basel Plant Science Center, University of Zürich Zürich, Switzerland.

ABSTRACT
Plants have the remarkable ability to establish new cell fates throughout their life cycle, in contrast to most animals that define all cell lineages during embryogenesis. This ability is exemplified during sexual reproduction in flowering plants where novel cell types are generated in floral tissues of the adult plant during sporogenesis, gametogenesis, and embryogenesis. While the molecular and genetic basis of cell specification during sexual reproduction is being studied for a long time, recent works disclosed an unsuspected role of global chromatin organization and its dynamics. In this review, we describe the events of chromatin dynamics during the different phases of sexual reproduction and discuss their possible significance particularly in cell fate establishment.

No MeSH data available.


Related in: MedlinePlus