Systemic acquired resistance (SAR) is a defence mechanism that induces protection against a wide range of pathogens in distant, pathogen-free parts of plants after a primary inoculation. Multiple mobile compounds were identified as putative SAR signals or important factors for influencing movement of SAR signalling elements in Arabidopsis and tobacco. These include compounds with very different chemical structures like lipid transfer protein DIR1 (DEFECTIVE IN INDUCED RESISTANCE1), methyl salicylate (MeSA), dehydroabietinal (DA), azelaic acid (AzA), glycerol-3-phosphate dependent factor (G3P) and the lysine catabolite pipecolic acid (Pip). Genetic studies with different SAR-deficient mutants and silenced lines support the idea that some of these compounds (MeSA, DIR1 and G3P) are activated only when SAR is induced in darkness. In addition, although AzA doubled in phloem exudate of tobacco mosaic virus (TMV) infected tobacco leaves, external AzA treatment could not induce resistance neither to viral nor bacterial pathogens, independent of light conditions. Besides light intensity and timing of light exposition after primary inoculation, spectral distribution of light could also influence the SAR induction capacity. Recent data indicated that TMV and CMV (cucumber mosaic virus) infection in tobacco, like bacteria in Arabidopsis, caused massive accumulation of Pip. Treatment of tobacco leaves with Pip in the light, caused a drastic and significant local and systemic decrease in lesion size of TMV infection. Moreover, two very recent papers, added in proof, demonstrated the role of FMO1 (FLAVIN-DEPENDENT-MONOOXYGENASE1) in conversion of Pip to N-hydroxypipecolic acid (NHP). NHP systemically accumulates after microbial attack and acts as a potent inducer of plant immunity to bacterial and oomycete pathogens in Arabidopsis. These results argue for the pivotal role of Pip and NHP as an important signal compound of SAR response in different plants against different pathogens.

Phytophthora Research Centre Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 613 00 Brno Czech Republic

Plant Protection Institute Centre for Agricultural Research Hungarian Academy of Sciences 15 Herman Ottó út H 1022 Budapest Hungary

Zobrazit více v PubMed

Winter P.S., Bowman C.E., Villani P.J., Dolan T.E., Hauck N.R. Systemic acquired resistance in moss: Further evidence for conserved defence mechanisms in plants. PLoS ONE. 2014;9:e101880. doi: 10.1371/journal.pone.0101880. PubMed DOI PMC

Ross A.F. Systemic acquired resistance induced by localized virus infections in plants. Virology. 1961;14:340–358. doi: 10.1016/0042-6822(61)90319-1. PubMed DOI

Luna E., Bruce T.J., Roberts M.R., Flors V., Ton J. Next-generation systemic acquired resistance. Plant Physiol. 2012;158:844–853. doi: 10.1104/pp.111.187468. PubMed DOI PMC

Sánchez A.L., Stassen J.H., Furci L., Smith L.M., Ton J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. 2016;88:361–374. doi: 10.1111/tpj.13252. PubMed DOI PMC

Conrath U. Molecular aspects of defence priming. Trends Plant Sci. 2011;16:524–531. doi: 10.1016/j.tplants.2011.06.004. PubMed DOI

Spoel S.H., Dong X. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 2012;12:89–100. doi: 10.1038/nri3141. PubMed DOI

Shah J., Zeier J. Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 2013;4:30. doi: 10.3389/fpls.2013.00030. PubMed DOI PMC

Jaskiewicz M., Conrath U., Peterhänsel C. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 2011;12:50–55. doi: 10.1038/embor.2010.186. PubMed DOI PMC

Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 2000;403:41–45. doi: 10.1038/47412. PubMed DOI

Cameron R.K., Paiva N.T., Lamb C.J., Dixon R.A. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 1999;55:121–130. doi: 10.1006/pmpp.1999.0214. DOI

Shulaev V., Silverman P., Raskin I. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature. 1997;385:718–721. doi: 10.1038/385718a0. DOI

Park S.W., Kaimoyo E., Kumar D., Mosher S., Klessig D.F. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science. 2007;318:113–116. doi: 10.1126/science.1147113. PubMed DOI

Manosalva P.M., Park S.W., Forouhar F., Tong L., Fry W.E., Klessig D.F. Methyl esterase 1 (stmes1) is required for systemic acquired resistance in potato. Mol. Plant Microbe Interact. 2010;23:1151–1163. doi: 10.1094/MPMI-23-9-1151. PubMed DOI

