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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

Differential gene expression in competition-grown plants. RT-qPCR analysis of salicylic acid (SA)-responsive PR1 expression and Jasmonic acid (JA)-responsive VSP2 expression in competition-grown plants 24 h after treatment with a mock, SA, MeJA, or SA/MeJA solution. Mock vs. SA and Mock vs. MeJA competition experiments were performed in one experimental round, and Mock vs. SA/MeJA, SA vs. SA/MeJA, and MeJA vs. SA/MeJA competition experiments were performed in another experimental round. Indicated are expression levels relative to those of mock-treated plants in one of the competition trays. Asterisks indicate a statistically significant difference between the indicated treatment and the mock-treated plants (ANOVA, Dunnet post hoc test; ∗∗ = P < 0.01; ∗ = P < 0.05). Error bars represent SE, n = 3 plants.
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Figure 5: Differential gene expression in competition-grown plants. RT-qPCR analysis of salicylic acid (SA)-responsive PR1 expression and Jasmonic acid (JA)-responsive VSP2 expression in competition-grown plants 24 h after treatment with a mock, SA, MeJA, or SA/MeJA solution. Mock vs. SA and Mock vs. MeJA competition experiments were performed in one experimental round, and Mock vs. SA/MeJA, SA vs. SA/MeJA, and MeJA vs. SA/MeJA competition experiments were performed in another experimental round. Indicated are expression levels relative to those of mock-treated plants in one of the competition trays. Asterisks indicate a statistically significant difference between the indicated treatment and the mock-treated plants (ANOVA, Dunnet post hoc test; ∗∗ = P < 0.01; ∗ = P < 0.05). Error bars represent SE, n = 3 plants.

Mentions: Since competition for light and nutrients can increase the probability of detecting fitness costs of activating different hormone signaling pathways (Dietrich et al., 2005), Arabidopsis plants were grown in competition trays, consisting of separate small pots positioned very close together. This set-up led to competition of the above-ground plant parts, but not of the root-systems. Each tray consisted of 49 plants, of which 25 plants were supplied with a soil drench containing 500 μM SA, 50 μM MeJA, or a combination of both hormones. The other 24 plants were treated with either a mock solution or a combination of both hormones (Figure 4). Only the inner nine plants were used for measurements, to circumvent any edge effect. In all trays, SA and SA/MeJA treatment induced PR1 expression, whereas VSP2 expression was only induced by the single MeJA treatment and not by the SA/MeJA combination treatment (Figure 5), confirming that the hormone treatments induced the expected effects on SA- and JA-responsive gene expression.


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)

Differential gene expression in competition-grown plants. RT-qPCR analysis of salicylic acid (SA)-responsive PR1 expression and Jasmonic acid (JA)-responsive VSP2 expression in competition-grown plants 24 h after treatment with a mock, SA, MeJA, or SA/MeJA solution. Mock vs. SA and Mock vs. MeJA competition experiments were performed in one experimental round, and Mock vs. SA/MeJA, SA vs. SA/MeJA, and MeJA vs. SA/MeJA competition experiments were performed in another experimental round. Indicated are expression levels relative to those of mock-treated plants in one of the competition trays. Asterisks indicate a statistically significant difference between the indicated treatment and the mock-treated plants (ANOVA, Dunnet post hoc test; ∗∗ = P < 0.01; ∗ = P < 0.05). Error bars represent SE, n = 3 plants.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4538242&req=5

Figure 5: Differential gene expression in competition-grown plants. RT-qPCR analysis of salicylic acid (SA)-responsive PR1 expression and Jasmonic acid (JA)-responsive VSP2 expression in competition-grown plants 24 h after treatment with a mock, SA, MeJA, or SA/MeJA solution. Mock vs. SA and Mock vs. MeJA competition experiments were performed in one experimental round, and Mock vs. SA/MeJA, SA vs. SA/MeJA, and MeJA vs. SA/MeJA competition experiments were performed in another experimental round. Indicated are expression levels relative to those of mock-treated plants in one of the competition trays. Asterisks indicate a statistically significant difference between the indicated treatment and the mock-treated plants (ANOVA, Dunnet post hoc test; ∗∗ = P < 0.01; ∗ = P < 0.05). Error bars represent SE, n = 3 plants.
Mentions: Since competition for light and nutrients can increase the probability of detecting fitness costs of activating different hormone signaling pathways (Dietrich et al., 2005), Arabidopsis plants were grown in competition trays, consisting of separate small pots positioned very close together. This set-up led to competition of the above-ground plant parts, but not of the root-systems. Each tray consisted of 49 plants, of which 25 plants were supplied with a soil drench containing 500 μM SA, 50 μM MeJA, or a combination of both hormones. The other 24 plants were treated with either a mock solution or a combination of both hormones (Figure 4). Only the inner nine plants were used for measurements, to circumvent any edge effect. In all trays, SA and SA/MeJA treatment induced PR1 expression, whereas VSP2 expression was only induced by the single MeJA treatment and not by the SA/MeJA combination treatment (Figure 5), confirming that the hormone treatments induced the expected effects on SA- and JA-responsive gene expression.

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