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Transcriptome analysis reveals regulatory networks underlying differential susceptibility to Botrytis cinerea in response to nitrogen availability in Solanum lycopersicum

View Article: PubMed Central

ABSTRACT

Nitrogen (N) is one of the main limiting nutrients for plant growth and crop yield. It is well documented that changes in nitrate availability, the main N source found in agricultural soils, influences a myriad of developmental programs and processes including the plant defense response. Indeed, many agronomical reports indicate that the plant N nutritional status influences their ability to respond effectively when challenged by different pathogens. However, the molecular mechanisms involved in N-modulation of plant susceptibility to pathogens are poorly characterized. In this work, we show that Solanum lycopersicum defense response to the necrotrophic fungus Botrytis cinerea is affected by plant N availability, with higher susceptibility in nitrate-limiting conditions. Global gene expression responses of tomato against B. cinerea under contrasting nitrate conditions reveals that plant primary metabolism is affected by the fungal infection regardless of N regimes. This result suggests that differential susceptibility to pathogen attack under contrasting N conditions is not only explained by a metabolic alteration. We used a systems biology approach to identify the transcriptional regulatory network implicated in plant response to the fungus infection under contrasting nitrate conditions. Interestingly, hub genes in this network are known key transcription factors involved in ethylene and jasmonic acid signaling. This result positions these hormones as key integrators of nitrate and defense against B. cinerea in tomato plants. Our results provide insights into potential crosstalk mechanisms between necrotrophic defense response and N status in plants.

No MeSH data available.


Related in: MedlinePlus

Hierarchical clustering of mRNA levels for selected TFs showing a differential gene expression pattern in response to the fungus infection under different N conditions. The dendrogram and colored image were produced using gene expression data after RT-qPCR (n = 3). The color scale ranges from saturated green for log2 ratios −3.0 and below, to saturated red for log2 ratios +3.0 and above. Fold change in gene expression for each gene upon B. cinerea infection are referred to mock-treated samples. Each TF is represented by a single row of colored boxes. Six clusters were identified, and are numbered and denoted with a vertical line (from top to bottom) as follows: cluster #1 in gray, #2 in brown, #3 in light blue, #4 in orange, #5 in green, and #6 in blue.
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Figure 6: Hierarchical clustering of mRNA levels for selected TFs showing a differential gene expression pattern in response to the fungus infection under different N conditions. The dendrogram and colored image were produced using gene expression data after RT-qPCR (n = 3). The color scale ranges from saturated green for log2 ratios −3.0 and below, to saturated red for log2 ratios +3.0 and above. Fold change in gene expression for each gene upon B. cinerea infection are referred to mock-treated samples. Each TF is represented by a single row of colored boxes. Six clusters were identified, and are numbered and denoted with a vertical line (from top to bottom) as follows: cluster #1 in gray, #2 in brown, #3 in light blue, #4 in orange, #5 in green, and #6 in blue.

Mentions: The results depicted in Figure 5 support the importance of plant N metabolism in plant defense pathways. To validate this prediction, we analyzed the expression levels of 18 TF-encoding genes in leaves or fruits infected by B. cinerea, from tomato plants grown under all nitrate concentrations used throughout this work (Table S5). An RT-qPCR analysis of selected TFs supported microarray results and network analysis (Figure 6). Hierarchical clustering analysis of the RT-qPCR data revealed 6 clusters. Cluster #1 (Figure 6, in gray), composed of four TF-encoding genes (NAC-like, WRKY15, BIM, and WRKY70), groups genes that are induced by fungal infection under N-sufficient conditions, but repressed in leaves or marginally induced in fruits of plants grown under N-limiting conditions. In Arabidopsis, WRKY 15 and WRKY 70 (Figure 5, Modules 3 and 8, respectively) have been reported as induced when infected with B. cinerea. Interestingly, wrky70 mutant plants showed enhanced susceptibility to this fungus, in a SA dependent manner (AbuQamar et al., 2006).


