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• W2005906963 abstract "The evolution of land plants approximately 470 million years ago created a new adaptive zone for natural enemies (attackers) of plants. In response to attack, plants evolved highly effective, inducible defense systems. Two plant hormones modulating inducible defenses are salicylic acid (SA) and jasmonic acid (JA). Current thinking is that SA induces resistance against biotrophic pathogens and some phloem feeding insects and JA induces resistance against necrotrophic pathogens, some phloem feeding insects and chewing herbivores. Signaling crosstalk between SA and JA commonly manifests as a reciprocal antagonism and may be adaptive, but this remains speculative. We examine evidence for and against adaptive explanations for antagonistic crosstalk, trace its phylogenetic origins and provide a hypothesis-testing framework for future research on the adaptive significance of SA–JA crosstalk. The evolution of land plants approximately 470 million years ago created a new adaptive zone for natural enemies (attackers) of plants. In response to attack, plants evolved highly effective, inducible defense systems. Two plant hormones modulating inducible defenses are salicylic acid (SA) and jasmonic acid (JA). Current thinking is that SA induces resistance against biotrophic pathogens and some phloem feeding insects and JA induces resistance against necrotrophic pathogens, some phloem feeding insects and chewing herbivores. Signaling crosstalk between SA and JA commonly manifests as a reciprocal antagonism and may be adaptive, but this remains speculative. We examine evidence for and against adaptive explanations for antagonistic crosstalk, trace its phylogenetic origins and provide a hypothesis-testing framework for future research on the adaptive significance of SA–JA crosstalk. Sessile organisms, such as terrestrial green plants, are subject to pervasive attack by diverse attackers. These attackers include microbial pathogens (e.g. viruses, bacteria and fungi), macroscopic herbivores and parasites (e.g. parasitic plants and arthropods) and browsing herbivores (e.g. ungulates). The vast majority of attackers are relatively specialized in terms of the number of host species that they utilize (specialists), and a minority are less restricted in host range (generalists) [1Frankel G. The raison d’etre of secondary plant substances.Science. 1959; 129: 1466-1470Crossref PubMed Scopus (801) Google Scholar, 2Jaenike J. Host specialization in phytophagous insects.Annu. Rev. Ecol. Syst. 1990; 21: 243-273Crossref Scopus (956) Google Scholar]. Over the past 470 million years [3Rubinstein C.V. et al.Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana).New Phytol. 2010; 188: 365-369Crossref PubMed Scopus (239) Google Scholar], plants have evolved effective inducible defense systems [4Ausubel F.M. Are innate immune signaling pathways in plants and animals conserved?.Nat. Immunol. 2005; 6: 973-979Crossref PubMed Scopus (742) Google Scholar] to cope with attack by these diverse and abundant enemies. Yet, the specific match between particular attackers and plant defense traits, and whether attackers have the upper hand in these interactions, is poorly understood [5Erb, M. et al. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 5, doi: 10.1016/j.tplants.2012.01.003.Google Scholar]. The specificity of plant–attacker interactions, from both sides of the equation, has important implications for understanding the evolution of resistance in plants and the evolution of virulence in the enemies [6Lambrechts L. Dissecting the genetic architecture of host–pathogen specificity.PLoS Pathog. 