Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato.

Whether salicylic acid (SA) plays a role in systemic acquired resistance (SAR) signaling in potato is currently unclear because potato, unlike tobacco and Arabidopsis, contains highly elevated levels of endogenous SA. Recent studies have indicated that the SA derivative methyl salicylate (MeSA) serves as a long-distance phloem-mobile SAR signal in tobacco and Arabidopsis. Once in the distal, uninfected tissue of these plant species, MeSA must be converted into biologically active SA by the esterase activity of SA-binding protein 2 (SABP2) in tobacco or members of the AtMES family in Arabidopsis. In this study, we have identified the potato ortholog of tobacco SABP2 (StMES1) and shown that the recombinant protein converts MeSA to SA; this MeSA esterase activity is feedback inhibited by SA or its synthetic analog, 2, 2, 2, 2'-tetra-fluoroacetophenone (tetraFA). Potato plants (cv. Désirée) in which StMES1 activity was suppressed, due to either tetraFA treatment or silencing of StMES1 expression, were compromised for arachidonic acid (AA)-induced SAR development against Phytophthora infestans. Presumably due to the inability of these plants to convert MeSA to SA, the SAR-defective phenotype correlated with elevated levels of MeSA and reduced expression of pathogenesis-related (PR) genes in the untreated distal tissue. Together, these results strongly suggest that SAR signaling in potato requires StMES1, its corresponding MeSA esterase activity, and MeSA. Furthermore, the similarities between SAR signaling in potato, tobacco, and Arabidopsis suggest that at least certain SAR signaling components are conserved among plants, regardless of endogenous SA levels.

[1]  E. Pichersky,et al.  Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in arabidopsis. , 2010, Molecular plant-microbe interactions : MPMI.

[2]  D. Klessig,et al.  Salicylic Acid, a multifaceted hormone to combat disease. , 2009, Annual review of phytopathology.

[3]  Jane Glazebrook,et al.  Priming in Systemic Plant Immunity , 2009, Science.

[4]  K. Tietjen,et al.  Use of a Synthetic Salicylic Acid Analog to Investigate the Roles of Methyl Salicylate and Its Esterases in Plant Disease Resistance* , 2009, Journal of Biological Chemistry.

[5]  J. Zeier,et al.  Methyl Salicylate Production and Jasmonate Signaling Are Not Essential for Systemic Acquired Resistance in Arabidopsis[W] , 2009, The Plant Cell Online.

[6]  D. Scheel,et al.  PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid. , 2009, The Plant journal : for cell and molecular biology.

[7]  T. Tschaplinski,et al.  Two poplar methyl salicylate esterases display comparable biochemical properties but divergent expression patterns. , 2009, Phytochemistry.

[8]  E. Pichersky,et al.  Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[9]  D. Klessig,et al.  Systemic acquired resistance: the elusive signal(s). , 2008, Current opinion in plant biology.

[10]  J. Zeier,et al.  Light Regulation and Daytime Dependency of Inducible Plant Defenses in Arabidopsis: Phytochrome Signaling Controls Systemic Acquired Resistance Rather Than Local Defense1 , 2008, Plant Physiology.

[11]  R. Welti,et al.  Plastid omega3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. , 2007, The Plant journal : for cell and molecular biology.

[12]  D. Garvin,et al.  Enhancing beta-carotene content in potato by rnai-mediated silencing of the beta-carotene hydroxylase gene , 2007, American Journal of Potato Research.

[13]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[14]  D. Scheel,et al.  Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. , 2007, Molecular plant-microbe interactions : MPMI.

[15]  Dhirendra Kumar,et al.  Methyl Salicylate Is a Critical Mobile Signal for Plant Systemic Acquired Resistance , 2007, Science.

[16]  J. Zeier,et al.  Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[17]  M. Grant,et al.  Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates , 2007, Proceedings of the National Academy of Sciences.

