Export of Salicylic Acid from the Chloroplast Requires the Multidrug and Toxin Extrusion-Like Transporter EDS5    

Abstract

Salicylic acid (SA) is central for the defense of plants to pathogens and abiotic stress. SA is synthesized in chloroplasts from chorismic acid by an isochorismate synthase (ICS1); SA biosynthesis is negatively regulated by autoinhibitory feedback at ICS1. Genetic studies indicated that the multidrug and toxin extrusion transporter ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) of Arabidopsis (Arabidopsis thaliana) is necessary for SA accumulation after biotic and abiotic stress, but so far it is not understood how EDS5 controls the biosynthesis of SA. Here, we show that EDS5 colocalizes with a marker of the chloroplast envelope and that EDS5 functions as a multidrug and toxin extrusion-like transporter in the export of SA from the chloroplast to the cytoplasm in Arabidopsis, where it controls the innate immune response. The location at the chloroplast envelope supports a model of the effect of EDS5 on SA biosynthesis: in the eds5 mutant, stress-induced SA is trapped in the chloroplast and inhibits its own accumulation by autoinhibitory feedback.

Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways

“…This response not only becomes apparent in the ICS1-defective sid2 plants, but also in another SA induction-deficient mutant, sid1, which bears a defect in the multidrug and toxin extrusion-like transporter ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) ( Figure 2C). EDS5 is required for the export of chloroplast-synthesized SA from this organelle, and SA accumulation in sid1/eds5 is supposedly inhibited by autoinhibitory feedback (Serrano et al, 2013). Furthermore, the partial SAR response is established in ics1 ics2, in which both isochorismate synthase isoforms of Col-0 are inactive (Supplemental Figure 3).…”

PROHIBITIN3 Forms Complexes with ISOCHORISMATE SYNTHASE1 to Regulate Stress-Induced Salicylic Acid Biosynthesis in Arabidopsis

“…Interestingly, the Enhanced Disease 97 Susceptibility 5 (EDS5) SA transporter in the chloroplast envelope of Arabidopsis is 98 necessary for stress-induced SA accumulation, possibly due to a regulatory coupling of SA 99 transport and synthesis (Serrano et al, 2013;Yamasaki et al, 2013). Recently, a catabolic 100 enzyme that converts SA to 2,3 dihydroxybenzoic acid in Arabidopsis was described 101 (Zhang et al, 2013).…”

“…ICS1 transcript and SA levels are induced by UV-C stress in Arabidopsis (Garcion 169 et al, 2008;Martínez et al, 2004;Nawrath et al, 2002;Serrano et al, 2013;Shapiro and 170 …”

The multidrug and toxic compound extrusion (MATE) family in plants

“…In contrast, overexpression of AtEDS5 in Arabidopsis enhanced SA accumulation and resistance to viruses (Ishihara et al 2008). Recent genetic and biochemical analyses showed that this MATE transporter functioned in epidermal cells by exporting SA from its site of biosynthesis in the chloroplast to the cytosol (Serrano et al 2013;Yamasaki et al 2013). This intracellular SA transport by AtEDS5, leading to SA accumulation, plays an essential role in plant innate immune signaling and in disease resistance.…”