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Over-expression of Arabidopsis AtCHR23 chromatin remodeling ATPase results in increased variability of growth and gene expression.

Folta A, Severing EI, Krauskopf J, van de Geest H, Verver J, Nap JP, Mlynarova L - BMC Plant Biol. (2014)

Bottom Line: Already modest (2-fold) over-expression of the AtCHR23 ATPase gene in Arabidopsis results in overall reduced growth compared to the wild-type.Detailed analyses show that in the root, the reduction of growth is due to reduced cell elongation.In contrast, the knockout mutation of AtCHR23 does not lead to such visible phenotypic effects.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory of Molecular Biology, Plant Sciences Group, Wageningen University and Research Centre, Droevendaalsesteeg 1, Wageningen 6708 PB, The Netherlands. ludmila.mlynarova@wur.nl.

ABSTRACT

Background: Plants are sessile organisms that deal with their -sometimes adverse- environment in well-regulated ways. Chromatin remodeling involving SWI/SNF2-type ATPases is thought to be an important epigenetic mechanism for the regulation of gene expression in different developmental programs and for integrating these programs with the response to environmental signals. In this study, we report on the role of chromatin remodeling in Arabidopsis with respect to the variability of growth and gene expression in relationship to environmental conditions.

Results: Already modest (2-fold) over-expression of the AtCHR23 ATPase gene in Arabidopsis results in overall reduced growth compared to the wild-type. Detailed analyses show that in the root, the reduction of growth is due to reduced cell elongation. The reduced-growth phenotype requires sufficient light and is magnified by applying deliberate abiotic (salt, osmotic) stress. In contrast, the knockout mutation of AtCHR23 does not lead to such visible phenotypic effects. In addition, we show that over-expression of AtCHR23 increases the variability of growth in populations of genetically identical plants. These data indicate that accurate and controlled expression of AtCHR23 contributes to the stability or robustness of growth. Detailed RNAseq analyses demonstrate that upon AtCHR23 over-expression also the variation of gene expression is increased in a subset of genes that associate with environmental stress. The larger variation of gene expression is confirmed in individual plants with the help of independent qRT-PCR analysis.

Conclusions: Over-expression of AtCHR23 gives Arabidopsis a phenotype that is markedly different from the growth arrest phenotype observed upon over-expression of AtCHR12, the paralog of AtCHR23, in response to abiotic stress. This demonstrates functional sub-specialization of highly similar ATPases in Arabidopsis. Over-expression of AtCHR23 increases the variability of growth among genetically identical individuals in a way that is consistent with increased variability of expression of a distinct subset of genes that associate with environmental stress. We propose that ATCHR23-mediated chromatin remodeling is a potential component of a buffer system in plants that protects against environmentally-induced phenotypic and transcriptional variation.

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Frequency distribution of root (A) and hypocotyl (B) length. Seedlings (40 for each panel) were grown on agar plates for eight days at 23°C (A) or 28°C (B) in long-day conditions. In each panel, the arrow indicates the median length.
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Figure 2: Frequency distribution of root (A) and hypocotyl (B) length. Seedlings (40 for each panel) were grown on agar plates for eight days at 23°C (A) or 28°C (B) in long-day conditions. In each panel, the arrow indicates the median length.

Mentions: The variability in the phenotypic assays was assessed in more detail by analysis of the frequency distributions of the length data (Figure 2). The frequency distribution of the root lengths shows that the distribution is shifted to shorter roots when AtCHR23 is over-expressed (Figure 2A), but still quite a number of individual seedlings have roots as long as the wild-type (Figure 2A, middle two panels). Also for the distribution of the hypocotyl length, the variation is larger in populations of over-expressing seedlings than in the wild-type (Figure 2B, middle two panels). In view of all experimental efforts to standardize the environment in the phenotypic assays, we think the variation between individuals of over-expressing lines is likely to have a molecular and/or functional basis.


