Abstract
Background
Plant pathogens are responsible for many of history’s greatest famines. Understanding how plants defend themselves against pathogens is crucial to preventing future famines. Salicylic acid (SA)-mediated plant defense is a key defense pathway, which plants use to defend against biotrophic and hemi-biotrophic pathogens. As a master regulator of SAmediated plant defense, NPR1 interacts with TGA and WRKY transcription factor families, individual members of which positively or negatively regulate plant defense.
Objective
In this review we describe the recent developments and predict future directions of research on the involvement of circadian rhythm-, autophagy-, and viral RNA silencing-related genes in SA-mediated plant defense on SA, on plant defense, the induction effects of PR proteins, and the mechanisms by which NPR1 regulates defense-related genes.
Methods
We performed an extensive search of current and past literature using the PubMed, Google Scholar, and Google search engines. Our search terms included: “SA-mediated plant defense,” and “NPR1 [AND] salicylic acid.” Other search terms, wildcards, and Boolean operators were paired with “NPR1” or “plant defense” as needed to research more detailed information related to specific topics covered within this review. We also used Google to search for, “economic impact citrus greening,” “aspirin,” “Irish potato famine,” and “rice blast,” among other terms, to gather background information on the history and impact of plant diseases, and the historical use of aspirin.
Results
Of 148 sources found, 132 were directly related to plant defense. The remaining sources are related to the historical and economic impact of plant diseases and the historical use and mechanism of action of aspirin or salicylate. All reviewed sources have been documented in the references section.
Conclusion
The topic of salicylic acid-mediated plant defense is broad, and new research is expanding our understanding of this topic quickly. In this review, we give a basic overview of the historical economic impact of plant diseases, and how an understanding of SA-mediated plant defense can prevent future famines. We provide a basic overview of plant defense, then discuss how SA acts as a defense signaling molecule.We discuss how SA regulates NPR1, which goes on to activate expression of SA-related genes including PR genes. Later, we discuss current research topics, including the role of NPR1 and SA in autophagy, circadian rhythmicity, viral gene silencing, SA biosynthesis, and SAR. We also discuss the potential roles of PR proteins, other SA binding proteins, WRKYand TGA family transcription factors, Elongator, and ER transport proteins in plant defense. Finally, we discuss the potential future routes that research into this topic could take, in order to further our understanding of role SA plays in plant defense.
Similar content being viewed by others
References
Agriculture, U.S.D.o. and N.A.S. Service (2015). Citrus Fruits 2015 Summary (September 2015)
Alabadí D, Yanovsky M J, Más P, Harmer S L, Kay S A (2002). Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr Biol, 12(9): 757–761
Alamillo J M, Saénz P, García J A (2006). Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. Plant J, 48(2): 217–227
An C, Ding Y, Zhang X, Wang C, Mou Z (2016). Elongator plays a positive role in exogenous NAD-induced defense responses in Arabidopsis. Mol Plant Microbe Interact, 29(5): 396–404
An C, Mou Z (2011). Salicylic acid and its function in plant immunity. J Integr Plant Biol, 53(6): 412–428
Anand A, Uppalapati S R, Ryu C M, Allen S N, Kang L, Tang Y, Mysore K S (2008). Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by Agrobacterium tumefaciens. Plant Physiol, 146(2): 703–715
Attaran E, Zeier T E, Griebel T, Zeier J (2009). Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell, 21(3): 954–971
Axtell M J, McNellis T W, Mudgett M B, Hsu C S, Staskawicz B J (2001). Mutational analysis of the Arabidopsis RPS2 disease resistance gene and the corresponding pseudomonas syringae avrRpt2 avirulence gene. Mol Plant Microbe Interact, 14(2): 181–188
Bhattacharjee S, Halane M K, Kim S H, Gassmann W (2011). Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science, 334(6061): 1405–1408
