BACKGROUND AND AIMS: Current strategies for increased crop protection of susceptible tomato plants against pathogen infections include treatment with synthetic chemicals, application of natural pathogen-derived compounds or transfer of resistance genes from wild tomato species within breeding programmes. In this study, a series of 45 genes potentially involved in defence mechanisms was retrieved from the genome sequence of inbred reference tomato cultivar Solanum lycopersicum 'Heinz 1706'. The aim of the study was to analyse expression of these selected genes in wild and cultivated tomato plants contrasting in resistance to the biotrophic pathogen Oidium neolycopersici , the causative agent of powdery mildew. Plants were treated either solely with potential resistance inducers or by inducers together with the pathogen. METHODS: The resistance against O. neolycopersici infection as well as RT-PCR-based analysis of gene expression in response to the oomycete elicitor oligandrin and chemical agent β-aminobutyric acid (BABA) were investigated in the highly susceptible domesticated inbred genotype Solanum lycopersicum 'Amateur' and resistant wild genotype Solanum habrochaites . KEY RESULTS: Differences in basal expression levels of defensins, germins, β-1,3-glucanases, heveins, chitinases, osmotins and PR1 proteins in non-infected and non-elicited plants were observed between the highly resistant and susceptible genotypes. Moreover, these defence genes showed an extensive up-regulation following O. neolycopersici infection in both genotypes. Application of BABA and elicitin induced expression of multiple defence-related transcripts and, through different mechanisms, enhanced resistance against powdery mildew in the susceptible tomato genotype. CONCLUSIONS: The results indicate that non-specific resistance in the resistant genotype S. habrochaites resulted from high basal levels of transcripts with proven roles in defence processes. In the susceptible genotype S. lycopersicum 'Amateur', oligandrin- and BABA-induced resistance involved different signalling pathways, with BABA-treated leaves displaying direct activation of the ethylene-dependent signalling pathway, in contrast to previously reported jasmonic acid-mediated signalling for elicitins.

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

Department of Biochemistry Faculty of Science Palacký University Šlechtitelu 27 78371 Olomouc Czech Republic

Department of Botany Faculty of Science Palacký University Šlechtitelu 27 78371 Olomouc Czech Republic

Laboratory of Growth Regulators and Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University and Institute of Experimental Botany ASCR Šlechtitelu 27 78371 Olomouc Czech Republic

Zobrazit více v PubMed

Anand A, Lei ZT, Sumner LW, et al. 2004. Apoplastic extracts from a transgenic wheat line exhibiting lesion-mimic phenotype have multiple pathogenesis-related proteins that are antifungal. Molecular Plant-Microbe Interactions 17: 1306–1317. PubMed

Bengtsson T, Holefors A, Witzell J, Andreasson E, Liljeroth E.. 2014a. Activation of defence responses to Phytophthora infestans in potato by BABA. Journal of Experimental Botany 63: 193–202.

Bengtsson T, Weighill D, Proux-Wera E, et al. 2014b. Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genomics 15. PubMed PMC

Benhamou N, Belanger RR, Rey P, Tirilly Y.. 2001. Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiology and Biochemistry 39: 681–696.

Bonnet P, Bourdon E, Ponchet M, Blein JP, Ricci P.. 1996. Acquired resistance triggered by elicitins in tobacco and other plants. European Journal of Experimental Botany 102: 181–192.

Chang WC, Lee TY, Huang HD, Huang HY, Pan RL.. 2008. PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9. PubMed PMC

Cohen Y. 2002. β-Aminobutyric acid-induced resistance against plant pathogens. Plant Disease 86: 448–457. PubMed

Cohen Y, Niderman T, Mosinger E, Fluhr R.. 1994. Beta-aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato (Lycopersicon esculentum L.) plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiology 104: 59–66. PubMed PMC

Cohen Y, Rubin AE, Kilfin G.. 2010. Mechanisms of induced resistance in lettuce against Bremia lactucae by DL-β-amino-butyric acid (BABA). European Journal of Plant Pathology 126: 553–573.

Cohn JR, Martin GB.. 2005. Pseudomonas syringae pv. tomato type III effectors AvrPto and AvrPtoB promote ethylene-dependent cell death in tomato. The Plant Journal 44: 139–154. PubMed

Conrath U. 2009. Priming of induced plant defense responses. Plant Innate Immunity 51: 361–395.

