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SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development.

Yao X, Feng H, Yu Y, Dong A, Shen WH - PLoS ONE (2013)

Bottom Line: Loss of SDG2 results in drastically reduced H3K4me3 levels in root SCN and differentiated cells and causes the loss of auxin gradient maximum in the root quiescent centre.Genetic interaction analysis reveals that SDG2 and CHROMATIN ASSEMBLY FACTOR-1 act synergistically in root SCN and genome integrity maintenance but not in telomere length maintenance.We conclude that SDG2-mediated H3K4me3 plays a distinctive role in the regulation of chromatin structure and genome integrity, which are key features in pluripotency of stem cells and crucial for root growth and development.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Engineering, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, School of Life Sciences, Fudan University, Shanghai, PR China.

ABSTRACT
Trithorax group (TrxG) proteins are evolutionarily conserved in eukaryotes and play critical roles in transcriptional activation via deposition of histone H3 lysine 4 trimethylation (H3K4me3) in chromatin. Several Arabidopsis TrxG members have been characterized, and among them SET DOMAIN GROUP 2 (SDG2) has been shown to be necessary for global genome-wide H3K4me3 deposition. Although pleiotropic phenotypes have been uncovered in the sdg2 mutants, SDG2 function in the regulation of stem cell activity has remained largely unclear. Here, we investigate the sdg2 mutant root phenotype and demonstrate that SDG2 is required for primary root stem cell niche (SCN) maintenance as well as for lateral root SCN establishment. Loss of SDG2 results in drastically reduced H3K4me3 levels in root SCN and differentiated cells and causes the loss of auxin gradient maximum in the root quiescent centre. Elevated DNA damage is detected in the sdg2 mutant, suggesting that impaired genome integrity may also have challenged the stem cell activity. Genetic interaction analysis reveals that SDG2 and CHROMATIN ASSEMBLY FACTOR-1 act synergistically in root SCN and genome integrity maintenance but not in telomere length maintenance. We conclude that SDG2-mediated H3K4me3 plays a distinctive role in the regulation of chromatin structure and genome integrity, which are key features in pluripotency of stem cells and crucial for root growth and development.

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Loss of SDG2 drastically reduces nuclear H3K4me3 levels in root cells.Whole-mount root immunofluorescence staining was performed using an antibody specifically recognizing H3K4me3. Panels from left to right subsequently show confocal images of DAPI, H3K4me3 and merged signals. Close-up images show regions around the root stem cell niche with the QC cells circled. Bar = 50 µm.
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pone-0056537-g006: Loss of SDG2 drastically reduces nuclear H3K4me3 levels in root cells.Whole-mount root immunofluorescence staining was performed using an antibody specifically recognizing H3K4me3. Panels from left to right subsequently show confocal images of DAPI, H3K4me3 and merged signals. Close-up images show regions around the root stem cell niche with the QC cells circled. Bar = 50 µm.

Mentions: Finally, we addressed the questions whether SDG2 is required for H3K4me3 deposition in specific root cells and whether it affects genome integrity. Previous western blot analyses have shown that H3K4m3 level is reduced in sdg2 mutant plants [39], [40]. We analyzed H3K4me3 levels in individual cells by whole-mount root immunofluorescence [53]. In WT roots, a strong H3K4me3 signal was detected in the nuclei of all cells except for stele cells which showed a weak H3K4me3 signal (Figure 6). In sdg2-3 roots, the H3K4me3 signal was drastically reduced, with only a small number of cells showing clear visible immunofluorescence (Figure 6). Most remarkably, root SCN cells and in particular QC cells showed strong H3K4me3 immunostaining in WT but a very weak signal in sdg2-3 (Figure 6). These observations demonstrate that SDG2 is a H3K4-methyltransferase required for global H3K4me3 deposition in root cells, and that impaired H3K4me3 deposition correlates with interrupted stem cell function in the sdg2-3 mutant root SCN.


SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development.

