Skip to main content
SpringerLink
Log in

Molecular and physiological stages of priming: how plants prepare for environmental challenges

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Being sessile organisms, plants must respond to various challenges in the environment. The priming process consists of three clear stages. The first stage includes all the cellular changes in the absence of the challenge so-called pre-challenge priming stage. These changes are expected to be rather subtle, affecting the preparation of the plant to properly manage subsequent responses to pathogens with no major fitness costs. Most of the research that has been conducted at this stage has been dedicated to the study of changes in gene expression and protein phosphorylation. However, the metabolic changes that occur during the pre-challenge priming stage are poorly understood. The second stage affects the early to late stages of the defence response, which occurs after the interaction with a pathogen has been established. Most studies involving priming are dedicated to the molecular events that take place during this stage. Most studies have shown that defence priming is strongly hormonally regulated; however, there is also evidence of the involvement of phenolic derivative compounds and many other secondary metabolites, leading to stronger and faster plant responses. The third priming phase ranges from long lasting defence priming to trans-generational acquired resistance. Long-term metabolic transitions, that occur in the offspring of primed plants, remain to be elucidated. Here we review existing information in the literature that relates to the metabolic changes that occur during all three defence priming stages and highlight the metabolic transitions that are associated with the stimulation of priming and the characteristics of the pathogens whenever possible.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adie BAT, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano J, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19(5):1665–1681

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ahn IP, Kim S, Lee YH (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138:1505–1515

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ahn IP, Kim S, Lee YH, Suh SC (2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol 143:838–848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Antoni JF, White RF (1980) The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopathol Z 98:331–341

    Google Scholar 

  • Balmer D, De Papajewski DV, Planchamp C, Glauser G, Mauch-Mani B (2013) Induced resistance in maize is based on organ-specific defence responses. Plant J 74(2):213–225

    CAS  PubMed  Google Scholar 

  • Barsch A, Carvalho HG, Cullimore JV, Niehaus K (2006) GC–MS based metabolite profiling implies three interdependent ways of ammonium assimilation in Medicago truncatula root nodules. J Biotechnol 127(1):79–83

    CAS  PubMed  Google Scholar 

  • Bednarek P (2012) Chemical warfare or modulators of defence responses—the function of secondary metabolites in plant immunity. Curr Opin Plant Biol 15(4):407–414

    CAS  PubMed  Google Scholar 

  • Bednarek P, Piślewska-Bednarek M, Svatoš A, Schneider B, Doubský J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323(5910):101–106

    CAS  PubMed  Google Scholar 

  • Bengtsson T, Holefors A, Witzell J, Andreasson E, Liljeroth E (2014) Activation of defence responses to Phytophthora infestans in potato by BABA. Plant Pathol 63(1):193–202

    CAS  Google Scholar 

  • Boachon B, Gamir J, Pastor V, Erb M, Dean JV, Flors V, Mauch-Mani B (2014) Role of two UDP-glycosyltransferases from the F group of Arabidopsis in resistance against Pseudomonas syringae. Eur J Plant Pathol 139(4):707–720

  • Borges AA, Dobon A, Expósito-Rodríguez M, Jiménez-Arias D, Borges-Pérez A, Casañas-Sánchez V, Pérez JA, Luis JC, Tornero P (2009) Molecular analysis of menadione-induced resistance against biotic stress in Arabidopsis. Plant Biotechnol J 7(8):744–762

    CAS  PubMed  Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Bertsch C, Mliki A, Soustre-Gacougnolle I (2012) Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR like-cell death. Plant Physiol Biochem 57:120–133

    CAS  PubMed  Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Gertz C, Gandoura S, Mliki A, Bertsch C, Soustre-Gacougnolle I (2013) Methionine elicits H2O2 generation and defense gene expression in grapevine and reduces Plasmopara viticola infection. J Plant Physiol 170(18):1561–1568

    CAS  PubMed  Google Scholar 

  • Brotman Y, Lisec J, Méret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158(1):139–146

    CAS  PubMed  Google Scholar 

  • Camañes G, Pastor V, Cerezo M, García-Agustín P, Herrero VF (2012) A deletion in the nitrate high affinity transporter NRT21 alters metabolomic and transcriptomic responses to Pseudomonas syringae. Plant Signal Behav 7(6):619–622