Dana MD, Pintor-Toro JA, Cubero B.. 2006. Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiology 142: 722–730. PubMed PMC

Exposito-Rodriguez M, Borges AA, Borges-Perez A, Perez JA.. 2008. Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biology 8. PubMed PMC

Foolad MR. 2007. Genome mapping and molecular breeding of tomato. International Journal of Plant Genomics 2007: 1–52. PubMed PMC

Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227. PubMed

Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA.. 2013. Current understanding on ethylene signalling in plants: the influence of nutrient availability. Plant Physiology and Biochemistry 73: 128–138. PubMed

Jakab G, Cottier V, Toquin V, et al. 2001. β-Aminobutyric acid-induced resistance in plants. European Journal of Experimental Botany 107: 29–37.

Jupe J, Stam R, Howden AJM, et al. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biology 14. PubMed PMC

Kamoun S, Young M, Glascock CB, Tyler BM.. 1993. Extracellular protein elicitors from Phytophthora - host-specificity and induction of resistance to bacterial and fungal phytopathogens. Molecular Plant-Microbe Interactions 6: 15–25.

Kawamura Y, Hase S, Takenaka S, et al. 2009. INF1 elicitin activates jasmonic acid- and ethylene-mediated signalling pathways and induces resistance to bacterial wilt disease in tomato. Journal of Phytopathology 157: 287–297.

Kim YS, Choi D, Lee MM, Lee SH, Kim WT.. 1998. Biotic and abiotic stress-related expression of 1-aminocyclopropane-1-carboxylate oxidase gene family in Nicotiana glutinosa L. Plant and Cell Physiology 39: 565–573. PubMed

Koressaar T, Remm M.. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics 23: 1289–1291. PubMed

Lebeda A, Reinink K.. 1994. Histological characterization of resistance in Lactuca-Saligna to lettuce downy mildew (Bremia-Lactucae). Physiological and Molecular Plant Pathology 44: 125–139.

Lebeda A, Mieslerová B, Petřivalský M, et al. 2014. Resistance mechanisms of wild tomato germplasm to infection of Oidium neolycopersici. European Journal of Experimental Botany 138: 569–596.

Lherminier J, Benhamou N, Larrue J, et al. 2003. Cytological characterization of elicitin-induced protection in tobacco plants infected by Phytophthora parasitica or phytoplasma. Phytopathology 93: 1308–1319. PubMed

Li GJ, Meng XZ, Wang RG, Mao GH, Han L, Liu YD, Zhang SQ.. 2012. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genetics 8: e1002767. PubMed PMC

Lin T, Zhu GT, Zhang JH, et al. 2014. Genomic analyses provide insights into the history of tomato breeding. Nature Genetics 46: 1220–1226. PubMed

Lincoln JE, Campbell AD, Oetiker J, et al. 1993. Le-Acs4, a fruit ripening and wound-induced 1-aminocyclopropane-1-carboxylate synthase gene of tomato (Lycopersicon esculentum) – Expression in Escherichia coli, structural characterization, expression characteristics, and phylogenetic analysis. Journal of Biological Chemistry 268: 19422–19430. PubMed

Liu D, Raghothama KG, Hasegawa PM, Bressan RA.. 1994. Osmotin overexpression in potato delays development of disease symptoms. Proceedings of the National Academy of Sciences of the USA 91: 1888–1892. PubMed PMC

Lopez-Kleine L, Pinzon A, Chaves D, Restrepo S, Riano-Pachon DM.. 2013. Chromosome 10 in the tomato plant carries clusters of genes responsible for field resistance/defence to Phytophthora infestans. Genomics 101: 249–255. PubMed

Luna E, van Hulten M, Zhang Y, et al. 2014. Plant perception of beta-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nature Chemical Biology 10: 450–456. PubMed PMC

Malá J, Machová P, Cvrčková H, et al. 2009. Micropropagation of wild service tree (Sorbus torminalis [L.] Crantz): the regulative role of different aromatic cytokinins during organogenesis. Journal of Plant Growth Regulation 28: 341–348.

Menda N, Strickler SR, Edwards JD, et al. 2014. Analysis of wild-species introgressions in tomato inbreds uncovers ancestral origins. BMC Plant Biology 14. PubMed PMC

Mieslerová B, Lebeda A, Chetelat RT.. 2000. Variation in response of wild Lycopersicon and Solanum spp. against tomato powdery mildew (Oidium lycopersici). Journal of Phytopathology 148: 303–311.