Billington R A, Bruzzone S, De Flora A, Genazzani A A, Koch-Nolte F, Ziegler M, Zocchi E (2006). Emerging functions of extracellular pyridine nucleotides. Mol Med, 12(11-12): 324–327
Boller T, Felix G (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu Rev Plant Biol, 60(1): 379–406
Cameron R, Zaton K (2004). Intercellular salicylic acid accumulation is important for age-related resistance in Arabidopsis to Pseudomonas syringae. Physiol Mol Plant Pathol, 65(4): 197–209
Campos L, Granell P, Tárraga S, López-Gresa P, Conejero V, Bellés J M, Rodrigo I, Lisón P (2014). Salicylic acid and gentisic acid induce RNA silencing-related genes and plant resistance to RNA pathogens. Plant Physiol Biochem, 77: 35–43
Carr J P, Beachy R N, Klessig D F (1989). Are the PR1 proteins of tobacco involved in genetically engineered resistance to TMV? Virology, 169(2): 470–473
Carviel J L, Al-Daoud F, Neumann M, Mohammad A, Provart N J, Moeder W, Yoshioka K, Cameron R K (2009). Forward and reverse genetics to identify genes involved in the age-related resistance response in Arabidopsis thaliana. Mol Plant Pathol, 10(5): 621–634
Carviel J L, Wilson D C, Isaacs M, Carella P, Catana V, Golding B, Weretilnyk E A, Cameron R K (2014). Investigation of intercellular salicylic acid accumulation during compatible and incompatible Arabidopsis-Pseudomonas syringae interactions using a fast neutrongenerated mutant allele of EDS5 identified by genetic mapping and whole-genome sequencing. PLoS One, 9(3): e88608
Chai J, Liu J, Zhou J, Xing D (2014). Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J Exp Bot, 65(22): 6513–6528
Chen C, Chen Z (2002). Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol, 129(2): 706–716
Chen F, D’Auria J C, Tholl D, Ross J R, Gershenzon J, Noel J P, Pichersky E (2003). An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J, 36(5): 577–588
Cheng W, Munkvold K R, Gao H, Mathieu J, Schwizer S, Wang S, Yan Y B, Wang J, Martin G B, Chai J (2011). Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III Effector. Cell Host Microbe, 10(6): 616–626
Choi H W, Manohar M, Manosalva P, Tian M, Moreau M, Klessig D F (2016). Activation of plant innate immunity by extracellular high mobility group Box 3 and its inhibition by salicylic acid. PLoS Pathog, 12(3): e1005518
Colaneri A C, Tunc-Ozdemir M, Huang J P, Jones A M (2014). Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex. BMC Plant Biol, 14(1): 129–139
Curto M, Camafeita E, Lopez J A, Maldonado A M, Rubiales D, Jorrín J V (2006). A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics, 6(S1 Suppl 1): S163–S174
De Meyer G HM (1997). Salicylic acid produced by the Rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean., Gent, Belgium: Phytopathology.
Dean J V, Mohammed L A, Fitzpatrick T (2005). The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta, 221(2): 287–296
Dean J V M, Mills J D (2004). Uptake of salicylic acid 2-O-beta-Dglucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol Plant, 120(4): 603–612
Delaney T P (2005). Salicylic Acid. In: Davies P J (Ed.), Plant Hormones: Biosynthesis, Signal Tranduction, Action!, Kluwer Academic Publishers, Dordrecht, The Netherlands. pp. 635–653
Delaney T P, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994). A central role of salicylic acid in plant disease resistance. Science, 266(5188): 1247–1250
Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert P R (2003). The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell, 15(9): 2181–2191
Després C, De Long C, Glaze S, Liu E, Fobert P R (2000). The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell, 12(2): 279–290
De Witt D L, el-Harith E A, Kraemer S A, Andrews M J, Yao E F, Armstrong R L, Smith W L (1990). The aspirin and heme-binding sites of ovine and murine prostaglandin endoperoxide synthases. J Biol Chem, 265(9): 5192–5198
Ding Y, Dommel M, Mou Z (2016). Abscisic acid promotes proteasomemediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J, 86(1): 20–34
Dong J, Chen C, Chen Z (2003). Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol, 51(1): 21–37
Durrant W E, Dong X (2004). Systemic acquired resistance. Annu Rev Phytopathol, 42(1): 185–209
Edgar R S, Green E W, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja U K, Feeney K A, Maywood E S, Hastings M H, Baliga N S, Merrow M, Millar A J, Johnson C H, Kyriacou C P, O’Neill J S, Reddy A B (2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature, 485(7399): 459–464
