Prior exposure to microbial-associated molecular patterns or specific chemical compounds can promote plants into a primed state with stronger defence responses. β-aminobutyric acid (BABA) is an endogenous stress metabolite that induces resistance protecting various plants towards diverse stresses. In this study, by integrating BABA-induced changes in selected metabolites with transcriptome and proteome data, we generated a global map of the molecular processes operating in BABA-induced resistance (BABA-IR) in tomato. BABA significantly restricts the growth of the pathogens Oidium neolycopersici and Phytophthora parasitica but not Botrytis cinerea. A cluster analysis of the upregulated processes showed that BABA acts mainly as a stress factor in tomato. The main factor distinguishing BABA-IR from other stress conditions was the extensive induction of signaling and perception machinery playing a key role in effective resistance against pathogens. Interestingly, the signalling processes and immune response activated during BABA-IR in tomato differed from those in Arabidopsis with substantial enrichment of genes associated with jasmonic acid (JA) and ethylene (ET) signalling and no change in Asp levels. Our results revealed key differences between the effect of BABA on tomato and other model plants studied until now. Surprisingly, salicylic acid (SA) is not involved in BABA downstream signalization whereas ET and JA play a crucial role.

Central European Institute of Technology Masaryk University Kamenice 5 625 00 Brno Czech Republic

Department of Biochemistry Faculty of Science Masaryk University Kotlářská 2 61137 Brno Czech Republic

UMR Institut de Pharmacologie Moléculaire et Cellulaire Université Côte d'Azur CNRS 7275 660 Route des Lucioles 06560 Valbonne France

UMR Institut Sophia Agrobiotech INRAE 1355 CNRS 6254 Université Côte d'Azur 400 Route des Chappes 06903 Sophia Antipolis France

Unité 407 Pathologie végétale INRAE Domaine Saint Maurice 84143 Montfavet cedex France

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Savary S, Ficke A, Aubertot J-Net al. . Crop losses due to diseases and their implications for global food production losses and food security. Food Secur. 2012;4:519–37.

Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–9. PubMed

Conrath U, Beckers GJM, Langenbach CJGet al. . Priming for enhanced defense. Annu Rev Phytopathol. 2015;53:97–119. PubMed

Westman SM, Kloth KJ, Hanson Jet al. . Defence priming in Arabidopsis – a meta-analysis. Sci Rep. 2019;9:13309. PubMed PMC

Vijayakumari K, Jisha KC, Puthur JT. GABA/BABA priming: a means for enhancing abiotic stress tolerance potential of plants with less energy investments on defence cache. Acta Physiol Plant. 2016;38:1-14.

Baccelli I, Mauch-Mani B. Beta-aminobutyric acid priming of plant defense: the role of ABA and other hormones. Plant Mol Biol. 2016;91:703–11. PubMed

Pieterse CMJ, Zamioudis C, Berendsen RLet al. . Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol. 2014;52:347–75. PubMed

Chassot C, Buchala A, Schoonbeek H-Jet al. . Wounding of Arabidopsis leaves causes a powerful but transient protection against botrytis infection. Plant J Cell Mol Biol. 2008;55:555–67. PubMed

Cohen Y, Vaknin M, Mauch-Mani B. BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica. 2016;44:513–38.

Kuźnicki D, Meller B, Arasimowicz-Jelonek Met al. . BABA-induced DNA Methylome adjustment to intergenerational Defense priming in potato to Phytophthora infestans. Front Plant Sci. 2019;10:650, 1-16. PubMed PMC

Luna E, López A, Kooiman Jet al. . Role of NPR1 and KYP in long-lasting induced resistance by β-aminobutyric acid. Front Plant Sci. 2014;5:184. PubMed PMC

Thevenet D, Pastor V, Baccelli Iet al. . The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol. 2017;213:552–9. PubMed

Baccelli I, Glauser G, Mauch-Mani B. The accumulation of β-aminobutyric acid is controlled by the plant’s immune system. Planta. 2017;246:791–6. PubMed

Ton J, Jakab G, Toquin Vet al. . Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell. 2005;17:987–99. PubMed PMC

Zimmerli L, Jakab G, Metraux JPet al. . Potentiation of pathogen-specific defense mechanisms in Arabidopsis by beta -aminobutyric acid. Proc Natl Acad Sci U S A. 2000;97:12920–5. PubMed PMC

Hamiduzzaman MM, Jakab G, Barnavon Let al. . 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. 2005;18:819–29. PubMed

Schwarzenbacher RE, Wardell G, Stassen Jet al. . The IBI1 receptor of β-aminobutyric acid interacts with VOZ transcription factors to regulate Abscisic acid Signaling and callose-associated Defense. Mol Plant. 2020;13:1455–69. PubMed PMC

