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Long-Distance Signaling in Systemic Acquired Resistance

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Part of the Signaling and Communication in Plants book series (SIGCOMM,volume 19)

Abstract

Systemic acquired resistance (SAR) is an inducible defense mechanism in plants that is activated throughout the foliage in response to a prior localized exposure to a foliar pathogen. The enhanced resistance status resulting from the activation of SAR can be maintained over a couple of generations. Critical to SAR is effective long-distance communication by the pathogen-inoculated organ with rest of the foliage, which requires the lipid transfer protein DIR1. The emerging consensus is that long-distance signaling in SAR involves networking between multiple vascular-translocated signaling molecules. The proposed salicylic acid receptor NPR1 is important for downstream signaling that involves defense priming. Chromatin remodeling is projected as an important mechanism in priming and memory associated with SAR.

Keywords

  • Azelaic acid
  • Dehydroabietinal
  • Glycerol-3-phosphate
  • Methyl salicylate
  • Pipecolic acid
  • DIR1

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References

  • Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–971

    PubMed  CrossRef  CAS  Google Scholar 

  • Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953

    PubMed  CrossRef  CAS  Google Scholar 

  • Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669

    PubMed  CrossRef  CAS  Google Scholar 

  • Chanda B, Xia Y, Mandal MK, Yu K, Sekine K-T, Gao Q-M, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427

    PubMed  CrossRef  CAS  Google Scholar 

  • Chassot C, Métraux J-P (2005) The cuticle as source of signals for plant defense. Plant Biosyst 139:28–31

    CrossRef  Google Scholar 

  • Chassot C, Nawrath C, Métraux J-P (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49:972–980

    PubMed  CrossRef  CAS  Google Scholar 

  • Chaturvedi R, Shah J (2007) Salicylic acid in plant disease resistance. In: Hayat S, Ahmad A (eds) Salicylic acid – a plant hormone. Springer, Dordrecht, pp 335–370

    CrossRef  Google Scholar 

  • Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks A, Roth MR, Welti R, Shah J (2008) Plastid ω-3 desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54:106–117

    PubMed  CrossRef  CAS  Google Scholar 

  • Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172

    PubMed  CrossRef  CAS  Google Scholar 

  • Chester KS (1933) The problem of acquired physiological immunity in plants. Q Rev Biol 8:275–324

    CrossRef  Google Scholar 

  • Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531

    PubMed  CrossRef  CAS  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–1796

    PubMed  CrossRef  CAS  Google Scholar 

  • Depmsey DA, Klessig DF (2012) SOS – too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545

    CrossRef  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    PubMed  CrossRef  CAS  Google Scholar 

  • Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102:1773–1778

    PubMed  CrossRef  CAS  Google Scholar 

  • Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232

    PubMed  CAS  Google Scholar 

  • Gessler C, Kuc J (1982) Induction of resistance to Fusarium wilt in cucumber by root and foliar pathogens. Phytopathology 72:1439–1441

    CrossRef  Google Scholar 

  • Griebel T, Zeier J (2008) Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol 147:790–801

    PubMed  CrossRef  CAS  Google Scholar 

  • Guedes MEM, Richmond S, Kuc J (1980) lnduced 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 17:229–233

    CrossRef  Google Scholar 

  • Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168:2197–2206

    PubMed  CrossRef  CAS  Google Scholar 

  • Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55

    PubMed  CrossRef  CAS  Google Scholar 

  • pJenns A, Kuc J (1979) Graft transmission of systemic resistance of cucumber to anthracnose induced by Colletotrichum lagenarium and tobacco necrosis virus. Phytopathology 69:753–756

    CrossRef  Google Scholar 

  • Jing B, Xu S, Xu M, Li Y, Li S, Ding J, Zhang Y (2011) Brush and spray: a high-throughput systemic acquired resistance assay suitable for large-scale genetic screening. Plant Physiol 157:973–980

    PubMed  CrossRef  CAS  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91

    PubMed  CrossRef  Google Scholar 

  • Kiefer IW, Slusarenko AJ (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol 132:840–847

