Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco.

Systemic acquired resistance (SAR) is a salicylic acid (SA)-dependent heightened state of resistance against a broad spectrum of pathogens activated in the uninoculated systemic tissue of a pathogen-infected plant. For systemic protection to be initiated, a mobile signal that is produced at the site of primary infection needs to travel through the plant. Although the mobile signal (s) for SAR has been the subject of considerable research over several decades, its identity remains controversial. Our analyses of Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum) defective in induced resistance1 (dir1) mutants, which are unable to develop SAR, reveal a connection between two candidate mobile signals: methyl salicylate (MeSA) and the so-far-unidentified lipid-derived signal or signal complex missing in the dir1 mutant. The demonstration that SA accumulates in the phloem and is required to activate SAR led to the proposal of SA as the mobile signal (Yalpani et al., 1991). However, grafting experiments with tobacco plants expressing the bacterial NahG gene, which encodes the SA-degrading enzyme SA hydroxylase, suggested otherwise. Tobacco mosaic virus (TMV)-infected NahG rootstocks were still capable of generating the signal for induction of SAR in wild-type scions, despite their inability to accumulate SA. Strikingly, NahGexpressing scions failed to develop SAR, arguing that SA was essential for SAR development in the healthy systemic tissue (Vernooij et al., 1994). The requirement of SA in the systemic tissue for SAR development is now well established (for review, see Vlot et al., 2008a). Subsequent studies involving quantification of MeSA and SA levels, along with characterization of grafted plants in which the genes responsible for MeSA biosynthesis (SA methyltransferase1 [SAMT1]) or MeSA cleavage to SA (SA-binding protein2 [SABP2]) were silenced in the rootstock or scion, suggested that MeSA is a mobile SAR signal in tobacco. Analysis of these chimeric tobacco plants indicated that NtSAMT1 activity, and thus MeSA biosynthesis, is required in the primary infected leaves where the SAR signal is produced. In contrast, MeSA esterase (MSE) activity is needed in the uninoculated systemic leaves, where the SAR signal is perceived and processed (Park et al., 2007). MeSA does not induce defense responses (Seskar et al., 1998); instead, it must be converted to SA by a MSE for biological activity. Further research revealed that SABP2’s MSE activity must be inhibited in the primary infected tissue (by SA binding in its active site pocket) to facilitate the accumulation of sufficient levels of MeSA to signal SAR (Park et al., 2007, 2009). Subsequent characterization of MSEs in Arabidopsis and potato (Solanum tuberosum) confirmed the relevance of MSE activity for SAR signaling in these two species (Vlot et al., 2008b; Manosalva et al., 2010). The demonstration that 2,2,2,2#-tetrafluoracetophenone, a synthetic SA analog that inhibits MSE activity, blocks SAR development in tobacco, Arabidopsis, and potato further confirmed the importance of this enzyme and MeSA for SAR development in these plant species (Park et al., 2009). Other candidate mobile signals can be broadly categorized as lipid based/related. The first link between lipid synthesis and SAR came from analyses of the Arabidopsis suppressor of SA insensitivity2 (ssi2) mutant. These plants constitutively exhibit SAR and fail to convert stearic acid (18:0) to oleic acid (18:1) because of a mutation in a stearoyl-acyl carrier protein desaturase (Kachroo et al., 2001). Interestingly, the ssi2 suppressor mutant suppressor of fatty acid desaturase1 (sfd1; also known as gly1 [Kachroo et al., 2004]), which is compromised for SAR but not for local resistance against virulent and avirulent pathogens, contains a mutation in an enzyme involved in themetabolism of glycerol-3-P, the backbone of glycerolipids (Browse and Somerville, 1991; Nandi et al., 2003, 2004). Further evidence of a lipid-derived SAR signal came from characterization of the dir1-1 Arabidopsis mutant. These plants contain a mutation in a putative apoplastic protein with ho1 This work was supported by the National Science Foundation (grant nos. IOS–0525360 and IOS–0820405 to D.F.K.) and a German Research Foundation fellowship (grant no. DA1239/1–1 to C.C.v.D.). 2 Present address: Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. * Corresponding author; e-mail [email protected]. [W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.110.171694