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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.


Tomato leaves susceptibility to B. cinerea in plants grown under different nitrate concentrations. (A) Representative inoculated leaves (3 dpi) for each nitrate condition used throughout this study. (B) Lesion size, measured as diameter of expanding lesions, for the indicated nitrate concentrations. (C) Disease incidence (percentage of leaf area with disease symptoms). Different letters indicate significant differences among treatments at a given time point (p ≤ 0.05; error bars indicate SEM; n = 6).
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Figure 1: Tomato leaves susceptibility to B. cinerea in plants grown under different nitrate concentrations. (A) Representative inoculated leaves (3 dpi) for each nitrate condition used throughout this study. (B) Lesion size, measured as diameter of expanding lesions, for the indicated nitrate concentrations. (C) Disease incidence (percentage of leaf area with disease symptoms). Different letters indicate significant differences among treatments at a given time point (p ≤ 0.05; error bars indicate SEM; n = 6).

Mentions: To evaluate whether contrasting nitrate concentrations impact the susceptibility of tomato plants to fungal infection, plants were grown under 2, 4, 6, or 12 mM nitrate as the only N source and challenged with B. cinerea. Leaves in planta were inoculated with an aqueous suspension of 5 × 103 conidia. Typical B. cinerea symptoms, such as necrotic lesions, were observed in leaves under all N regimes. The first visual symptoms of the infections were detected 2 days post inoculation (dpi), at which time darkening of the leaf surface under the inoculum was observed (data not shown). As shown in Figure 1, disease symptoms developed faster in plants grown under N-limiting than in N-sufficient conditions. At 3 dpi, larger lesions were observed under N-limiting conditions, with evident tissue maceration surrounding primary infection sites in leaves (Figure 1A). Conversely, only discrete necrotic lesions were observed under N-sufficient conditions (Figure 1A). Even though, disease symptoms (expanding necrosis, chlorosis, and tissue maceration) were observed in leaves from plants grown under all N regimes at 5 dpi (data not shown), the size of the lesions and the percentage of the leaf exhibiting symptoms were always larger in leaves from plants grown under N-limiting conditions (Figures 1B,C).


Transcriptome analysis reveals regulatory networks underlying differential susceptibility to Botrytis cinerea in response to nitrogen availability in Solanum lycopersicum
Tomato leaves susceptibility to B. cinerea in plants grown under different nitrate concentrations. (A) Representative inoculated leaves (3 dpi) for each nitrate condition used throughout this study. (B) Lesion size, measured as diameter of expanding lesions, for the indicated nitrate concentrations. (C) Disease incidence (percentage of leaf area with disease symptoms). Different letters indicate significant differences among treatments at a given time point (p ≤ 0.05; error bars indicate SEM; n = 6).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4631835&req=5

Figure 1: Tomato leaves susceptibility to B. cinerea in plants grown under different nitrate concentrations. (A) Representative inoculated leaves (3 dpi) for each nitrate condition used throughout this study. (B) Lesion size, measured as diameter of expanding lesions, for the indicated nitrate concentrations. (C) Disease incidence (percentage of leaf area with disease symptoms). Different letters indicate significant differences among treatments at a given time point (p ≤ 0.05; error bars indicate SEM; n = 6).
Mentions: To evaluate whether contrasting nitrate concentrations impact the susceptibility of tomato plants to fungal infection, plants were grown under 2, 4, 6, or 12 mM nitrate as the only N source and challenged with B. cinerea. Leaves in planta were inoculated with an aqueous suspension of 5 × 103 conidia. Typical B. cinerea symptoms, such as necrotic lesions, were observed in leaves under all N regimes. The first visual symptoms of the infections were detected 2 days post inoculation (dpi), at which time darkening of the leaf surface under the inoculum was observed (data not shown). As shown in Figure 1, disease symptoms developed faster in plants grown under N-limiting than in N-sufficient conditions. At 3 dpi, larger lesions were observed under N-limiting conditions, with evident tissue maceration surrounding primary infection sites in leaves (Figure 1A). Conversely, only discrete necrotic lesions were observed under N-sufficient conditions (Figure 1A). Even though, disease symptoms (expanding necrosis, chlorosis, and tissue maceration) were observed in leaves from plants grown under all N regimes at 5 dpi (data not shown), the size of the lesions and the percentage of the leaf exhibiting symptoms were always larger in leaves from plants grown under N-limiting conditions (Figures 1B,C).

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.