Chemical priming of plant defense responses to pathogen attacks

. 2023 ; 14 () : 1146577. [epub] 20230508

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid37223806

Plants can acquire an improved resistance against pathogen attacks by exogenous application of natural or artificial compounds. In a process called chemical priming, application of these compounds causes earlier, faster and/or stronger responses to pathogen attacks. The primed defense may persist over a stress-free time (lag phase) and may be expressed also in plant organs that have not been directly treated with the compound. This review summarizes the current knowledge on the signaling pathways involved in chemical priming of plant defense responses to pathogen attacks. Chemical priming in induced systemic resistance (ISR) and systemic acquired resistance (SAR) is highlighted. The roles of the transcriptional coactivator NONEXPRESSOR OF PR1 (NPR1), a key regulator of plant immunity, induced resistance (IR) and salicylic acid signaling during chemical priming are underlined. Finally, we consider the potential usage of chemical priming to enhance plant resistance to pathogens in agriculture.

Zobrazit více v PubMed

Akagi A., Fukushima S., Okada K., Jiang C. J., Yoshida R., Nakayama A., et al. . (2014). WRKY45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction. Plant Mol. Biol. 86, 171–183. doi: 10.1007/s11103-014-0221-x PubMed DOI PMC

Ameye M., Allmann S., Verwaeren J., Smagghe G., Haesaert G., Schuurink R. C., et al. . (2018). Green leaf volatile production by plants: a meta-analysis. New Phytol. 220, 666–683. doi: 10.1111/nph.14671 PubMed DOI

Antoniou C., Savvides A., Christou A., Fotopoulos V. (2016). Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr. Opin. Plant Biol. 33, 101–107. doi: 10.1016/j.pbi.2016.06.020 PubMed DOI

Aranega-Bou P., de la O Leyva M., Finiti I., Garcfa-Agustfn P., Gonzalez-Bosch C. (2014). Priming of plant resistance by natural compounds. hexanoic acid as a model. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00488 PubMed DOI PMC

Argueso C. T., Ferreira F. J., Epple P., To J. P. C., Hutchison C. E., Schaller G. E., et al. . (2012). Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PloS Genet. 8, e1002448. doi: 10.1371/journal.pgen.1002448 PubMed DOI PMC

Baccelli I., Glauser G., Mauch-Mani B. (2017). The accumulation of β-aminobutyric acid is controlled by the plant’s immune system. Planta 246, 791–796. doi: 10.1007/s00425-017-2751-3 PubMed DOI

Backer R., Naidoo S., van den Berg N. (2019). The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00102 PubMed DOI PMC

Bagheri A., Fathipour Y. (2021). “Induced resistance and defense primings,” in Molecular approaches for sustainable insect pest management (Singapore: Springer Singapore; ), 73–139.

Balmer A., Glauser G., Mauch-Mani B., Baccelli I. (2019). Accumulation patterns of endogenous β-aminobutyric acid during plant development and defence in Arabidopsis thaliana . Plant Biol. 21, plb.12940. doi: 10.1111/plb.12940 PubMed DOI

Banday Z. Z., Cecchini N. M., Speed D. J., Scott A. T., Parent C., Hu C. T., et al. . (2022). Friend or foe: hybrid proline-rich proteins determine how plants respond to beneficial and pathogenic microbes. Plant Physiol. 190, 860–881. doi: 10.1093/plphys/kiac263 PubMed DOI PMC

Bartsch M., Gobbato E., Bednarek P., Debey S., Schultze J. L., Bautor J., et al. . (2006). Salicylic acid–independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18, 1038–1051. doi: 10.1105/tpc.105.039982 PubMed DOI PMC

Bauer S., Mekonnen D. W., Hartmann M., Yildiz I., Janowski R., Lange B., et al. . (2021). UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates n-hydroxypipecolic acid, and balances plant immunity. Plant Cell 33, 714–734. doi: 10.1093/plcell/koaa044 PubMed DOI PMC

Beckers G. J. M., Jaskiewicz M., Liu Y., Underwood W. R., He S. Y., Zhang S., et al. . (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in. Arabidopsis Thaliana Plant Cell 21, 944–953. doi: 10.1105/tpc.108.062158 PubMed DOI PMC

Bengtsson T., Weighill D., Proux-Wéra E., Levander F., Resjö S., Burra D. D., et al. . (2014). Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genomics 15, 315. doi: 10.1186/1471-2164-15-315 PubMed DOI PMC

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

Borges A. A., Dobon A., Expósito-Rodríguez M., Jiménez-Arias D., Borges-Pérez A., Casañas-Sánchez V., et al. . (2009). Molecular analysis of menadione-induced resistance against biotic stress in arabidopsis. Plant Biotechnol. J. 7, 744–762. doi: 10.1111/j.1467-7652.2009.00439.x PubMed DOI

Borges A. A., Jiménez-Arias D., Expósito-Rodríguez M., Sandalio L. M., Pérez J. A. (2014). Priming crops against biotic and abiotic stresses: MSB as a tool for studying mechanisms. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00642 PubMed DOI PMC

