Plants often face a wide range of biotic and extreme environmental stresses as sessile organisms. These stresses cause physiological changes, resulting in plant growth and yield penalty. Since plants lack a circulatory immune system, they solely depend on the cell-autonomous local responses, for example, the transportation of signaling molecules through a membrane-separated vesicular system (Kwon et al., 2020; Won and Kim, 2020). Elevated temperature profoundly impacts plant defense responses and render plants vulnerable to pathogens. Research breakthroughs elucidating the underlying molecular mechanisms of this pathway were made in the last decade. Zhu et al. (2010) reported that a mutation in the resistance (R) gene sufficiently changes the temperature sensitivity of the plant immune response and confers resistance at high temperatures. Another study (Cheng et al., 2013) reported that high temperature decreased the secretion of pathogenic effectors but accelerated the proliferation of pathogenic organisms, inhibiting effector-triggered immunity (ETI) while enhancing PAMP-triggered immunity (PTI). Defense-related hormones, such as jasmonic acid, salicylic acid (SA), and ethylene, play an essential role in pathogen-induced hypersensitive responses (Huot et al., 2014). Previous studies have indicated that a higher temperature significantly suppresses pathogen-induced SA production while enhancing other hormone pathways (Gangappa et al., 2017; Huot et al., 2017; Malamy et al., 1992). However, the mechanism underlying the selective inhibition of SA signaling under high ambient temperatures in the presence of pathogens has remained elusive (Gangappa et al., 2017; Huot et al., 2017). Recently, Kim et al. (2022) found that the calmodulin-binding protein 60-like g (CBP60g) transcription factor impacts SA production, basal immunity, and ETI at an elevated temperature. CBP60g proteins are highly conserved in plants. Therefore, they might play an essential role in mediating the triangular interactions among crop plants, the pathogen, and the environment (Kim et al., 2022; Zhu et al., 2010).

Calcium signaling is essential in plant defense responses associated with PTI and ETI (Wang et al., 2009). Within the cell, calcium signals are transduced by binding calcium ions to calmodulins (CaMs), which subsequently bind to CaM binding proteins (Bouché et al., 2005). In Arabidopsis thaliana, Arabidopsis hereafter, the CBP60 family comprised seven members (CBP60a-CBP60g). A previous report (Wang et al., 2009) suggested that CBP60g is induced by infection with Pseudomonas and plays a critical role in disease resistance through the activation of SA signaling. In a recently published study, Kim et al. (2022) discovered that the temperature-induced inhibition of SA biosynthesis in response to pathogens is because of the transcriptional suppression of CBP60g. Through bulk RNA-sequencing analysis between Col-0 seedlings, which were challenged with Pseudomonas syringae pv. tomato (Pst) DC3000 at ambient (23°C) and high temperatures (28°C), the authors discovered that the transcription of CBP60g and SARD1, a closely related gene of CBP60g (Wang et al., 2011), were down-regulated at the high temperature. Kim et al. (2022) further examined the upstream regulators that transcriptionally repressed CBP60g and SARD1 expression.

GUANYLATE BINDING PROTEIN-LIKE 3 (GBPL3) forms GBPL defense-activated biomolecular condensates called GDACs, which bind to the promoters of CBP60g and other defense-related genes by recruiting mediator complex and RNA polymerase II (Huang et al., 2021). Kim et al. (2022) discovered the disassembly of the GDACs at a higher growth temperature (28°C) and concomitant inhibition in the expression of CBP60g and SARD1. This observation unveils a previously unknown pathway behind the inhibition of SA production at elevated temperatures when plants are challenged with a pathogenic elicitor.

To survive in an unfavorable environment, plants must manage limited resources to relocate to the designated organ for growth and accelerate their defense mechanisms. During this process, plants often activate defense signaling at the expense of growth. However, recent studies (Figueroa-Macías et al., 2021; Neuser et al., 2019) suggested that there could be an alternative instead of this ‘trade-off’ signaling between growth and defense regulatory mechanism that reprogram developmental pathways based on the hostile environment. When Kim et al. (2022) over-expressed CBP60g under the 35S promoter using the uORFsTBF1 strategy, which contains the upstream open reading frame (uORF) region of the TBF1 gene, they found that transgenic Arabidopsis plants could maintain a defense system and SA production even at high temperatures. Notably, the uORFsTBF1 region allows controlled protein translation in response to pathogenic infection (Xu et al., 2017). This observation, with the other conclusion led by Kim et al. (2022), strongly proposed that CBP60g is the missing link that inversely regulates plant vulnerability toward the pathogen under high temperatures.

Recent studies (Jing et al., 2019; Okada et al., 2021; Poncini et al., 2017) reported that root growth was impaired by perceiving biotic or abiotic stress signals. Consistent with this finding, we also identified that plant elicitor peptide 1 (PEP1), a general sensor of biotic and abiotic stresses, affects the reprograming of Arabidopsis root apical meristem and vascular development (Dhar et al., 2021). In addition, PEP1 strongly impacts the cell-to-cell symplastic connection, which is responsible for transporting developmental signals over a long distance. A molecular link between PEP1 perception and reprograming of the developmental signal is yet to be uncovered, which could also be employed in engineering plants with intact danger sensing without root growth penalty.

In summary, the study led by Kim et al. (2022) provided comprehensive evidence of how environmental factors control the SA-induced defense signaling pathway in connection to plant immunity. The author’s results will serve as a benchmark for understanding the concept of the plant-environment-disease triangle and prompt future researchers to identify the mechanistic approach toward the underlying defense response pathways.

We thank all members of the Lee lab for their discussions and comments at various stages. This work was supported by the grants NRF-2018R1A5A1023599 and NRF-2021R1A2C3006061 to J.-Y.L. from the National Research Foundation of Korea. S.D. was supported by the Brain Korea 21 Four Program.

S.D. and J.-Y.L. wrote the paper.

The authors have no potential conflicts of interest to disclose.