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

Shields, A.; Yao, L.; Kim, J. H.; Mudher Abo Al-Timmen, W.; Li, S.; Marchetta, E.; Shivnauth, V.; Chen, T.; He, S. Y.; Xin, X.; Castroverde, C. D.

doi:10.1101/2023.10.31.564368

bioRxiv · 10.1101/2023.10.31.564368

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

Shields, A.·Yao, L.·Kim, J. H.·Mudher Abo Al-Timmen, W.·Li, S.·Marchetta, E.·Shivnauth, V.·Chen, T.·He, S. Y.·Xin, X.·Castroverde, C. D.

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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) in Arabidopsis thaliana is 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 metabolite N-hydroxypipecolic acid (NHP) in Arabidopsis and other plant species (such as tomato and rapeseed), as demonstrated by downregulation of NHP biosynthetic genes (ALD1 and FMO1) and reduced NHP and pipecolic acid (Pip) levels. Although multiple SAR signals have been shown previously, exogenous NHP or Pip was sufficient to restore disease protection at elevated temperature, indicating that heat-mediated SAR suppression is due to downregulation of the NHP pathway. Along with ALD1 and FMO1, local and systemic expression of the SA biosynthetic gene ICS1 were 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 NHP biosynthesis, providing a roadmap towards engineering climate-resilient plant immune systems.

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Shields, A., Yao, L., Kim, J. H., Mudher Abo Al-Timmen, W., Li, S., Marchetta, E., Shivnauth, V., Chen, T., He, S. Y., Xin, X., Castroverde, C. D.. 2023-11-01. Warm temperature suppresses plant systemic acquired resistance by intercepting the N-hydroxypipecolic acid immune pathway. https://doi.org/10.1101/2023.10.31.564368

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