Brambilla A., Lenk M., Ghirardo A., Eccleston L., Knappe C., Weber B., et al. . (2023). Pipecolic acid synthesis is required for systemic acquired resistance and plant-to-plant-induced immunity in barley. J. Exp. Bot., 1–14. doi: 10.1093/JXB/ERAD095 PubMed DOI

Brilli F., Loreto F., Baccelli I. (2019). Exploiting plant volatile organic compounds (VOCs) in agriculture to improve sustainable defense strategies and productivity of crops. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00264 PubMed DOI PMC

Bryksová M., Dabravolski S., Kučerová Z., Zavadil Kokáš F., Špundová M., Plíhalová L., et al. . (2020). Aromatic cytokinin arabinosides promote PAMP-like responses and positively regulate leaf longevity. ACS Chem. Biol. 15, 1949–1963. doi: 10.1021/acschembio.0c00306 PubMed DOI

Cai J., Jozwiak A., Holoidovsky L., Meijler M. M., Meir S., Rogachev I., et al. . (2021). Glycosylation of n-hydroxy-pipecolic acid equilibrates between systemic acquired resistance response and plant growth. Mol. Plant 14, 440–455. doi: 10.1016/j.molp.2020.12.018 PubMed DOI

Cao H., Li X., Dong X. (1998). Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. 95, 6531–6536. doi: 10.1073/pnas.95.11.6531 PubMed DOI PMC

Catoni M., Alvarez-Venegas R., Worrall D., Holroyd G., Barraza A., Luna E., et al. . (2022). Long-lasting defence priming by β-aminobutyric acid in tomato is marked by genome-wide changes in DNA methylation. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.836326 PubMed DOI PMC

Cecchini N. M., Roychoudhry S., Speed D. J., Steffes K., Tambe A., Zodrow K., et al. . (2019). Underground azelaic acid–conferred resistance to Pseudomonas syringae in arabidopsis. Mol. Plant-Microbe Interact. 32, 86–94. doi: 10.1094/MPMI-07-18-0185-R PubMed DOI

Cecchini N. M., Speed D. J., Roychoudhry S., Greenberg J. T. (2021). Kinases and protein motifs required for AZI1 plastid localization and trafficking during plant defense induction. Plant J. 105, 1615–1629. doi: 10.1111/tpj.15137 PubMed DOI PMC

Cecchini N. M., Steffes K., Schlappi M. R., Gifford A. N., Greenberg J. T. (2015). Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nat. Commun. 6, 1–12. doi: 10.1038/ncomms8658 PubMed DOI

Chalupowicz L., Manulis-Sasson S., Barash I., Elad Y., Rav-David D., Brandl M. T. (2021). Effect of plant systemic resistance elicited by biological and chemical inducers on the colonization of the lettuce and basil leaf apoplast by salmonella enterica. Appl. Environ. Microbiol. 87, 1–14. doi: 10.1128/AEM.01151-21 PubMed DOI PMC

Chen Y.-C., Holmes E. C., Rajniak J., Kim J.-G., Tang S., Fischer C. R., et al. . (2018). N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in arabidopsis. Proc. Natl. Acad. Sci. 115, E4920–E4929. doi: 10.1073/pnas.1805291115 PubMed DOI PMC

Choi J., Huh S. U., Kojima M., Sakakibara H., Paek K.-H., Hwang I. (2010). The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in arabidopsis. Dev. Cell 19, 284–295. doi: 10.1016/j.devcel.2010.07.011 PubMed DOI

Cohen Y., Vaknin M., Mauch-Mani B. (2016). BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica 44, 513–538. doi: 10.1007/s12600-016-0546-x DOI

Conrath U. (2009). “Chapter 9 priming of induced plant defense responses,” in Advances in botanical research (Elsevier Ltd; ), 361–395. doi: 10.1016/S0065-2296(09)51009-9 DOI

Conrath U., Beckers G. J. M., Flors V., García-Agustín P., Jakab G., Mauch F., et al. . (2006). Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19, 1062–1071. doi: 10.1094/MPMI-19-1062 PubMed DOI

Conrath U., Pieterse C. M. J., Mauch-Mani B. (2002). Priming in plant–pathogen interactions. Trends Plant Sci. 7, 210–216. doi: 10.1016/S1360-1385(02)02244-6 PubMed DOI

Cooper A., Ton J. (2022). Immune priming in plants: from the onset to transgenerational maintenance. Essays Biochem. 66, 635–646. doi: 10.1042/EBC20210082 PubMed DOI PMC

Cortleven A., Leuendorf J. E., Frank M., Pezzetta D., Bolt S., Schmülling T. (2019). Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ. 42, 998–1018. doi: 10.1111/pce.13494 PubMed DOI

De Kesel J., Conrath U., Flors V., Luna E., Mageroy M. H., Mauch-Mani B., et al. . (2021). The induced resistance lexicon: do’s and don’ts. Trends Plant Sci. 26, 685–691. doi: 10.1016/j.tplants.2021.01.001 PubMed DOI

