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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

Chromatin dynamics during female gametogenesis. This scheme summarizes mostly cytogenetic and GFP reporter protein analyses suggesting large-scale chromatin dynamics events during female gametophyte development. Although genome-wide, molecular profiling of the chromatin state is currently missing, these data provide, like for Figure 3, a conceptual framework for apprehending the extent and potential significance of chromatin dynamics during this developmental stage. Following cellularization, a dimorphic chromatin landscapes are established between the egg cell and the central cell. The central cell chromatin harbors a decondensed chromatin with a low heterochromatin content, correlating with low levels of H3K9me2 and the H3K27me3 reader protein LHP1, but is enriched in active PolII (Ser2 phosphorylated PolII) allowing for active transcription (Pillot et al., 2010). The notable absence of DNA methyltransferases and the presence of the DNA glycosylase DEMETER catalyzing DNA methylation suggest a hypomethylated genome. In contrast, the egg cell harbors heterochromatin foci, though not as prominently as in somatic nuclei and high levels of H3K9me2 and LHP1, but undetectable levels of PolII, suggesting a repressed transcriptional state. Somatic histone variants are depleted from both gametes, with only HTR3, HTR8 and HTR14 retained in the central cell and HTR5 in the egg cell. The model for dynamic changes of CG and CHH methylation is speculative, and is inferred from the analysis of DNA methylation in the endosperm and embryo (Hsieh et al., 2009; Ibarra et al., 2012), as well as the differential expression of DNA methyltransferases between the central cell and egg cell (Jullien et al., 2012). The epigenetic dimorphism concerning heterochromatin content, H3K9me2 and LHP1 seems established just after cellularization.
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Figure 4: Chromatin dynamics during female gametogenesis. This scheme summarizes mostly cytogenetic and GFP reporter protein analyses suggesting large-scale chromatin dynamics events during female gametophyte development. Although genome-wide, molecular profiling of the chromatin state is currently missing, these data provide, like for Figure 3, a conceptual framework for apprehending the extent and potential significance of chromatin dynamics during this developmental stage. Following cellularization, a dimorphic chromatin landscapes are established between the egg cell and the central cell. The central cell chromatin harbors a decondensed chromatin with a low heterochromatin content, correlating with low levels of H3K9me2 and the H3K27me3 reader protein LHP1, but is enriched in active PolII (Ser2 phosphorylated PolII) allowing for active transcription (Pillot et al., 2010). The notable absence of DNA methyltransferases and the presence of the DNA glycosylase DEMETER catalyzing DNA methylation suggest a hypomethylated genome. In contrast, the egg cell harbors heterochromatin foci, though not as prominently as in somatic nuclei and high levels of H3K9me2 and LHP1, but undetectable levels of PolII, suggesting a repressed transcriptional state. Somatic histone variants are depleted from both gametes, with only HTR3, HTR8 and HTR14 retained in the central cell and HTR5 in the egg cell. The model for dynamic changes of CG and CHH methylation is speculative, and is inferred from the analysis of DNA methylation in the endosperm and embryo (Hsieh et al., 2009; Ibarra et al., 2012), as well as the differential expression of DNA methyltransferases between the central cell and egg cell (Jullien et al., 2012). The epigenetic dimorphism concerning heterochromatin content, H3K9me2 and LHP1 seems established just after cellularization.

Mentions: The female gametophyte has a syncytial mode of development until the eight-nuclear stage. The bipolar organization of the gametophyte is short lived and migration of two polar nuclei toward the center of the syncytium quickly sets the future pattern of the mature embryo sac, which is definitively set at cellularization (Sprunck and Gross-Hardt, 2011). A microscopic observation of the nuclear size and chromatin appearance at the consecutive stages of development suggests a rather decondensed state of the chromatin but also rapid changes entailed by cellularization (Célia Baroux, unpublished). Particularly, while the antipodals and synergids seem to regain a chromatin organization similar to that of sporophytic cells, the egg and the central cells reveal globally less condensed chromatin state, with fewer heterochromatin foci compared to that of the somatic cells (Jullien and Berger, 2010; Baroux et al., 2011). Yet, the gametes appear clearly dimorphic with a more pronounced decondensation in the central cell and this dimorphism, similar to that between the vegetative cell and the sperm cells, respectively, in the male gametophyte, is further illustrated by the distinct epigenetic and transcriptional landscapes detected using cytogenetic investigations (Pillot et al., 2010). The chromatin in the central cell shows a dramatic reduction of H3K9me2 and LHP1 induced at/after cellularization of the gametophyte, while being transcriptionally active. In contrast, the egg cell chromatin harbors high levels of LHP1 and H3K9me2 at conspicuous foci, coincidentally with low-to-undetectable levels of active RNA PolII, reflecting a relatively transcriptional quiescent state (Pillot et al., 2010; Figure 4). Concomitantly, unequal expression of DNA methyltransferases in the central cell and egg cell – with notably undetectable level of these enzymes in the central cell contrasting with the presence of de novo DNA methyltransferases DRM1/2 in the egg – may contribute to reinforce the epigenetic dimorphism (Jullien et al., 2012).