[18]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[19]  Dhirendra Kumar,et al.  Validation of RNAi silencing specificity using synthetic genes: salicylic acid-binding protein 2 is required for innate immunity in plants. , 2006, The Plant journal : for cell and molecular biology.

[20]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[21]  J. Glazebrook Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. , 2005, Annual review of phytopathology.

[22]  Liang Tong,et al.  Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[23]  R. Cameron,et al.  Intercellular salicylic acid accumulation is important for age-related resistance in Arabidopsis to Pseudomonas syringae , 2004 .

[24]  A. Dmitriev Induction of systemic resistance in plants. , 2004, TSitologiia i genetika.

[25]  Martin J. Mueller,et al.  Light conditions influence specific defence responses in incompatible plant–pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation , 2004, Planta.

[26]  D. Navarre,et al.  Differential characteristics of salicylic acid-mediated signaling in potato , 2004 .

[27]  N. Yao,et al.  The role and regulation of programmed cell death in plant–pathogen interactions , 2004, Cellular microbiology.

[28]  R. Welti,et al.  The Arabidopsis thaliana Dihydroxyacetone Phosphate Reductase Gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 Is Required for Glycerolipid Metabolism and for the Activation of Systemic Acquired Resistance On-line version contains Web-only data. , 2004, The Plant Cell Online.

[29]  Xinnian Dong,et al.  Systemic acquired resistance. , 2003, Annual review of phytopathology.

[30]  A. Gleave A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome , 1992, Plant Molecular Biology.

[31]  Dhirendra Kumar,et al.  High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Dixon,et al.  A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis , 2002, Nature.

[33]  P. Waterhouse,et al.  Construct design for efficient, effective and high-throughput gene silencing in plants. , 2001, The Plant journal : for cell and molecular biology.

[34]  N. Chua,et al.  Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. , 2000, The Plant journal : for cell and molecular biology.

[35]  Jyoti Shah,et al.  Salicylic acid and disease resistance in plants. , 1999 .

[36]  D. Klessig,et al.  Is the High Basal Level of Salicylic Acid Important for Disease Resistance in Potato? , 1997, Plant physiology.

[37]  D. Klessig,et al.  Identification of a Soluble, High-Affinity Salicylic Acid-Binding Protein in Tobacco , 1997, Plant physiology.

[38]  D. Klessig,et al.  Identification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related beta-1,3-glucanase gene, PR-2d. , 1996, The Plant journal : for cell and molecular biology.

[39]  I. Raskin,et al.  Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role) , 1995, Plant physiology.

[40]  J. Metraux,et al.  Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance in potato plants to Phytophthora infestans and Alternaria solani , 1995 .

[41]  E. Ward,et al.  Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. , 1994, The Plant cell.

[42]  P. Hasegawa,et al.  Osmotin overexpression in potato delays development of disease symptoms. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Y. Cohen,et al.  Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester , 1993 .

[44]  H. Yamamoto,et al.  Rapid stimulation of 5-lipoxygenase activity in potato by the fungal elicitor arachidonic Acid. , 1992, Plant physiology.

[45]  E. Kombrink,et al.  Temporal and spatial patterns of 1, 3-beta-glucanase and chitinase induction in potato leaves infected by Phytophthora infestans , 1992 .

[46]  I. Raskin Role of Salicylic Acid in Plants , 1992 .

[47]  S. Vaughn,et al.  Further evidence that lipoxygenase activity is required for arachidonic acid-elicited hypersensitivity in potato callus cultures , 1992 .

[48]  Y. Cohen,et al.  Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids , 1991 .

[49]  D F Klessig,et al.  Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection , 1990, Science.

[50]  H. Signer,et al.  Increase in Salicylic Acid at the Onset of Systemic Acquired Resistance in Cucumber , 1990, Science.

[51]  J. Varns Terpenoid Accumulation as a Biochemical Response of the Potato Tuber to Phytophthora Infestans , 1971 .