De la Rubia A. G., Mélida H., Centeno M. L., Encina A., García-Angulo P. (2021). Immune priming triggers cell wall remodeling and increased resistance to halo blight disease in common bean. Plants 10, 1–25. doi: 10.3390/plants10081514 PubMed DOI PMC

Devika O. S., Singh S., Sarkar D., Barnwal P., Suman J., Rakshit A. (2021). Seed priming: a potential supplement in integrated resource management under fragile intensive ecosystems. Front. Sustain. Food Syst. 5. doi: 10.3389/fsufs.2021.654001 DOI

Ding P., Ding Y. (2020). Stories of salicylic acid: a plant defense hormone. trends. Plant Sci. 25, 549–565. doi: 10.1016/j.tplants.2020.01.004 PubMed DOI

Ding Y., Sun T., Ao K., Peng Y., Zhang Y., Li X., et al. . (2018). Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173, 1454–1467.e15. doi: 10.1016/j.cell.2018.03.044 PubMed DOI

Engelberth J., Alborn H. T., Schmelz E. A., Tumlinson J. H. (2004). Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. 101, 1781–1785. doi: 10.1073/pnas.0308037100 PubMed DOI PMC

Fauth M., Merten A., Hahn M. G., Jeblick W., Kauss H. (1996). Competence for elicitation of H2O2 in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol. 110, 347–354. doi: 10.1104/pp.110.2.347 PubMed DOI PMC

Finiti I., de la O. Leyva M., Vicedo B., Gómez-Pastor R., López-Cruz J., García-Agustín P., et al. . (2014). Hexanoic acid protects tomato plants against Botrytis cinerea by priming defence responses and reducing oxidative stress. Mol. Plant Pathol. 15, 550–562. doi: 10.1111/mpp.12112 PubMed DOI PMC

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

Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., et al. . (1993). Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756. doi: 10.1126/science.261.5122.754 PubMed DOI

Glazebrook J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227. doi: 10.1146/annurev.phyto.43.040204.135923 PubMed DOI

González-Bosch C. (2018). Priming plant resistance by activation of redox-sensitive genes. Free Radic. Biol. Med. 122, 171–180. doi: 10.1016/j.freeradbiomed.2017.12.028 PubMed DOI

Großkinsky D. K., Naseem M., Abdelmohsen U. R., Plickert N., Engelke T., Griebel T., et al. . (2011). Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiol. 157, 815–830. doi: 10.1104/pp.111.182931 PubMed DOI PMC

Guerra T., Romeis T. (2020). N-hydroxypipecolic acid: a general and conserved activator of systemic plant immunity. J. Exp. Bot. 71, 6193–6196. doi: 10.1093/jxb/eraa345 PubMed DOI PMC

Guerra T., Schilling S., Hake K., Gorzolka K., Sylvester F., Conrads B., et al. . (2020). Calcium-dependent protein kinase 5 links calcium signaling with n-hydroxy-L-pipecolic acid- and SARD1-dependent immune memory in systemic acquired resistance. New Phytol. 225, 310–325. doi: 10.1111/nph.16147 PubMed DOI

Hake K., Romeis T. (2019). Protein kinase-mediated signalling in priming: immune signal initiation, propagation, and establishment of long-term pathogen resistance in plants. Plant Cell Environ. 42, 904–917. doi: 10.1111/pce.13429 PubMed DOI

Hamiduzzaman M. M., Jakab G., Barnavon L., Neuhaus J.-M., 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, 819–829. doi: 10.1094/MPMI-18-0819 PubMed DOI

Hartmann M., Zeier J. (2019). N-hydroxypipecolic acid and salicylic acid: a metabolic duo for systemic acquired resistance. Curr. Opin. Plant Biol. 50, 44–57. doi: 10.1016/j.pbi.2019.02.006 PubMed DOI

Hartmann M., Zeier T., Bernsdorff F., Reichel-Deland V., Kim D., Hohmann M., et al. . (2018). Flavin monooxygenase-generated n-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173, 456–469.e16. doi: 10.1016/j.cell.2018.02.049 PubMed DOI

Heil M., Hilpert A., Kaiser W., Linsenmair K. E. (2000). Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? J. Ecol. 88, 645–654. doi: 10.1046/j.1365-2745.2000.00479.x DOI

Hilker M., Schmülling T. (2019). Stress priming, memory, and signalling in plants. Plant Cell Environ. 42, 753–761. doi: 10.1111/pce.13526 PubMed DOI

Hilker M., Schwachtje J., Baier M., Balazadeh S., Bäurle I., Geiselhardt S., et al. . (2016). Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. 91, 1118–1133. doi: 10.1111/brv.12215 PubMed DOI

Hõrak H. (2021). How to achieve immune balance and harmony: glycosyltransferase UGT76B1 inactivates n -hydroxy-pipecolic acid to suppress defense responses. Plant Cell 33, 453–454. doi: 10.1093/plcell/koaa053 PubMed DOI PMC

Janse van Rensburg H. C., Takács Z., Freynschlag F., Toksoy Öner E., Jonak C., van den Ende W. (2020). Fructans prime ROS dynamics and Botrytis cinerea resistance in Arabidopsis . Antioxidants 9, 805. doi: 10.3390/antiox9090805 PubMed DOI PMC