2010; 6: e1001019Crossref PubMed Scopus (57) Google Scholar]. Plants have to balance the costs and potential benefits of investing in defense in an environment where enemy attack is variable. On the one hand, defenses are costly to produce; in the absence of enemies, deploying defenses reduces plant fitness [7Heil M. Baldwin I.T. Fitness costs of induced resistance: emerging experimental support for a slippery concept.Trends Plant Sci. 2002; 7: 61-67Abstract Full Text Full Text PDF PubMed Scopus (458) Google Scholar]. Because they are costly to produce, natural selection is presumed to favor the evolution of inducibility, meaning that these defenses are only produced in the presence of attack. On the other hand, having an immediate impact on an attacker could be paramount to deterring further attacks. Plants generally strike a balance and maintain constitutive and inducible defenses. However, individual plants are likely to be attacked by more than one organism. Microbial pathogens, which are typically endophagous and single-celled, require vastly different defenses than macroscopic herbivores, which may even move among plant individuals while feeding. Among herbivores, different defenses are required for different guilds. For example, defense traits that are effective against aphids, which feed on plant phloem, are distinct from those that are effective against caterpillars, which typically defoliate plants [8De Vos M. et al.Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack.Mol. Plant Microbe Interact. 2005; 18: 923-937Crossref PubMed Scopus (776) Google Scholar]. Characterization of the specificity of the plant response is a focus of intense research among ecologists and plant scientists [5Erb, M. et al. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 5, doi: 10.1016/j.tplants.2012.01.003.Google Scholar, 9Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotphic pathogens.Ann. Rev. Phytopathol. 2005; 43: 205-227Crossref PubMed Scopus (3085) Google Scholar, 10Cui J. et al.Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores.Proc. Natl. Acad. Sci. U.S.A. 2005; 102: 1791-1796Crossref PubMed Scopus (223) Google Scholar]. Of particular interest in this review is whether adaptive tailoring of the response occurs, or if tailoring is a byproduct of manipulation by enemies. Despite the caveats discussed above, the inducible plant defense system can be generally divided into two branches – one effective primarily against biotrophic (feeding on living tissue) pathogens and one against herbivores and necrotrophic (feeding on dead tissue) pathogens [11Stout M.J. et al.Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods.Annu. Rev. Entomol. 2006; 51: 663-689Crossref PubMed Scopus (365) Google Scholar]. Inducible defenses are incredibly diverse and include morphological structures such as trichomes, fast-killing toxins such as alkaloids, digestibility reducers such as proteinase inhibitors and indirect defenses such as extrafloral nectaries and plant volatiles that can recruit other insects that deter herbivores [1Frankel G. The raison d’etre of secondary plant substances.Science. 1959; 129: 1466-1470Crossref PubMed Scopus (801) Google Scholar, 12Karban R. Baldwin I.T. Induced Responses to Herbivory. The University of Chicago Press, 1997Crossref Google Scholar, 13Green T.R. Ryan C.A. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects.Science. 1972; 175: 776-777Crossref PubMed Scopus (889) Google Scholar, 14Heil M. et al.Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid.Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 1083-1088Crossref PubMed Scopus (246) Google Scholar]. Several plant hormones regulate the production of downstream resistance molecules in each branch. The SA pathway is primarily induced by and effective in mediating resistance against biotrophic pathogens and the JA pathway is primarily induced by and effective in mediating resistance against herbivores and necrotrophic pathogens [9Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotphic pathogens.Ann. Rev. Phytopathol. 2005; 43: 205-227Crossref PubMed Scopus (3085) Google Scholar]. This is an overly simplistic view of the complex repertoire of plant hormones that probably play a role in mediating inducible defenses, including abscisic acid (ABA), auxin, brassinosteroids, cytokinins, ethylene (ET) and gibberellic acid [15Robert-Seilaniantz A. et al.Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism.Annu. Rev. Phytopathol. 2011; 49: 317-343Crossref PubMed Scopus (1336) Google Scholar]. Interestingly, evidence from several distantly related plant species suggests that there can be evolutionarily conserved SA- and JA-signaling crosstalk resulting in reciprocal antagonism between the SA and JA signaling pathways [9Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotphic pathogens.Ann. Rev. Phytopathol. 2005; 43: 205-227Crossref PubMed Scopus (3085) Google Scholar]. The adaptive significance of this crosstalk, if any, is the focus of this review. The dynamics and genetic bases of SA–JA crosstalk, including the reciprocal antagonism often observed as a result, has mainly been dissected in the model plant Arabidopsis thaliana (Arabidopsis) [16Koornneef A. Pieterse C.M.J. Cross talk in defense signaling.Plant Physiol. 2008; 146: 839-844Crossref PubMed Scopus (763) Google Scholar, 17Verhage A. et al.Plant immunity: it's the hormones talking, but what do they say?.Plant Physiol. 2010; 154: 536-540Crossref PubMed Scopus (233) Google Scholar, 18Pieterse C.M. et al.Networking by small-molecule hormones in plant immunity.Nat. Chem. Biol. 2009; 5: 308-316Crossref PubMed Scopus (1623) Google Scholar]. The genetic basis of the reciprocal antagonism is extremely complex and an overview is presented below, in the context of the evolution of each of the major genetic players. Here we focus on SA and JA; however, ET is a critical third player from the perspective of understanding how plants prioritize and tailor their responses to diverse attackers and a brief focus on its role in mediating crosstalk is warranted. SA is typically prioritized over JA in Arabidopsis [19Leon-Reyes A. et al.Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway.Planta. 2010; 232: 1423-1432Crossref PubMed Scopus (186) Google Scholar]. However, plants use ET to fine tune defenses by prioritizing JA induction over SA in response to multiple attackers [20Leon-Reyes A. et al.Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic Acid.Mol. Plant Microbe Interact. 2010; 23: 187-197Crossref PubMed Scopus (128) Google Scholar]. ET also modifies the effect of a key protein (NPR1; NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1) involved in SA suppression of JA. In Arabidopsis, NPR1 is necessary for expression of SA-responsive genes and for repression of JA by SA. However, when ET is present, NPR1 function is no longer required for SA suppression of JA [20Leon-Reyes A. et al.Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic Acid.Mol. Plant Microbe Interact. 2010; 23: 187-197Crossref PubMed Scopus (128) Google Scholar, 21Leon-Reyes A. et al.Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling.Plant Physiol. 2009; 149: 1797-1809Crossref PubMed Scopus (235) Google Scholar], suggesting that ET signaling acts to suppress JA in the presence of SA by bypassing NPR1. Many other plant hormones are also important in mediating the crosstalk, but the genetic bases of this crosstalk are less well studied. Recent approaches that examine genetic interaction networks in Arabidopsis have been fruitful for identifying candidate loci to be studied in detail for their potential role in defense signaling crosstalk [22Arabidopsis Interactome Mapping Consortium Evidence for network evolution in an Arabidopsis interactome map.Science. 2011; 333: 601-607Crossref PubMed Google Scholar]. The SA–JA crosstalk that often results in reciprocal antagonism between these two pathways has been interpreted as being an adaptive plant strategy, representing a cost-saving measure given that phenotypically different enemies are susceptible to distinct defense strategies. However, specific defenses that induce resistance to one attacker may render the plant more susceptible to another if alternative defenses are repressed by crosstalk [23Beckers G.J.M. Spoel S.H. Fine-tuning plant defence signalling: salicylate versus jasmonate.Plant Biol. 2006; 8: 1-10Crossref PubMed Scopus (344) Google Scholar]. We first focus