Luna E, Hulten M, Zhang Yet al. . Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol. 2014;10:450–6. PubMed PMC

Satková P, Starý T, Plešková Vet al. . Diverse responses of wild and cultivated tomato to BABA, oligandrin and Oidium neolycopersici infection. Ann Bot. 2016;119:mcw188–840. PubMed PMC

Home | Food and Agriculture Organization of the United Nations . [cited 15 Feb 2021]. Available: http://www.fao.org/home/en/

Cohen Y. Local and systemic control of Phytophthora infestans in tomato plants by dl-3-amino-n-butanoic acids. Phytopathology. 1994;84:55-59.

Bengtsson T, Weighill D, Proux-Wéra Eet al. . Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genomics. 2014;15:315. PubMed PMC

Luna E, Beardon E, Ravnskov Set al. . Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Dis. 2016;100:704–10. PubMed

Worrall D, Holroyd GH, Moore JPet al. . Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytol. 2012;193:770–8. PubMed

Xu G, Greene GH, Yoo Het al. . Global translational reprogramming is a fundamental layer of immune regulation in plants. Nature. 2017;545:487–90. PubMed PMC

Zimmerli L, Hou B-H, Tsai C-Het al. . The xenobiotic beta-aminobutyric acid enhances Arabidopsis thermotolerance. Plant J. 2008;53:144–56. PubMed

Pombo MA, Zheng Y, Fernandez-Pozo Net al. . Transcriptomic analysis reveals tomato genes whose expression is induced specifically during effector-triggered immunity and identifies the Epk1 protein kinase which is required for the host response to three bacterial effector proteins. Genome Biol. 2014;15:492. PubMed PMC

Rosli HG, Zheng Y, Pombo MAet al. . Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol. 2013;14:R139. PubMed PMC

Solanský M, Mikulášek K, Zapletalová Met al. . Elicitins’ oligomeric states affect the hypersensitive response and resistance in tobacco. J Exp Bot. 2021;72:3219–34. PubMed

Geng X, Jin L, Shimada Met al. . The phytotoxin coronatine is a multifunctional component of the virulence armament of pseudomonas syringae. Planta. 2014;240:1149–65. PubMed PMC

Kawamura SHY, Hase S, Takenaka Set al. . INF1 Elicitin activates jasmonic acid- and ethylene-mediated signalling pathways and induces resistance to bacterial wilt disease in tomato. J Phytopathol. 2009;157:287–97.

Uppalapati SR, Ishiga Y, Wangdi Tet al. . The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with pseudomonas syringae pv. Tomato DC3000. MPMI. 2007;20:955–65. PubMed

Szklarczyk D, Morris JH, Cook Het al. . The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–8. PubMed PMC

Supek F, Bošnjak M, Škunca Net al. . REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6:e21800, 1-9. PubMed PMC

Jain M, Aggarwal S, Nagar Pet al. . A D-lactate dehydrogenase from rice is involved in conferring tolerance to multiple abiotic stresses by maintaining cellular homeostasis. Sci Rep. 2020;10:12835, 1-17. PubMed PMC

Chen H, McCaig BC, Melotto Met al. . Regulation of plant Arginase by wounding, jasmonate, and the Phytotoxin Coronatine *. J Biol Chem. 2004;279:45998–6007. PubMed

Meteignier L-V, El Oirdi M, Cohen Met al. . Translatome analysis of an NB-LRR immune response identifies important contributors to plant immunity in Arabidopsis. J Exp Bot. 2017;68:2333–44. PubMed

Chen H, Chen X, Chen Det al. . A comparison of the low temperature transcriptomes of two tomato genotypes that differ in freezing tolerance: Solanum lycopersicum and Solanum habrochaites. BMC Plant Biol. 2015;15:132, 1-16. PubMed PMC

Sun W, Xu X, Zhu Het al. . Comparative Transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant Cell Physiol. 2010;51:997–1006. PubMed

Yang H, Zhao T, Jiang Jet al. . Transcriptome analysis of the Sm-mediated hypersensitive response to Stemphylium lycopersici in tomato. Front Plant Sci. 2017;8:1257, 1-14. PubMed PMC

Li G, Meng X, Wang Ret al. . Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 2012;8:e1002767, 1-14. PubMed PMC

Skottke KR, Yoon GM, Kieber JJet al. . Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 2011;7:e1001370, 1-13. PubMed PMC

Bürstenbinder K, Rzewuski G, Wirtz Met al. . The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J. 2007;49:238–49. PubMed