Maldonado A.M., Doerner P., Dixon R.A., Lamb C.J., Cameron R.K. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature. 2002;419:399–403. doi: 10.1038/nature00962. PubMed DOI

Carella P., Isaacs M., Cameron R.K. Plasmodesmata-located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long-distance movement of Defective in Induced Resistance1 in Arabidopsis. Plant Biol. 2015;17:395–401. doi: 10.1111/plb.12234. PubMed DOI

Chaturvedi R., Venables B., Petros R.A., Nalam V., Li M., Wang X., Takemoto L.J., Shah J. An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 2012;71:161–172. doi: 10.1111/j.1365-313X.2012.04981.x. PubMed DOI

Jung H.W., Tschaplinski T.J., Wang L., Glazebrook J., Greenberg J.T. Priming in systemic plant immunity. Science. 2009;324:89–91. doi: 10.1126/science.1170025. PubMed DOI

Yu K., Soares J.M., Mandal M.K., Wang C., Chanda B., Gifford A.N., Fowler J.S., Navarre D., Kachroo A., Kachroo P. A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep. 2013;3:1266–1278. doi: 10.1016/j.celrep.2013.03.030. PubMed DOI

Nandi A., Welti R., Shah J. The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell. 2004;16:465–477. doi: 10.1105/tpc.016907. PubMed DOI PMC

Chanda B., Xia Y., Mandal M.K., Yu K., Sekine K.T., Gao Q.M., Selote D., Hu Y., Stromberg A., Navarre D. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 2011;43:421–427. doi: 10.1038/ng.798. PubMed DOI

Návarová H., Bernsdorff F., Doring A.C., Zeier J. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell. 2012;24:5123–5141. doi: 10.1105/tpc.112.103564. PubMed DOI PMC

Hartmann M., Kim D., Bernsdorff F., Ajami-Rashidi Z., Scholten N., Schreiber S., Zeier T., Schuck S., Reichel-Deland V., Zeier J. Biochemical principles and functional aspects of pipecolic acid biosynthesis in plant immunity. Plant Physiol. 2017;174:124–153. doi: 10.1104/pp.17.00222. PubMed DOI PMC

Bernsdorff F., Doring A.C., Gruner K., Schuck S., Brautigam A., Zeier J. Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and -independent pathways. Plant Cell. 2016;28:102–129. doi: 10.1105/tpc.15.00496. PubMed DOI PMC

Song J.T., Lu H., McDowell J.M., Greenberg J.T. A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 2004;40:200–212. doi: 10.1111/j.1365-313X.2004.02200.x. PubMed DOI

Breitenbach H.H., Wenig M., Wittek F., Jordá L., Maldonado-Alconada A.M., Satioglu H., Colby T., Knappe C., Bichlmeier M., Pabst E., et al. Contracting roles of the apoplastic ASPARTYL PROTEASE APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT and LEGUME LECTIN-LIKE PROTEIN in Arabidopsis systemic acquired resistance. Plant Physiol. 2014;165:791–809. doi: 10.1104/pp.114.239665. PubMed DOI PMC

Lee H.H., Park Y.-J., Seo P.J., Kim J.-H., Sim H.-J., Kim S.-K., Park C.-M. Systemic immunity requires SnRK2.8-mediated nuclear import of NPR1 in Arabidopsis. Plant Cell. 2015;37:3425–3438. doi: 10.1105/tpc.15.00371. PubMed DOI PMC

Fu Z.Q., Yan S., Saleh A., Wang W., Ruble J., Oka N., Mohan R., Spoel S.H., Tada Y., Zheng N., et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature. 2012;486:228–232. doi: 10.1038/nature11162. PubMed DOI PMC

Ádám A.L., Nagy Z.Á. A szisztemikus szerzett rezisztencia szignálátvitele: Eredmények és kihívások. Signal transduction of systemic acquired resistance: Results and new challenges. Növényvédelem Plant Prot. 2016;77:435–461.

