Building a temperature-resilient immunity of plants in a changing climate

Abstract

Recent findings highlight a positive correlation between the increasing spread of plant diseases and pests and climate change. salicylic acid (SA), a key defense phytohormone, is known to be one of the central molecules to defend against not only pathogens and pests but also tolerance to various abiotic stresses. Under elevated temperatures above the optimal growth range, SA production and signaling are particularly compromised by elevated temperatures, suggesting that the growth temperature of plants is one of the rate-limiting factors for plant immunity. In this study, we show that suppressed SA production and signaling are conserved phenomena across plant taxa, causing compromised SA-mediated immunity. Using the Arabidopsis thaliana-Pseudomonas syringe model pathosystem, we identified the transcription of CBP60g/SARD1 as the temperature-vulnerable module in SA biosynthesis pathway, and unique rate-limiting steps to recover SA-mediated immunity under elevated temperatures since constitutive activation of other SA signaling components, including the major SA receptor gene NPR1 and biosynthetic gene ICS1, failed to restore SA-mediated defenses at elevated temperatures. Further mechanism study reveals that suppression of CBP60g/SARD1 pathways occurs independently of the canonical thermo-sensing molecules PHYTOCHROME B or EARLY FLOWERING 3 in thermomorphogenesis or flowering, respectively. Instead, elevated temperature negatively reprograms the recruitment of GUANYLATE BINDING PROTEIN-LIKE 3 (GBPL3) defense-associated biomolecular condensates (GDAC) along with general transcription machinery such as Mediator and RNA polymerase II at CBP60g locus. Collectively, our result may be a promising strategy to build temperature-resilient plant immunity under warming climates.