Warm temperature suppresses plant systemic acquired resistance by intercepting theN-hydroxypipecolic acid immune pathway

Abstract

Climate warming influences disease development by targeting critical components of the plant immune system, including pattern-triggered immunity (PTI), effector-triggered immunity (ETI) and production of the central defence hormone salicylic acid (SA) at the primary pathogen infection site. However, it is not clear if and/or how temperature impacts systemic immunity. Here we show that pathogen-triggered systemic acquired resistance (SAR) inArabidopsis thalianais suppressed at elevated temperature. This was accompanied by global downregulation of SAR-induced genes at elevated temperature. Abolished SAR under warmer conditions was associated with reduced biosynthesis of the SAR metaboliteN-hydroxypipecolic acid (NHP) inArabidopsisand other plant species, as demonstrated by downregulation of NHP biosynthetic genes (ALD1andFMO1) and NHP precursor pipecolic acid (Pip) levels. Although multiple SAR signals have been shown previously, exogenous Pip was sufficient to restore disease protection at elevated temperature, indicating that heat-mediated SAR suppression is due to Pip-NHP downregulation. Along withALD1andFMO1, systemic expression of the SA biosynthetic geneICS1was also suppressed at warm temperature. Finally, we define a transcriptional network controlling thermosensitive NHP pathway via the master transcription factors CBP60g and SARD1. Our findings demonstrate that warm temperatures impact not only local but also systemic immunity by impinging on the NHP pathway, providing a roadmap towards engineering climate-resilient plant immune systems.

Distinct mechanisms of plant immune resilience revealed by natural variation in warm temperature-modulated disease resistance amongArabidopsisaccessions

“…This aimed to establish if these two genes are the driving force behind temperature-resilient SA levels and immunity in naturally occurring Arabidopsis accessions. As shown in Figure 3A-B, Col-0 expectedly showed temperature-sensitive CBP60g and SARD1 gene expression, with significantly lower transcript levels at 28°C compared to 23°C after pathogen infection (Kim et al, 2022; Shields et al, 2023). Interestingly, the temperature-resilient accessions Se-0 and NFA-8 behaved similarly as Col-0 in terms of defence gene expression, showing significantly lower levels of pathogen-induced CBP60g and SARD1 at 28°C compared to 23°C (Figure 3A-B).…”

“…Three leaves of 4-to 5-week-old Arabidopsis plants were syringe-infiltrated with the Pst DC3000 suspension (OD600=0.001), which was prepared as previously described (Huot et al, 2017; Kim et al, 2022; Shields et al, 2023). Plants were then incubated at 23°C (normal) or 28°C (elevated) with the same relative humidity and light cycling conditions.…”

“…Previous studies have demonstrated that elevated temperatures inhibit specific components of the plant immune system, including PTI, ETI, and SA production (De Jong et al, 2002; Wang et al, 2009; Zhu et al, 2010; Cheng et al, 2013; Menna et al, 2015; Huot et al, 2017; Velasquez et al, 2018; Kim et al, 2021; Kim et al, 2022; Shields et al, 2023). In particular, ISOCHORISMATE SYNTHASE 1(ICS1)-mediated SA biosynthesis is downregulated at elevated temperature (Malamy et al, 1992; Huot et al, 2017; Castroverde and Dina, 2021; Shields et al, 2023). Heat suppression of the SA pathway is governed through the thermosensitive, rate-limiting transcription of the master immune regulatory genes CBP60g and SARD1 (Kim et al, 2022).…”