    PubMed Central  PubMed  Google Scholar 

  • Chamarthi SK, Kumar K, Gunnaiah R, Kushalaa AC, Dion Y, Choo TM (2014) Identification of fusarium head blight resistance related metabolites specific to doubled-haploid lines in barley. Eur J Plant Pathol 138(1):67–78

    CAS  Google Scholar 

  • Chao Y, Chen C, Huang W, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329(1):327–337

    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(1):161–172

    CAS  PubMed  Google Scholar 

  • Chavan V, Kamble A (2013) β-Aminobutyric acid primed expression of WRKY and defence genes in brassica carinata against alternaria blight. J Phytopathol 161(11–12):859–865

    CAS  Google Scholar 

  • Conrath U (2009) Chapter 9 priming of induced plant defense responses. Adv Bot Res 51:361–395

    CAS  Google Scholar 

  • Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16(10):524–531

    CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7(5):210–216

    CAS  PubMed  Google Scholar 

  • Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19(10):1062–1071

    CAS  PubMed  Google Scholar 

  • Crampton BG, Hein I, Berger DK (2009) Salicylic acid confers resistance to a biotrophic rust pathogen, Puccinia substriata, in pearl millet (Pennisetum glaucum). Mol Plant Pathol 10:291–304

    CAS  PubMed  Google Scholar 

  • Dean JV, Delaney SP (2008) Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol Plant 132(4):417–425

    CAS  PubMed  Google Scholar 

  • Del Pozo O, Lam E (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8(20):1129–1132

    PubMed  Google Scholar 

  • Dempsey DA, Klessig DF (2012) SOS—too many signals for systemic acquired resistance? Trends Plant Sci 17(9):538–545

    CAS  PubMed  Google Scholar 

  • Denance N, Sanchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35(2):193–205

    CAS  PubMed  Google Scholar 

  • Fester T, Fetzer I, Buchert S, Lucas R, Rillig MC, Härtig C (2011) Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction. Oecologia 167(4):913–924

    PubMed  Google Scholar 

  • Flors V, Ton J, Jakab G, Mauch-Mani B (2005) Abscisic acid and callose: team players in defence against pathogens? J Phytopathol 153(7–8):377–383

    CAS  Google Scholar 

  • Flors V, Ton J, Van Doorn R, Jakab G, García-Agustín P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54(1):81–92

    CAS  PubMed  Google Scholar 

  • Forcat S, Bennett M, Grant M, Mansfield JW (2010) Rapid linkage of indole carboxylic acid to the plant cell wall identified as a component of basal defence in Arabidopsis against hrp mutant bacteria. Phytochemistry 71(8–9):870–875

    CAS  PubMed  Google Scholar 

  • Gamir J, Pastor V, Cerezo M, Flors V (2012) Identification of indole-3-carboxylic acid as mediator of priming against Plectosphaerella cucumerina. Plant Physiol Biochem 61:169–179

    CAS  PubMed  Google Scholar 

  • Gamir J, Pastor V, Kaever A, Cerezo M, Flors V (2014a) Targeting novel chemical and constitutive primed metabolites against Plectosphaerella cucumerina. Plant J 78(2):227–240

    CAS  PubMed  Google Scholar 

  • Gamir J, Cerezo M, Flors V (2014b) The plasticity of priming phenomenon activates not only common metabolomic fingerprint but also specific responses against P. cucumerina. Plant Signal Behav 9(4):e28916

    PubMed  Google Scholar 

  • García-Andrade J, Ramírez V, Flors V, Vera P (2011) Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. Plant J 67:783–794

    PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    CAS  PubMed  Google Scholar 

  • Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus J, Mauch-Mani B (2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol Plant Microbe Interact 18(8):819–829

    CAS  PubMed  Google Scholar 

  • Hao F, Zhao S, Dong H, Zhang H, Sun L, Miao C (2010) Nia1 and Nia2 are inved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J Integr Plant Biol 52:298–307

    CAS  PubMed  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68(1):14–25

    CAS  Google Scholar 

  • Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44(3):321–334

    CAS  PubMed  Google Scholar 

  • Iiyama K, Lam TBT, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 7:315–320

    Google Scholar 

  • Iriti M, Rossoni M, Borgo M, Ferrara L, Faoro F (2005) Induction of resistance to gray mold with benzothiadiazole modifies amino acid profile and increases proanthocyanidins in grape: primary versus secondary metabolism. J Agric Food Chem 53(23):9133–9139