Canonne J, Froidure-Nicolas S, Rivas S. Phospholipases in action during plant defense signaling. Plant Signal Behav. 2011;6:13–8. PubMed PMC

Ishiga Y, Ishiga T, Uppalapati SRet al. . Jasmonate ZIM-domain (JAZ) protein regulates host and nonhost pathogen-induced cell death in tomato and Nicotiana benthamiana. PLoS One. 2013;8:e75728, 1-7. PubMed PMC

Janotík A, Dadáková K, Lochman Jet al. . L-aspartate and L-glutamine inhibit Beta-aminobutyric acid-induced resistance in tomatoes. Plants. 2022;11:2908, 1-12. PubMed PMC

Lehti-Shiu MD, Zou C, Hanada Ket al. . Evolutionary history and stress regulation of plant receptor-like kinase/Pelle genes. Plant Physiol. 2009;150:12–26. PubMed PMC

Jonge R, Esse HP, Maruthachalam Ket al. . Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci U S A. 2012;109:5110–5. PubMed PMC

Zhou J-M, Tang D, Wang G. Receptor kinases in plant pathogen interactions: more than pattern recognition. Plant cell. Online. 2017;29:618–37. PubMed PMC

Peng K-C, Wang C-W, Wu C-Het al. . Tomato SOBIR1/EVR homologs are involved in Elicitin perception and plant Defense against the Oomycete pathogen Phytophthora parasitica. Mol Plant-Microbe Interact. 2015;28:913–26. PubMed

Kim J-G, Li X, Roden JAet al. . Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell. 2009;21:1305–23. PubMed PMC

iTAK. iTAK - Plant Transcription factor & Protein Kinase Identifier and Classifier . [cited 26 Jul 2017]. Available: http://bioinfo.bti.cornell.edu/cgi-bin/itak/index.cgi

Pan Y, Seymour GB, Lu Cet al. . An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep. 2012;31:349–60. PubMed

Sharma MK, Kumar R, Solanke AUet al. . Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Gen Genomics. 2010;284:455–75. PubMed

Huang S, Gao Y, Liu Jet al. . Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Gen Genet. 2012;287:495–513. PubMed

Du H, Wang Y-B, Xie Yet al. . Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants. DNA Res Int J Rapid Publ Rep Genes Genomes. 2013;20:437–48. PubMed PMC

Li Z, Peng R, Tian Yet al. . Genome-wide identification and analysis of the MYB transcription factor superfamily in Solanum lycopersicum. Plant Cell Physiol. 2016;57:1657–77. PubMed

Hildebrandt TM, Nunes Nesi A, Araújo WLet al. . Amino acid catabolism in plants. Mol Plant. 2015;8:1563–79. PubMed

Rojas CM, Senthil-Kumar M, Tzin Vet al. . Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front Plant Sci. 2014;5:17, 1-12. PubMed PMC

Hu CA, Delauney AJ, Verma DP. A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci. 1992;89:9354–8. PubMed PMC

Hua XJ, Van De Cotte B, Van Montagu Met al. . The 5′ untranslated region of the at-P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J. 2001;26:157–69. PubMed

Deuschle K, Funck D, Forlani Get al. . The role of Δ1-Pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell. 2004;16:3413–25. PubMed PMC

Yang H, Ludewig U. Lysine catabolism, amino acid transport, and systemic acquired resistance. Plant Signal Behav. 2014;9:e28933, 1-4. PubMed PMC

Sivaguru M, Pike S, Gassmann Wet al. . Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol. 2003;44:667–75. PubMed

Lu G, Wang X, Liu Jet al. . Application of T-DNA activation tagging to identify glutamate receptor-like genes that enhance drought tolerance in plants. Plant Cell Rep. 2014;33:617–31. PubMed

Bird CR, Smith TA. The biosynthesis of coumarylagmatine in barley seedlings. Phytochemistry. 1981;20:2345–6.

Roepenack Lahaye E, Newman M-A, Schornack Set al. . P-Coumaroylnoradrenaline, a novel plant metabolite implicated in tomato Defense against pathogens. J Biol Chem. 2003;278:43373–83. PubMed

Scheideler M, Schlaich NL, Fellenberg Ket al. . Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem. 2002;277:10555–61. PubMed

Mutuku JM, Nose A. Changes in the contents of metabolites and enzyme activities in Rice plants responding to Rhizoctonia solani Kuhn infection: activation of glycolysis and connection to Phenylpropanoid pathway. Plant Cell Physiol. 2012;53:1017–32. PubMed

Ton J, Mauch-Mani B. Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 2004;38:119–30. PubMed

Yan Z, Reddy MS, Ryu C-Met al. . Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology. 2002;92:1329–33. PubMed

Klessig DF, Tian M, Choi HW. Multiple targets of salicylic acid and its derivatives in plants and animals. Front Immunol 2016;7, 1-10. Available: 10.3389/fimmu.2016.00206 PubMed DOI PMC

Ponchet M, Duprez V, Ricci P. SUPPRESSION OF BOTH INDUCED RESISTANCE AND PHYTOALEXIN PRODUCTION BY SALICYLIC ACID DURING ELICITATION OF CARNATION CUTTINGS. In A. M. Kofranek (Eds.), Acta Horticulturae. International Society for Horticultural Science (ISHS): Leuven, Belgium, 1983,61–70.

