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Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids.

Yang L, Li B, Zheng XY, Li J, Yang M, Dong X, He G, An C, Deng XW - Nat Commun (2015)

Bottom Line: Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored.Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000.Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids.

View Article: PubMed Central - PubMed

Affiliation: 1] Peking-Yale Joint Center for Plant Molecular Genetics and Agro-Biotechnology, State Key Laboratory of Protein and Plant Gene Research, The Peking-Tsinghua Center for Life Sciences, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China [2] Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA.

ABSTRACT
Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored. Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids. Moreover, SA levels are higher in hybrids than in either parent. Increased resistance to Pst DC3000 is significantly compromised in hybrids of pad4 mutants in which the SA biosynthesis pathway is blocked. Finally, increased histone H3 acetylation of key SA biosynthesis genes correlates with their upregulation in infected hybrids. Our data demonstrate that enhanced activation of SA biosynthesis in A. thaliana hybrids may contribute to their increased resistance to a biotrophic bacterial pathogen.

No MeSH data available.


Related in: MedlinePlus

DEGs involved in bacterial defence selected by cluster and functional classification analyses.(a) Venn diagram showing the number of ‘above-high parent' and ‘below-low parent' genes in each Arabidopsis thaliana hybrid at three time points. (b) Venn diagram showing the number of genes (selected from (a)) in each Cluster Analysis Group in F1 hybrids. Group I: expression continuously increased; group II: expression continuously decreased; group III: expression increased first and then decreased; and group IV: expression decreased first and then increased. (c) Enrichment of selected GO categories for genes selected from (b). The biological process with false discovery rate (adjusted P<0.05, Student's t-test) is shown. (d) Some genes in the salicylic acid pathway, categorized as ‘response to bacterium' by GO analysis, were upregulated in F1 hybrids.
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f2: DEGs involved in bacterial defence selected by cluster and functional classification analyses.(a) Venn diagram showing the number of ‘above-high parent' and ‘below-low parent' genes in each Arabidopsis thaliana hybrid at three time points. (b) Venn diagram showing the number of genes (selected from (a)) in each Cluster Analysis Group in F1 hybrids. Group I: expression continuously increased; group II: expression continuously decreased; group III: expression increased first and then decreased; and group IV: expression decreased first and then increased. (c) Enrichment of selected GO categories for genes selected from (b). The biological process with false discovery rate (adjusted P<0.05, Student's t-test) is shown. (d) Some genes in the salicylic acid pathway, categorized as ‘response to bacterium' by GO analysis, were upregulated in F1 hybrids.

Mentions: At each time point after inoculation, we identified differentially expressed genes (DEGs) between parents and hybrids (Supplementary Figs 3, 4 and 5). We identified between 2,506 and 5,577 DEGs that showed non-additive actions in reciprocal hybrids. The non-additive group was subdivided into four distinct modes: above-high parent, high parent, low parent and below-low parent (Supplementary Fig. 3c,d). A total of 3,194 DEGs that showed above-high parent or below-low parent expression in both hybrids (Fig. 2a; Supplementary Data 1) were chosen for further analysis. These 3,194 genes were further classified into four groups based on expression changes across the three time points: expression continuously increased; expression continuously decreased; expression increased and then decreased; and expression decreased and then increased. On the basis of these criteria, 1,827 genes showing the same expression patterns between reciprocal hybrids were selected for Gene Ontology (GO) analysis (Fig. 2b; Supplementary Data 1). The most significantly enriched GO term was ‘response to stimulus' (P<5.00e−7, Hypergeometric test; Fig. 2c). A set of 80 genes termed ‘response to bacterium' (Fig. 2d; Supplementary Data 1) seemed the most relevant to the goal of this study and was studied further. We compared the expression levels of these 80 genes between hybrids and parents, and found that the genes with the most significant change in expression between parents and hybrids were enriched in the SA pathway. These included CBP60g and SARD1, which encode the transcriptional activators of ICS1, and PR1, the most commonly used marker gene for SA signalling (Fig. 2d).


Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids.

Yang L, Li B, Zheng XY, Li J, Yang M, Dong X, He G, An C, Deng XW - Nat Commun (2015)

DEGs involved in bacterial defence selected by cluster and functional classification analyses.(a) Venn diagram showing the number of ‘above-high parent' and ‘below-low parent' genes in each Arabidopsis thaliana hybrid at three time points. (b) Venn diagram showing the number of genes (selected from (a)) in each Cluster Analysis Group in F1 hybrids. Group I: expression continuously increased; group II: expression continuously decreased; group III: expression increased first and then decreased; and group IV: expression decreased first and then increased. (c) Enrichment of selected GO categories for genes selected from (b). The biological process with false discovery rate (adjusted P<0.05, Student's t-test) is shown. (d) Some genes in the salicylic acid pathway, categorized as ‘response to bacterium' by GO analysis, were upregulated in F1 hybrids.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4490401&req=5

f2: DEGs involved in bacterial defence selected by cluster and functional classification analyses.(a) Venn diagram showing the number of ‘above-high parent' and ‘below-low parent' genes in each Arabidopsis thaliana hybrid at three time points. (b) Venn diagram showing the number of genes (selected from (a)) in each Cluster Analysis Group in F1 hybrids. Group I: expression continuously increased; group II: expression continuously decreased; group III: expression increased first and then decreased; and group IV: expression decreased first and then increased. (c) Enrichment of selected GO categories for genes selected from (b). The biological process with false discovery rate (adjusted P<0.05, Student's t-test) is shown. (d) Some genes in the salicylic acid pathway, categorized as ‘response to bacterium' by GO analysis, were upregulated in F1 hybrids.
Mentions: At each time point after inoculation, we identified differentially expressed genes (DEGs) between parents and hybrids (Supplementary Figs 3, 4 and 5). We identified between 2,506 and 5,577 DEGs that showed non-additive actions in reciprocal hybrids. The non-additive group was subdivided into four distinct modes: above-high parent, high parent, low parent and below-low parent (Supplementary Fig. 3c,d). A total of 3,194 DEGs that showed above-high parent or below-low parent expression in both hybrids (Fig. 2a; Supplementary Data 1) were chosen for further analysis. These 3,194 genes were further classified into four groups based on expression changes across the three time points: expression continuously increased; expression continuously decreased; expression increased and then decreased; and expression decreased and then increased. On the basis of these criteria, 1,827 genes showing the same expression patterns between reciprocal hybrids were selected for Gene Ontology (GO) analysis (Fig. 2b; Supplementary Data 1). The most significantly enriched GO term was ‘response to stimulus' (P<5.00e−7, Hypergeometric test; Fig. 2c). A set of 80 genes termed ‘response to bacterium' (Fig. 2d; Supplementary Data 1) seemed the most relevant to the goal of this study and was studied further. We compared the expression levels of these 80 genes between hybrids and parents, and found that the genes with the most significant change in expression between parents and hybrids were enriched in the SA pathway. These included CBP60g and SARD1, which encode the transcriptional activators of ICS1, and PR1, the most commonly used marker gene for SA signalling (Fig. 2d).

Bottom Line: Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored.Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000.Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids.

View Article: PubMed Central - PubMed

Affiliation: 1] Peking-Yale Joint Center for Plant Molecular Genetics and Agro-Biotechnology, State Key Laboratory of Protein and Plant Gene Research, The Peking-Tsinghua Center for Life Sciences, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China [2] Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA.

ABSTRACT
Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored. Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids. Moreover, SA levels are higher in hybrids than in either parent. Increased resistance to Pst DC3000 is significantly compromised in hybrids of pad4 mutants in which the SA biosynthesis pathway is blocked. Finally, increased histone H3 acetylation of key SA biosynthesis genes correlates with their upregulation in infected hybrids. Our data demonstrate that enhanced activation of SA biosynthesis in A. thaliana hybrids may contribute to their increased resistance to a biotrophic bacterial pathogen.

No MeSH data available.


Related in: MedlinePlus