    CAS  PubMed  Google Scholar 

  • Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5(6):1389–1402

    CAS  PubMed  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324(5923):89–91

    PubMed  Google Scholar 

  • Kaliff M, Staal J, Myrenås M, Dixelius C (2007) ABA is required for Leptosphaeria maculans resistance via ABI1 and ABI4-dependent signaling. Mol Plant Microbe Interact 20(4):335–345

    CAS  PubMed  Google Scholar 

  • Kauss H, Krause K, Jeblick W (1992) Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses. Biochem Biophys Res Commun 189(1):304–308

    CAS  PubMed  Google Scholar 

  • Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128(3):1046–1056

    CAS  PubMed Central  PubMed  Google Scholar 

  • Llorente F, Muskett P, Sánchez-Vallet A, López G, Ramos B, Sánchez-Rodríguez C, Jordá L, Parker J, Molina A (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant 1(3):496–509

    CAS  PubMed  Google Scholar 

  • López-Ráez JA, Pozo MJ (2013) Chemical signalling in the arbuscular mycorrhizal symbiosis. In: Aroca R (ed) Progress in symbiotic endophytes. Springer, New York, pp 215–232

    Google Scholar 

  • López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61(10):2589–2601

    PubMed Central  PubMed  Google Scholar 

  • Luna E, Ton J (2012) The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal Behav 7(6):615–618

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24(2):183–193

    CAS  PubMed  Google Scholar 

  • Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiol 158(2):844–853

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luna E, van Hulten M, Zhang Y, Berkowitz O, López A, Pétriacq P, Sellwood MA, Chen B, Burrell M, van de Meene A, Pieterse CMJ, Flors V, Ton Jurriaan (2014) Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10(6):450–456

  • Luzzatto T, Golan A, Yishay M, Bilkis I, Ben-Ari J, Yedidia I (2007) Priming of antimicrobial phenolics during induced resistance response towards Pectobacterium carotovorum in the ornamental monocot calla lily. J Agric Food Chem 55(25):10315–10322

    CAS  PubMed  Google Scholar 

  • Małolepsza U (2005) Spatial and temporal variation of reactive oxygen species and antioxidant enzymes in o-hydroxyethylorutin-treated tomato leaves inoculated with Botrytis cinerea. Plant Pathol 54(3):317–324

    Google Scholar 

  • Mandal R, Kathiria P, Psychogios N, Bouatra S, Krishnamurthy R, Wishart D, Kovalchuk I (2012) Progeny of tobacco mosaic virus-infected Nicotiana tabacum plants exhibit trans-generational changes in metabolic profiles. Biocatal Agric Biotechnol 1(2):115–123

    CAS  Google Scholar 

  • Marina M, Maiale SJ, Rossi FR, Romero MF, Rivas EI, Gárriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147(4):2164–2178

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mitsuya Y, Takahashi Y, Berberich T, Miyazaki A, Matsumura H, Takahashi H, Terauchi R, Kusano T (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J Plant Physiol 166(6):626–643

    CAS  PubMed  Google Scholar 

  • Návarová H, Bernsdorff F, Döring A, Zeier J (2013) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24(12):5123–5141

    Google Scholar 

  • Octave S, Amborabé B-, Luini E, Ferreira T, Fleurat-Lessard P, Roblin G (2005) Antifungal effects of cysteine towards Eutypa lata, a pathogen of vineyards. Plant Physiol Biochem 43(10–11):1006–1013

    CAS  PubMed  Google Scholar 

  • Oide S, Bejai S, Staal J, Guan N, Kaliff M, Dixelius C (2013) A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. New Phytol 200(4):1187–1199

    CAS  PubMed  Google Scholar 

  • Park S, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318(5847):113–116

    CAS  PubMed  Google Scholar 

  • Pastor V, Luna E, Ton J, Cerezo M, García-Agustín P, Flors V (2013) Fine tuning of reactive oxygen species homeostasis regulates primed immune responses in arabidopsis. Mol Plant Microbe Interact 26(11):1334–1344

    CAS  PubMed  Google Scholar 

  • Pastor V, Gamir J, Camañes G, Cerezo M, Sánchez-Bel P, Flors V (2014a) Disruption the ammonium transporter AMT11 alters basal defences generating resistance against P. syringae and P. cucumerina. Front Plant Sci 5:231