Yao X, Feng H, Yu Y, Dong A, Shen WH - PLoS ONE (2013)

Loss of SDG2 drastically reduces nuclear H3K4me3 levels in root cells.Whole-mount root immunofluorescence staining was performed using an antibody specifically recognizing H3K4me3. Panels from left to right subsequently show confocal images of DAPI, H3K4me3 and merged signals. Close-up images show regions around the root stem cell niche with the QC cells circled. Bar = 50 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585709&req=5

pone-0056537-g006: Loss of SDG2 drastically reduces nuclear H3K4me3 levels in root cells.Whole-mount root immunofluorescence staining was performed using an antibody specifically recognizing H3K4me3. Panels from left to right subsequently show confocal images of DAPI, H3K4me3 and merged signals. Close-up images show regions around the root stem cell niche with the QC cells circled. Bar = 50 µm.
Mentions: Finally, we addressed the questions whether SDG2 is required for H3K4me3 deposition in specific root cells and whether it affects genome integrity. Previous western blot analyses have shown that H3K4m3 level is reduced in sdg2 mutant plants [39], [40]. We analyzed H3K4me3 levels in individual cells by whole-mount root immunofluorescence [53]. In WT roots, a strong H3K4me3 signal was detected in the nuclei of all cells except for stele cells which showed a weak H3K4me3 signal (Figure 6). In sdg2-3 roots, the H3K4me3 signal was drastically reduced, with only a small number of cells showing clear visible immunofluorescence (Figure 6). Most remarkably, root SCN cells and in particular QC cells showed strong H3K4me3 immunostaining in WT but a very weak signal in sdg2-3 (Figure 6). These observations demonstrate that SDG2 is a H3K4-methyltransferase required for global H3K4me3 deposition in root cells, and that impaired H3K4me3 deposition correlates with interrupted stem cell function in the sdg2-3 mutant root SCN.

Bottom Line: Loss of SDG2 results in drastically reduced H3K4me3 levels in root SCN and differentiated cells and causes the loss of auxin gradient maximum in the root quiescent centre.Genetic interaction analysis reveals that SDG2 and CHROMATIN ASSEMBLY FACTOR-1 act synergistically in root SCN and genome integrity maintenance but not in telomere length maintenance.We conclude that SDG2-mediated H3K4me3 plays a distinctive role in the regulation of chromatin structure and genome integrity, which are key features in pluripotency of stem cells and crucial for root growth and development.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Engineering, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, School of Life Sciences, Fudan University, Shanghai, PR China.

ABSTRACT
Trithorax group (TrxG) proteins are evolutionarily conserved in eukaryotes and play critical roles in transcriptional activation via deposition of histone H3 lysine 4 trimethylation (H3K4me3) in chromatin. Several Arabidopsis TrxG members have been characterized, and among them SET DOMAIN GROUP 2 (SDG2) has been shown to be necessary for global genome-wide H3K4me3 deposition. Although pleiotropic phenotypes have been uncovered in the sdg2 mutants, SDG2 function in the regulation of stem cell activity has remained largely unclear. Here, we investigate the sdg2 mutant root phenotype and demonstrate that SDG2 is required for primary root stem cell niche (SCN) maintenance as well as for lateral root SCN establishment. Loss of SDG2 results in drastically reduced H3K4me3 levels in root SCN and differentiated cells and causes the loss of auxin gradient maximum in the root quiescent centre. Elevated DNA damage is detected in the sdg2 mutant, suggesting that impaired genome integrity may also have challenged the stem cell activity. Genetic interaction analysis reveals that SDG2 and CHROMATIN ASSEMBLY FACTOR-1 act synergistically in root SCN and genome integrity maintenance but not in telomere length maintenance. We conclude that SDG2-mediated H3K4me3 plays a distinctive role in the regulation of chromatin structure and genome integrity, which are key features in pluripotency of stem cells and crucial for root growth and development.

Show MeSH
Related in: MedlinePlus