Unwiring jasmonic acid defense signaling: Molecular regulation and ecological costs

Abstract

In natural environments, plants have to deal with a wide diversity of attackers, resulting in major crop losses in agricultural settings. Plant can activate defense responses against these attackers, however, there are fitness penalties like reduced plant growth associated with this. The production of plant hormones plays a crucial role in the activation of induced defense responses. The hormonal blend that is produced upon pathogen or insect attack is dependent on the lifestyle and invasion strategy of the attacker. Salicylic acid (SA) plays an important role in the activation of induced plant defenses against biotrophic pathogens. On the other hand, jasmonic acid (JA) together with abscisic acid (ABA) results in activation of the MYC-branch of the JA signaling pathway, which induces defense responses against herbivorous insects, whereas JA together with ethylene (ET) results in activation of the ERF-branch, which is effective against necrotrophic pathogens. The main goal of this study was to investigate how activation of defense signaling pathways and the crosstalk between them influences plant defense and plant fitness. We show that ABA is required for both the activation of the MYC-branch and the suppression of the ERF-branch of the JA pathway in Arabidopsis leaves infested with Pieris rapae caterpillars (small cabbage white). This antagonistic effect on the ERF-branch seems to be caused by MYC-mediated production of ABA. ABA is shown to suppress the ERF-branch at the level of transcriptional activation at the GCC-box of JA-responsive genes. Furthermore, systemic leaves of P. rapae-infested plants become primed for activation of the MYC-branch. Production of ABA upon secondary herbivore attack leads to elevated activation of defenses and improved resistance to P. rapae caterpillars. Together, we provide evidence that ABA is a crucial regulator of JA-dependent defense responses during the Arabidopsis-P. rapae interaction. Crosstalk between the different hormone signaling pathways is hypothesized to contribute to plant fitness by prioritizing one set of defense responses over others, thereby prioritizing effective over ineffective defenses, and thus minimizing fitness costs. We show that there are no additional long-term negative effects on plant fitness when plants encounter multiple attackers that activate different antagonistic defense pathways, providing a first suggestion that hormonal crosstalk might indeed be a cost-saving strategy. In a field study, we observed that Arabidopsis plants that were infected with the biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis even displayed enhanced fitness, as evidenced by a 70% increase in seed production. We show that under low nutrient availability, long-day conditions and low disease pressure, this positive effect of H. arabidopsidis infection on plant fitness was most pronounced, likely due to enhanced resource allocation from the roots to the shoots. Hence, we show that interactions between plants and pathogens do not necessarily lead to negative fitness effects for the plants, which in this case might be associated with the biotrophic lifestyle of H. arabidopsidis. Overall, understanding whether and how the functioning of the defense signaling pathways and the crosstalk between them influences plant defense and plant fitness is necessary for successful application of defense traits in crops.