Chromatin dynamics during plant sexual reproduction.

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

Chromatin dynamics during female gametogenesis. This scheme summarizes mostly cytogenetic and GFP reporter protein analyses suggesting large-scale chromatin dynamics events during female gametophyte development. Although genome-wide, molecular profiling of the chromatin state is currently missing, these data provide, like for Figure 3, a conceptual framework for apprehending the extent and potential significance of chromatin dynamics during this developmental stage. Following cellularization, a dimorphic chromatin landscapes are established between the egg cell and the central cell. The central cell chromatin harbors a decondensed chromatin with a low heterochromatin content, correlating with low levels of H3K9me2 and the H3K27me3 reader protein LHP1, but is enriched in active PolII (Ser2 phosphorylated PolII) allowing for active transcription (Pillot et al., 2010). The notable absence of DNA methyltransferases and the presence of the DNA glycosylase DEMETER catalyzing DNA methylation suggest a hypomethylated genome. In contrast, the egg cell harbors heterochromatin foci, though not as prominently as in somatic nuclei and high levels of H3K9me2 and LHP1, but undetectable levels of PolII, suggesting a repressed transcriptional state. Somatic histone variants are depleted from both gametes, with only HTR3, HTR8 and HTR14 retained in the central cell and HTR5 in the egg cell. The model for dynamic changes of CG and CHH methylation is speculative, and is inferred from the analysis of DNA methylation in the endosperm and embryo (Hsieh et al., 2009; Ibarra et al., 2012), as well as the differential expression of DNA methyltransferases between the central cell and egg cell (Jullien et al., 2012). The epigenetic dimorphism concerning heterochromatin content, H3K9me2 and LHP1 seems established just after cellularization.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Chromatin dynamics during female gametogenesis. This scheme summarizes mostly cytogenetic and GFP reporter protein analyses suggesting large-scale chromatin dynamics events during female gametophyte development. Although genome-wide, molecular profiling of the chromatin state is currently missing, these data provide, like for Figure 3, a conceptual framework for apprehending the extent and potential significance of chromatin dynamics during this developmental stage. Following cellularization, a dimorphic chromatin landscapes are established between the egg cell and the central cell. The central cell chromatin harbors a decondensed chromatin with a low heterochromatin content, correlating with low levels of H3K9me2 and the H3K27me3 reader protein LHP1, but is enriched in active PolII (Ser2 phosphorylated PolII) allowing for active transcription (Pillot et al., 2010). The notable absence of DNA methyltransferases and the presence of the DNA glycosylase DEMETER catalyzing DNA methylation suggest a hypomethylated genome. In contrast, the egg cell harbors heterochromatin foci, though not as prominently as in somatic nuclei and high levels of H3K9me2 and LHP1, but undetectable levels of PolII, suggesting a repressed transcriptional state. Somatic histone variants are depleted from both gametes, with only HTR3, HTR8 and HTR14 retained in the central cell and HTR5 in the egg cell. The model for dynamic changes of CG and CHH methylation is speculative, and is inferred from the analysis of DNA methylation in the endosperm and embryo (Hsieh et al., 2009; Ibarra et al., 2012), as well as the differential expression of DNA methyltransferases between the central cell and egg cell (Jullien et al., 2012). The epigenetic dimorphism concerning heterochromatin content, H3K9me2 and LHP1 seems established just after cellularization.
Mentions: The female gametophyte has a syncytial mode of development until the eight-nuclear stage. The bipolar organization of the gametophyte is short lived and migration of two polar nuclei toward the center of the syncytium quickly sets the future pattern of the mature embryo sac, which is definitively set at cellularization (Sprunck and Gross-Hardt, 2011). A microscopic observation of the nuclear size and chromatin appearance at the consecutive stages of development suggests a rather decondensed state of the chromatin but also rapid changes entailed by cellularization (Célia Baroux, unpublished). Particularly, while the antipodals and synergids seem to regain a chromatin organization similar to that of sporophytic cells, the egg and the central cells reveal globally less condensed chromatin state, with fewer heterochromatin foci compared to that of the somatic cells (Jullien and Berger, 2010; Baroux et al., 2011). Yet, the gametes appear clearly dimorphic with a more pronounced decondensation in the central cell and this dimorphism, similar to that between the vegetative cell and the sperm cells, respectively, in the male gametophyte, is further illustrated by the distinct epigenetic and transcriptional landscapes detected using cytogenetic investigations (Pillot et al., 2010). The chromatin in the central cell shows a dramatic reduction of H3K9me2 and LHP1 induced at/after cellularization of the gametophyte, while being transcriptionally active. In contrast, the egg cell chromatin harbors high levels of LHP1 and H3K9me2 at conspicuous foci, coincidentally with low-to-undetectable levels of active RNA PolII, reflecting a relatively transcriptional quiescent state (Pillot et al., 2010; Figure 4). Concomitantly, unequal expression of DNA methyltransferases in the central cell and egg cell – with notably undetectable level of these enzymes in the central cell contrasting with the presence of de novo DNA methyltransferases DRM1/2 in the egg – may contribute to reinforce the epigenetic dimorphism (Jullien et al., 2012).

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