    PubMed  CrossRef  CAS  Google Scholar 

  • Koo YJ, Kim MA, Kim EH, Song JT, Jung C, Moon J-K, Kim J-H, Seo HS, Song SI, Kim JK, Lee JS, Cheong JL, Choi YD (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64:1–15

    PubMed  CrossRef  CAS  Google Scholar 

  • Kumar D, Gustafsson C, Klessig DF (2006) Validation of RNAi silencing specificity using synthetic genes: salicylic acid-binding protein 2 is required for innate immunity in plants. Plant J 45:863–868

    PubMed  CrossRef  CAS  Google Scholar 

  • Lascombe M-B, Bakan B, Buhot N, Marion D, Blein J-P, Larue V, Lamb C, Prange T (2008) The structure of “defective in induced resistance” protein of Arabidopsis thaliana, DIR1, reveals a new type of lipid transfer protein. Protein Sci 17:1522–1530

    PubMed  CrossRef  CAS  Google Scholar 

  • Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576

    PubMed  CrossRef  CAS  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    PubMed  CrossRef  CAS  Google Scholar 

  • Liu P-P, Yang Y, Pichersky E, Klessig DF (2010) Altering expression of Benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in Arabidopsis. Mol Plant-Microbe Interact 23:82–90

    PubMed  CrossRef  CAS  Google Scholar 

  • Liu PP, von Dahl CC, Klessig DF (2011a). The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol 157:2216–2226. doi:10.3389/fpls.2013.00030

    PubMed  CrossRef  CAS  Google Scholar 

  • Liu PP, von Dahl CC, Park SW, Klessig DF (2011b) Interconnection between methyl salicylate and lipid-based long distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol 144:1762–1768

    CrossRef  Google Scholar 

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

    PubMed  CrossRef  CAS  Google Scholar 

  • Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next generation systemic acquired resistance. Plant Physiol 158:844–853

    PubMed  CrossRef  CAS  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    PubMed  CrossRef  CAS  Google Scholar 

  • Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic acquired resistance signalling in Arabidopsis. Nature 419:399–403

    PubMed  CrossRef  CAS  Google Scholar 

  • Manosalva PM, Park SW, Forouhar F, Tong L, Fry WE, Klessig DF (2010) Methyl Esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol Plant-Microbe Interact 23:1151–1163

    PubMed  CrossRef  CAS  Google Scholar 

  • Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverard B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004–1006

    PubMed  CrossRef  Google Scholar 

  • Mishina TE, Zeier J (2006) The Arabidopsis favin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol 141:1666–1675

    PubMed  CrossRef  CAS  Google Scholar 

  • Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513

    PubMed  CrossRef  CAS  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    PubMed  CrossRef  CAS  Google Scholar 

  • Nandi A, Welti R, Shah J (2004) 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. Plant Cell 16:465–477

    PubMed  CrossRef  CAS  Google Scholar 

  • Návarová H, Bernsdorff F, Döring A-C, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141.

    PubMed  CrossRef  Google Scholar 

  • Pajerowska-Mukhtar KM, Wang W, Tada Y, Oka N, Tucker CL, Fonesca JP, Dong X (2012) The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr Biol 22:103–112

    PubMed  CrossRef  CAS  Google Scholar 

  • Pallas JA, Paiva NL, Lamb C, Dixon RA (1996) 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 10:281–293

    CrossRef  CAS  Google Scholar 

  • Park S-W, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    PubMed  CrossRef  CAS  Google Scholar 

  • Park S-W, Liu P-P, Forouhar F, Vlot AC, Tong L, Tietjen K, Klessig DF (2009) Use of a synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. J Biol Chem 284:7307–7317

    PubMed  CrossRef  CAS  Google Scholar 

  • Pick T, Jaskiewicz M, Peterhänsel C, Conrath U (2012) Heat Shock Factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol 159:52–55

    PubMed  CrossRef  CAS  Google Scholar 

  • Ross AF (1966) Systemic effects of local lesion formation. In: Beemster ABR, Dijkstra J (eds) Viruses of plants. North-Holland, Amsterdam, pp 127–150