Jenns A., Kuć J. Graft transmission of systemic resistance of cucumber to anthracnose induced by Colletotrichum lagenarium and tobacco necrosis virus. Phytopathology. 1979;69:753–756. doi: 10.1094/Phyto-69-753. DOI

Nagy Z.Á., Kátay G., Gullner G., Ádám A.L. Evaluation of TMV lesion formation and timing of signal transduction during induction of systemic acquired resistance (SAR) in tobacco with a computer-assisted method. In: Shanker A.K., Shanker C., editors. Biotic and Abiotic Stress—Recent Advances and Future Perspectives. InTech; London, UK: 2016. pp. 363–372.

Nagy Z.Á., Kátay G., Gullner G., Király L., Ádám A.L. Azelaic acid accumulates in phloem exudates of TMV-infected tobacco leaves, but its application does not induce local or systemic resistance against selected viral and bacterial pathogens. Acta Physiol. Plant. 2017;39:9. doi: 10.1007/s11738-016-2303-7. DOI

Nagy Z.Á., Jung A., Varga Z., Kátay Gy., Ádám A. Effect of artificial light conditions on local and systemic resistance response of tobacco to TMV infection. Not. Bot. Horti. Agrobot. Cluj-Napoca. 2017;45:270–275. doi: 10.15835/nbha45110751. DOI

Choi J., Tanaka K., Cao Y., Qi Y., Qiu J., Liang Y., Lee S.Y., Stacey G. Identification of a plant receptor for extracellular ATP. Science. 2014;343:290–294. doi: 10.1126/science.343.6168.290. PubMed DOI

Tanaka K., Choi J., Cao Y., Stacey G. Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front. Plant Sci. 2014;5:446. doi: 10.3389/fpls.2014.00446. PubMed DOI PMC

Kørner C.J., Klauser D., Niehl A., Domínguez-Ferreras A., Chinchilla D., Boller T., Heinlein M., Hann D.R. The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol. Plant Microbe Interact. 2013;26:1271–1280. doi: 10.1094/MPMI-06-13-0179-R. PubMed DOI

Aan den Toorn M., Albrecht C., de Vries S. On the origin of SERKs: Bioinformatics analysis of the somatic embryogenesis receptor kinases. Mol. Plant. 2015;8:762–782. doi: 10.1016/j.molp.2015.03.015. PubMed DOI

He K., Gou X., Yuan T., Lin H., Asami T., Yoshida S., Russell S.D., Li J. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 2007;17:1109–1115. doi: 10.1016/j.cub.2007.05.036. PubMed DOI

Roux M., Schwessinger B., Albrecht C., Chinchilla D., Jones A., Holton N., Malinovsky F.G., Tör M., de Vries S., Zipfel C. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell. 2011;23:2440–2455. doi: 10.1105/tpc.111.084301. PubMed DOI PMC

Mishina T.E., Zeier J. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 2007;50:500–513. doi: 10.1111/j.1365-313X.2007.03067.x. PubMed DOI

Kátay Gy., Mergenthaler E., Viczián O., Nagy Z.Á., Ádám A.L. Centre for Agricultural Research, Hungarian Academy of Sciences, Plant Protection Institute, Budapest, Hungary. Different aspects of systemic immunity in tobacco. 2018. Unpublished work.

Divéki Z., Salánki K., Balázs E. The necrotic pathotype of the Cucumber mosaic virus (CMV) ns strain is solely determined by amino acid 461 of the 1a protein. Mol. Plant Microbe Interact. 2004;17:837–845. doi: 10.1094/MPMI.2004.17.8.837. PubMed DOI

Vogel-Adghough D., Stahl E., Navarova H., Zeier J. Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco. Plant Signal. Behav. 2013;8:e26366. doi: 10.4161/psb.26366. PubMed DOI PMC

Kovalev N., Pogany J., Nagy P.D. Template role of double-stranded RNA in tombusvirus replication. J. Virol. 2014;88:5638–5651. doi: 10.1128/JVI.03842-13. PubMed DOI PMC

Son K.N., Liang Z., Lipton H.L. Double-stranded RNA is detected by immunofluorescence analysis in RNA and DNA virus infections, including those by negative-stranded RNA viruses. J. Virol. 2015;89:9383–9392. doi: 10.1128/JVI.01299-15. PubMed DOI PMC

Niehl A., Wyrsch I., Boller T., Heinlein M. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol. 2016;211:1008–1019. doi: 10.1111/nph.13944. PubMed DOI

Ziebell H., Carr J.P. Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by Cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene. J. Gen. Virol. 2009;90:2288–2292. doi: 10.1099/vir.0.012070-0. PubMed DOI