Janse van Rensburg H. C., van den Ende W. (2020). Priming with γ-aminobutyric acid against botrytis cinerea reshuffles metabolism and reactive oxygen species: dissecting signalling and metabolism. Antioxidants 9, 1–22. doi: 10.3390/antiox9121174 PubMed DOI PMC

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

Jones J. D. G., Dangl J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286 PubMed DOI

Jung H. W., Tschaplinski T. J., Wang L., Glazebrook J., Greenberg J. T. (2009). Priming in systemic plant immunity. Sci. (80-) 324, 89–91. doi: 10.1126/science.1170025 PubMed DOI

Kachroo A., Kachroo P. (2020). Mobile signals in systemic acquired resistance. Curr. Opin. Plant Biol. 58, 41–47. doi: 10.1016/j.pbi.2020.10.004 PubMed DOI

Katz V., Fuchs A., Conrath U. (2002). Pretreatment with salicylic acid primes parsley cells for enhanced ion transport following elicitation. FEBS Lett. 520, 53–57. doi: 10.1016/S0014-5793(02)02759-X PubMed DOI

Katz V. A., Thulke O. U., Conrath U. (1998). A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol. 117, 1333–1339. doi: 10.1104/pp.117.4.1333 PubMed DOI PMC

Kauss H., Jeblick W. (1995). Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol. 108, 1171–1178. doi: 10.1104/pp.108.3.1171 PubMed DOI PMC

Kauss H., Krause K., Jeblick W. (1992. a). Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses. Biochem. Biophys. Res. Commun. 189, 304–308. doi: 10.1016/0006-291X(92)91558-8 PubMed DOI

Kauss H., Theisinger-Hinkel E., Mindermann R., Conrath U. (1992. b). Dichloroisonicotinic and salicylic acid, inducers of systemic acquired resistance, enhance fungal elicitor responses in parsley cells. Plant J. 2, 655–660. doi: 10.1111/j.1365-313X.1992.tb00134.x DOI

Kerchev P., van der Meer T., Sujeeth N., Verlee A., Stevens C. V., van Breusegem F., et al. . (2020). Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol. Adv. 40, 107503. doi: 10.1016/j.biotechadv.2019.107503 PubMed DOI

Klessig D. F., Choi H. W., Dempsey D. A. (2018). Systemic acquired resistance and salicylic acid: past, present, and future. Mol. Plant-Microbe Interact. 31, 871–888. doi: 10.1094/MPMI-03-18-0067-CR PubMed DOI

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, 1046–1056. doi: 10.1104/pp.010744 PubMed DOI PMC

Koley P., Brahmachari S., Saha A., Deb C., Mondal M., Das N., et al. . (2022). Phytohormone priming of tomato plants evoke differential behavior in Rhizoctonia solani during infection, with salicylate priming imparting greater tolerance than jasmonate. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.766095 PubMed DOI PMC

Kravchuk Z., Vicedo B., Flors V., Camañes G., González-Bosch C., García-Agustín P. (2011). Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea . J. Plant Physiol. 168, 359–366. doi: 10.1016/j.jplph.2010.07.028 PubMed DOI

Latunde-Dada A. O., Lucas J. A. (2001). The plant defence activator acibenzolar-s-methyl primes cowpea [Vigna unguiculata (L.) walp.] seedlings for rapid induction of resistance. Physiol. Mol. Plant Pathol. 58, 199–208. doi: 10.1006/pmpp.2001.0327 DOI

Lenk M., Wenig M., Bauer K., Hug F., Knappe C., Lange B., et al. . (2019). Pipecolic acid is induced in barley upon infection and triggers immune responses associated with elevated nitric oxide accumulation. Mol. Plant-Microbe Interact. 32, 1303–1313. doi: 10.1094/MPMI-01-19-0013-R PubMed DOI

Leyva M. O., Vicedo B., Finiti I., Flors V., Del Amo G., Real M. D., et al. . (2008). Preventive and post-infection control of botrytis cinerea in tomato plants by hexanoic acid. Plant Pathol. 57, 1038–1046. doi: 10.1111/j.1365-3059.2008.01891.x DOI

Li T., Cofer T., Engelberth M., Engelberth J. (2016). Defense priming and jasmonates: a role for free fatty acids in insect elicitor-induced long distance signaling. Plants 5, 5. doi: 10.3390/plants5010005 PubMed DOI PMC

Li C., Wang K., Huang Y., Lei C., Cao S., Qiu L., et al. . (2021). Activation of the BABA-induced priming defence through redox homeostasis and the modules of TGA1 and MAPKK5 in postharvest peach fruit. Mol. Plant Pathol. 22, 1624–1640. doi: 10.1111/mpp.13134 PubMed DOI PMC

Lim G.-H., Liu H., Yu K., Liu R., Shine M. B., Fernandez J., et al. . (2020). The plant cuticle regulates apoplastic transport of salicylic acid during systemic acquired resistance. Sci. Adv. 6, 1–14. doi: 10.1126/sciadv.aaz0478 PubMed DOI PMC

