Limits...
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.


Chromatin dynamics in plant MMCs shows similarities to that in animal PGCs. (A) The MMC (red contour) originates from a subepidermal somatic cell in the ovule primordium, it is distinct from the surrounding nucellar cells by its enlarged nuclear size, as shown by whole-mount DNA staining using propidium iodide of the early ovule primordium as described (She et al., 2013). Scale bar: 10 μm. (B) Specification of PMCs (red contour) in the anther, which are marked by the enlarged nuclear and nucleolar size compared to the surrounding somatic cells. The anther was stained by propidium iodide in whole-mount as described for ovule primordia (She et al., 2013). Scale bar: 10 μm. (C) Likewise in animal PGCs, plant MMCs undergo drastic changes in chromatin modification patterns. The schemes summarize studies from Hajkova et al. (2008) and She et al. (2013). However and in contrast, events are asynchronous in plant MMCs and are characterized by both gain and depletion of marks, while animal PGCs at stage 10.5 show a marked depletion of all marks analyzed (Reprinted by permission from Macmillan Publishers Ltd: Nature, Hajkova et al., 2008),© 2008 and Prof. Azim Surani (The Gurdon Institute, University of Cambridge). The schematic images for PGCs development were modified after Ohno et al. (2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4109563&req=5

Figure 2: Chromatin dynamics in plant MMCs shows similarities to that in animal PGCs. (A) The MMC (red contour) originates from a subepidermal somatic cell in the ovule primordium, it is distinct from the surrounding nucellar cells by its enlarged nuclear size, as shown by whole-mount DNA staining using propidium iodide of the early ovule primordium as described (She et al., 2013). Scale bar: 10 μm. (B) Specification of PMCs (red contour) in the anther, which are marked by the enlarged nuclear and nucleolar size compared to the surrounding somatic cells. The anther was stained by propidium iodide in whole-mount as described for ovule primordia (She et al., 2013). Scale bar: 10 μm. (C) Likewise in animal PGCs, plant MMCs undergo drastic changes in chromatin modification patterns. The schemes summarize studies from Hajkova et al. (2008) and She et al. (2013). However and in contrast, events are asynchronous in plant MMCs and are characterized by both gain and depletion of marks, while animal PGCs at stage 10.5 show a marked depletion of all marks analyzed (Reprinted by permission from Macmillan Publishers Ltd: Nature, Hajkova et al., 2008),© 2008 and Prof. Azim Surani (The Gurdon Institute, University of Cambridge). The schematic images for PGCs development were modified after Ohno et al. (2013).

Mentions: The first visible signs of SMC differentiation are cellular and nuclear enlargement in the sporogenous tissue. Visible changes in nuclear morphology during MMC differentiation were reported on early drawings or micrographs with clear nuclear and nucleolar enlargement compared to the surrounding nucellar cells (Cooper, 1937; Schulz and Jensen, 1981; Armstrong and Jones, 2003; Sniezko, 2006). In light of our current understanding, these observations suggest large-scale chromatin reorganization. Nuclear swelling and chromatin decondensation in differentiating MMC was recently confirmed and quantified (Figure 2A, She et al., 2013). Interestingly, it correlates with the depletion of canonical linker histones and the concomitant, yet progressive reduction in heterochromatin content (She et al., 2013). This H1 depletion is the earliest event of MMC differentiation at a stage where cellular differentiation is barely visible strongly suggests a causal link between chromatin dynamics and the somatic-to-reproductive fate transition in this cell. Following this event, the MMC chromatin undergoes further nucleosome remodeling and biphasic changes in histone modifications (Figure 2C). Nucleosome remodeling is illustrated by a presumably dynamic turnover of the centromeric-specific H3 variant (CENH3). This was incidentally detected in the MMC by the depletion of a C-terminally tagged CENH3 variant that failed to be reloaded, in contrast to its N-terminally tagged counterpart (She et al., 2013), in agreement with the model established in male SMCs (Ravi et al., 2011; Schubert et al., 2014). Moreover, the incorporation of a specific H3.3 variant (HTR8) in the MMC suggests global changes in nucleosome composition. Further chromatin dynamics events affecting histone modifications occur along a long meiotic S-phase and seem to establish a transcriptionally permissive state (She et al., 2013). This is suggested by a quantitative increase in the permissive-associated mark H3K4me3, and the reduction of repressive-related marks including H3K27me1, H3K27me3, and H3K9me1 in MMCs, compared to that in surrounding nucellar cells (She et al., 2013). However, decreasing levels of Ser2-phosphorylated RNA PolII and H4Kac16 indicated a moderate transcriptional competence.