Henderson I.R., Zhang X., Lu C., Johnson L., Meyers B.C., Green P.J., Jacobsen S.E. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 2006;38:721–725. doi: 10.1038/ng1804. PubMed DOI

Lee B., Park Y.S., Lee S., Song G.C., Ryu C.M. Bacterial RNAs activate innate immunity in Arabidopsis. New Phytol. 2015;209:785–797. doi: 10.1111/nph.13717. PubMed DOI

Breen S., Williams S.J., Outram M., Kobe B., Solomon P.S. Emerging insights into the functions of PATHOGENESIS-RELATED PROTEIN1. Trends Plant Sci. 2017;10:871–879. doi: 10.1016/j.tplants.2017.06.013. PubMed DOI

Gamir J., Darwiche R., Van’t Hof P., Choudhary V., Stumpe M., Schneiter R., Mauch F. The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN1 reveals the mode of action of an antimicrobial protein. Plant J. 2016;89:502–509. doi: 10.1111/tpj.13398. PubMed DOI

Chen Y.L., Lee C.Y., Cheng K.T., Chang W.H., Huang R.N., Nam H.G., Chen Y.R. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signalling in tomato. Plant Cell. 2014;26:4135–4148. doi: 10.1105/tpc.114.131185. PubMed DOI PMC

Klessig D.F., Tian M., Choi H.W. Multiple targets of salicylic acid and its derivatives in plants and animals. Front. Immunol. 2016;7:206. doi: 10.3389/fimmu.2016.00206. PubMed DOI PMC

Champigny M.J., Isaacs M., Carella P., Faubert J., Fobert P., Cameron R.K. Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis. Front. Plant Sci. 2013;4:230. doi: 10.3389/fpls.2013.00230. PubMed DOI PMC

Carella P., Kempthorne C.J., Wilson D.C., Isaacs M., Cameron R.K. Exploring the role of DIR1, DIR1-like and other lipid transfer proteins during systemic immunity in Arabidopsis. Physiol. Mol. Plant Pathol. 2017;9:49–57. doi: 10.1016/j.pmpp.2016.12.005. DOI

Cecchini N.M., Steffes K., Schlappi M.R., Gifford A.N., Greenberg J.T. Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nat. Commun. 2015;6:7658. doi: 10.1038/ncomms8658. PubMed DOI

Isaacs M., Carella P., Faubert J., Rose J.K.C., Cameron R.K. Orthology analysis and in vivo complementation studies to elucidate the role of DIR1 during systemic acquired resistance in Arabidopsis thaliana and Cucumis sativus. Front. Plant Sci. 2016;7:566. doi: 10.3389/fpls.2016.00566. PubMed DOI PMC

Liu P.P., von Dahl C.C., Park S.W., Klessig D.F. Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol. 2011;155:1762–1768. doi: 10.1104/pp.110.171694. PubMed DOI PMC

Xia Y., Yu K., Gao Q.-M., Wilson R.V., Navarre D., Kachroo P., Kachroo A. Acyl CoA binding proteins are required for cuticle formation and plant responses to microbes. Front. Plant Sci. 2012;3:224. doi: 10.3389/fpls.2012.00224. PubMed DOI PMC

Carella P., Merl-Pham J., Wilson D.C., Dey S., Hauck S.M., Vlot A.C., Cameron R.K. Comparative proteomics analysis of phloem exudates collected during the induction of systemic acquired resistance. Plant Physiol. 2016;171:1495–1510. doi: 10.1104/pp.16.00269. PubMed DOI PMC

Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic acid for the induction of systemic acquired resistance. Science. 1993;261:754–756. doi: 10.1126/science.261.5122.754. PubMed DOI

Malamy J., Carr J.P., Klessig D.F., Raskin I. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990;250:1002–1004. doi: 10.1126/science.250.4983.1002. PubMed DOI

Métraux J.P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science. 1990;250:1004–1006. doi: 10.1126/science.250.4983.1004. PubMed DOI

Delaney T.P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., et al. A central role of salicylic acid in plant disease resistance. Science. 1994;266:1247–1250. doi: 10.1126/science.266.5188.1247. PubMed DOI

Zhang Y., Xu S., Ding P., Wang D., Cheng Y.T., He J., Gao M., Xu F., Li Y., Zhu Z., et al. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. USA. 2010;107:18220–18225. doi: 10.1073/pnas.1005225107. PubMed DOI PMC