    Google Scholar 

  • Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464

    PubMed  CrossRef  CAS  Google Scholar 

  • Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance. Frontiers Plant Sci. 4:30

    Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    PubMed  CrossRef  CAS  Google Scholar 

  • Song J, Lu H, Greenberg J (2004a) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16:353–366

    PubMed  CrossRef  CAS  Google Scholar 

  • Song J, Lu H, McDowell JM, Greenberg J (2004b) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J 40:200–212

    PubMed  CrossRef  CAS  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100

    PubMed  CrossRef  CAS  Google Scholar 

  • Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual role in regulating plant immunity. Cell 317:860–872

    CrossRef  Google Scholar 

  • Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Phtopathol 35:235–270

    CrossRef  CAS  Google Scholar 

  • Tahiri-Alaoui A, Dumas-Gaudot E, Gianinazzi S, Antoniw JF (1993) Expression of the PR-b1 gene in roots of two Nicotiana species and their amphidiploid hybrid infected with virulent and avirulent races of Chalara elegans. Plant Pathol 42:728–736

    CrossRef  CAS  Google Scholar 

  • Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304

    PubMed  CrossRef  CAS  Google Scholar 

  • Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Annu Rev Plant Physiol Plant Mol Biol 52:689–724

    PubMed  CrossRef  CAS  Google Scholar 

  • Traw MB, Kniskern JM, Bergelson J (2007) SAR increases fitness of Arabidopsis thaliana in the presence of natural bacterial pathogens. Evolution 61:2444–2449

    PubMed  CrossRef  Google Scholar 

  • Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104:1075–1080

    PubMed  CrossRef  CAS  Google Scholar 

  • Tuzun S, Kuc J (1985) Movement of a factor in tobacco infected with Peranospora tabacina Adam which systemically protects against blue mold. Physiol Plant Pathol 26:321–330

    CrossRef  Google Scholar 

  • Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656

    PubMed  CAS  Google Scholar 

  • van den Burg HA, Takken FLW (2009) Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14:286–294

    PubMed  CrossRef  Google Scholar 

  • van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–354

    CrossRef  Google Scholar 

  • van Wees SCM, de Swart EAM, van Pelt JA, van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716

    PubMed  CrossRef  Google Scholar 

  • Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquire. Plant Cell 6:959–965

    PubMed  CAS  Google Scholar 

  • Vlot AC, Liu P-P, Cameron RK, Park S-W, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456

    PubMed  CrossRef  CAS  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647

    PubMed  CrossRef  CAS  Google Scholar 

  • Xia Y, Gao Q-M, Yu K, Navarre D, Hildebrand D, Kachroo A, Kachroo P (2009) An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe 5:151–165

    PubMed  CrossRef  CAS  Google Scholar 

  • Xia Y, Yu K, Navarre D, Seebold K, Kachroo A, Kachroo P (2010) The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol 154:833–846

    PubMed  CrossRef  CAS  Google Scholar 

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

    PubMed  CrossRef  Google Scholar 

  • Yalpani N, Silverman P, Wilson TMA, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809–818

    PubMed  CAS  Google Scholar 

  • Zeier J, Pink B, Müeller MJ, Berger S (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219:673–683

    PubMed  CrossRef  CAS  Google Scholar 

  • Zoeller M, Stingl N, Krischke M, Fekete A, Waller F, Berger S, Mueller MJ (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol 160:365–378

    PubMed  CrossRef  CAS  Google Scholar 

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Acknowledgments

The authors thank Jürgen Zeier for sharing unpublished results. This work was supported by grants from the National Science Foundation (IOS-1121570 and MCB-0920600) and the U.S. Department of Agriculture as a cooperative project with the U.S. Wheat & Barley Scab Initiative (Agreement No. 59-0790-8-060).

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Correspondence to Jyoti Shah .

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Shah, J., Chaturvedi, R. (2013). Long-Distance Signaling in Systemic Acquired Resistance. In: Baluška, F. (eds) Long-Distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36470-9_1

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