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Comparative transcriptomics of Central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew.

Amrine KC, Blanco-Ulate B, Riaz S, Pap D, Jones L, Figueroa-Balderas R, Walker MA, Cantu D - Hortic Res (2015)

Bottom Line: To identify potential Ren1-dependent transcriptional responses and functions associated with the different levels of resistance, we sequenced and analyzed the transcriptomes of these Central Asian accessions at two time points of PM infection.Transcriptomes were compared to identify constitutive differences and PM-inducible responses that may underlie their disease resistant phenotype.This study provides a first exploration of the functions associated with varying levels of partial resistance to PM in V. vinifera accessions that can be exploited as sources of genetic resistance in grape breeding programs.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California , Davis, Davis, CA 95616, USA.

ABSTRACT
Grape powdery mildew (PM), caused by the biotrophic ascomycete Erysiphe necator, is a devastating fungal disease that affects most Vitis vinifera cultivars. We have previously identified a panel of V. vinifera accessions from Central Asia with partial resistance to PM that possess a Ren1-like local haplotype. In this study, we show that in addition to the typical Ren1-associated late post-penetration resistance, these accessions display a range of different levels of disease development suggesting that alternative alleles or additional genes contribute to determining the outcome of the interaction with the pathogen. To identify potential Ren1-dependent transcriptional responses and functions associated with the different levels of resistance, we sequenced and analyzed the transcriptomes of these Central Asian accessions at two time points of PM infection. Transcriptomes were compared to identify constitutive differences and PM-inducible responses that may underlie their disease resistant phenotype. Responses to E. necator in all resistant accessions were characterized by an early up-regulation of 13 genes, most encoding putative defense functions, and a late down-regulation of 32 genes, enriched in transcriptional regulators and protein kinases. Potential Ren1-dependent responses included a hotspot of co-regulated genes on chromosome 18. We also identified 81 genes whose expression levels and dynamics correlated with the phenotypic differences between the most resistant accessions 'Karadzhandahal', DVIT3351.27, and O34-16 and the other genotypes. This study provides a first exploration of the functions associated with varying levels of partial resistance to PM in V. vinifera accessions that can be exploited as sources of genetic resistance in grape breeding programs.

No MeSH data available.


Related in: MedlinePlus

GO term enrichment overlap between genes under positive selection (ω > 1), genes with higher constitutive expression in the Central Asian accessions, and genes with higher constitutive expression in ‘Carignan’ (a) Venn diagram showing numbers of overlapping and specific GO terms in each of the three groups of genes. (b) Graphical representation of relationships between enriched GO terms. To highlight closely related enriched GO terms, terms were organized in undirected sub-graphs using the REViGO web server.37 Colors indicate the gene group in which the GO terms are enriched, consistent with panel A. Dashed boxes indicate similar biological functions among the GO terms. Supplementary Dataset S3 provides all the GO terms and numeric IDs that are not described in panel C. (c) GO Categories with the greatest number of gene members are listed for each gene group, with the color coding of column 1 consistent with the gene groups shown in panel (a). Column 1 identifiers correspond to the circles in panel (b).
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fig3: GO term enrichment overlap between genes under positive selection (ω > 1), genes with higher constitutive expression in the Central Asian accessions, and genes with higher constitutive expression in ‘Carignan’ (a) Venn diagram showing numbers of overlapping and specific GO terms in each of the three groups of genes. (b) Graphical representation of relationships between enriched GO terms. To highlight closely related enriched GO terms, terms were organized in undirected sub-graphs using the REViGO web server.37 Colors indicate the gene group in which the GO terms are enriched, consistent with panel A. Dashed boxes indicate similar biological functions among the GO terms. Supplementary Dataset S3 provides all the GO terms and numeric IDs that are not described in panel C. (c) GO Categories with the greatest number of gene members are listed for each gene group, with the color coding of column 1 consistent with the gene groups shown in panel (a). Column 1 identifiers correspond to the circles in panel (b).

Mentions: Rates of synonymous and non-synonymous substitutions (ω values or dN/dS ratios) were calculated by pairwise comparisons of the synthetic genes of each accession against the ‘PN40024’ reference genome. The analysis focused on the identification of genes with ω > 1, which indicates positive selection favoring amino acid replacements. In total 1971 (average per accession: 490.5 ± 35.8) genes had ω > 1 in the pairwise comparisons. These genes showed significant over-representation of 57 GO terms (P < 0.05), which included functions related to apoptotic processes and defense responses against pathogens (Figure 3; Supplementary Dataset S2). These results are in agreement with previous studies that reported elevated rates of non-synonymous over synonymous substitutions in genes associated with defense responses.51–57


Comparative transcriptomics of Central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew.