Nicot N, Hausman JF, Hoffmann L, Evers D.. 2005. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56: 2907–2914. PubMed

Oka Y, Cohen Y.. 2001. Induced resistance to cyst and root-knot nematodes in cereals by dl-beta-amino-N-butyric acid. European Journal of Plant Pathology 107: 219–227.

Oldach KH, Becker D, Lorz H.. 2001. Heterologous expression of genes mediating enhanced fungal resistance in transgenic wheat. Molecular Plant-Microbe Interactions 14: 832–838. PubMed

Picard K, Ponchet M, Blein JP, Rey P, Tirilly Y, Benhamou N.. 2000. Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiology 124: 379–395. PubMed PMC

Piękna-Grochala J, Kępczyńska E.. 2013. Induction of resistance against pathogens by beta-aminobutyric acid. Acta Physiologiae Plantarum 35: 1735–1748.

Piterková J, Petřivalský M, Luhová L, Mieslerová B, Sedlářová M, Lebeda A.. 2009. Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Molecular Plant Pathology 10: 501–513. PubMed PMC

Piterková J, Hofman J, Mieslerová B, et al. 2011. Dual role of nitric oxide in Solanum spp.–Oidium neolycopersici interactions. Environmental and Experimental Botany 74: 37–44.

Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF.. 2008. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiology and Biochemistry 46: 941–950. PubMed

Shi HY, Zhang YX.. 2014. Expression and regulation of pear 1-aminocyclopropane-1-carboxylic acid synthase gene (PpACS1a) during fruit ripening, under salicylic acid and indole-3-acetic acid treatment, and in diseased fruit. Molecular Biology Reports 41: 4147–4154. PubMed

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. Physiological and Molecular Plant Pathology 56: 95–106.

Sim SC, Robbins MD, Van Deynze A, Michel AP, Francis DM.. 2011. Population structure and genetic differentiation associated with breeding history and selection in tomato (Solanum lycopersicum L.). Heredity 106: 927–935. PubMed PMC

Skottke KR, Yoon GM, Kieber JJ, DeLong A.. 2011. Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genetics 7: e1001370. PubMed PMC

Spoel SH, Dong X.. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology 12: 89–100. PubMed

Tománková K, Luhová L, Petřivalský M, Peč P, Lebeda A.. 2006. Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiological and Molecular Plant Pathology 68: 22–32.

Ton J, Jakab G, Toquin V, et al. 2005. Dissecting the beta-aminobutyric acid-induced priming phenomenon in arabidopsis. The Plant Cell 17: 987–999. PubMed PMC

van Loon LC, Geraats BPJ, Linthorst HJM.. 2006. Ethylene as a modulator of disease resistance in plants. Trends in Plant Science 11: 184–191. PubMed

Vleeshouwers VGA, Oliver RP.. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular Plant-Microbe Interactions 27: 196–206. PubMed

Worrall D, Holroyd GH, Moore JP, et al. 2012. Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytologist 193: 770–778. PubMed

Wu CC, Singh P, Chen MC, Zimmerli L.. 2010. l-Glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis. Journal of Experimental Botany 61: 995–1002. PubMed PMC

Yim WJ, Kim KY, Lee YW, Sundaram SP, Lee Y, Sa TM.. 2014. Real time expression of ACC oxidase and PR-protein genes mediated by Methylobacterium spp. in tomato plants challenged with Xanthomonas campestris pv. vesicatoria. Journal of Plant Physiology 171: 1064–1075. PubMed

Zhu BL, Chen THH, Li PH.. 1996. Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198: 70–77. PubMed

Zimmerli L, Metraux JP, Mauch-Mani B.. 2001. β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiology 126: 517–23. PubMed PMC

BABA-induced pathogen resistance: a multi-omics analysis of the tomato response reveals a hyper-receptive status involving ethylene

L-Aspartate and L-Glutamine Inhibit Beta-Aminobutyric Acid-Induced Resistance in Tomatoes

Seed Protection of Solanum lycopersicum with Pythium oligandrum against Alternaria brassicicola and Verticillium albo-atrum

The elicitin β-cryptogein's activity in tomato is mediated by jasmonic acid and ethylene signalling pathways independently of elicitin-sterol interactions