Lim G.-H., Shine M. B., de Lorenzo L., Yu K., Cui W., Navarre D., et al. . (2016). Plasmodesmata localizing proteins regulate transport and signaling during systemic acquired immunity in plants. Cell Host Microbe 19, 541–549. doi: 10.1016/j.chom.2016.03.006 PubMed DOI

Liu Y., Sun T., Sun Y., Zhang Y., Radojičić A., Ding Y., et al. . (2020). Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32, 4002–4016. doi: 10.1105/tpc.20.00499 PubMed DOI PMC

Llorens E., Camañes G., Lapeña L., García-Agustín P. (2016). Priming by hexanoic acid induce activation of mevalonic and linolenic pathways and promotes the emission of plant volatiles. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00495 PubMed DOI PMC

Luna E., Beardon E., Ravnskov S., Scholes J., Ton J. (2016). Optimizing chemically induced resistance in tomato against Botrytis cinerea . Plant Dis. 100, 704–710. doi: 10.1094/PDIS-03-15-0347-RE PubMed DOI

Luna E., López A., Kooiman J., Ton J. (2014. a). Role of NPR1 and KYP in long-lasting induced resistance by β-aminobutyric acid. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00184 PubMed DOI PMC

Luna E., van Hulten M., Zhang Y., Berkowitz O., López A., Pétriacq P., et al. . (2014. b). Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat. Chem. Biol. 10, 450–456. doi: 10.1038/nchembio.1520 PubMed DOI PMC

Lutts S., Benincasa P., Wojtyla L., Kubala S., Pace R., Lechowska K., et al. . (2016). “Seed priming: new comprehensive approaches for an old empirical technique,” in New challenges in seed biology - basic and translational research driving seed technology (InTech; ), 1–46.

Martínez-Aguilar K., Ramírez-Carrasco G., Hernández-Chávez J. L., Barraza A., Alvarez-Venegas R. (2016). Use of BABA and INA as activators of a primed state in the common bean (Phaseolus vulgaris l.). Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00653 PubMed DOI PMC

Mauch-Mani B., Baccelli I., Luna E., Flors V. (2017). Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68, 485–512. doi: 10.1146/annurev-arplant-042916-041132 PubMed DOI

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

Mohnike L., Rekhter D., Huang W., Feussner K., Tian H., Herrfurth C., et al. . (2021). The glycosyltransferase UGT76B1 modulates n-hydroxy-pipecolic acid homeostasis and plant immunity. Plant Cell 33, 735–749. doi: 10.1093/plcell/koaa045 PubMed DOI PMC

Mur L. A. J., Naylor G., Warner S. A. J., Sugars J. M., White R. F., Draper J. (1996). Salicylic acid potentiates defence gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J. 9, 559–571. doi: 10.1046/j.1365-313X.1996.09040559.x DOI

Nair A. (2021). Salicylic acid (SA)-independent processes in systemic acquired resistance (SAR). doi: 10.53846/goediss-8517 DOI

Nanda S., Kumar G., Hussain S. (2022). Utilization of seaweed-based biostimulants in improving plant and soil health: current updates and future prospective. Int. J. Environ. Sci. Technol. 19, 12839–12852. doi: 10.1007/s13762-021-03568-9 DOI

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

Ngou B. P. M., Ahn H.-K., Ding P., Jones J. D. G. (2021). Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110–115. doi: 10.1038/s41586-021-03315-7 PubMed DOI

Noutoshi Y., Ikeda M., Saito T., Osada H., Shirasu K. (2012. a). Sulfonamides identified as plant immune-priming compounds in high-throughput chemical screening increase disease resistance in Arabidopsis thaliana . Front. Plant Sci. 3. doi: 10.3389/fpls.2012.00245 PubMed DOI PMC

Noutoshi Y., Ikeda M., Shirasu K. (2012. b). Diuretics prime plant immunity in Arabidopsis thaliana . PloS One 7, e48443. doi: 10.1371/journal.pone.0048443 PubMed DOI PMC

Oliveira M. B., Junior M. L., Grossi-de-Sá M. F., Petrofeza S. (2015). Exogenous application of methyl jasmonate induces a defense response and resistance against Sclerotinia sclerotiorum in dry bean plants. J. Plant Physiol. 182, 13–22. doi: 10.1016/j.jplph.2015.04.006 PubMed DOI

Panpatte D. G., Jhala Y. K., Vyas R. V. (2020). Signaling pathway of induced systemic resistance. INC 133–141. doi: 10.1016/b978-0-12-818469-1.00011-0 DOI

Papavizas G. C., Davey C. B. (1963). Effect of amino compounds and related substances lacking sulfur on aphanomyces root rot of peas. Phytopathology 53, 116–122.

