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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.


Three main waves of chromatin dynamics during plant reproduction (Model). Sexual plant reproduction can be seen as a three-step process involving sporogenesis, gametogenesis, and embryogenesis taking place in floral organs. Sporogenesis initiates with the specification of spore mother cells (SMCs) within the sporangium tissues. SMCs are primed toward meiosis while undergoing a somatic-to-reproductive cellular fate transition that generates a pluripotent spore. The spore develops a (male or female) multicellular gametophyte generating distinct cell types: the companion (or accessory) cells and the gametic cells (a schematically reduced form is shown, for more details see Figure 1). Fertilization enables the formation of a totipotent zygote, generating in turn the plant embryo. The acquisition of the SMC fate, the gametic fate and the totipotent zygotic fate is associated with three main waves of chromatin dynamics (I.–III., colored nuclei) comprising large-scale reorganization of the chromatin structure, composition and organization, hence reshaping the epigenetic landscape (as reviewed in the text). Whereas some of those events clearly contribute to cell fate establishment (e.g., I., see the text), the challenge of future investigations is to elucidate the functional role of chromatin dynamics in defining the cells’ potency versus operating cell fate establishment during sexual reproduction.
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Figure 5: Three main waves of chromatin dynamics during plant reproduction (Model). Sexual plant reproduction can be seen as a three-step process involving sporogenesis, gametogenesis, and embryogenesis taking place in floral organs. Sporogenesis initiates with the specification of spore mother cells (SMCs) within the sporangium tissues. SMCs are primed toward meiosis while undergoing a somatic-to-reproductive cellular fate transition that generates a pluripotent spore. The spore develops a (male or female) multicellular gametophyte generating distinct cell types: the companion (or accessory) cells and the gametic cells (a schematically reduced form is shown, for more details see Figure 1). Fertilization enables the formation of a totipotent zygote, generating in turn the plant embryo. The acquisition of the SMC fate, the gametic fate and the totipotent zygotic fate is associated with three main waves of chromatin dynamics (I.–III., colored nuclei) comprising large-scale reorganization of the chromatin structure, composition and organization, hence reshaping the epigenetic landscape (as reviewed in the text). Whereas some of those events clearly contribute to cell fate establishment (e.g., I., see the text), the challenge of future investigations is to elucidate the functional role of chromatin dynamics in defining the cells’ potency versus operating cell fate establishment during sexual reproduction.

Mentions: To date, a broad range of genetic and molecular regulators have been identified that contribute to cell specification processes during sexual reproduction in flowering plants. Yet, with the increasing body of evidence that these processes are accompanied by large-scale chromatin dynamics events, an exciting area is opening; further efforts are needed to comprehend a yet, underestimated level of control mediated by chromatin dynamics likely potentiating the (re)programming of genome expression during those processes. Exciting findings in the past decades uncovered dynamic events of chromatin modifications, DNA methylation, nucleosome remodeling, and small RNA regulation that take place throughout sexual reproduction in flowering plants, particularly during cell fate specification (Figure 5). The possible functions of these events range from epigenetic reprogramming of the genome toward pluri- or totipotency, maintenance of genome integrity, regulation of imprinting but may also functions in immediate cellular tasks at meiosis, mitosis cellularization and patterning in the gametophyte and embryo. In the absence of cell-specific epigenome profiles, however, the impact of chromatin dynamics on epigenetic reprogramming remains largely speculative. Establishing a dogma still requires efforts to overcome the daunting obstacles that obstruct cell-specific epigenome profiling in the reproductive lineage, particularly in the model plant Arabidopsis thaliana. For these experiments, the choice of other model plants (e.g., model crops) where the gametes are more amenable to mechanical isolation may be judicious. The development of cell-specific nuclei isolation approaches (Deal and Henikoff, 2010) may prove a real asset in these efforts, though it still requires improvement for optimization (Wuest et al., 2013). Alternatively, probing the genome at the microscopic scale for its chromatin composition and organization, at high-resolution, at the single-cell level and in a quantitative manner, has proven a valid and fruitful approach (She et al., 2014). It enabled describing unsuspected chromatin dynamics events during SMC and female gamete specification and, in combination with genetic analyses, revealed a functional link with the acquisition of developmental competences (Pillot et al., 2010; She et al., 2013). The completion of such analyses on the male reproductive lineage, in several (model or non-model plants) will be instrumental in determining whether cell specification during reproduction relies on robust, reiterative chromatin dynamics events across developmental phases and genders, and whether an evolutionary conserved scenario exists across eudicots and monocots.