on the phylogenetic distribution of crosstalk, candidate loci underlying crosstalk and the nature of the evidence used to assay for crosstalk. We then evaluate adaptive and nonadaptive evidence for the SA–JA reciprocal antagonism and illuminate a research path that integrates phylogenetic, genetic and ecological approaches towards testing explicit hypotheses on the origins and adaptive value of signal crosstalk. We end with a discussion of SA–JA signal interactions as a mechanism that generates specificity in plant–attacker interactions. Although the SA–JA antagonism is clearly present in many plant species, an open question is whether there is a common genetic basis to this crosstalk and if so, whether the trait is conserved across all plants. Similarly, although it can be a reciprocal antagonism, the strength of the downregulation from each side of the SA and JA equation is not identical and may not be antagonistic across plants. We searched for all studies that tested for antagonisms in SA–JA signaling (Table 1). A paper was included as presenting evidence for SA–JA antagonism if there was a genetic or biochemical measure widely believed to be regulated by the jasmonate and salicylate pathways, or if one pathway was genetically manipulated and a response was measured in the other. Our survey included papers that measured JA, SA or their derivatives, gene expression or chemical end-products known to be regulated by one of the pathways. In some studies, one pathway was elicited and had direct effects on the other pathway. In other studies, SA–JA antagonism was seen when induction of one pathway reduced the response to elicitation of the other pathway. We did not include studies that only found antagonisms in resistance to bioassay organisms if there was not evidence that the antagonism was due to SA–JA crosstalk. From the well-studied systems including Arabidopsis, tomato (Solanum lycopersicum) and tobacco (Nicotiana spp.), a subset of studies is included to highlight the ecological conditions under which antagonism can occur. There are systems that show conditionality in the antagonism and these were scored as having SA–JA antagonism for the purposes of Table 1 and are discussed in the text. It is important to point out that although there are a growing number of studies using biological inducers, most of the evidence for antagonism is based on treating plants with exogenous SA and JA, either singly or in combination. In most cases, there have not been studies that test whether there is a common genetic basis or a correlated gene expression phenotype that underlies the gross SA–JA antagonism reported across plants. Therefore, the results of this survey and our inferences on trait evolution need to be interpreted with caution because of the inherent limitations of screening for SA–JA antagonism using chemical elicitors and the lack of direct evidence for a common mechanism. The evolutionary interpretations below and our interpretations are hypotheses to be tested.Table 1Evidence for SA–JA antagonism across plant speciesPlant speciesMethod of SA elicitationMethod of JA elicitationSA pathway inducibility measurementJA pathway inducibility measurementBioassay resultRefsArabidopsis thalianaPieris brassicae eggs/egg extracts–SA inducedTen insect-induced JA regulated transcripts decreaseDecreased resistance to Spodoptera littoralis44Bruessow F. et al.Insect eggs suppress plant defence against chewing herbivores.Plant J. 2010; 62: 876-885Crossref PubMed Scopus (163) Google ScholarArabidopsis thalianaSA––Peroxidase, polyphenol oxidase, chitinase, glucosinolates decreaseDecreased resistance to Spodoptera exigua84Cipollini D. et al.Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua.Mol. Ecol. 2004; 13: 1643-1653Crossref PubMed Scopus (172) Google ScholarArabidopsis thalianaSAPathogens: Alternaria brassicola, Botrytis cinerea, insects: Frankliniella occidentalis, Pieris rapae–PDF 1.2 (PLANT DEFENSIN 1.2) decreases–59Koornneef A. et al.Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation.Plant Physiol. 