Transcriptome analysis reveals regulatory networks underlying differential susceptibility to Botrytis cinerea in response to nitrogen availability in Solanum lycopersicum
Hierarchical clustering of mRNA levels for selected TFs showing a differential gene expression pattern in response to the fungus infection under different N conditions. The dendrogram and colored image were produced using gene expression data after RT-qPCR (n = 3). The color scale ranges from saturated green for log2 ratios −3.0 and below, to saturated red for log2 ratios +3.0 and above. Fold change in gene expression for each gene upon B. cinerea infection are referred to mock-treated samples. Each TF is represented by a single row of colored boxes. Six clusters were identified, and are numbered and denoted with a vertical line (from top to bottom) as follows: cluster #1 in gray, #2 in brown, #3 in light blue, #4 in orange, #5 in green, and #6 in blue.
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Related In: Results  -  Collection

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Figure 6: Hierarchical clustering of mRNA levels for selected TFs showing a differential gene expression pattern in response to the fungus infection under different N conditions. The dendrogram and colored image were produced using gene expression data after RT-qPCR (n = 3). The color scale ranges from saturated green for log2 ratios −3.0 and below, to saturated red for log2 ratios +3.0 and above. Fold change in gene expression for each gene upon B. cinerea infection are referred to mock-treated samples. Each TF is represented by a single row of colored boxes. Six clusters were identified, and are numbered and denoted with a vertical line (from top to bottom) as follows: cluster #1 in gray, #2 in brown, #3 in light blue, #4 in orange, #5 in green, and #6 in blue.
Mentions: The results depicted in Figure 5 support the importance of plant N metabolism in plant defense pathways. To validate this prediction, we analyzed the expression levels of 18 TF-encoding genes in leaves or fruits infected by B. cinerea, from tomato plants grown under all nitrate concentrations used throughout this work (Table S5). An RT-qPCR analysis of selected TFs supported microarray results and network analysis (Figure 6). Hierarchical clustering analysis of the RT-qPCR data revealed 6 clusters. Cluster #1 (Figure 6, in gray), composed of four TF-encoding genes (NAC-like, WRKY15, BIM, and WRKY70), groups genes that are induced by fungal infection under N-sufficient conditions, but repressed in leaves or marginally induced in fruits of plants grown under N-limiting conditions. In Arabidopsis, WRKY 15 and WRKY 70 (Figure 5, Modules 3 and 8, respectively) have been reported as induced when infected with B. cinerea. Interestingly, wrky70 mutant plants showed enhanced susceptibility to this fungus, in a SA dependent manner (AbuQamar et al., 2006).

View Article: PubMed Central

ABSTRACT

Nitrogen (N) is one of the main limiting nutrients for plant growth and crop yield. It is well documented that changes in nitrate availability, the main N source found in agricultural soils, influences a myriad of developmental programs and processes including the plant defense response. Indeed, many agronomical reports indicate that the plant N nutritional status influences their ability to respond effectively when challenged by different pathogens. However, the molecular mechanisms involved in N-modulation of plant susceptibility to pathogens are poorly characterized. In this work, we show that Solanum lycopersicum defense response to the necrotrophic fungus Botrytis cinerea is affected by plant N availability, with higher susceptibility in nitrate-limiting conditions. Global gene expression responses of tomato against B. cinerea under contrasting nitrate conditions reveals that plant primary metabolism is affected by the fungal infection regardless of N regimes. This result suggests that differential susceptibility to pathogen attack under contrasting N conditions is not only explained by a metabolic alteration. We used a systems biology approach to identify the transcriptional regulatory network implicated in plant response to the fungus infection under contrasting nitrate conditions. Interestingly, hub genes in this network are known key transcription factors involved in ethylene and jasmonic acid signaling. This result positions these hormones as key integrators of nitrate and defense against B. cinerea in tomato plants. Our results provide insights into potential crosstalk mechanisms between necrotrophic defense response and N status in plants.

No MeSH data available.


Related in: MedlinePlus