Amrine KC, Blanco-Ulate B, Riaz S, Pap D, Jones L, Figueroa-Balderas R, Walker MA, Cantu D - Hortic Res (2015)

GO term enrichment overlap between genes under positive selection (ω > 1), genes with higher constitutive expression in the Central Asian accessions, and genes with higher constitutive expression in ‘Carignan’ (a) Venn diagram showing numbers of overlapping and specific GO terms in each of the three groups of genes. (b) Graphical representation of relationships between enriched GO terms. To highlight closely related enriched GO terms, terms were organized in undirected sub-graphs using the REViGO web server.37 Colors indicate the gene group in which the GO terms are enriched, consistent with panel A. Dashed boxes indicate similar biological functions among the GO terms. Supplementary Dataset S3 provides all the GO terms and numeric IDs that are not described in panel C. (c) GO Categories with the greatest number of gene members are listed for each gene group, with the color coding of column 1 consistent with the gene groups shown in panel (a). Column 1 identifiers correspond to the circles in panel (b).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4591678&req=5

fig3: GO term enrichment overlap between genes under positive selection (ω > 1), genes with higher constitutive expression in the Central Asian accessions, and genes with higher constitutive expression in ‘Carignan’ (a) Venn diagram showing numbers of overlapping and specific GO terms in each of the three groups of genes. (b) Graphical representation of relationships between enriched GO terms. To highlight closely related enriched GO terms, terms were organized in undirected sub-graphs using the REViGO web server.37 Colors indicate the gene group in which the GO terms are enriched, consistent with panel A. Dashed boxes indicate similar biological functions among the GO terms. Supplementary Dataset S3 provides all the GO terms and numeric IDs that are not described in panel C. (c) GO Categories with the greatest number of gene members are listed for each gene group, with the color coding of column 1 consistent with the gene groups shown in panel (a). Column 1 identifiers correspond to the circles in panel (b).
Mentions: Rates of synonymous and non-synonymous substitutions (ω values or dN/dS ratios) were calculated by pairwise comparisons of the synthetic genes of each accession against the ‘PN40024’ reference genome. The analysis focused on the identification of genes with ω > 1, which indicates positive selection favoring amino acid replacements. In total 1971 (average per accession: 490.5 ± 35.8) genes had ω > 1 in the pairwise comparisons. These genes showed significant over-representation of 57 GO terms (P < 0.05), which included functions related to apoptotic processes and defense responses against pathogens (Figure 3; Supplementary Dataset S2). These results are in agreement with previous studies that reported elevated rates of non-synonymous over synonymous substitutions in genes associated with defense responses.51–57

Bottom Line: To identify potential Ren1-dependent transcriptional responses and functions associated with the different levels of resistance, we sequenced and analyzed the transcriptomes of these Central Asian accessions at two time points of PM infection.Transcriptomes were compared to identify constitutive differences and PM-inducible responses that may underlie their disease resistant phenotype.This study provides a first exploration of the functions associated with varying levels of partial resistance to PM in V. vinifera accessions that can be exploited as sources of genetic resistance in grape breeding programs.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California , Davis, Davis, CA 95616, USA.

ABSTRACT
Grape powdery mildew (PM), caused by the biotrophic ascomycete Erysiphe necator, is a devastating fungal disease that affects most Vitis vinifera cultivars. We have previously identified a panel of V. vinifera accessions from Central Asia with partial resistance to PM that possess a Ren1-like local haplotype. In this study, we show that in addition to the typical Ren1-associated late post-penetration resistance, these accessions display a range of different levels of disease development suggesting that alternative alleles or additional genes contribute to determining the outcome of the interaction with the pathogen. To identify potential Ren1-dependent transcriptional responses and functions associated with the different levels of resistance, we sequenced and analyzed the transcriptomes of these Central Asian accessions at two time points of PM infection. Transcriptomes were compared to identify constitutive differences and PM-inducible responses that may underlie their disease resistant phenotype. Responses to E. necator in all resistant accessions were characterized by an early up-regulation of 13 genes, most encoding putative defense functions, and a late down-regulation of 32 genes, enriched in transcriptional regulators and protein kinases. Potential Ren1-dependent responses included a hotspot of co-regulated genes on chromosome 18. We also identified 81 genes whose expression levels and dynamics correlated with the phenotypic differences between the most resistant accessions 'Karadzhandahal', DVIT3351.27, and O34-16 and the other genotypes. This study provides a first exploration of the functions associated with varying levels of partial resistance to PM in V. vinifera accessions that can be exploited as sources of genetic resistance in grape breeding programs.

No MeSH data available.


Related in: MedlinePlus