Eulgem T, Rushton P J, Robatzek S, Somssich I E (2000). The WRKY superfamily of plant transcription factors. Trends Plant Sci, 5(5): 199–206
Eulgem T, Somssich I E (2007). Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol, 10(4): 366–371
Falk A, Feys B J, Frost L N, Jones J D, Daniels M J, Parker J E (1999). EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA, 96(6): 3292–3297
Fan W, Dong X (2002). In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell, 14(6): 1377–1389
Feys B J, Moisan L J, Newman M A, Parker J E (2001). Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J, 20(19): 5400–5411
Feys B J, Wiermer M, Bhat R A, Moisan L J, Medina-Escobar N, Neu C, Cabral A, Parker J E (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell, 17(9): 2601–2613
Fragnière C, Serrano M, Abou-Mansour E, Métraux J P, L’Haridon F (2011). Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett, 585(12): 1847–1852
Fu J, Kreibich G (2000). Retention of subunits of the oligosaccharyltransferase complex in the endoplasmic reticulum. J Biol Chem, 275(6): 3984–3990
Fu Z Q, Dong X (2013). Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol, 64(1): 839–863
Gamir J, Darwiche R, Van't Hof P, Choudhary V, Stumpe M, Schneiter R, Mauch F (2017). The sterol-binding activity of PATHOGENESISRELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein. The Plant Journal, 89(3):502–509
Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43(1): 205–227
Goldfine A B, Fonseca V, Jablonski K A, Chen Y D, Tipton L, Staten M A, Shoelson S E, and the Targeting Inflammation Using Salsalate in Type 2 Diabetes Study Team (2013). Salicylate (salsalate) in patients with type 2 diabetes: a randomized trial. Ann Intern Med, 159(1): 1–12
Govrin E M L, Levine A (2002). Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol, 48(3): 267–276
Gráda Ó C (2007). Ireland's Great Famine. Dublin: University College Dublin Press
Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol, 129(3): 1181–1193
Harmer S L (2009). The circadian system in higher plants. Annu Rev Plant Biol, 60(1): 357–377
Hawley S A, Fullerton M D, Ross F A, Schertzer J D, Chevtzoff C, Walker K J, Peggie MW, Zibrova D, Green K A, Mustard K J, Kemp B E, Sakamoto K, Steinberg G R, Hardie D G (2012). The ancient drug salicylate directly activates AMP-activated protein kinase. Science, 336(6083): 918–922
Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker J E (2011). Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science, 334(6061): 1401–1404
Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou Y H, Yu J Q, Chen Z (2010). Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol, 153(4): 1526–1538
Ishikawa A (2009). The Arabidopsis G-protein-subunit is required for defense response against Agrobacterium tumefaciens. Biosci Biotechnol Biochem, 73(1): 47–52
Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F, and the bZIP Research Group (2002). bZIP transcription factors in Arabidopsis. Trends Plant Sci, 7(3): 106–111
Jelenska J, Yao N, Vinatzer B A, Wright C M, Brodsky J L, Greenberg J T (2007). A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol, 17(6): 499–508
Ji L H, Ding S W (2001). The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acidmediated virus resistance. Mol Plant Microbe Interact, 14(6): 715–724
Jirage D, Tootle T L, Reuber T L, Frost L N, Feys B J, Parker J E, Ausubel F M, Glazebrook J (1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA, 96(23): 13583–13588
Jovel J, Walker M, Sanfaçon H (2011). Salicylic acid-dependent restriction of Tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance. Mol Plant Microbe Interact, 24(6): 706–718
Kasprzewska A (2003). Plant chitinases–regulation and function. Cell Mol Biol Lett, 8(3): 809–824
Kauffmann S, Legrand M, Geoffroy P, Fritig B (1987). Biological function of; pathogenesis-related’ proteins: four PR proteins of tobacco have 1, 3-β-glucanase activity. EMBO J, 6(11): 3209–3212
Kim H S, Delaney T P (2002). Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J, 32(2): 151–163
Kim S H, Kwon S I, Bhattacharjee S, Gassmann W (2009). Regulation of defense gene expression by Arabidopsis SRFR1. Plant Signal Behav, 4(2): 149–150