Pastor V., Balmer A., Gamir J., Flors V., Mauch-Mani B. (2014). Preparing to fight back: generation and storage of priming compounds. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00295 PubMed DOI PMC

Pawar V. A., Laware S. L. (2018). Seed priming a critical review. Int. J. Sci. Res. Biol. Sci. 5, 94–101. doi: 10.26438/ijsrbs/v5i5.94101 DOI

Peng Y., Yang J., Li X., Zhang Y. (2021). Salicylic acid: biosynthesis and signaling. Annu. Rev. Plant Biol. 72, 761–791. doi: 10.1146/annurev-arplant-081320-092855 PubMed DOI

Picazo-Aragonés J., Terrab A., Balao F. (2020). Plant volatile organic compounds evolution: transcriptional regulation, epigenetics and polyploidy. Int. J. Mol. Sci. 21, 8956. doi: 10.3390/ijms21238956 PubMed DOI PMC

Pieterse C. M. J., Berendsen R. L., de Jonge R., Stringlis I. A., van Dijken A. J. H., van Pelt J. A., et al. . (2021). Pseudomonas simiae WCS417: star track of a model beneficial rhizobacterium. Plant Soil 461, 245–263. doi: 10.1007/s11104-020-04786-9 DOI

Pieterse C. M. J., Leon-Reyes A., van der Ent S., van Wees S. C. M. (2009). Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308–316. doi: 10.1038/nchembio.164 PubMed DOI

Pieterse C. M. J., van Pelt J. A., Ton J., Parchmann S., Mueller M. J., Buchala A. J., et al. . (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, 123–134. doi: 10.1006/pmpp.2000.0291 DOI

Pieterse C. M. J., van Wees S. C. M., van Pelt J. A., Knoester M., Laan R., Gerrits H., et al. . (1998). A novel signaling pathway controlling induced systemic resistance in Arabidopsis . Plant Cell 10, 1571–1580. doi: 10.1105/tpc.10.9.1571 PubMed DOI PMC

Pieterse C. M. J., Zamioudis C., Berendsen R. L., Weller D. M., van Wees S. C. M., Bakker P. A. H. M. (2014). Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375. doi: 10.1146/annurev-phyto-082712-102340 PubMed DOI

Pozo M. J., van der Ent S., van Loon L. C., Pieterse C. M. J. (2008). Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana . New Phytol. 180, 511–523. doi: 10.1111/j.1469-8137.2008.02578.x PubMed DOI

Pruitt R. N., Gust A. A., Nürnberger T. (2021). Plant immunity unified. Nat. Plants 7, 382–383. doi: 10.1038/s41477-021-00903-3 PubMed DOI

Ren X., Wang J., Zhu F., Wang Z., Mei J., Xie Y., et al. . (2022). β-aminobutyric acid (BABA)-induced resistance to tobacco black shank in tobacco (Nicotiana tabacum l.). PloS One 17, e0267960. doi: 10.1371/journal.pone.0267960 PubMed DOI PMC

Rhaman M. S., Imran S., Rauf F., Khatun M., Baskin C. C., Murata Y., et al. . (2021). Seed priming with phytohormones: an effective approach for the mitigation of abiotic stress. Plants 10, 37. doi: 10.3390/plants10010037 PubMed DOI PMC

Rivas-San Vicente M., Plasencia J. (2011). Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321–3338. doi: 10.1093/jxb/err031 PubMed DOI

Ryals J. A., Neuenschwander U. H., Willits M. G., Molina A., Steiner H. Y., Hunt M. D. (1996). Systemic acquired resistance. Plant Cell 8, 1809–1819. doi: 10.1105/tpc.8.10.1809 PubMed DOI PMC

Sako K., Nguyen H. M., Seki M. (2021). Advances in chemical priming to enhance abiotic stress tolerance in plants. Plant Cell Physiol. 61, 1995–2003. doi: 10.1093/pcp/pcaa119 PubMed DOI

Saleem M., Fariduddin Q., Castroverde C. D. M. (2021). Salicylic acid: a key regulator of redox signalling and plant immunity. Plant Physiol. Biochem. 168, 381–397. doi: 10.1016/j.plaphy.2021.10.011 PubMed DOI

Savvides A., Ali S., Tester M., Fotopoulos V. (2016). Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci. 21, 329–340. doi: 10.1016/j.tplants.2015.11.003 PubMed DOI

Scalschi L., Vicedo B., Camañes G., Fernandez-Crespo E., Lapeña L., González-Bosch C., et al. . (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, 342–355. doi: 10.1111/mpp.12010 PubMed DOI PMC

Schaller G. E., Street I. H., Kieber J. J. (2014). Cytokinin and the cell cycle. Curr. Opin. Plant Biol. 21, 7–15. doi: 10.1016/j.pbi.2014.05.015 PubMed DOI

Schillheim B., Jansen I., Baum S., Beesley A., Bolm C., Conrath U. (2018). Sulforaphane modifies histone H3, unpacks chromatin, and primes defense. Plant Physiol. 176, 2395–2405. doi: 10.1104/pp.17.00124 PubMed DOI PMC

Schnake A., Hartmann M., Schreiber S., Malik J., Brahmann L., Yildiz I., et al. . (2020). Inducible biosynthesis and immune function of the systemic acquired resistance inducer n-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants. J. Exp. Bot. 71, 6444–6459. doi: 10.1093/jxb/eraa317 PubMed DOI PMC