Chromatin dynamics during plant sexual reproduction.

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

Three main waves of chromatin dynamics during plant reproduction (Model). Sexual plant reproduction can be seen as a three-step process involving sporogenesis, gametogenesis, and embryogenesis taking place in floral organs. Sporogenesis initiates with the specification of spore mother cells (SMCs) within the sporangium tissues. SMCs are primed toward meiosis while undergoing a somatic-to-reproductive cellular fate transition that generates a pluripotent spore. The spore develops a (male or female) multicellular gametophyte generating distinct cell types: the companion (or accessory) cells and the gametic cells (a schematically reduced form is shown, for more details see Figure 1). Fertilization enables the formation of a totipotent zygote, generating in turn the plant embryo. The acquisition of the SMC fate, the gametic fate and the totipotent zygotic fate is associated with three main waves of chromatin dynamics (I.–III., colored nuclei) comprising large-scale reorganization of the chromatin structure, composition and organization, hence reshaping the epigenetic landscape (as reviewed in the text). Whereas some of those events clearly contribute to cell fate establishment (e.g., I., see the text), the challenge of future investigations is to elucidate the functional role of chromatin dynamics in defining the cells’ potency versus operating cell fate establishment during sexual reproduction.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Three main waves of chromatin dynamics during plant reproduction (Model). Sexual plant reproduction can be seen as a three-step process involving sporogenesis, gametogenesis, and embryogenesis taking place in floral organs. Sporogenesis initiates with the specification of spore mother cells (SMCs) within the sporangium tissues. SMCs are primed toward meiosis while undergoing a somatic-to-reproductive cellular fate transition that generates a pluripotent spore. The spore develops a (male or female) multicellular gametophyte generating distinct cell types: the companion (or accessory) cells and the gametic cells (a schematically reduced form is shown, for more details see Figure 1). Fertilization enables the formation of a totipotent zygote, generating in turn the plant embryo. The acquisition of the SMC fate, the gametic fate and the totipotent zygotic fate is associated with three main waves of chromatin dynamics (I.–III., colored nuclei) comprising large-scale reorganization of the chromatin structure, composition and organization, hence reshaping the epigenetic landscape (as reviewed in the text). Whereas some of those events clearly contribute to cell fate establishment (e.g., I., see the text), the challenge of future investigations is to elucidate the functional role of chromatin dynamics in defining the cells’ potency versus operating cell fate establishment during sexual reproduction.
Mentions: To date, a broad range of genetic and molecular regulators have been identified that contribute to cell specification processes during sexual reproduction in flowering plants. Yet, with the increasing body of evidence that these processes are accompanied by large-scale chromatin dynamics events, an exciting area is opening; further efforts are needed to comprehend a yet, underestimated level of control mediated by chromatin dynamics likely potentiating the (re)programming of genome expression during those processes. Exciting findings in the past decades uncovered dynamic events of chromatin modifications, DNA methylation, nucleosome remodeling, and small RNA regulation that take place throughout sexual reproduction in flowering plants, particularly during cell fate specification (Figure 5). The possible functions of these events range from epigenetic reprogramming of the genome toward pluri- or totipotency, maintenance of genome integrity, regulation of imprinting but may also functions in immediate cellular tasks at meiosis, mitosis cellularization and patterning in the gametophyte and embryo. In the absence of cell-specific epigenome profiles, however, the impact of chromatin dynamics on epigenetic reprogramming remains largely speculative. Establishing a dogma still requires efforts to overcome the daunting obstacles that obstruct cell-specific epigenome profiling in the reproductive lineage, particularly in the model plant Arabidopsis thaliana. For these experiments, the choice of other model plants (e.g., model crops) where the gametes are more amenable to mechanical isolation may be judicious. The development of cell-specific nuclei isolation approaches (Deal and Henikoff, 2010) may prove a real asset in these efforts, though it still requires improvement for optimization (Wuest et al., 2013). Alternatively, probing the genome at the microscopic scale for its chromatin composition and organization, at high-resolution, at the single-cell level and in a quantitative manner, has proven a valid and fruitful approach (She et al., 2014). It enabled describing unsuspected chromatin dynamics events during SMC and female gamete specification and, in combination with genetic analyses, revealed a functional link with the acquisition of developmental competences (Pillot et al., 2010; She et al., 2013). The completion of such analyses on the male reproductive lineage, in several (model or non-model plants) will be instrumental in determining whether cell specification during reproduction relies on robust, reiterative chromatin dynamics events across developmental phases and genders, and whether an evolutionary conserved scenario exists across eudicots and monocots.

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.