Salicylic Acid Binding Proteins (SABPs): The Hidden Forefront of Salicylic Acid Signalling

Abstract

Salicylic acid (SA) is a phytohormone that plays important roles in many aspects of plant life, notably in plant defenses against pathogens. Key mechanisms of SA signal transduction pathways have now been uncovered. Even though details are still missing, we understand how SA production is regulated and which molecular machinery is implicated in the control of downstream transcriptional responses. The NPR1 pathway has been described to play the main role in SA transduction. However, the mode of SA perception is unclear. NPR1 protein has been shown to bind SA. Nevertheless, NPR1 action requires upstream regulatory events (such as a change in cell redox status). Besides, a number of SA-induced responses are independent from NPR1. This shows that there is more than one way for plants to perceive SA. Indeed, multiple SA-binding proteins of contrasting structures and functions have now been identified. Yet, all of these proteins can be considered as candidate SA receptors and might have a role in multinodal (decentralized) SA input. This phenomenon is unprecedented for other plant hormones and is a point of discussion of this review.

Keywords: NPR1; SABP; Salicylic acid; pathogens; salicylic acid binding protein; stress response.

Figure 1

SA biosynthesis pathways in plants. Solid arrows represent single enzymatic steps. Dashed arrows represent multiple consecutive enzymatic steps. AA-SA, amino acid-SA conjugate; BA2H, benzoic acid 2-hydroxylase; DHBA, dihydroxybenzoic acid; EPS1, Enhanced Pseudomonas Susceptibility 1; GH3.5, Gretchen Hagen 3.5; ICS, isochorismate synthase; IC-Glu, isochorismate-9-glutamate; IPL, isochorismate pyruvate lyase; MeSA, methyl-salicylate; MES, methyl-salicylate esterase; MT, metyl transferase; PAL, phenylalanine ammonia-lyase; PBS3, avrPphB susceptible 3; SAG, salicylic acid glucoside; SAH, salicylic acid hydroxylase; SGE, salicylic acid glucose ester; SOT12, sulfotransferase 12; UDP-GST, UDP-glycosyltransferase; UGT76D1, UDP-glycosyltransferase 76D1; *, enzyme not cloned in plants; **, non-enzymatic decay.

Figure 2

Effect of SA on the in-vitro catalytic activity of SABPs from A. thaliana (A) and transcriptional responses of corresponding coding genes (B). *, effect observed in tobacco orthologs. Transcriptomic data was mined using Genevestigator [95]. Experiment IDs: SA 3 h, AT-00113; SA 24 h, AT-00320; MeJA 3 h, AT-00110; Psm, AT-00406; Pst avrRpm1, AT-00106; S. sclerotiorum, AT-00681; TuMV, AT-00324; flg22, AT-00392. Note that the hierarchical clustering was performed on more experiments than the one used for the heat map (see the main text).

Figure 3

Molecular interactions between SA and selected SABPs. Black dashed links represent hydrogen bonds. Green dashed lines represent pi-pi stacking. Green solid lines represent hydrophobic interactions. Molecular graphic images were produced using UCSF Chimera [97].

Figure 4

Model of conventional hormonal input via a single receptor (R) leading to downstream responses (a); model of SA multinodal input via multiple SABPs acting as independent receptors (b). Some receptors in model B may be in a functional connection (e.g., a putative SA-binding TRX acting on NPR1) and act in a single reception pathway.

Figure 5

Schematic representation of putative functional roles of SABPs in cell metabolism. Phe, phenylalanine; DAMP, damage-associated molecular pattern; ROS, reactive oxygen species. See the main text for protein abbreviations. Solid arrows represent single enzymatic steps. Dashed arrows represent multiple consecutive enzymatic steps. Hollow arrows represent functional connections to cell activities.