Klopffleisch K, Phan N, Augustin K, Bayne R S, Booker K S, Botella J R, Carpita N C, Carr T, Chen J G, Cooke T R, Frick-Cheng A, Friedman E J, Fulk B, Hahn MG, Jiang K, Jorda L, Kruppe L, Liu C, Lorek J, McCann M C, Molina A, Moriyama E N, Mukhtar M S, Mudgil Y, Pattathil S, Schwarz J, Seta S, Tan M, Temp U, Trusov Y, Urano D, Welter B, Yang J, Panstruga R, Uhrig J F, Jones A M (2011). Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis. Mol Syst Biol, 7(1): 532
Kong Q, Sun T, Qu N, Ma J, Li M, Cheng Y T, Zhang Q, Wu D, Zhang Z, Zhang Y (2016). Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis. Plant Physiol, 171(2): 1344–1354
Kopp E, Ghosh S (1994). Inhibition of NF-kappa B by sodium salicylate and aspirin. Science, 265(5174): 956–959
Kunta M, Sétamou M, Skaria M, Rascoe J E, Li W, Nakhla M K, da Graça J V (2012). First report of citrus huanglongbing in Texas. Phytopathology, 102: S4
Kwon S I, Kim S H, Bhattacharjee S, Noh J J, Gassmann W (2009). SRFR1, a suppressor of effector-triggered immunity, encodes a conserved tetratricopeptide repeat protein with similarity to transcriptional repressors. Plant J, 57(1): 109–119
Lee S, Rojas C M, Ishiga Y, Pandey S, Mysore K S (2013). Arabidopsis heterotrimeric G-proteins play a critical role in host and nonhost resistance against Pseudomonas syringae pathogens. PLoS One, 8(12): e82445
Legrand M, Kauffmann S, Geoffroy P, Fritig B (1987). Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci USA, 84(19): 6750–6754
Li J, Brader G, Palva E T (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell, 16(2): 319–331
Lin K H, Lin K H (1956) THE CITRUS HUANG LUNG BIN (GREENING) DISEASE IN CHINA. Acta Phytopathologica Sinica, Vol. II, Part 1, No. I, and Part 2, p. 1–11 and 14–38
Liu J, Ding P, Sun T, Nitta Y, Dong O, Huang X, Yang W, Li X, Botella J R, Zhang Y (2013). Heterotrimeric G proteins serve as a converging point in multiple receptor-like kinases. Plant Physiol, 161(4):: 2146–2158
Liu L, Sonbol F M, Huot B, Gu Y, Withers J, Mwimba M, Yao J, He S Y, Dong X (2016). Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effectortriggered immunity. Nat Commun, 7:13099
Lorek J, Griebel T, Jones A M, Kuhn H, Panstruga R (2013). The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity. Mol Plant Microbe Interact, 26(9): 991–1003
Lu H, Greenberg J T, Holuigue L (2016). Editorial: Salicylic acid signaling networks. Front Plant Sci, 7: 238
Lu S X, Knowles S M, Andronis C, Ong M S, Tobin E M (2009). CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL function synergistically in the circadian clock of Arabidopsis. Plant Physiol, 150(2): 834–843
Mackey D, Belkhadir Y, Alonso J M, Ecker J R, Dangl J L (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112(3): 379–389
Maeda K, Houjyou Y, Komatsu T, Hori H, Kodaira T, Ishikawa A (2009). AGB1 and PMR5 contribute to PEN2-mediated preinvasion resistance to Magnaporthe oryzae in Arabidopsis thaliana. Mol Plant Microbe Interact, 22(11): 1331–1340
Mangelsen E, Kilian J, Berendzen K W, Kolukisaoglu U H, Harter K, Jansson C, Wanke D (2008). Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics, 28(9):194
Mauch-Mani B, Slusarenko A J (1996). Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell, 8(2): 203–212
McClung C R (2008). Comes a time. Curr Opin Plant Biol, 11(5): 514–520
Miao Y, Laun T, Zimmermann P, Zentgraf U (2004). Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol, 55(6): 853–867
Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008). Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics, 279(4): 415–427
Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H R, Carré I A, Coupland G (2002). LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell, 2(5): 629–641
Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo S H, Urquhart W, Klessig D F, Kim S K, Nambara E, Yoshioka K (2010). The lesionmimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol, 152(4): 1901–1913
Mou Z, Fan W, Dong X (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113(7): 935–944
Munch D, Rodriguez E, Bressendorff S, Park O K, Hofius D, Petersen M (2014). Autophagy deficiency leads to accumulation of ubiquitinated proteins, ER stress, and cell death in Arabidopsis. Autophagy, 10(9): 1579–1587
Myers R L (2007). The 100 most important chemical compounds: a reference guide. p. 10–12.