2008; 147: 1358-1368Crossref PubMed Scopus (269) Google ScholarArabidopsis thalianaHyaloperonos-pora parasiticaMeJA–PDF1.2 expression decreases–59Koornneef A. et al.Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation.Plant Physiol. 2008; 147: 1358-1368Crossref PubMed Scopus (269) Google ScholarArabidopsis thalianaPseudomonas syringaeMeJA––Decreased resistance to Trichoplusia ni10Cui J. et al.Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores.Proc. Natl. Acad. Sci. U.S.A. 2005; 102: 1791-1796Crossref PubMed Scopus (223) Google ScholarArabidopsis thalianaMutant plants with elevated or suppressed SA–––Trichoplusia ni resistance decreased as SA expression increased65Cui J. et al.Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae.Plant Physiol. 2002; 129: 551-564Crossref PubMed Scopus (87) Google ScholarArabidopsis thalianaSAMeJA–Genome wide effects–85Schenk P.M. et al.Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.Proc. Natl. Acad. Sci. U.S.A. 2000; 97: 11655-11660Crossref PubMed Scopus (1133) Google ScholarArabidopsis thalianaCucumber mosaic virus–JA inducible transcripts decrease–45Lewsey M.G. et al.Disruption of two defensive signaling pathways by a viral RNA silencing suppressor.Mol. Plant Microbe Interact. 2010; 23: 835-845Crossref PubMed Scopus (149) Google ScholarSolanum lycopersicum (tomato)SAJA and systemin–Proteinase inhibitors decrease–86Doares S.H. et al.Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and sasmonic acid.Plant Physiol. 1995; 108: 1741-1746Crossref PubMed Scopus (430) Google ScholarSolanum lycopersicumBTHJAPR4 (PATHOGENESIS RELATED 4) transcripts downregulatedOxidative enzymes decreaseDecreased resistance to Spodoptera exigua and Trichoplusia ni53Thaler J.S. et al.Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance.J. Chem. Ecol. 1999; 25: 1597-1609Crossref Scopus (243) Google Scholar, 55Thaler J.S. et al.Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato.J. Chem. Ecol. 2002; 28: 1131-1159Crossref PubMed Scopus (147) Google ScholarSolanum lycopersicumBotrytis cinerea–SA inducedProteinase inhibitor transcripts decreaseB. cinerea disease increased47El Oirdi M. et al.Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato.Plant Cell. 2011; 23: 2405-2421Crossref PubMed Scopus (268) Google ScholarSolanum lycopersicumParasitic plant Cuscuta pentagona and SA deficient plants–SA inducedJA and herbivore induced plant volatiles decreaseSpodoptera exigua performance not affected48Runyon J.B. et al.Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores.Plant Physiol. 2008; 146: 987-995Crossref PubMed Scopus (49) Google ScholarSolanum lycopersicum cv. cerasiforme (wild tomato)BTHJA–Polyphenol oxidase activity decreaseSpodoptera exigua performance not affected52Thaler J. et al.Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites.Oecologia. 2002; 131: 227-235Crossref Scopus (171) Google ScholarOryza sativa (rice)Mechanical damage––Increased JA correlates with decreased SA70Lee A. et al.Inverse correlation between jasmonic acid and salicylic acid during early wound response in rice.Biochem. Biophys. Res. Commun. 2004; 318: 734-738Crossref PubMed Scopus (82) Google ScholarNicotiana tabacum (tobacco)Tobacco mosaic virus inoculation––JA and nicotine decreaseDecreased resistance to Manduca sexta46Preston C.A. et al.Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants.Planta. 1999; 209: 87-95Crossref PubMed Scopus (126) Google ScholarNicotiana tabacumGenetically reduced SA production––JA, nicotine, polyphenol oxidase increaseIncreased resistance to Heliothis virescens87Felton G.W. et al.Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory.Curr. Biol. 1999; 9: 317-320Abstract Full Text Full Text PDF PubMed Scopus (227) Google ScholarNicotiana attenuata–Fatty acid–amino acid conjugates from Spodoptera exigua oral secretionSA decreases––80Diezel C. et al.Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling.Plant Physiol. 