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Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions.

Vos IA, Moritz L, Pieterse CM, Van Wees SC - Front Plant Sci (2015)

Bottom Line: Induction of SA- or JA/ABA-dependent defense responses by the biotrophic pathogen Hyaloperonospora arabidopsidis or the herbivorous insect Pieris rapae, respectively, was shown to reduce the level of induced JA/ET-dependent defense against subsequent infection with the necrotrophic pathogen Botrytis cinerea.However, despite the enhanced susceptibility to this second attacker, no additional long-term negative effects were observed on plant fitness when plants had been challenged by multiple attackers.Similarly, when plants were grown in dense competition stands to enlarge fitness effects of induced defenses, treatment with a combination of SA and MeJA did not cause additional negative effects on plant fitness in comparison to the single MeJA treatment.

View Article: PubMed Central - PubMed

Affiliation: Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University Utrecht, Netherlands.

ABSTRACT
The hormone salicylic acid (SA) generally induces plant defenses against biotrophic pathogens. Jasmonic acid (JA) and its oxylipin derivatives together with ethylene (ET) are generally important hormonal regulators of induced plant defenses against necrotrophic pathogens, whereas JAs together with abscisic acid (ABA) are implicated in induced plant defenses against herbivorous insects. Hormonal crosstalk between the different plant defense pathways has often been hypothesized to be a cost-saving strategy that has evolved as a means of the plant to reduce allocation costs by repression of unnecessary defenses, thereby minimizing trade-offs between plant defense and growth. However, proof for this hypothesis has not been demonstrated yet. In this study the impact of hormonal crosstalk on disease resistance and fitness of Arabidopsis thaliana when under multi-species attack was investigated. Induction of SA- or JA/ABA-dependent defense responses by the biotrophic pathogen Hyaloperonospora arabidopsidis or the herbivorous insect Pieris rapae, respectively, was shown to reduce the level of induced JA/ET-dependent defense against subsequent infection with the necrotrophic pathogen Botrytis cinerea. However, despite the enhanced susceptibility to this second attacker, no additional long-term negative effects were observed on plant fitness when plants had been challenged by multiple attackers. Similarly, when plants were grown in dense competition stands to enlarge fitness effects of induced defenses, treatment with a combination of SA and MeJA did not cause additional negative effects on plant fitness in comparison to the single MeJA treatment. Together, these data support the notion that hormonal crosstalk in plants during multi-attacker interactions allows plants to prioritize their defenses, while limiting the fitness costs associated with induction of defenses.

No MeSH data available.


Related in: MedlinePlus

Effect of prior attack by H. arabidopsidis or P. rapae on disease resistance against B. cinerea. (A) Quantification of disease symptoms of Arabidopsis Col-0 plants infected with B. cinerea. Twenty-four hour before inoculation with B. cinerea, plants were inoculated with H. arabidopsidis or infested with P. rapae. Disease severity of the inoculated leaves was scored in three classes. Percentage of leaves in each class was calculated per plant (X2-test; n = 20 plants). (B) Disease symptoms of B. cinerea infection in control plants, H. arabidopsidis-induced plants and P. rapae-induced plants. (C) RT-qPCR analysis of B. cinerea Tubulin levels relative to Arabidopsis reference gene mRNA levels after single and double treatments. Samples were taken at the indicated time points after the first treatment (A,B). Different letters indicate a statistically significant difference between the different treatments within one time point (ANOVA, Tukey post hoc test; P < 0.05; NS, not significant). Error bars represent SE, n = 3 plants.
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Figure 2: Effect of prior attack by H. arabidopsidis or P. rapae on disease resistance against B. cinerea. (A) Quantification of disease symptoms of Arabidopsis Col-0 plants infected with B. cinerea. Twenty-four hour before inoculation with B. cinerea, plants were inoculated with H. arabidopsidis or infested with P. rapae. Disease severity of the inoculated leaves was scored in three classes. Percentage of leaves in each class was calculated per plant (X2-test; n = 20 plants). (B) Disease symptoms of B. cinerea infection in control plants, H. arabidopsidis-induced plants and P. rapae-induced plants. (C) RT-qPCR analysis of B. cinerea Tubulin levels relative to Arabidopsis reference gene mRNA levels after single and double treatments. Samples were taken at the indicated time points after the first treatment (A,B). Different letters indicate a statistically significant difference between the different treatments within one time point (ANOVA, Tukey post hoc test; P < 0.05; NS, not significant). Error bars represent SE, n = 3 plants.

Mentions: To investigate whether suppression of the ERF-branch by prior attack with either H. arabidopsidis or P. rapae is accompanied by a reduced level of resistance against B. cinerea, we performed disease resistance bioassays. Plants that were induced by H. arabidopsidis or P. rapae were significantly more susceptible to B. cinerea than control plants (Figures 2A,B). Accordingly, B. cinerea Tubulin transcript levels were significantly higher in induced plants than in control plants (Figure 2C). Plants that were treated with exogenous application of 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA were also more susceptible to subsequent B. cinerea infection (Supplementary Figure S2). Together, these results show that suppression of the ERF-branch of the JA pathway by either the SA inducer H. arabidopsidis or the MYC-branch inducer P. rapae coincides with a reduction in the level of resistance against B. cinerea.


Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions.

