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Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses.

Nafisi M, Stranne M, Fimognari L, Atwell S, Martens HJ, Pedas PR, Hansen SF, Nawrath C, Scheller HV, Kliebenstein DJ, Sakuragi Y - Front Plant Sci (2015)

Bottom Line: A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type.In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type.These results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads to global stress responses in Arabidopsis.

View Article: PubMed Central - PubMed

Affiliation: Copenhagen Plant Science Center Frederiksberg, Denmark ; Department of Plant and Environmental Sciences, University of Copenhagen Frederiksberg, Denmark.

ABSTRACT
The epidermis on leaves protects plants from pathogen invasion and provides a waterproof barrier. It consists of a layer of cells that is surrounded by thick cell walls, which are partially impregnated by highly hydrophobic cuticular components. We show that the Arabidopsis T-DNA insertion mutants of REDUCED WALL ACETYLATION 2 (rwa2), previously identified as having reduced O-acetylation of both pectins and hemicelluloses, exhibit pleiotrophic phenotype on the leaf surface. The cuticle layer appeared diffused and was significantly thicker and underneath cell wall layer was interspersed with electron-dense deposits. A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type. A massive reprogramming of the transcriptome was observed in rwa2 as compared to the wild type, including a coordinated up-regulation of genes involved in responses to abiotic stress, particularly detoxification of reactive oxygen species and defense against microbial pathogens (e.g., lipid transfer proteins, peroxidases). In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type. These results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads to global stress responses in Arabidopsis.

No MeSH data available.


Related in: MedlinePlus

Global transcript analysis. (A) Shown is a principal component analysis of the entire dataset with the individual samples plotted. Wild type samples are shown as diamonds and rwa2 samples are shown as squares with the blue to orange transition showing the time course of the experiment. The first two PCA vectors are utilized that explain 86% of the total variance. (B) VENN diagrams showing the overlap of genes differentially expressed (left side: upregulated genes, right side repressed genes) in rwa2 control vs. wild type control, and wild type infected with B. cinerea vs. wild type mock across the time points. The genes that are differentially expressed in rwa2 control vs. the corresponding wild-type samples have a high overlap with the expression profile of genes in wild type infected with B. cinerea. The numbers in brackets represent the overlap expected by chance. The overlaps are highly significant both for induced (P < 0.001) and for repressed genes (P < 0.001) as determined by χ2-test.
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Figure 7: Global transcript analysis. (A) Shown is a principal component analysis of the entire dataset with the individual samples plotted. Wild type samples are shown as diamonds and rwa2 samples are shown as squares with the blue to orange transition showing the time course of the experiment. The first two PCA vectors are utilized that explain 86% of the total variance. (B) VENN diagrams showing the overlap of genes differentially expressed (left side: upregulated genes, right side repressed genes) in rwa2 control vs. wild type control, and wild type infected with B. cinerea vs. wild type mock across the time points. The genes that are differentially expressed in rwa2 control vs. the corresponding wild-type samples have a high overlap with the expression profile of genes in wild type infected with B. cinerea. The numbers in brackets represent the overlap expected by chance. The overlaps are highly significant both for induced (P < 0.001) and for repressed genes (P < 0.001) as determined by χ2-test.

Mentions: We hypothesized that the surface damage caused by the rwa2 mutation could have a significant impact on plant stress responses and that transcriptome profiling would shed light on which stress response(s) is affected. Wild-type and rwa2-3 leaves were either untreated or treated with mock [potato dextrose broth (PDB) only] or B. cinerea spore solution in PDB for 24 and 48 h and mRNA sequencing was performed (Supplementary Table 1). The largest difference in the transcriptome profile was observed between the untreated wild type and rwa2-3, indicating that the untreated rwa2-3 perceives the environment differently from the wild type (Table 2). Out of 21,178 transcripts that were sequenced in both the wild-type and rwa2-3, 1650 transcripts showed statistically significant differential abundance: 857 genes up-regulated and 763 genes down-regulated [log2 fold ≥ 2, false discovery rate (FDR) ≤ 0.05]. The mock and B. cinerea treatments led to smaller differences between rwa2-3 and the wild type in terms of the number of genes with altered expression levels at both 24 h and 48 h after infection (Table 2). Principal component analysis showed that genotype and treatments describe 86% of the total transcriptomic variance detected (Figure 7). The first vector (PCA vector 1) largely describes the differences between the genotypes at the untreated and early mock treated samples (untreated wild type vs. rwa2-3), while the second vector (PCA vector 2) largely describes the response of the genotypes to infection with B. cinerea (untreated, mock, and B. cinerea treatments). In the wild type, the mock treatment (detachment of leaves followed by incubation in a water-agar medium and application of PDB) caused a notable change in the transcriptome profiles. Interestingly, both the untreated and mock-treated rwa2-3 for 24 h showed a significant overlap with the mock-treated wild type. Upon treatment with B. cinerea, the transcriptomes of the wild type and rwa2-3 showed an even higher degree of overlap (Figure 7). This indicates that the rwa2-3 responds to B. cinerea similarly to the wild type even though their initial transcriptomes are highly divergent.


Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses.