2009; 150: 1576-1586Crossref PubMed Scopus (253) Google ScholarHordeum vulgare (barley)SA––13-Hydroxyoctadecatri(di)enoic (JA suppressor) increase–88Weichert H. et al.Metabolic profiling of oxylipins upon salicylate treatment in barley leaves – preferential induction of the reductase pathway by salicylate.FEBS Lett. 1999; 464: 133-137Abstract Full Text Full Text PDF PubMed Scopus (82) Google ScholarCucumis sativus (cucumber)BTHJAReduced chitinase levels on dual-elicited plants–Colletotrichum orbiculare disease severity lower on dual elicited plants58Liu C. et al.Antagonism between acibenzolar-S-methyl-induced systemic acquired resistance and jasmonic acid-induced systemic acquired susceptibility to Colletotrichum orbiculare infection in cucumber.Physiol. Mol. Plant Pathol. 2008; 72: 141-145Crossref Scopus (20) Google ScholarPisum sativum (pea)SAWounding, JA–JA, polyphenol oxidase downregulated–51Yang H.R. et al.Effect of salicylic acid on jasmonic acid-related defense response of pea seedlings to wounding.Sci. Horticult. 2011; 128: 166-173Crossref Scopus (17) Google ScholarPhaseolus lunatus (lima bean)Whitefly, SAJA–JA, volatilesPredatory mite attraction reduced49Zhang P.-J. et al.Whiteflies interfere with indirect plant defense against spider mites in Lima bean.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 21202-21207Crossref PubMed Scopus (222) Google ScholarGossypium hirsutum (cotton)Phenacoccus solenopsis (mealy bugs)–SA-induced volatiles and upregulation of SA-dependent transcriptsGossypol and other transcripts downregulated–50Zhang P. et al.Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis.PLoS ONE. 2011; 6: e22378Crossref PubMed Scopus (46) Google ScholarSorghum bicolor (sorghum)SAMeJASome SA transcripts downregulatedsome JA transcripts downregulated–56Salzman R.A. et al.Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses.Plant Physiol. 2005; 138: 352-368Crossref PubMed Scopus (181) Google ScholarGinkgo bilobaTransgenic suppression of SA–JA, OPDA levels decrease–72Xu M. et al.Complementary action of jasmonic acid on salicylic acid in mediating fungal elicitor-induced flavonol glycoside accumulation of Ginkgo biloba cells.Plant Cell Environ. 2009; 32: 960-967Crossref PubMed Scopus (64) Google ScholarBrassica carinata (Ethiopian mustard)Sclerotinia sclerotiorum (white mold)Sclerotinia sclerotiorumJA transcripts upregulated after SA transcripts downregulatedSA transcripts upregulated only after JA transcripts are downregulated–89Yang B. et al.Characterization of defense signaling pathways of Brassica napus and Brassica carinata in response to Sclerotinia sclerotiorum challenge.Plant Mol. Biol. Rep. 2010; 28: 253-263Crossref Scopus (23) Google ScholarBrassica nigra (black mustard)SA applied to roots––JA downregulated in roots–66van Dam N.M. et al.Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species.New Phytol. 2004; 161: 801-810Crossref Scopus (177) Google ScholarBrassica oleracea (cabbage)SA applied to roots––JA downregulated in roots–66van Dam N.M. et al.Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species.New Phytol. 2004; 161: 801-810Crossref Scopus (177) Google ScholarBrassica napus (oilseed rape)SAMechanical wounding, Methyl jasmonate–Myrosinase-associated protein downregulated in dual-elicited plants–90Taipalensuu J. et al.Regulation of the wound-induced myrosinase-associated protein transcript in Brassica napus plants.Eur. J. Biochem. 1997; 247: 963-971Crossref PubMed Scopus (49) Google ScholarAsclepias tuberosa (butterfly milkweed)–Danaus plexippus (monarch) herbivorySA decreasesJA upregulated–A.A. Agrawal, unpublishedAbbreviations: BTH, benzothiadiazole; JA, jasmonic acid; SA, salicylic acid. Open table in a new tab Abbreviations: BTH, benzothiadiazole; JA, jasmonic acid; SA, salicylic acid. The pathways that produce both hormones at the center of this story have ancient origins. SA is produced downstream of isochorismate synthase (ICS), which occurs in many green and red algae as well as in bacteria, and may have a plastid origin in plants [24Wildermuth M.C. et al.Isochorismate synthase is required to synthesize salicylic acid for plant defence.Nature. 