Wang L., Tsuda K., Truman W., Sato M., Nguyen le V., Katagiri F., Glazebrook J. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J. 2011;67:1029–1041. doi: 10.1111/j.1365-313X.2011.04655.x. PubMed DOI

Nawrath C., Métraux J.P. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 1999;11:1393–1404. doi: 10.2307/3870970. PubMed DOI PMC

Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001;414:562–565. doi: 10.1038/35107108. PubMed DOI

Nawrath C., Heck S., Parinthawong N., Métraux J.P. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell. 2002;14:275–286. doi: 10.1105/tpc.010376. PubMed DOI PMC

Koo Y.J., Kim M.A., Kim E.H., Song J.T., Jung C., Moon J.K., Kim J.H., Seo H.S., Song S.I., Kim J.K., et al. Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol. Biol. 2007;64:1–15. doi: 10.1007/s11103-006-9123-x. PubMed DOI

Meuwly P., Molders W., Buchala A., Metraux J.P. Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol. 1995;109:1107–1114. doi: 10.1104/pp.109.3.1107. PubMed DOI PMC

Pallas J.A., Paiva N.L., Lamb C., Dixon R.A. Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 1996;10:281–293. doi: 10.1046/j.1365-313X.1996.10020281.x. DOI

Catinot J., Buchala A., Abou-Mansour E., Metraux J.P. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett. 2008;582:473–478. doi: 10.1016/j.febslet.2007.12.039. PubMed DOI

Rasmussen J.B., Hammerschmidt R., Zook M.N. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol. 1991;97:1342–1347. doi: 10.1104/pp.97.4.1342. PubMed DOI PMC

Vernooij B., Friedrich L., Morse A., Reist R., Kolditz-Jawhar R., Ward E., Uknes S., Kessmann H., Ryals J. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance. Plant Cell. 1994;6:959–965. doi: 10.1105/tpc.6.7.959. PubMed DOI PMC

Attaran E., Zeier T.E., Griebel T., Zeier J. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell. 2009;21:954–971. doi: 10.1105/tpc.108.063164. PubMed DOI PMC

Singh V., Roy S., Giri M.K., Chaturvedi R., Chowdhury Z., Shah J., Nandi A.K. Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. Mol. Plant Microbe Interact. 2013;26:1079–1088. doi: 10.1094/MPMI-04-13-0096-R. PubMed DOI

Mishina T.E., Zeier J. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 2006;141:1666–1675. doi: 10.1104/pp.106.081257. PubMed DOI PMC

Malamy J., Hennig J., Klessig D.F. Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell. 1992;4:359–366. doi: 10.1105/tpc.4.3.359. PubMed DOI PMC

Lee H.I., Raskin I. Purification, cloning, and expression of a pathogen inducible UDP-glucose: Salicylic acid glucosyltransferase from tobacco. J. Biol. Chem. 1999;274:36637–36642. doi: 10.1074/jbc.274.51.36637. PubMed DOI

Park S.W., Liu P.P., Forouhar F., Vlot A.C., Tong L., Tietjen K., Klessig D.F. Use of a synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. J. Biol. Chem. 2009;284:7307–7317. doi: 10.1074/jbc.M807968200. PubMed DOI PMC

Vlot A.C., Klessig D.F., Park S.W. Systemic acquired resistance: The elusive signal(s) Curr. Opin. Plant Biol. 2008;11:436–442. doi: 10.1016/j.pbi.2008.05.003. PubMed DOI

Vlot A.C., Liu P.P., Cameron R.K., Park S.W., Yang Y., Kumar D., Zhou F., Padukkavidana T., Gustafsson C., Pichersky E., et al. Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J. 2008;56:445–456. doi: 10.1111/j.1365-313X.2008.03618.x. PubMed DOI

Dempsey D.A., Klessig D.F. SOS—Too many signals for systemic acquired resistance? Trends Plant Sci. 2012;17:538–545. doi: 10.1016/j.tplants.2012.05.011. PubMed DOI

Liu P.P., von Dahl C.C., Klessig D.F. The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 2011;157:2216–2226. doi: 10.1104/pp.111.187773. PubMed DOI PMC

