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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

Growth parameters in competition-grown plants. Leaf area (cm2) and dry weight (mg) of the rosettes of competition-grown plants 3 weeks 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. Asterisks indicate a statistically significant difference between the two treatments of the indicated competition tray (Students t-test; ∗∗P < 0.01; ∗P < 0.05). Error bars represent SE, n = 20–25 plants.
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Figure 6: Growth parameters in competition-grown plants. Leaf area (cm2) and dry weight (mg) of the rosettes of competition-grown plants 3 weeks 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. Asterisks indicate a statistically significant difference between the two treatments of the indicated competition tray (Students t-test; ∗∗P < 0.01; ∗P < 0.05). Error bars represent SE, n = 20–25 plants.

Mentions: When MeJA- or SA/MeJA-treated plants competed with mock-treated plants, leaf area and dry weight of the hormone-treated plants were reduced compared to the mock-treated plants (Figure 6). SA-treated plants did not show a significant reduction in leaf area or dry weight in competition with mock-treated plants, although a trend toward a reduction in leaf area and dry weight was detected. There was no significant difference in leaf area or dry weight when MeJA- and SA/MeJA-treated plants competed with each other, although a trend toward increased dry weight and leaf area was observed in the double treatment. Together, this indicates that there was no extra negative fitness effect of the double treatment compared to the MeJA treatment alone, but rather a trend toward a reduction of MeJA-induced fitness costs in the double treatment. On the other hand, when SA-treated plants competed with SA/MeJA-treated plants, SA/MeJA-treated plants had lower dry weight than SA-treated plants, but there was no significant difference in leaf area in this competition. The observed differences in PR1 and VSP2 expression levels and in growth between plants that had received the same treatment but were placed in different competition trays can likely be ascribed to their dependency on the competition partner, but possibly also to unexpected environmental differences between trays or between experimental rounds. Still, the within tray comparisons show that especially the activation of the JA pathway resulted in lower fitness and lower competitive ability. Activation of the SA pathway did not have major negative effects on fitness in a competitive environment. Treatment with a combination of SA and MeJA reduced plant fitness, but did not result in an extra negative effect compared to the single MeJA treatment, indicating that also in dense competition stands, hormonal crosstalk might be a cost-saving strategy in induced plant immunity.


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)

Growth parameters in competition-grown plants. Leaf area (cm2) and dry weight (mg) of the rosettes of competition-grown plants 3 weeks 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. Asterisks indicate a statistically significant difference between the two treatments of the indicated competition tray (Students t-test; ∗∗P < 0.01; ∗P < 0.05). Error bars represent SE, n = 20–25 plants.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 6: Growth parameters in competition-grown plants. Leaf area (cm2) and dry weight (mg) of the rosettes of competition-grown plants 3 weeks 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. Asterisks indicate a statistically significant difference between the two treatments of the indicated competition tray (Students t-test; ∗∗P < 0.01; ∗P < 0.05). Error bars represent SE, n = 20–25 plants.
Mentions: When MeJA- or SA/MeJA-treated plants competed with mock-treated plants, leaf area and dry weight of the hormone-treated plants were reduced compared to the mock-treated plants (Figure 6). SA-treated plants did not show a significant reduction in leaf area or dry weight in competition with mock-treated plants, although a trend toward a reduction in leaf area and dry weight was detected. There was no significant difference in leaf area or dry weight when MeJA- and SA/MeJA-treated plants competed with each other, although a trend toward increased dry weight and leaf area was observed in the double treatment. Together, this indicates that there was no extra negative fitness effect of the double treatment compared to the MeJA treatment alone, but rather a trend toward a reduction of MeJA-induced fitness costs in the double treatment. On the other hand, when SA-treated plants competed with SA/MeJA-treated plants, SA/MeJA-treated plants had lower dry weight than SA-treated plants, but there was no significant difference in leaf area in this competition. The observed differences in PR1 and VSP2 expression levels and in growth between plants that had received the same treatment but were placed in different competition trays can likely be ascribed to their dependency on the competition partner, but possibly also to unexpected environmental differences between trays or between experimental rounds. Still, the within tray comparisons show that especially the activation of the JA pathway resulted in lower fitness and lower competitive ability. Activation of the SA pathway did not have major negative effects on fitness in a competitive environment. Treatment with a combination of SA and MeJA reduced plant fitness, but did not result in an extra negative effect compared to the single MeJA treatment, indicating that also in dense competition stands, hormonal crosstalk might be a cost-saving strategy in induced plant immunity.

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