    PubMed Central  PubMed  Google Scholar 

  • Pastor V, Pena A, Gamir J, Flors V, Mauch-Mani B (2014b) Preparing to fight back: generation and storage of defensive compounds during the priming phase in Arabidopsis. Front Plant Sci. doi:10.3389/fpls.00295

    Google Scholar 

  • Petti C, Reiber K, Ali SS, Berney M, Doohan FM (2012) Auxin as a player in the biocontrol of Fusarium head blight disease of barley and its potential as a disease control agent. BMC Plant Biol 12:224

    CAS  PubMed Central  PubMed  Google Scholar 

  • Piękna-Grochala J, Kępczyńska E (2013) Induction of resistance against pathogens by β-aminobutyric acid. Acta Physiol Plant 35(6):1735–1748

    Google Scholar 

  • Pieterse CMJ, Van Pelt JA, Ton J, Parchmann S, Mueller MJ, Buchala AJ, Métraux J, Van Loon LC (2000) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol Mol Plant Pathol 57(3):123–134

    CAS  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316

    CAS  PubMed  Google Scholar 

  • Pourcel L, Irani NG, Koo AJK, Bohorquez-Restrepo A, Howe GA, Grotewold E (2013) A chemical complementation approach reveals genes and interactions of flavonoids with other pathways. Plant J 74:383–397

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10(4):393–398

    CAS  PubMed  Google Scholar 

  • Rairdan GJ, Terrence P, Delaney TP (2002) Role of salicylic acid and NIM1/NPR1 in racespecific resistance in Arabidopsis. Genetics 161:803–811

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rasmann S, Bauerle TL, Poveda K, Vannette R (2011) Predicting root defence against herbivores during succession. Funct Ecol 25(2):368–379

    Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    CAS  PubMed  Google Scholar 

  • Scalschi L, Vicedo B, Camañes G, Fernandez-Crespo E, Lapeña L, González-Bosch C, García-Agustín P (2013) Hexanoic acid is a resistance inducer that protects tomato plants against Pseudomonas syringae by priming the jasmonic acid and salicylic acid pathways. Mol Plant Pathol 14(4):342–355

    CAS  PubMed  Google Scholar 

  • Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69(1):112–146

    CAS  PubMed  Google Scholar 

  • Schuster B, Rjetey J (1995) The mechanism of action of phenylalanine ammonia-lyase: the role of prosthetic dehydroalanine. Proc Natl Acad Sci 92:8433–8437

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol 43:229–260

    CAS  PubMed  Google Scholar 

  • Singh DP, Moore CA, Gilliland A, Carr JP (2004) Activation of multiple antiviral defense mechanisms by salicylic acid. Mol Plant Pathol 5:57–63

    CAS  PubMed  Google Scholar 

  • Slaughter AR, Hamiduzzaman MM, Gindro K, Neuhaus J, Mauch-Mani B (2008) Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur J Plant Pathol 122(1):185–195

    CAS  Google Scholar 

  • Stinson M, Ezra D, Hess WW, Sears J, Strobel G (2003) An endophytic Gliocladium sp of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Sci 165(4):913–922

    CAS  Google Scholar 

  • Stuttmann J, Hubberten H-, Rietz S, Kaur J, Muskett P, Guerois R, Bednarek P, Hoefgen R, Parker JE (2011) Perturbation of Arabidopsis amino acid metabolism causes incompatibility with the adapted biotrophic pathogen Hyaloperonospora arabidopsidis. Plant Cell 23(7):2788–2803

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taheri P, Tarighi S (2010) Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J Plant Physiol 167(3):201–208

    CAS  PubMed  Google Scholar 

  • Takahashi Y, Berberich T, Yamashita K, Uehara Y, Miyazaki A, Kusano T (2004) Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower-senescence. Plant Mol Biol 54(4):613–622

    CAS  PubMed  Google Scholar 

  • Thomma BPHJ, Nelissen I, Eggermont K, Broekaert WF (1999) Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19(2):163–171

    CAS  PubMed  Google Scholar 

  • Ton J, Mauch-Mani B (2004) β-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130

    CAS  PubMed  Google Scholar 

  • Ton J, Jakab G, Toquin V, Iavicoli A, Flors V, Maeder MN, Metraux JP, Mauch-Mani B (2005) Dissecting the b-aminobutyric acid induced priming pathways in Arabidopsis. Plant Cell 17:987–999