Schwarzenbacher R. E., Luna E., Ton J. (2014). The discovery of the BABA receptor: scientific implications and application potential. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00304 PubMed DOI PMC

Schwarzenbacher R. E., Wardell G., Stassen J., Guest E., Zhang P., Luna E., et al. . (2020). The IBI1 receptor of β-aminobutyric acid interacts with VOZ transcription factors to regulate abscisic acid signaling and callose-associated defense. Mol. Plant 13, 1455–1469. doi: 10.1016/j.molp.2020.07.010 PubMed DOI PMC

Shen Q., Liu L., Wang L., Wang Q. (2018). Indole primes plant defense against necrotrophic fungal pathogen infection. PloS One 13, 1–15. doi: 10.1371/journal.pone.0207607 PubMed DOI PMC

Shields A., Shivnauth V., Castroverde C. D. M. (2022). Salicylic acid and n-hydroxypipecolic acid at the fulcrum of the plant immunity-growth equilibrium. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.841688 PubMed DOI PMC

Shirasu K., Nakajima H., Rajasekhar V. K., Dixon R. A., Lamb C. (1997). Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261–270. doi: 10.1105/tpc.9.2.261 PubMed DOI PMC

Siegrist J., Orober M., Buchenauer H. (2000). β-aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol. Mol. Plant Pathol. 56, 95–106. doi: 10.1006/pmpp.1999.0255 DOI

Silué D., Pajot E., Cohen Y. (2002). Induction of resistance to downy mildew (Peronospora parasitica) in cauliflower by DL-β-amino-n-butanoic acid (BABA). Plant Pathol. 51, 97–102. doi: 10.1046/j.1365-3059.2002.00649.x DOI

Slaughter A., Daniel X., Flors V., Luna E., Hohn B., Mauch-Mani B. (2012). Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835–843. doi: 10.1104/pp.111.191593 PubMed DOI PMC

Tarkowski Ł.P., Signorelli S., Höfte M. (2020). γ-aminobutyric acid and related amino acids in plant immune responses: emerging mechanisms of action. Plant Cell Environ. 43, 1103–1116. doi: 10.1111/pce.13734 PubMed DOI

Tarkowski Ł., van de Poel B., Höfte M., van den Ende W. (2019). Sweet immunity: inulin boosts resistance of lettuce (Lactuca sativa) against grey mold (Botrytis cinerea) in an ethylene-dependent manner. Int. J. Mol. Sci. 20, 1052. doi: 10.3390/ijms20051052 PubMed DOI PMC

Tateda C., Zhang Z., Shrestha J., Jelenska J., Chinchilla D., Greenberg J. T. (2014). Salicylic acid regulates arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26, 4171–4187. doi: 10.1105/tpc.114.131938 PubMed DOI PMC

Tavallali V., Karimi S., Mohammadi S., Hojati S. (2008). Effects of ß-aminobutyric acid on the induction of resistance to Penicillium italicum . World Appl. Sci. J. 5, 345–351.

Thevenet D., Pastor V., Baccelli I., Balmer A., Vallat A., Neier R., et al. . (2017). The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol. 213, 552–559. doi: 10.1111/nph.14298 PubMed DOI

Thulke O., Conrath U. (1998). Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J. 14, 35–42. doi: 10.1046/j.1365-313X.1998.00093.x PubMed DOI

Ton J., Jakab G., Toquin V., Flors V., Iavicoli A., Maeder M. N., et al. . (2005). Dissecting the β-aminobutyric acid–induced priming phenomenon in Arabidopsis . Plant Cell 17, 987–999. doi: 10.1105/tpc.104.029728 PubMed DOI PMC

Vallad G. E., Goodman R. M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci. 44, 1920–1934. doi: 10.2135/cropsci2004.1920 DOI

van Butselaar T., van den Ackerveken G. (2020). Salicylic acid steers the growth–immunity tradeoff. Trends Plant Sci. 25, 566–576. doi: 10.1016/j.tplants.2020.02.002 PubMed DOI

van der Ent S., van Hulten M., Pozo M. J., Czechowski T., Udvardi M. K., Pieterse C. M. J., et al. . (2009). Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: differences and similarities in regulation. New Phytol. 183, 419–431. doi: 10.1111/j.1469-8137.2009.02851.x PubMed DOI

van Hulten M., Pelser M., van Loon L. C., Pieterse C. M. J. J., Ton J. (2006). Costs and benefits of priming for defense in Arabidopsis . Proc. Natl. Acad. Sci. 103, 5602–5607. doi: 10.1073/pnas.0510213103 PubMed DOI PMC

van Loon L. C., Rep M., Pieterse C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162. doi: 10.1146/annurev.phyto.44.070505.143425 PubMed DOI

van Wees S. C. M., Luijendijk M., Smoorenburg I., van Loon L. C., Pieterse C. M. J. (1999). Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol. 41, 537–549. doi: 10.1023/A:1006319216982 PubMed DOI