Nawrath C, Heck S, Parinthawong N, Métraux J P (2002). EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14(1): 275–286
Ndamukong I, Abdallat A A, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007). SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J, 50(1): 128–139
Nobuta K, Okrent R A, Stoutemyer M, Rodibaugh N, Kempema L, Wildermuth M C, Innes RW (2007). The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol, 144(2): 1144–1156
Pajerowska-Mukhtar K M, Emerine D K, Mukhtar M S (2013). Tell me more: roles of NPRs in plant immunity. Trends Plant Sci, 18(7): 402–411
Parker J E, Holub E B, Frost L N, Falk A, Gunn N D, Daniels M J (1996). Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell, 8(11): 2033–2046
Pieterse CM J, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees S C (2012). Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol, 28(1): 489–521
Pontier D, Miao Z H, Lam E (2001). Trans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses. Plant J, 27(6): 529–538
Preston F E, Whipps S, Jackson C A, French A J, Wyld P J, Stoddard C J (1981). Inhibition of prostacyclin and platelet thromboxane A2 after low-dose aspirin. N Engl J Med, 304(2): 76–79
Prins T W, Tudzynski P, von Tiedemann A, Tudzynski B, Have A T, Hansen M E, Tenberge K, van Kan J A L (2000). Infection Strategies of Botrytis cinerea and related necrotrophic pathogens. Fungal Pathology: p. 33–64
Raskin I (1992). Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol, 43(1): 439–462
Raskin I, Skubatz H, Tang W, Meeuse B J D (1990). Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot (Lond), 66(4): 369–373
Ross D (2002). Ireland: History of a Nation. Glasgow: Geddes& Grosset.
Saleh A, Withers J, Mohan R, Marqués J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X (2015). Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe, 18(2): 169–182
Scardaci S C (2016). Rice Blast: A New Disease in California. (Web Document)April 5.
Shine MB, Yang J W, El-Habbak M, Nagyabhyru P, Fu D Q, Navarre D, Ghabrial S, Kachroo P, Kachroo A (2016). Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytologist, 212(3):627–636
Shulaev V, Silverman P, Raskin I (1997). Methyl salicylate–an airborn signal in pathogen resistance. Nature, 6618: 718–721
Slaymaker D H, Navarre D A, Clark D, del Pozo O, Martin G B, Klessig D F (2002). The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci USA, 99(18): 11640–11645
Smith W L, Garavito R M, DeWitt D L (1996). Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and-2. J Biol Chem, 271(52): 33157–33160
Spoel S H, Johnson J S, Dong X (2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA, 104(47): 18842–18847
Spoel S H, Mou Z, Tada Y, Spivey N W, Genschik P, Dong X (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell, 137(5): 860–872
Spoel S H, Mou Z, Zhang X, Pieterse CMJ, Dong X (2006). Regulatory Roles of NPR1 in Plant Defense: Regulation and Function. Utrecht University Repository
Strawn M A, Marr S K, Inoue K, Inada N, Zubieta C, Wildermuth M C (2007). Arabidopsis isochorismate synthase functional in pathogeninduced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J Biol Chem, 282(8): 5919–5933
Tada Y, Spoel S H, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008). Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science, 321(5891): 952–956
Talbot N J (2003). On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu Rev Microbiol, 57(1): 177–202
Spreen T H (2012). The Economic Impact of HLB on the Florida Citrus Industry, in Food and Resource Economics. University of Florida
Tian M, von Dahl C C, Liu P P, Friso G, van Wijk K J, Klessig D F (2012). The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins. Plant J, 72(6): 1027–1038
Torres M A, Morales J, Sánchez-Rodríguez C, Molina A, Dangl J L (2013). Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Mol Plant Microbe Interact, 26(6): 686–694
Trombetta E S, Parodi A J (2003). Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol, 19(1): 649–676
Tsuda K, Katagiri F (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol, 13(4): 459–465
Tully J P, Hill A E, Ahmed H M, Whitley R, Skjellum A, Mukhtar M S (2014). Expression-based network biology identifies immune-related functional modules involved in plant defense. BMC Genomics, 15 (1): 421
