Too hot to defend: elevated temperature compromises systemic acquired resistance

Abstract

When exposed to pathogens, plants activate immune responses at the infection site to fend off the invader; these include both broad-spectrum pattern-triggered immunity (PTI) and more specialized effector-triggered immunity (ETI). Local immune responses also generate long-distance signals that prepare distal, uninfected tissues for secondary pathogen attack in a process called systemic acquired resistance (SAR). SAR depends on major signaling molecules that act through partially parallel pathways, including the central defense phytohormone salicylic acid (SA) and N-hydroxypipecolic acid (NHP), a major constituent of the SAR signal (Gao et al., 2021).

Pathogen attack typically slows plant growth, while conditions favoring rapid growth—such as shade or elevated temperature—increase susceptibility to disease. This balance, commonly referred to as the “growth-defense trade-off,” is usually attributed to the reallocation of resources from one process to the other (He et al., 2022). Elevated temperature reduces the level and activity of multiple immunity-promoting factors (Hua & Dong, 2022), and the transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) links the promotion of growth under high temperature with the suppression of immunity (Gangappa et al., 2017). But while the effects of elevated temperature on local immunity signaling and response have been well-documented, its impact on SAR remained unexplored.

Christian Danve Castroverde and his team at Wilfrid Laurier University study how temperature affects plant immunity and disease resistance, aiming to better understand the “plant–pathogen–environment” disease triangle and to leverage this knowledge for improving plant resilience in a warming climate. In the highlighted study, MSc student Alyssa Shields tackled a key question in this context: does elevated temperature influence immunity only locally or also systemically? To address this, she infected lower leaves of Arabidopsis thaliana plants with the model pathogen Pseudomonas syringae pv tomato (Pst), which causes bacterial speck disease; upper, previously uninfected (systemic) leaves were then challenged with Pst 2 days later. At 23°C, bacterial growth in the systemic leaves was strongly suppressed, indicating effective SAR; at 28°C, however, this protection was lost, suggesting that SAR is impaired at elevated temperatures.

Lingya Yao, an assistant research fellow under the supervision of Xiu-Fang Xin at the CAS Center for Excellence in Molecular Plant Science at the time, joined the project to help uncover the underlying mechanisms. Integrating a SAR transcriptome (Hartmann et al., 2018) with the group's own temperature-regulated transcriptome (Kim et al., 2022), they found more than 1100 SAR-induced genes that are downregulated at elevated temperature, many of them involved in the PTI, ETI, SA, and NHP pathways. Strikingly, this set comprised all genes required for the biosynthesis of NHP and its precursor pipecolic acid (Pip). Upon Pst infection, transcript levels of the early NHP biosynthesis gene AGD2-LIKE DEFENSE RESPONSE PROTEIN 1 (ALD1) and the late biosynthesis gene FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1) were lower at 28°C than at 23°C. These gene expression changes correlated with reduced levels of NHP and Pip. Crucially, these effects were observed not only locally but also in systemic (i.e., uninfected) leaves, confirming that elevated temperature disrupts systemic immunity signaling.

Reduced NHP biosynthesis appeared central to the weakened SAR at elevated temperatures and could be overcome by the application of NHP: infiltrating leaves with NHP prior to infection significantly reduced pathogen growth even at 28°C (Figure 1a). Pip treatment reduced infection to a lesser degree, likely because reduced FMO1 levels limited its conversion to NHP. Interestingly, NHP treatment restored the expression level of many SAR genes but not that of the SA biosynthesis gene ISOCHORISMATE SYNTHASE 1 (ICS1), suggesting that NHP-induced SAR does not require ICS1-dependent SA biosynthesis.

Expression of NHP biosynthesis genes during pathogen attack is activated by the transcription factors CALMODULIN-BINDING PROTEIN 60-LIKE G (CBP60g) and SAR-DEFICIENT 1 (SARD1) (Huang et al., 2020). Shields et al. found that transcript levels of both transcription factors increase locally and systemically after Pst infection at 23°C but not at 28°C. These findings point to a role for CBP60g and SARD1 in temperature-dependent attenuation of SAR. Indeed, overexpression of either CBP60g or SARD1 restored induction of NHP biosynthesis genes and increased Pip accumulation at 28°C. In the CBP60g overexpression lines, effective SAR was observed at both 23°C and 28°C, whereas overexpression of SARD1 conferred constitutively elevated resistance even without prior exposure to pathogens. These distinct effects suggest functional divergence between the two otherwise highly redundant transcription factors.

Overall, Shields et al. showed that elevated temperature compromises the plant's ability to mount effective SAR by suppressing NHP biosynthesis (Figure 1b). SAR is broadly conserved across the plant kingdom; the authors found that elevated temperature also reduced NHP biosynthesis in other Brassicaceae and Solanaceae species, suggesting that the temperature sensitivity of SAR may likewise be conserved. This knowledge is not only relevant to better understand plant disease responses in an environmental context but can also inform strategies for improving plant resilience in a changing climate. Applying such knowledge for crop improvement, however, is not straightforward. Direct application of NHP, Pip, or other SAR-inducing chemicals is impractical because they are expensive to synthesize. Manipulating the levels of rate-limiting regulators such as CBP60g and SARD1 is more attractive, but their constitutive overexpression risks negative pleiotropic effects. Castroverde thus thinks more precise strategies, such as adding or modifying cis-regulatory elements using precision breeding, are the most promising approach for improving climate resilience.