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

Growth and fitness parameters of single- and double-attacked plants. Rosette diameter (cm), flowering time (days post inoculation), and total seed production (mg) of Arabidopsis plants. Plants were either inoculated with H. arabidopsidis(A) or infested with P. rapae caterpillars (B). At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea(A,B). Different letters indicate a statistically significant difference between the different treatments (ANOVA, Tukey post hoc test; P < 0.05; NS = not significant). Error bars represent SE, n = 20 plants.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Growth and fitness parameters of single- and double-attacked plants. Rosette diameter (cm), flowering time (days post inoculation), and total seed production (mg) of Arabidopsis plants. Plants were either inoculated with H. arabidopsidis(A) or infested with P. rapae caterpillars (B). At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea(A,B). Different letters indicate a statistically significant difference between the different treatments (ANOVA, Tukey post hoc test; P < 0.05; NS = not significant). Error bars represent SE, n = 20 plants.

Mentions: To investigate whether these hormonal crosstalk-mediated effects on PDF1.2 gene expression and resistance to B. cinerea impacted the fitness of the plants under multi-attacker conditions, the rosette size, flowering time and seed production were measured. Neither H. arabidopsidis infection nor P. rapae infestation affected any of these fitness parameters by themselves (Figures 3A,B), which could be explained by the non-optimal temperature for infection with H. arabidopsidis from 24 h onward and the removal of the P. rapae caterpillars at 24 h. In contrast, B. cinerea infection had a strong negative effect on rosette size and seed production and prolonged the flowering time (Figures 3A,B). Prior attack with either H. arabidopsidis or P. rapae did not result in an additional effect on the fitness traits compared to B. cinerea infection alone. Similar results were found when plants were induced by exogenous application of 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA (Supplementary Figure S3). Overall, it can be concluded that infection with B. cinerea led to reduced fitness. Nonetheless, although prior attack by H. arabidopsidis or P. rapae or induction by exogenously applied SA or a combination of MeJA and ABA resulted in enhanced susceptibility to B. cinerea infection, which was likely due to the suppression of the ERF-branch, this was not associated with additional fitness costs.


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 and fitness parameters of single- and double-attacked plants. Rosette diameter (cm), flowering time (days post inoculation), and total seed production (mg) of Arabidopsis plants. Plants were either inoculated with H. arabidopsidis(A) or infested with P. rapae caterpillars (B). At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea(A,B). Different letters indicate a statistically significant difference between the different treatments (ANOVA, Tukey post hoc test; P < 0.05; NS = not significant). Error bars represent SE, n = 20 plants.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Growth and fitness parameters of single- and double-attacked plants. Rosette diameter (cm), flowering time (days post inoculation), and total seed production (mg) of Arabidopsis plants. Plants were either inoculated with H. arabidopsidis(A) or infested with P. rapae caterpillars (B). At 24 h the caterpillars were removed after which all plants were inoculated with B. cinerea(A,B). Different letters indicate a statistically significant difference between the different treatments (ANOVA, Tukey post hoc test; P < 0.05; NS = not significant). Error bars represent SE, n = 20 plants.
Mentions: To investigate whether these hormonal crosstalk-mediated effects on PDF1.2 gene expression and resistance to B. cinerea impacted the fitness of the plants under multi-attacker conditions, the rosette size, flowering time and seed production were measured. Neither H. arabidopsidis infection nor P. rapae infestation affected any of these fitness parameters by themselves (Figures 3A,B), which could be explained by the non-optimal temperature for infection with H. arabidopsidis from 24 h onward and the removal of the P. rapae caterpillars at 24 h. In contrast, B. cinerea infection had a strong negative effect on rosette size and seed production and prolonged the flowering time (Figures 3A,B). Prior attack with either H. arabidopsidis or P. rapae did not result in an additional effect on the fitness traits compared to B. cinerea infection alone. Similar results were found when plants were induced by exogenous application of 1 mM SA or a combination of 100 μM MeJA and 100 μM ABA (Supplementary Figure S3). Overall, it can be concluded that infection with B. cinerea led to reduced fitness. Nonetheless, although prior attack by H. arabidopsidis or P. rapae or induction by exogenously applied SA or a combination of MeJA and ABA resulted in enhanced susceptibility to B. cinerea infection, which was likely due to the suppression of the ERF-branch, this was not associated with additional fitness costs.

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