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14(6):310–317

    CAS  PubMed  Google Scholar 

  • Truman W, Bennet 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(3):1075–1080

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uehara Y, Takahashi Y, Berberich T, Miyazaki A, Takahashi H, Matsui K, Ohme-Takagi M, Saitoh H, Terauchi R, Kusano T (2005) Tobacco ZFT1, a transcriptional repressor with a Cys2/His 2 type zinc finger motif that functions in spermine-signaling pathway. Plant Mol Biol 59(3):435–448

    CAS  PubMed  Google Scholar 

  • Van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L, Bouwmeester K, van Loon JJA, Dicke M, Raaijmakers JM (2012) Metabolic and transcriptomic changes induced in arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160(4):2173–2188

    PubMed Central  PubMed  Google Scholar 

  • Van Wees SCM, Chang H-, Zhu T, Glazebrook J (2003) Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132(2):606–617

    PubMed Central  PubMed  Google Scholar 

  • Verhagen BWM, Glazebrook J, Zhu T, Chang H-, Van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant Microbe Interact 17(8):895–908

    CAS  PubMed  Google Scholar 

  • Verhagen BWM, Trotel-Aziz P, Couderchet M, Höfte M, Aziz A (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61(1):249–260

    CAS  PubMed  Google Scholar 

  • Vicedo B, Flors V, De La O, Leyva M, Finiti I, Kravchuk Z, Real MD, García-Agustín P, González-Bosch C (2009) Hexanoic acid-induced resistance against botrytis cinerea in tomato plants. Mol Plant Microbe Interact 22(11):1455–1465

    CAS  PubMed  Google Scholar 

  • Vicente J, Cascón T, Vicedo B, García-Agustín P, Hamberg M, Castresana C (2012) Role of 9-lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol Plant 5(4):914–928

    CAS  PubMed  Google Scholar 

  • Vogel-Adghough D, Stahl E, Návarová H, Zeier J (2013) “Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco. Plant Signal Behav, 8–11

  • Von Saint PV, Zhang W, Kanawati B, Geist B, Faus-Keßler T, Schmitt-Kopplin P, Schäffner AR (2011) The arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23(11):4124–4145

    Google Scholar 

  • Wang Y, Liu J (2012) Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J Plant Physiol 169(12):1143–1149

    CAS  PubMed  Google Scholar 

  • White RF (1979) Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99(2):410–412

    CAS  PubMed  Google Scholar 

  • Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection. Plant Physiol 118(4):1213–1222

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    CAS  PubMed  Google Scholar 

  • Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142(1):193–206

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu K, Soares J, Mandal M, Wang C, Chanda B, Gifford A, Fowler J, Navarre D, Kachroo A, Kachroo P (2013) A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3(4):1266–1278

    CAS  PubMed  Google Scholar 

  • Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36(12):2085–2103

    CAS  PubMed  Google Scholar 

  • Zhang S, Yang X, Sun M, Sun F, Deng S, Dong H (2009) Riboflavin-induced priming for pathogen defense in Arabidopsis thaliana. J Integr Plant Biol 51(2):167–174

    PubMed  Google Scholar 

  • Zimmerli L, Jakab G, Métraux J, Mauch-Mani B (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proc Natl Acad Sci USA 97(23):12920–12925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmerli L, Métraux J-, Mauch-Mani B (2001) β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol 126(2):517–523

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Spanish ministry MINECO AGL2012-39923-C02-02 and the Plan de Promoción de la Investigación Universitat Jaume I P1-B2013-68.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Metabolic Integration and Cell Signaling Group, Plant Physiology Section, Department of CAMN, Universitat Jaume I, Avd Vicente Sos Baynat, 12071, Castellón, Spain

    J. Gamir, P. Sánchez-Bel & V. Flors

Authors
  1. J. Gamir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Sánchez-Bel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Flors
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. Flors.

Additional information

Communicated by Neal Stewart.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gamir, J., Sánchez-Bel, P. & Flors, V. Molecular and physiological stages of priming: how plants prepare for environmental challenges. Plant Cell Rep 33, 1935–1949 (2014). https://doi.org/10.1007/s00299-014-1665-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1665-9

Keywords

Search

Navigation