Immune signaling networks must be tunable to alleviate fitness costs associated with immunity and, at the same time, robust against pathogen interferences. How these properties mechanistically emerge in plant immune signaling networks is poorly understood. Here, we discovered a molecular mechanism by which the model plant species Arabidopsis thaliana achieves robust and tunable immunity triggered by the microbe‐associated molecular pattern, flg22. Salicylic acid (SA) is a major plant immune signal molecule. Another signal molecule jasmonate (JA) induced expression of a gene essential for SA accumulation, EDS5. Paradoxically, JA inhibited expression of PAD4, a positive regulator of EDS5 expression. This incoherent type‐4 feed‐forward loop (I4‐FFL) enabled JA to mitigate SA accumulation in the intact network but to support it under perturbation of PAD4, thereby minimizing the negative impact of SA on fitness as well as conferring robust SA‐mediated immunity. We also present evidence for evolutionary conservation of these gene regulations in the family Brassicaceae. Our results highlight an I4‐FFL that simultaneously provides the immune network with robustness and tunability in A. thaliana and possibly in its relatives.
This study identifies an incoherent type‐4 feed‐forward loop (I4‐FFL) consisting of jasmonate, PAD4, and EDS5 in Arabidopsis. This I4‐FFL ensures robust and tunable accumulation of salicylic acid during immune activation through flagellin sensing.
Jasmonate (JA) induces EDS5 expression while repressing the positive EDS5 regulator PAD4.
MYC transcription factors mediate gene regulation by JA.
JA mitigates salicylic acid (SA) accumulation and bacterial resistance through PAD4 inhibition.
Upon perturbation of PAD4, JA supports SA accumulation and bacterial resistance via the regulation of EDS5.
EMBO Reports (2017) 18: 464–476
- Received July 13, 2016.
- Revision received November 9, 2016.
- Accepted December 8, 2016.
- © 2017 The Authors
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