Nafisi M, Stranne M, Fimognari L, Atwell S, Martens HJ, Pedas PR, Hansen SF, Nawrath C, Scheller HV, Kliebenstein DJ, Sakuragi Y - Front Plant Sci (2015)

Global transcript analysis. (A) Shown is a principal component analysis of the entire dataset with the individual samples plotted. Wild type samples are shown as diamonds and rwa2 samples are shown as squares with the blue to orange transition showing the time course of the experiment. The first two PCA vectors are utilized that explain 86% of the total variance. (B) VENN diagrams showing the overlap of genes differentially expressed (left side: upregulated genes, right side repressed genes) in rwa2 control vs. wild type control, and wild type infected with B. cinerea vs. wild type mock across the time points. The genes that are differentially expressed in rwa2 control vs. the corresponding wild-type samples have a high overlap with the expression profile of genes in wild type infected with B. cinerea. The numbers in brackets represent the overlap expected by chance. The overlaps are highly significant both for induced (P < 0.001) and for repressed genes (P < 0.001) as determined by χ2-test.
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Related In: Results  -  Collection

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Figure 7: Global transcript analysis. (A) Shown is a principal component analysis of the entire dataset with the individual samples plotted. Wild type samples are shown as diamonds and rwa2 samples are shown as squares with the blue to orange transition showing the time course of the experiment. The first two PCA vectors are utilized that explain 86% of the total variance. (B) VENN diagrams showing the overlap of genes differentially expressed (left side: upregulated genes, right side repressed genes) in rwa2 control vs. wild type control, and wild type infected with B. cinerea vs. wild type mock across the time points. The genes that are differentially expressed in rwa2 control vs. the corresponding wild-type samples have a high overlap with the expression profile of genes in wild type infected with B. cinerea. The numbers in brackets represent the overlap expected by chance. The overlaps are highly significant both for induced (P < 0.001) and for repressed genes (P < 0.001) as determined by χ2-test.
Mentions: We hypothesized that the surface damage caused by the rwa2 mutation could have a significant impact on plant stress responses and that transcriptome profiling would shed light on which stress response(s) is affected. Wild-type and rwa2-3 leaves were either untreated or treated with mock [potato dextrose broth (PDB) only] or B. cinerea spore solution in PDB for 24 and 48 h and mRNA sequencing was performed (Supplementary Table 1). The largest difference in the transcriptome profile was observed between the untreated wild type and rwa2-3, indicating that the untreated rwa2-3 perceives the environment differently from the wild type (Table 2). Out of 21,178 transcripts that were sequenced in both the wild-type and rwa2-3, 1650 transcripts showed statistically significant differential abundance: 857 genes up-regulated and 763 genes down-regulated [log2 fold ≥ 2, false discovery rate (FDR) ≤ 0.05]. The mock and B. cinerea treatments led to smaller differences between rwa2-3 and the wild type in terms of the number of genes with altered expression levels at both 24 h and 48 h after infection (Table 2). Principal component analysis showed that genotype and treatments describe 86% of the total transcriptomic variance detected (Figure 7). The first vector (PCA vector 1) largely describes the differences between the genotypes at the untreated and early mock treated samples (untreated wild type vs. rwa2-3), while the second vector (PCA vector 2) largely describes the response of the genotypes to infection with B. cinerea (untreated, mock, and B. cinerea treatments). In the wild type, the mock treatment (detachment of leaves followed by incubation in a water-agar medium and application of PDB) caused a notable change in the transcriptome profiles. Interestingly, both the untreated and mock-treated rwa2-3 for 24 h showed a significant overlap with the mock-treated wild type. Upon treatment with B. cinerea, the transcriptomes of the wild type and rwa2-3 showed an even higher degree of overlap (Figure 7). This indicates that the rwa2-3 responds to B. cinerea similarly to the wild type even though their initial transcriptomes are highly divergent.

Bottom Line: A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type.In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type.These results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads to global stress responses in Arabidopsis.

View Article: PubMed Central - PubMed

Affiliation: Copenhagen Plant Science Center Frederiksberg, Denmark ; Department of Plant and Environmental Sciences, University of Copenhagen Frederiksberg, Denmark.

ABSTRACT
The epidermis on leaves protects plants from pathogen invasion and provides a waterproof barrier. It consists of a layer of cells that is surrounded by thick cell walls, which are partially impregnated by highly hydrophobic cuticular components. We show that the Arabidopsis T-DNA insertion mutants of REDUCED WALL ACETYLATION 2 (rwa2), previously identified as having reduced O-acetylation of both pectins and hemicelluloses, exhibit pleiotrophic phenotype on the leaf surface. The cuticle layer appeared diffused and was significantly thicker and underneath cell wall layer was interspersed with electron-dense deposits. A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type. A massive reprogramming of the transcriptome was observed in rwa2 as compared to the wild type, including a coordinated up-regulation of genes involved in responses to abiotic stress, particularly detoxification of reactive oxygen species and defense against microbial pathogens (e.g., lipid transfer proteins, peroxidases). In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type. These results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads to global stress responses in Arabidopsis.

No MeSH data available.


Related in: MedlinePlus