Verhagen B. W. M., Glazebrook J., Zhu T., Chang H.-S., van Loon L. C., Pieterse C. M. J. (2004). The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis . Mol. Plant-Microbe Interact. 17, 895–908. doi: 10.1094/MPMI.2004.17.8.895 PubMed DOI

Vicedo B., Flors V., de la O Leyva M., Finiti I., Kravchuk Z., Real M. D., et al. . (2009). Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol. Plant-Microbe Interact. 22, 1455–1465. doi: 10.1094/MPMI-22-11-1455 PubMed DOI

Vlot A. C., Dempsey D. A., Klessig D. F. (2009). Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177–206. doi: 10.1146/annurev.phyto.050908.135202 PubMed DOI

Vlot A. C., Sales J. H., Lenk M., Bauer K., Brambilla A., Sommer A., et al. . (2021). Systemic propagation of immunity in plants. New Phytol. 229, 1234–1250. doi: 10.1111/nph.16953 PubMed DOI

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, 1–9. doi: 10.4161/psb.26366 PubMed DOI PMC

Walters D. R., Ratsep J., Havis N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64, 1263–1280. doi: 10.1093/jxb/ert026 PubMed DOI

Wang K., Jin P., Han L., Shang H., Tang S., Rui H., et al. . (2014). Methyl jasmonate induces resistance against Penicillium citrinum in Chinese bayberry by priming of defense responses. Postharvest Biol. Technol. 98, 90–97. doi: 10.1016/j.postharvbio.2014.07.009 DOI

Wang C., Liu R., Lim G.-H., de Lorenzo L., Yu K., Zhang K., et al. . (2018). Pipecolic acid confers systemic immunity by regulating free radicals. Sci. Adv. 4, 1–12. doi: 10.1126/sciadv.aar4509 PubMed DOI PMC

Wang W., Withers J., Li H., Zwack P. J., Rusnac D.-V., Shi H., et al. . (2020). Structural basis of salicylic acid perception by Arabidopsis NPR proteins. Nature 586, 311–316. doi: 10.1038/s41586-020-2596-y PubMed DOI PMC

Wendehenne D., Durner J., Chen Z., Klessig D. F. (1998). Benzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidase. Phytochemistry 47, 651–657. doi: 10.1016/S0031-9422(97)00604-3 DOI

Wittek F., Hoffmann T., Kanawati B., Bichlmeier M., Knappe C., Wenig M., et al. . (2014). Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid. J. Exp. Bot. 65, 5919–5931. doi: 10.1093/jxb/eru331 PubMed DOI PMC

Wu C.-C., Singh P., Chen M.-C., Zimmerli L. (2010). L-glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis . J. Exp. Bot. 61, 995–1002. doi: 10.1093/jxb/erp363 PubMed DOI PMC

Wu Y., Zhang D., Chu J. Y., Boyle P., Wang Y., Brindle I. D., et al. . (2012). The arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639–647. doi: 10.1016/j.celrep.2012.05.008 PubMed DOI

Yassin M., Ton J., Rolfe S. A., Valentine T. A., Cromey M., Holden N., et al. . (2021). The rise, fall and resurrection of chemical-induced resistance agents. Pest Manage. Sci. 77, 3900–3909. doi: 10.1002/ps.6370 PubMed DOI

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, 192–194. doi: 10.5423/PPJ.NT.10.2014.0112 PubMed DOI PMC

Yi S. Y., Shirasu K., Moon J. S., Lee S.-G., Kwon S.-Y. (2014). The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PloS One 9, e88951. doi: 10.1371/journal.pone.0088951 PubMed DOI PMC

Yildiz I., Mantz M., Hartmann M., Zeier T., Kessel J., Thurow C., et al. . (2021). The mobile SAR signal n-hydroxypipecolic acid induces NPR1-dependent transcriptional reprogramming and immune priming. Plant Physiol. 186, 1679–1705. doi: 10.1093/PLPHYS/KIAB166 PubMed DOI PMC

Yu K., Soares J. M., Mandal M. K., Wang C., Chanda B., Gifford A. N., et al. . (2013). A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-Acid-Induced systemic immunity. Cell Rep. 3, 1266–1278. doi: 10.1016/j.celrep.2013.03.030 PubMed DOI

Yuan M., Jiang Z., Bi G., Nomura K., Liu M., Wang Y., et al. . (2021). Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109. doi: 10.1038/s41586-021-03316-6 PubMed DOI PMC

Zhou M., Wang W. (2018). Recent advances in synthetic chemical inducers of plant immunity. Front. Plant Sci. 871. doi: 10.3389/fpls.2018.01613 PubMed DOI PMC

Zhou J.-M., Zhang Y. (2020). Plant immunity: danger perception and signaling. Cell 181, 978–989. doi: 10.1016/j.cell.2020.04.028 PubMed DOI

Zimmerli L., Jakab G., Métraux J.-P., Mauch-Mani B. (2000). Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proc. Natl. Acad. Sci. 97, 12920–12925. doi: 10.1073/pnas.230416897 PubMed DOI PMC

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...