Vos IA, Moritz L, Pieterse CM, Van Wees SC - Front Plant Sci (2015)

Effect of prior attack by H. arabidopsidis or P. rapae on disease resistance against B. cinerea. (A) Quantification of disease symptoms of Arabidopsis Col-0 plants infected with B. cinerea. Twenty-four hour before inoculation with B. cinerea, plants were inoculated with H. arabidopsidis or infested with P. rapae. Disease severity of the inoculated leaves was scored in three classes. Percentage of leaves in each class was calculated per plant (X2-test; n = 20 plants). (B) Disease symptoms of B. cinerea infection in control plants, H. arabidopsidis-induced plants and P. rapae-induced plants. (C) RT-qPCR analysis of B. cinerea Tubulin levels relative to Arabidopsis reference gene mRNA levels after single and double treatments. Samples were taken at the indicated time points after the first treatment (A,B). Different letters indicate a statistically significant difference between the different treatments within one time point (ANOVA, Tukey post hoc test; P < 0.05; NS, not significant). Error bars represent SE, n = 3 plants.
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Related In: Results  -  Collection

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Figure 2: Effect of prior attack by H. arabidopsidis or P. rapae on disease resistance against B. cinerea. (A) Quantification of disease symptoms of Arabidopsis Col-0 plants infected with B. cinerea. Twenty-four hour before inoculation with B. cinerea, plants were inoculated with H. arabidopsidis or infested with P. rapae. Disease severity of the inoculated leaves was scored in three classes. Percentage of leaves in each class was calculated per plant (X2-test; n = 20 plants). (B) Disease symptoms of B. cinerea infection in control plants, H. arabidopsidis-induced plants and P. rapae-induced plants. (C) RT-qPCR analysis of B. cinerea Tubulin levels relative to Arabidopsis reference gene mRNA levels after single and double treatments. Samples were taken at the indicated time points after the first treatment (A,B). Different letters indicate a statistically significant difference between the different treatments within one time point (ANOVA, Tukey post hoc test; P < 0.05; NS, not significant). Error bars represent SE, n = 3 plants.
Mentions: To investigate whether suppression of the ERF-branch by prior attack with either H. arabidopsidis or P. rapae is accompanied by a reduced level of resistance against B. cinerea, we performed disease resistance bioassays. Plants that were induced by H. arabidopsidis or P. rapae were significantly more susceptible to B. cinerea than control plants (Figures 2A,B). Accordingly, B. cinerea Tubulin transcript levels were significantly higher in induced plants than in control plants (Figure 2C). Plants that were treated with exogenous application of 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA were also more susceptible to subsequent B. cinerea infection (Supplementary Figure S2). Together, these results show that suppression of the ERF-branch of the JA pathway by either the SA inducer H. arabidopsidis or the MYC-branch inducer P. rapae coincides with a reduction in the level of resistance against B. cinerea.

Bottom Line: Induction of SA- or JA/ABA-dependent defense responses by the biotrophic pathogen Hyaloperonospora arabidopsidis or the herbivorous insect Pieris rapae, respectively, was shown to reduce the level of induced JA/ET-dependent defense against subsequent infection with the necrotrophic pathogen Botrytis cinerea.However, despite the enhanced susceptibility to this second attacker, no additional long-term negative effects were observed on plant fitness when plants had been challenged by multiple attackers.Similarly, when plants were grown in dense competition stands to enlarge fitness effects of induced defenses, treatment with a combination of SA and MeJA did not cause additional negative effects on plant fitness in comparison to the single MeJA treatment.

View Article: PubMed Central - PubMed

Affiliation: Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University Utrecht, Netherlands.

ABSTRACT
The hormone salicylic acid (SA) generally induces plant defenses against biotrophic pathogens. Jasmonic acid (JA) and its oxylipin derivatives together with ethylene (ET) are generally important hormonal regulators of induced plant defenses against necrotrophic pathogens, whereas JAs together with abscisic acid (ABA) are implicated in induced plant defenses against herbivorous insects. Hormonal crosstalk between the different plant defense pathways has often been hypothesized to be a cost-saving strategy that has evolved as a means of the plant to reduce allocation costs by repression of unnecessary defenses, thereby minimizing trade-offs between plant defense and growth. However, proof for this hypothesis has not been demonstrated yet. In this study the impact of hormonal crosstalk on disease resistance and fitness of Arabidopsis thaliana when under multi-species attack was investigated. Induction of SA- or JA/ABA-dependent defense responses by the biotrophic pathogen Hyaloperonospora arabidopsidis or the herbivorous insect Pieris rapae, respectively, was shown to reduce the level of induced JA/ET-dependent defense against subsequent infection with the necrotrophic pathogen Botrytis cinerea. However, despite the enhanced susceptibility to this second attacker, no additional long-term negative effects were observed on plant fitness when plants had been challenged by multiple attackers. Similarly, when plants were grown in dense competition stands to enlarge fitness effects of induced defenses, treatment with a combination of SA and MeJA did not cause additional negative effects on plant fitness in comparison to the single MeJA treatment. Together, these data support the notion that hormonal crosstalk in plants during multi-attacker interactions allows plants to prioritize their defenses, while limiting the fitness costs associated with induction of defenses.

No MeSH data available.


Related in: MedlinePlus