Over-expression of Arabidopsis AtCHR23 chromatin remodeling ATPase results in increased variability of growth and gene expression.

Folta A, Severing EI, Krauskopf J, van de Geest H, Verver J, Nap JP, Mlynarova L - BMC Plant Biol. (2014)

Frequency distribution of root (A) and hypocotyl (B) length. Seedlings (40 for each panel) were grown on agar plates for eight days at 23°C (A) or 28°C (B) in long-day conditions. In each panel, the arrow indicates the median length.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3987066&req=5

Figure 2: Frequency distribution of root (A) and hypocotyl (B) length. Seedlings (40 for each panel) were grown on agar plates for eight days at 23°C (A) or 28°C (B) in long-day conditions. In each panel, the arrow indicates the median length.
Mentions: The variability in the phenotypic assays was assessed in more detail by analysis of the frequency distributions of the length data (Figure 2). The frequency distribution of the root lengths shows that the distribution is shifted to shorter roots when AtCHR23 is over-expressed (Figure 2A), but still quite a number of individual seedlings have roots as long as the wild-type (Figure 2A, middle two panels). Also for the distribution of the hypocotyl length, the variation is larger in populations of over-expressing seedlings than in the wild-type (Figure 2B, middle two panels). In view of all experimental efforts to standardize the environment in the phenotypic assays, we think the variation between individuals of over-expressing lines is likely to have a molecular and/or functional basis.

Bottom Line: Already modest (2-fold) over-expression of the AtCHR23 ATPase gene in Arabidopsis results in overall reduced growth compared to the wild-type.Detailed analyses show that in the root, the reduction of growth is due to reduced cell elongation.In contrast, the knockout mutation of AtCHR23 does not lead to such visible phenotypic effects.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory of Molecular Biology, Plant Sciences Group, Wageningen University and Research Centre, Droevendaalsesteeg 1, Wageningen 6708 PB, The Netherlands. ludmila.mlynarova@wur.nl.

ABSTRACT

Background: Plants are sessile organisms that deal with their -sometimes adverse- environment in well-regulated ways. Chromatin remodeling involving SWI/SNF2-type ATPases is thought to be an important epigenetic mechanism for the regulation of gene expression in different developmental programs and for integrating these programs with the response to environmental signals. In this study, we report on the role of chromatin remodeling in Arabidopsis with respect to the variability of growth and gene expression in relationship to environmental conditions.

Results: Already modest (2-fold) over-expression of the AtCHR23 ATPase gene in Arabidopsis results in overall reduced growth compared to the wild-type. Detailed analyses show that in the root, the reduction of growth is due to reduced cell elongation. The reduced-growth phenotype requires sufficient light and is magnified by applying deliberate abiotic (salt, osmotic) stress. In contrast, the knockout mutation of AtCHR23 does not lead to such visible phenotypic effects. In addition, we show that over-expression of AtCHR23 increases the variability of growth in populations of genetically identical plants. These data indicate that accurate and controlled expression of AtCHR23 contributes to the stability or robustness of growth. Detailed RNAseq analyses demonstrate that upon AtCHR23 over-expression also the variation of gene expression is increased in a subset of genes that associate with environmental stress. The larger variation of gene expression is confirmed in individual plants with the help of independent qRT-PCR analysis.

Conclusions: Over-expression of AtCHR23 gives Arabidopsis a phenotype that is markedly different from the growth arrest phenotype observed upon over-expression of AtCHR12, the paralog of AtCHR23, in response to abiotic stress. This demonstrates functional sub-specialization of highly similar ATPases in Arabidopsis. Over-expression of AtCHR23 increases the variability of growth among genetically identical individuals in a way that is consistent with increased variability of expression of a distinct subset of genes that associate with environmental stress. We propose that ATCHR23-mediated chromatin remodeling is a potential component of a buffer system in plants that protects against environmentally-induced phenotypic and transcriptional variation.

Show MeSH
Related in: MedlinePlus