Limits...
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 expression of PR1, VSP2, and PDF1.2 in response to multiple attackers. RT-qPCR analysis of Hyaloperonospora arabidopsidis-responsive PR1 expression (A), Pieris rapae-responsive VSP2 expression (B) and Botrytis cinerea-responsive PDF1.2 expression (A,B). Plants were either inoculated with H. arabidopsidis or infested with P. rapae caterpillars. At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea. Samples were taken at the indicated time points after the first treatment. 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.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4538242&req=5

Figure 1: Differential expression of PR1, VSP2, and PDF1.2 in response to multiple attackers. RT-qPCR analysis of Hyaloperonospora arabidopsidis-responsive PR1 expression (A), Pieris rapae-responsive VSP2 expression (B) and Botrytis cinerea-responsive PDF1.2 expression (A,B). Plants were either inoculated with H. arabidopsidis or infested with P. rapae caterpillars. At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea. Samples were taken at the indicated time points after the first treatment. 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: In this research, fitness costs associated with defense against multiple attackers were investigated. To this end, 5-week-old Arabidopsis plants were exposed to two attackers that induce antagonizing defense pathways. Firstly, the plants were either inoculated with the biotrophic pathogen Hyaloperonospora arabidopsidis, which induces the SA pathway, or infested with P. rapae caterpillars, which induce the MYC-branch of the JA pathway. Twenty-four hour later, the caterpillars were removed after which all plants were inoculated with the necrotrophic pathogen B. cinerea, which induces the ERF-branch of the JA pathway. Figure 1 shows the gene expression results from the defense inductions by the different combinations of attackers. When plants were infected with H. arabidopsidis, expression of the SA pathway marker gene PR1 was enhanced, although the induction was not statistically significant due to high variation between the biological replicates (Figure 1A). In the combination treatment of H. arabidopsidis and B. cinerea, PR1 was significantly induced at 28 h, probably because B. cinerea triggers the SA pathway as a virulence strategy (El-Oirdi et al., 2011) and the tissue may be primed for SA responsiveness by the H. arabidopsidis infection. PR1 expression leveled off again toward 72 h. Feeding by P. rapae induced the MYC-branch, as indicated by high VSP2 expression (Figure 1B). VSP2 expression returned to basal levels at 48 h and was not altered in the combination treatment with B. cinerea at any of the time points investigated. In all cases, the ERF-branch marker gene PDF1.2 was activated in response to B. cinerea infection at 48 and 72 h, but was strongly repressed when plants were previously infected with H. arabidopsidis or infested with P. rapae (Figures 1A,B). Similar antagonistic effects on PDF1.2 gene expression were found when, before B. cinerea infection, plants were induced by exogenous application of either 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA (Supplementary Figure S1). This indicates that the activation of the SA pathway or the MYC-branch of the JA pathway prior to infection with B. cinerea suppressed the B. cinerea-induced activation of the ERF-branch, providing evidence for hormonal crosstalk on defense gene expression level induced by combinations of different attackers.


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 expression of PR1, VSP2, and PDF1.2 in response to multiple attackers. RT-qPCR analysis of Hyaloperonospora arabidopsidis-responsive PR1 expression (A), Pieris rapae-responsive VSP2 expression (B) and Botrytis cinerea-responsive PDF1.2 expression (A,B). Plants were either inoculated with H. arabidopsidis or infested with P. rapae caterpillars. At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea. Samples were taken at the indicated time points after the first treatment. 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.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 1: Differential expression of PR1, VSP2, and PDF1.2 in response to multiple attackers. RT-qPCR analysis of Hyaloperonospora arabidopsidis-responsive PR1 expression (A), Pieris rapae-responsive VSP2 expression (B) and Botrytis cinerea-responsive PDF1.2 expression (A,B). Plants were either inoculated with H. arabidopsidis or infested with P. rapae caterpillars. At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea. Samples were taken at the indicated time points after the first treatment. 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: In this research, fitness costs associated with defense against multiple attackers were investigated. To this end, 5-week-old Arabidopsis plants were exposed to two attackers that induce antagonizing defense pathways. Firstly, the plants were either inoculated with the biotrophic pathogen Hyaloperonospora arabidopsidis, which induces the SA pathway, or infested with P. rapae caterpillars, which induce the MYC-branch of the JA pathway. Twenty-four hour later, the caterpillars were removed after which all plants were inoculated with the necrotrophic pathogen B. cinerea, which induces the ERF-branch of the JA pathway. Figure 1 shows the gene expression results from the defense inductions by the different combinations of attackers. When plants were infected with H. arabidopsidis, expression of the SA pathway marker gene PR1 was enhanced, although the induction was not statistically significant due to high variation between the biological replicates (Figure 1A). In the combination treatment of H. arabidopsidis and B. cinerea, PR1 was significantly induced at 28 h, probably because B. cinerea triggers the SA pathway as a virulence strategy (El-Oirdi et al., 2011) and the tissue may be primed for SA responsiveness by the H. arabidopsidis infection. PR1 expression leveled off again toward 72 h. Feeding by P. rapae induced the MYC-branch, as indicated by high VSP2 expression (Figure 1B). VSP2 expression returned to basal levels at 48 h and was not altered in the combination treatment with B. cinerea at any of the time points investigated. In all cases, the ERF-branch marker gene PDF1.2 was activated in response to B. cinerea infection at 48 and 72 h, but was strongly repressed when plants were previously infected with H. arabidopsidis or infested with P. rapae (Figures 1A,B). Similar antagonistic effects on PDF1.2 gene expression were found when, before B. cinerea infection, plants were induced by exogenous application of either 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA (Supplementary Figure S1). This indicates that the activation of the SA pathway or the MYC-branch of the JA pathway prior to infection with B. cinerea suppressed the B. cinerea-induced activation of the ERF-branch, providing evidence for hormonal crosstalk on defense gene expression level induced by combinations of different attackers.

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