Van der Does D, Leon-Reyes A, Koornneef A, Van Verk M C, Rodenburg N, Pauwels L, Goossens A, Körbes A P, Memelink J, Ritsema T, Van Wees S C, Pieterse C M (2013). Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell, 25(2): 744–761
van Loon L C, Rep M, Pieterse C M (2006). Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol, 44(1): 135–162
van Verk M C, Neeleman L, Bol J F, Linthorst H J (2011). Tobacco transcription factor NtWRKY12 interacts with TGA2.2 in vitro and in vivo. Front Plant Sci, 2(32): 32
Vitale A, Denecke J (1999). The endoplasmic reticulum-gateway of the secretory pathway. Plant Cell, 11(4): 615–628
Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E, Bautor J, Niefind K, Parker J E (2013). Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe, 14(6): 619–630
Wang D, Amornsiripanitch N, Dong X (2006). A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog, 2(11): e123
Wang D, Weaver N D, Kesarwani M, Dong X (2005). Induction of protein secretory pathway is required for systemic acquired resistance. Science, 308(5724): 1036–1040
Wang G Y, Shi J L, Ng G, Battle S L, Zhang C, Lu H (2011). Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Mol Plant, 4(3): 516–526
Wang W, Barnaby J Y, Tada Y, Li H, Tör M, Caldelari D, Lee D U, Fu X D, Dong X (2011b). Timing of plant immune responses by a central circadian regulator. Nature, 470(7332): 110–114
Wiermer M, Feys B J, Parker J E (2005). Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol, 8(4): 383–389
Wu C T, Leubner-Metzger G, Meins F Jr, Bradford K J (2001). Class I- 1, 3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiol, 126(3): 1299–1313
Wu L, Chen H, Curtis C, Fu Z Q (2014). Go in for the kill: How plants deploy effector-triggered immunity to combat pathogens. Virulence, 5(7): 710–721
Xiang C, Miao Z, Lam E (1997). DNA-binding properties, genomic organization and expression pattern of TGA6, a new member of the TGA family of bZIP transcription factors in Arabidopsis thaliana. Plant Mol Biol, 34(3): 403–415
Yi S Y, Kwon S Y (2014). How does SA signaling link the Flg22 responses? Plant Signal Behav, 9(11): e972806
Yi S Y, Min S R, Kwon S Y (2015). NPR1 is instrumental in priming for the Enhanced flg22-induced MPK3 and MPK6 activation. Plant Pathol J, 31(2): 192–194
Yin M J, Yamamoto Y, Gaynor R B (1998). The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinasebeta. Nature, 396(6706): 77–80
Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009). Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell, 21(9): 2914–2927
Yu D, Chen C, Chen Z (2001). Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell, 13(7): 1527–1540
Zeng W, He S Y (2010). A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol, 153(3): 1188–1198
Zhang C, Xie Q, Anderson R G, Ng G, Seitz N C, Peterson T, McClung C R, McDowell J M, Kong D, Kwak J M, Lu H (2013). Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog, 9(6): e1003370
Zhang X, Mou Z (2009). Extracellular pyridine nucleotides induce PR gene expression and disease resistance in Arabidopsis. Plant J, 57(2): 302–312
Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999). Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA, 96(11): 6523–6528
Zheng Z, Qamar S A, Chen Z, Mengiste T (2006). Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J, 48(4): 592–605
Zhou J M, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig D F (2000). NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant Microbe Interact, 13(2): 191–202
Zhou M, Wang W, Karapetyan S, Mwimba M, Marqués J, Buchler N E, Dong X (2015). Redox rhythm reinforces the circadian clock to gate immune response. Nature, 523(7561): 472–476
Zhu S, Jeong R D, Venugopal S C, Lapchyk L, Navarre D, Kachroo A, Kachroo P (2011). SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLoS Pathog, 7(11): e1002318
Acknowledgments
This work is financially supported by NSF EAGER grant 1464527 (Z.F.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Palmer, I.A., Shang, Z. & Fu, Z.Q. Salicylic acid-mediated plant defense: Recent developments, missing links, and future outlook. Front. Biol. 12, 258–270 (2017). https://doi.org/10.1007/s11515-017-1460-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-017-1460-4