Czékus Z, Iqbal N, Pollák Bet al. . Role of ethylene and light in chitosan-induced local and systemic defence responses of tomato plants. J Plant Physiol. 2021;263:153461, 1-12. PubMed

Czékus Z, Kukri A, Hamow KÁet al. . Activation of local and systemic defence responses by Flg22 is dependent on daytime and ethylene in intact tomato plants. Int J Mol Sci. 2021;22:8354, 1-21. PubMed PMC

Pujol C, Bailly M, Kern Det al. . Dual-targeted tRNA-dependent amidotransferase ensures both mitochondrial and chloroplastic gln-tRNAGln synthesis in plants. Proc Natl Acad Sci U S A. 2008;105:6481–5. PubMed PMC

Pajerowska-Mukhtar KM, Wang W, Tada Yet al. . The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr Biol. 2012;22:103–12. PubMed PMC

Wu C-C, Singh P, Chen M-Cet al. . L-glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis. J Exp Bot. 2010;61:995–1002. PubMed PMC

Wang Y, Weide R, Govers Fet al. . L-type lectin receptor kinases in Nicotiana benthamiana and tomato and their role in Phytophthora resistance. J Exp Bot. 2015;66:6731–43. PubMed PMC

Miya A, Albert P, Shinya Tet al. . CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A. 2007;104:19613–8. PubMed PMC

AbuQamar S, Chai M-F, Luo Het al. . Tomato protein kinase 1b mediates Signaling of plant responses to Necrotrophic fungi and insect Herbivory. Plant Cell. 2008;20:1964–83. PubMed PMC

Liu G, Ji Y, Bhuiyan NHet al. . Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell. 2010;22:3845–63. PubMed PMC

Kadotani N, Akagi A, Takatsuji Het al. . Exogenous proteinogenic amino acids induce systemic resistance in rice. BMC Plant Biol. 2016;16:60, 1-10. PubMed PMC

Fabro G, Kovács I, Pavet Vet al. . Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. MPMI. 2004;17:343–50. PubMed

Cecchini NM, Monteoliva MI, Alvarez ME. Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiol. 2011;155:1947–59. PubMed PMC

Rizzi YS, Cecchini NM, Fabro Get al. . Differential control and function of Arabidopsis ProDH1 and ProDH2 genes on infection with biotrophic and necrotrophic pathogens. Mol Plant Pathol. 2017;18:1164–74. PubMed PMC

Kim D-R, Jeon C-W, Cho Get al. . Glutamic acid reshapes the plant microbiota to protect plants against pathogens. Microbiome. 2021;9:244, 1-18. PubMed PMC

Manzoor H, Kelloniemi J, Chiltz Aet al. . Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant J. 2013;76:466–80. PubMed

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106, 1-12. PubMed PMC

Wang Y, Coleman-Derr D, Chen Get al. . OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 2015;43:W78–84. PubMed PMC

eulerr citation info . [cited 21 Jan 2021]. Available: https://cran.r-project.org/web/packages/eulerr/citation.html

Tian T, Liu Y, Yan Het al. . agriGO v2.0: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2017;45:W122–9. PubMed PMC

Proost S, Van Bel M, Vaneechoutte Det al. . PLAZA 3.0: an access point for plant comparative genomics. Nucleic Acids Res. 2014;43:D974–81. PubMed PMC

Shannon P, Markiel A, Ozier Oet al. . Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504. PubMed PMC

Goenawan IH, Bryan K, Lynn DJ. DyNet: visualization and analysis of dynamic molecular interaction networks. Bioinformatics. 2016;32:2713–5. PubMed PMC

Gómez-Alonso S, Hermosín-Gutiérrez I, García-Romero E. Simultaneous HPLC analysis of biogenic amines, amino acids, and ammonium ion as Aminoenone derivatives in wine and beer samples. J Agric Food Chem. 2007;55:608–13. PubMed

Segarra G, Jáuregui O, Casanova Eet al. . Simultaneous quantitative LC–ESI-MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress. Phytochemistry. 2006;67:395–401. PubMed