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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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Numbers of genes with high expression variability. The number of plant-line specific and shared genes that are identified as variable are given for the wild-type (Col) and over-expressing mutant (AtCHR23-4ov) in long-day (A) and short-day (B) conditions.
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Figure 8: Numbers of genes with high expression variability. The number of plant-line specific and shared genes that are identified as variable are given for the wild-type (Col) and over-expressing mutant (AtCHR23-4ov) in long-day (A) and short-day (B) conditions.

Mentions: In long-day conditions, the AtCHR23 over-expressing mutant has no less than 2007 genes with larger variation (Figure 8A). Of these, 68 genes were also variable in wild-type (Figure 8; Additional file 4). This shows that AtCHR23 over-expression increases the expression variability of a considerable subgroup of genes compared to the wild-type. In contrast, in short-day conditions, 381 genes were identified as variable in the wild-type, whereas 276 genes were identified in the mutant line, of which 82 were shared (Figure 8B; Additional file 4). The larger subgroup of variable genes is therefore associated with the higher over-expression of AtCHR23 observed in long-day conditions. This may point to a causal relationship between AtCHR23 over-expression and increased variability of gene expression. The 68 long-day variable genes shared between the wild-type and the mutant are less correlated between the two replicates of AtCHR23 over-expressing mutant (R2 = 0.038) relative to the wild-type (R2 = 0.625) (Figure 9). It indicates that the expression of genes which are already noisy in natural conditions (the wild-type) become even more noisy when AtCHR23 is over-expressed.


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)

Numbers of genes with high expression variability. The number of plant-line specific and shared genes that are identified as variable are given for the wild-type (Col) and over-expressing mutant (AtCHR23-4ov) in long-day (A) and short-day (B) conditions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Numbers of genes with high expression variability. The number of plant-line specific and shared genes that are identified as variable are given for the wild-type (Col) and over-expressing mutant (AtCHR23-4ov) in long-day (A) and short-day (B) conditions.
Mentions: In long-day conditions, the AtCHR23 over-expressing mutant has no less than 2007 genes with larger variation (Figure 8A). Of these, 68 genes were also variable in wild-type (Figure 8; Additional file 4). This shows that AtCHR23 over-expression increases the expression variability of a considerable subgroup of genes compared to the wild-type. In contrast, in short-day conditions, 381 genes were identified as variable in the wild-type, whereas 276 genes were identified in the mutant line, of which 82 were shared (Figure 8B; Additional file 4). The larger subgroup of variable genes is therefore associated with the higher over-expression of AtCHR23 observed in long-day conditions. This may point to a causal relationship between AtCHR23 over-expression and increased variability of gene expression. The 68 long-day variable genes shared between the wild-type and the mutant are less correlated between the two replicates of AtCHR23 over-expressing mutant (R2 = 0.038) relative to the wild-type (R2 = 0.625) (Figure 9). It indicates that the expression of genes which are already noisy in natural conditions (the wild-type) become even more noisy when AtCHR23 is over-expressed.

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