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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

Genomic region with significant enrichment in PM-responsive genes in the Central Asian accessions. (a) Heatmap showing gene density along chromosome 18. Colors range from dark blue (smaller gene density) to red (greater gene density). (b) Graphical representation of the PGE analysis results. Bars represent regions of chromosome 18 with significant enrichment in differentially expressed genes (P < 0.05). (c) Graphical representation of the location of protein-coding genes in the region identified by PGE analysis. Each box represents the exon of a protein-coding gene. (d) Locations of genes that are either detected as differentially expressed specifically in the Central Asian accessions in response to E. necator (blue) or constitutively more expressed in the Central Asian accessions than in ‘Carignan’. Gray boxes identify genes in the same regions that are under positive selection (ω > 1). (e) Correlation between PM-induced fold-changes measured by qRT-PCR and RNAseq.
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fig5: Genomic region with significant enrichment in PM-responsive genes in the Central Asian accessions. (a) Heatmap showing gene density along chromosome 18. Colors range from dark blue (smaller gene density) to red (greater gene density). (b) Graphical representation of the PGE analysis results. Bars represent regions of chromosome 18 with significant enrichment in differentially expressed genes (P < 0.05). (c) Graphical representation of the location of protein-coding genes in the region identified by PGE analysis. Each box represents the exon of a protein-coding gene. (d) Locations of genes that are either detected as differentially expressed specifically in the Central Asian accessions in response to E. necator (blue) or constitutively more expressed in the Central Asian accessions than in ‘Carignan’. Gray boxes identify genes in the same regions that are under positive selection (ω > 1). (e) Correlation between PM-induced fold-changes measured by qRT-PCR and RNAseq.

Mentions: Chromosome 18 had the greatest number of differentially expressed genes in the PM-partially resistant varieties. Multiple PM resistance loci including Ren4 in V. romanetii, Run2.1, and Run2.2 in M. rotundifolia6 as well as 55% of the annotated NB-LRR genes are located on this chromosome.60 A positional gene enrichment analysis (PGE61) of chromosome 18 detected a significant over-representation of differentially regulated genes in response to PM between coordinates 3 401 893 to 8 421 561 (Figure 5), a region encompassing 496 protein-coding genes. Interestingly, the same region of chromosome 18 was enriched for genes undergoing positive selection (Figure 5d). Expression of the seven PM-responsive genes located in this region was confirmed by qRT-PCR (94.64% validation for 56 comparisons; Figure 5e).


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)

Genomic region with significant enrichment in PM-responsive genes in the Central Asian accessions. (a) Heatmap showing gene density along chromosome 18. Colors range from dark blue (smaller gene density) to red (greater gene density). (b) Graphical representation of the PGE analysis results. Bars represent regions of chromosome 18 with significant enrichment in differentially expressed genes (P < 0.05). (c) Graphical representation of the location of protein-coding genes in the region identified by PGE analysis. Each box represents the exon of a protein-coding gene. (d) Locations of genes that are either detected as differentially expressed specifically in the Central Asian accessions in response to E. necator (blue) or constitutively more expressed in the Central Asian accessions than in ‘Carignan’. Gray boxes identify genes in the same regions that are under positive selection (ω > 1). (e) Correlation between PM-induced fold-changes measured by qRT-PCR and RNAseq.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig5: Genomic region with significant enrichment in PM-responsive genes in the Central Asian accessions. (a) Heatmap showing gene density along chromosome 18. Colors range from dark blue (smaller gene density) to red (greater gene density). (b) Graphical representation of the PGE analysis results. Bars represent regions of chromosome 18 with significant enrichment in differentially expressed genes (P < 0.05). (c) Graphical representation of the location of protein-coding genes in the region identified by PGE analysis. Each box represents the exon of a protein-coding gene. (d) Locations of genes that are either detected as differentially expressed specifically in the Central Asian accessions in response to E. necator (blue) or constitutively more expressed in the Central Asian accessions than in ‘Carignan’. Gray boxes identify genes in the same regions that are under positive selection (ω > 1). (e) Correlation between PM-induced fold-changes measured by qRT-PCR and RNAseq.
Mentions: Chromosome 18 had the greatest number of differentially expressed genes in the PM-partially resistant varieties. Multiple PM resistance loci including Ren4 in V. romanetii, Run2.1, and Run2.2 in M. rotundifolia6 as well as 55% of the annotated NB-LRR genes are located on this chromosome.60 A positional gene enrichment analysis (PGE61) of chromosome 18 detected a significant over-representation of differentially regulated genes in response to PM between coordinates 3 401 893 to 8 421 561 (Figure 5), a region encompassing 496 protein-coding genes. Interestingly, the same region of chromosome 18 was enriched for genes undergoing positive selection (Figure 5d). Expression of the seven PM-responsive genes located in this region was confirmed by qRT-PCR (94.64% validation for 56 comparisons; Figure 5e).

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