Guedes M.E.M., Richmond S., Kuć J. Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting. Physiol. Plant Pathol. 1980;17:229–233. doi: 10.1016/0048-4059(80)90056-9. DOI

Van Bel A.J.E., Gaupels F. Pathogen-induced resistance and alarm signals in the phloem. Mol. Plant Pathol. 2004;5:495–504. doi: 10.1111/j.1364-3703.2004.00243.x. PubMed DOI

Riedlmeier M., Ghirardo A., Wenig M., Knappe C., Koch K., Georgii R., Dey S., Parker J.E., Schnitzler J.P., Vlot A.C. Monoterpenes support systemic acquired resistance within and between plants. Plant Cell. 2017;29:1440–1459. doi: 10.1105/tpc.16.00898. PubMed DOI PMC

Miquel M., Cassagne C., Browse J. A new class of Arabidopsis mutants with reduced hexadecatrienoic acid fatty acid levels. Plant Physiol. 1998;117:923–930. doi: 10.1104/pp.117.3.923. PubMed DOI PMC

Lorenc-Kukula K., Chaturvedi R., Roth M., Welti R., Shah J. Biochemical and molecular-genetic characterization of SFD1’s involvement in lipid metabolism and defense signaling. Front. Plant Sci. 2012;3:26. doi: 10.3389/fpls.2012.00026. PubMed DOI PMC

Chaturvedi R., Krothapalli K., Makandar R., Nandi A., Sparks A.A., Roth M.R., Welti R., Shah J. 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. Plant J. 2008;54:106–117. doi: 10.1111/j.1365-313X.2007.03400.x. PubMed DOI

Gao Q.M., Yu K., Xia Y., Shine M.B., Wang C., Navarre D., Kachroo A., Kachroo P. Mono- and digalactosyldiacylglycerol lipids function nonredundantly to regulate systemic acquired resistance in plants. Cell Rep. 2014;9:1681–1691. doi: 10.1016/j.celrep.2014.10.069. PubMed DOI

Draelos Z. Skin lightening preparations and the hydroquinone controversy. Dermatol. Ther. 2007;20:308–313. doi: 10.1111/j.1529-8019.2007.00144.x. PubMed DOI

Zoeller M., Stingl N., Krischke M., Fekete A., Waller F., Berger S., Mueller M.J. Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: Biogenesis of pimelic and azelaic acid. Plant Physiol. 2012;160:365–378. doi: 10.1104/pp.112.202846. PubMed DOI PMC

Wittek F., Hoffmann T., Kanawati B., Bichlmeier M., Knappe C., Wenig M., Schmitt-Kopplin P., Parker J.E., Schwab W., Vlot A.C. Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistence via azelaic acid and its precursor 9-oxo nonanoic acid. J. Exp. Bot. 2014;65:5919–5931. doi: 10.1093/jxb/eru331. PubMed DOI PMC

Djami-Tchatchou A.T., Ncube E.N., Steenkamp P.A., Dubery I.A. Similar, but different: Structurally related azelaic acid and hexanoic acid trigger differential metabolomic and transcriptomic responses in tobacco cells. BMC Plant Biol. 2017;17:227. doi: 10.1186/s12870-017-1157-5. PubMed DOI PMC

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2015.

Vicente J., Cascon T., Vicedo B., Garcia-Agustin P., Hamberg M., Castresana C. Role of 9-lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol. Plant. 2012;5:914–928. doi: 10.1093/mp/ssr105. PubMed DOI

Wang C., El-Shetehy M., Shine M.B., Yu K., Navarre D., Wendehenne D., Kachroo A., Kachroo P. Free radicals mediate systemic acquired resistance. Cell Rep. 2014;7:348–355. doi: 10.1016/j.celrep.2014.03.032. PubMed DOI

Shah J., Chaturvedi R., Chowdhury Z., Venables B., Petros R.A. Signaling by small metabolites in systemic acquired resistance. Plant J. 2014;79:645–658. doi: 10.1111/tpj.12464. PubMed DOI

Hamberger B., Ohnishi T., Hamberger B., Séguin A., Bohlmann J. Evolution of diterpene metabolism: Sitka spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiol. 2011;157:1677–1695. doi: 10.1104/pp.111.185843. PubMed DOI PMC

Kim D.H., Sung S. Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Curr. Opin. Plant Biol. 2012;15:51–56. doi: 10.1016/j.pbi.2011.10.004. PubMed DOI