Chromatin dynamics during plant sexual reproduction.

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

Chromatin dynamics in plant MMCs shows similarities to that in animal PGCs. (A) The MMC (red contour) originates from a subepidermal somatic cell in the ovule primordium, it is distinct from the surrounding nucellar cells by its enlarged nuclear size, as shown by whole-mount DNA staining using propidium iodide of the early ovule primordium as described (She et al., 2013). Scale bar: 10 μm. (B) Specification of PMCs (red contour) in the anther, which are marked by the enlarged nuclear and nucleolar size compared to the surrounding somatic cells. The anther was stained by propidium iodide in whole-mount as described for ovule primordia (She et al., 2013). Scale bar: 10 μm. (C) Likewise in animal PGCs, plant MMCs undergo drastic changes in chromatin modification patterns. The schemes summarize studies from Hajkova et al. (2008) and She et al. (2013). However and in contrast, events are asynchronous in plant MMCs and are characterized by both gain and depletion of marks, while animal PGCs at stage 10.5 show a marked depletion of all marks analyzed (Reprinted by permission from Macmillan Publishers Ltd: Nature, Hajkova et al., 2008),© 2008 and Prof. Azim Surani (The Gurdon Institute, University of Cambridge). The schematic images for PGCs development were modified after Ohno et al. (2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Chromatin dynamics in plant MMCs shows similarities to that in animal PGCs. (A) The MMC (red contour) originates from a subepidermal somatic cell in the ovule primordium, it is distinct from the surrounding nucellar cells by its enlarged nuclear size, as shown by whole-mount DNA staining using propidium iodide of the early ovule primordium as described (She et al., 2013). Scale bar: 10 μm. (B) Specification of PMCs (red contour) in the anther, which are marked by the enlarged nuclear and nucleolar size compared to the surrounding somatic cells. The anther was stained by propidium iodide in whole-mount as described for ovule primordia (She et al., 2013). Scale bar: 10 μm. (C) Likewise in animal PGCs, plant MMCs undergo drastic changes in chromatin modification patterns. The schemes summarize studies from Hajkova et al. (2008) and She et al. (2013). However and in contrast, events are asynchronous in plant MMCs and are characterized by both gain and depletion of marks, while animal PGCs at stage 10.5 show a marked depletion of all marks analyzed (Reprinted by permission from Macmillan Publishers Ltd: Nature, Hajkova et al., 2008),© 2008 and Prof. Azim Surani (The Gurdon Institute, University of Cambridge). The schematic images for PGCs development were modified after Ohno et al. (2013).
Mentions: The first visible signs of SMC differentiation are cellular and nuclear enlargement in the sporogenous tissue. Visible changes in nuclear morphology during MMC differentiation were reported on early drawings or micrographs with clear nuclear and nucleolar enlargement compared to the surrounding nucellar cells (Cooper, 1937; Schulz and Jensen, 1981; Armstrong and Jones, 2003; Sniezko, 2006). In light of our current understanding, these observations suggest large-scale chromatin reorganization. Nuclear swelling and chromatin decondensation in differentiating MMC was recently confirmed and quantified (Figure 2A, She et al., 2013). Interestingly, it correlates with the depletion of canonical linker histones and the concomitant, yet progressive reduction in heterochromatin content (She et al., 2013). This H1 depletion is the earliest event of MMC differentiation at a stage where cellular differentiation is barely visible strongly suggests a causal link between chromatin dynamics and the somatic-to-reproductive fate transition in this cell. Following this event, the MMC chromatin undergoes further nucleosome remodeling and biphasic changes in histone modifications (Figure 2C). Nucleosome remodeling is illustrated by a presumably dynamic turnover of the centromeric-specific H3 variant (CENH3). This was incidentally detected in the MMC by the depletion of a C-terminally tagged CENH3 variant that failed to be reloaded, in contrast to its N-terminally tagged counterpart (She et al., 2013), in agreement with the model established in male SMCs (Ravi et al., 2011; Schubert et al., 2014). Moreover, the incorporation of a specific H3.3 variant (HTR8) in the MMC suggests global changes in nucleosome composition. Further chromatin dynamics events affecting histone modifications occur along a long meiotic S-phase and seem to establish a transcriptionally permissive state (She et al., 2013). This is suggested by a quantitative increase in the permissive-associated mark H3K4me3, and the reduction of repressive-related marks including H3K27me1, H3K27me3, and H3K9me1 in MMCs, compared to that in surrounding nucellar cells (She et al., 2013). However, decreasing levels of Ser2-phosphorylated RNA PolII and H4Kac16 indicated a moderate transcriptional competence.

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.