Molecular regulation of the salicylic acid hormone pathway in plants under changing environmental conditions.

Salicylic acid (SA) is a central plant hormone mediating immunity, growth, and development. Recently, studies have highlighted the sensitivity of the SA pathway to changing climatic factors and the plant microbiome. Here we summarize organizing principles and themes in the regulation of SA biosynthesis, signaling, and metabolism by changing abiotic/biotic environments, focusing on molecular nodes governing SA pathway vulnerability or resilience. We especially highlight advances in the thermosensitive mechanisms underpinning SA-mediated immunity, including differential regulation of key transcription factors (e.g., CAMTAs, CBP60g, SARD1, bHLH059), selective protein-protein interactions of the SA receptor NPR1, and dynamic phase separation of the recently identified GBPL3 biomolecular condensates. Together, these nodes form a biochemical paradigm for how the external environment impinges on the SA pathway.

Distinct profiles of plant immune resilience revealed by natural variation in warm temperature-modulated disease resistance among Arabidopsis accessions.

Elevated temperature suppresses the plant defence hormone salicylic acid (SA) by downregulating the expression of master immune regulatory genes CALMODULIN BINDING PROTEIN 60-LIKE G (CBP60g) and SYSTEMIC ACQUIRED RESISTANCE DEFICIENT1 (SARD1). However, previous studies in Arabidopsis thaliana plants have primarily focused on the accession Columbia-0 (Col-0), while the genetic determinants of intraspecific variation in Arabidopsis immunity under elevated temperature remain unknown. Here we show that BASIC HELIX LOOP HELIX 059 (bHLH059), a thermosensitive SA regulator at nonstress temperatures, does not regulate immune suppression under warmer temperatures. In agreement, temperature-resilient and -sensitive Arabidopsis accessions based on disease resistance to the bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000 did not correlate with bHLH059 polymorphisms. Instead, we found that temperature-resilient accessions exhibit varying CBP60g and SARD1 expression profiles, potentially revealing CBP60g/SARD1-dependent and independent mechanisms of immune resilience to warming temperature. We identified thermoresilient accessions that exhibited either temperature-sensitive or -insensitive induction of the SA biosynthetic gene ICS1 (direct target gene of CBP60g and SARD1) and SA hormone levels. Collectively, this study has unveiled the intraspecific diversity of Arabidopsis immune responses under warm temperatures, which could aid in predicting plant responses to climate change and provide foundational knowledge for climate-resilient crop engineering.

Structural diversity and stress regulation of the plant immunity-associated CALMODULIN-BINDING PROTEIN 60 (CBP60) family of transcription factors in Solanum lycopersicum (tomato).

Cellular signaling generates calcium (Ca2+) ions, which are ubiquitous secondary messengers decoded by calcium-dependent protein kinases, calcineurins, calreticulin, calmodulins (CAMs), and CAM-binding proteins. Previous studies in the model plant Arabidopsis thaliana have shown the critical roles of the CAM-BINDING PROTEIN 60 (CBP60) protein family in plant growth, stress responses, and immunity. Certain CBP60 factors can regulate plant immune responses, like pattern-triggered immunity, effector-triggered immunity, and synthesis of major plant immune-activating metabolites salicylic acid (SA) and N-hydroxypipecolic acid (NHP). Although homologous CBP60 sequences have been identified in the plant kingdom, their function and regulation in most species remain unclear. In this paper, we specifically characterized 11 members of the CBP60 family in the agriculturally important crop tomato (Solanum lycopersicum). Protein sequence analyses revealed that three CBP60 homologs have the closest amino acid identity to Arabidopsis CBP60g and SARD1, master transcription factors involved in plant immunity. Strikingly, AlphaFold deep learning-assisted prediction of protein structures highlighted close structural similarity between these tomato and Arabidopsis CBP60 homologs. Conserved domain analyses revealed that they possess CAM-binding domains and DNA-binding domains, reflecting their potential involvement in linking Ca2+ signaling and transcriptional regulation in tomato plants. In terms of their gene expression profiles under biotic (Pseudomonas syringae pv. tomato DC3000 pathogen infection) and/or abiotic stress (warming temperatures), five tomato CBP60 genes were pathogen-responsive and temperature-sensitive, reminiscent of Arabidopsis CBP60g and SARD1. Overall, we present a genome-wide identification of the CBP60 gene/protein family in tomato plants, and we provide evidence on their regulation and potential function as Ca2+-sensing transcriptional regulators.

The plant disease triangle facing climate change: a molecular perspective.

Variations in climate conditions can dramatically affect plant health and the generation of climate-resilient crops is imperative to food security. In addition to directly affecting plants, it is predicted that more severe climate conditions will also result in greater biotic stresses. Recent studies have identified climate-sensitive molecular pathways that can result in plants being more susceptible to infection under unfavorable conditions. Here, we review how expected changes in climate will impact plant-pathogen interactions, with a focus on mechanisms regulating plant immunity and microbial virulence strategies. We highlight the complex interactions between abiotic and biotic stresses with the goal of identifying components and/or pathways that are promising targets for genetic engineering to enhance adaptation and strengthen resilience in dynamically changing environments.