Singh V., Roy S., Singh D., Nandi A.K. Arabidopsis FLOWERING LOCUS D influences systemic-acquired-resistance- induced expression and histone modifications of WRKY genes. J. Biosci. 2014;39:119–126. doi: 10.1007/s12038-013-9407-7. PubMed DOI

Plecko B., Hikel C., Korenke G.C. Pipecolic acid as a diagnostic marker of pyridoxine-dependent epilepsy. Neuropediatrics. 2005;36:200–205. doi: 10.1055/s-2005-865727. PubMed DOI

Tranchant C., Aubourg P., Mohr M., Rocchiccioli F., Zaenker C., Warter J.M. A new peroxisomal disease with impaired phytanic and pipecolic acid oxidation. Neurology. 1993;43:2044–2048. doi: 10.1212/WNL.43.10.2044. PubMed DOI

Kvenholden K.A., Lawless J.G., Ponnamperuma C. Nonprotein amino acids in the murchison meteorite. Proc. Natl. Acad. Sci. USA. 1971;68:486–490. doi: 10.1073/pnas.68.2.486. PubMed DOI PMC

Pálfi G., Dézsi L. Pipecolic acid as an indicator of abnormal protein metabolism in diseased plants. Plant Soil. 1968;29:285–291. doi: 10.1007/BF01348946. DOI

Song J.T., Lu H., Greenberg J.T. Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTRIN1, encoding novel aminotransferases. Plant Cell. 2004;16:353–366. doi: 10.1105/tpc.019372. PubMed DOI PMC

Ding P., Rekhter D., Ding Y., Feussner K., Busta L., Haroth S., Xu S., Li X., Jetter R., Feussner I., et al. Characterization of a pipecolic acid biosynthesis pathway required for systemic acquired resistance. Plant Cell. 2016;28:2603–2615. doi: 10.1105/tpc.16.00486. PubMed DOI PMC

Sun T., Busta L., Zhang Q., Ding P., Jetter R., Zhang Y. TGAGG-BINDING FACTOR1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g) New Phytol. 2018;217:344–354. doi: 10.1111/nph.14780. PubMed DOI

Hartmann M., Zeier T., Bernsdorff F., Reichel-Deland V., Kim D., Hohmann M., Scholten N., Schuck S., Bräutigam A., Hölzel T., et al. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell. 2018;17:456–469. doi: 10.1016/j.cell.2018.02.049. PubMed DOI

Chen Y.C., Holmes E.C., Rajniak J., Kim J.-G., Tang S., Fischer C.R., Mudgett M.B., Sattely E.S. (Stanford University, Stanford, CA, USA). N-hydroxy-pipecolic acid is a mobile signal that induces systemic disease resistance in Arabidopsis. [(accessed on 9 April 2018)];2018 Preprint. Available online: https://www.biorxiv.org/content/early/2018/03/25/288449. PubMed PMC

Zeier J., Pink B., Mueller M.J., Berger S. Light conditions influence specific defence responses in incompatible plant-pathogen interactions: Uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta. 2004;219:673–683. doi: 10.1007/s00425-004-1272-z. PubMed DOI

Griebel T., Zeier J. Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: Phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol. 2008;147:790–801. doi: 10.1104/pp.108.119503. PubMed DOI PMC

Genoud T., Buchala A.J., Chua N.H., Metraux J.P. Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J. 2002;31:87–95. doi: 10.1046/j.1365-313X.2002.01338.x. PubMed DOI

Muhlenbock P., Szechynska-Hebda M., Plaszczyca M., Baudo M., Mateo A., Mullineaux P.M., Parker J.E., Karpinska B., Karpinski S. Chloroplast signaling and lesion simulating disease1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell. 2008;20:2339–2356. doi: 10.1105/tpc.108.059618. PubMed DOI PMC

Fodor J., Gullner G., Ádám A.L., Barna B., Kőmíves T., Király Z. Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco (Role in systemic acquired resistance) Plant Physiol. 1997;114:1443–1451. doi: 10.1104/pp.114.4.1443. PubMed DOI PMC

Chandra-Shekara A.C., Gupte M., Navarre D., Raina S., Raina R., Klessig D., Kachroo P. Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. Plant J. 2006;45:320–334. doi: 10.1111/j.1365-313X.2005.02618.x. PubMed DOI