Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid

Abstract

The plant hormone salicylic acid (SA) is essential for local defense and systemic acquired resistance (SAR). When plants, such as Arabidopsis, are challenged by different pathogens, an increase in SA biosynthesis generally occurs through transcriptional induction of the key synthetic enzyme isochorismate synthase 1 (ICS1). However, the regulatory mechanism for this induction is poorly understood. Using a yeast one-hybrid screen, we identified two transcription factors (TFs), NTM1-LIKE 9 (NTL9) and CCA1 HIKING EXPEDITION (CHE), as activators of ICS1 during specific immune responses. NTL9 is essential for inducing ICS1 and two other SA synthesis-related genes, PHYTOALEXIN-DEFICIENT 4 (PAD4) and ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), in guard cells that form stomata. Stomata can quickly close upon challenge to block pathogen entry. This stomatal immunity requires ICS1 and the SA signaling pathway. In the ntl9 mutant, this response is defective and can be rescued by exogenous application of SA, indicating that NTL9-mediated SA synthesis is essential for stomatal immunity. CHE, the second identified TF, is a central circadian clock oscillator and is required not only for the daily oscillation in SA levels but also for the pathogen-induced SA synthesis in systemic tissues during SAR. CHE may also regulate ICS1 through the known transcription activators CALMODULIN BINDING PROTEIN 60g (CBP60g) and SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) because induction of these TF genes is compromised in the che-2 mutant. Our study shows that SA biosynthesis is regulated by multiple TFs in a spatial and temporal manner and therefore fills a gap in the signal transduction pathway between pathogen recognition and SA production.

Regulation of Stomatal Defense by Air Relative Humidity

“…On the other hand, the SA biosynthesis-related genes, ICS1, EDS1, and PAD4 are induced in guard cells within 1 h of exposure to the immunity elicitor flg22 (Zheng et al, 2015), suggesting that fast SA accumulation could happen in guard cells. Due to technical impediments to quantify SA accumulation in this specialized cell type, it was not possible to distinguish between these alternatives in this study.…”

Stomatal Defense a Decade Later

“…Furthermore, the SA-responsive genes ICS1, EDS1, and PAD4 are induced in guard cells within 1 h after exposure to flg22 (Zheng et al, 2015). Direct measurement of SA concentration in guard cell is currently not possible due to current technical challenges.…”

S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis

“…Plants generally maintain hormone homeostasis by fine-tuning the balance between the biosynthesis and catabolism of the hormone. ICS1 and ICS2 are two key genes in the SA biosynthesis pathway that are regulated by multiple factors, such as pathogen infections, ethylene signaling, and circadian rhythms (Chen et al, 2009;Wang et al, 2015;Zheng et al, 2015). Although a small amount of SA produced in planta remains in a free state, most SA is subjected to biologically relevant chemical modifications by different enzymes after synthesis (Dempsey et al, 2011).…”