2001; 414: 562-565Crossref PubMed Scopus (1658) Google Scholar]. By contrast, jasmonates are end-products of the ancient octadecanoid (C18) oxylipin pathway. Oxylipins are bioactive lipid derivatives that are used as signaling molecules in plants, animals, fungi [25Brodhun F. Feussner I. Oxylipins in fungi.FEBS J. 2011; 278: 1047-1063Crossref PubMed Scopus (145) Google Scholar], as well as in several marine algae species [26Gerwick W.H. Structure and biosynthesis of marine algal oxylipins.Biochim. Biophys. Acta. 1994; 1211: 243-255Crossref PubMed Scopus (92) Google Scholar]. An allene oxide synthase (AOS) homolog (the second enzyme in the octadecanoid biosynthetic pathway) has been discovered in the moss Physcomitrella patens [27Bandara P.K.G.S.S. et al.Cloning and functional analysis of an allene oxide synthase in Physcomitrella patens.Biosci. Biotechnol. Biochem. 2009; 73: 2356-2359Crossref PubMed Scopus (23) Google Scholar, 28Oliver J. et al.Pythium infection activates conserved plant defense responses in mosses.Planta. 2009; 230: 569-579Crossref PubMed Scopus (78) Google Scholar], and distant structural homologs to AOS have been putatively identified in three metazoan lineages [29Lee D.S. et al.Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes.Nature. 2008; 455: 363-368Crossref PubMed Scopus (230) Google Scholar]. The specific compounds JA and methyl JA also have been detected in P. patens [27Bandara P.K.G.S.S. et al.Cloning and functional analysis of an allene oxide synthase in Physcomitrella patens.Biosci. Biotechnol. Biochem. 2009; 73: 2356-2359Crossref PubMed Scopus (23) Google Scholar, 30Anterola A. et al.Physcomitrella patens has lipoxygenases for both eicosanoid and octadecanoid pathways.Phytochemistry. 2009; 70: 40-52Crossref PubMed Scopus (38) Google Scholar, 31Hashimoto T. et al.Cloning and characterization of an allene oxide cyclase, PpAOC3, in Physcomitrella patens.Plant Growth Regul. 2011; 65: 239-245Crossref Scopus (18) Google Scholar, 32Stumpe M. et al.The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology.New Phytol. 2010; 188: 740-749Crossref PubMed Scopus (108) Google Scholar], as well as in ferns [33Dathe W. et al.Occurrence of jasmonic acid, related compounds and abscisic acid in fertile and sterile fronds of three Equisetum species.Biochem. Physiol. Pflanzen. 1989; 185: 83-92Crossref Google Scholar], suggesting that JA production arose at least in the common ancestor of mosses, ferns and seed plants (Figure 1). Despite the ancient origins of each hormone, the antagonism between SA and JA may have more recent origins. SA–JA antagonism has been reported in a total of 17 plant species, including 11 crop plants and six wild species (Table 1). Ancestral state reconstruction [34Paradis E. et al.APE: analyses of phylogenetics and evolution in R language.Bioinformatics. 2004; 20: 289-290Crossref PubMed Scopus (8579) Google Scholar] indicates that SA–JA antagonism evolved at least at the base of angiosperms, but possibly before the split of gymnosperms and angiosperms (Figure 1; using data from Table 1). The presence of orthologs of genes known to be involved in the SA–JA antagonism including NPR1, WRKY70 (WRKY DNA-binding protein 70), GRX480 (Glutaredoxin 480), ERF1 (ETHYLENE RESPONSE FACTOR 1), MYC2 (JASMONATE INSENSITIVE 1, JIN1), ORA59 (OCTADECANOID-RESPONSIVE ARABIDOPSIS AP2/ERF 59), JAZ1-JAZ3 (JASMONATE ZIM-DOMAIN) are predicted, based on reciprocal best blastp searches using Arabidopsis proteins as subjects (Table 2), to have been present in the first land plants, after this lineage split with green algae. This suggests that many regulatory features of SA–JA crosstalk have diverse and potentially ancient roles in the" @default.
• W2005906963 created "2016-06-24" @default.
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• W2005906963 date "2012-05-01" @default.
• W2005906963 modified "2023-10-14" @default.
• W2005906963 title "Evolution of jasmonate and salicylate signal crosstalk" @default.
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