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

Abstract

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.

Acknowledgements

D.P. acknovledges support of the European Regional Development Fund-Project “Centre for Experimental Plant Biology”: No. CZ.02.1.01/0.0/0.0/16_019/0000738 funded by MEYS CR and by the Institutional Research Fund of Masaryk university, MUNI/A/1492/2021. CIISB research infrastructure project LM2018127 funded by MEYS CR are gratefully acknowledged for the financial support of the measurements at the CEITEC Proteomics Core Facility. This work was also supported by INRAE, Département Santé des Plantes et Environnement through the funding of the ELICITOM project. This project was supported by the National Infrastructure France Génomique (Commissariat aux Grands Investissements, ANR-10-INBS-09-03, ANR-10-INBS-09-02).

Author Contributions

Conceptualization: JL, MP, CR and ZZ; Data curation: MZ, CR, BI, MB, KLB, PN, VM, AS, PB, and DP; Data analysis: MZ, CR, DP, AS and BI; Funding acquisition: JL, MP and ZZ; Methodology: MZ, CR, JL, MP and ZZ; Project administration: JL and MP; Resources: JL, MP and ZZ; Validation: MZ, CR, JL, MP and ZZ; Writing, review, and editing: MZ, JL, and MP; Supervision: JL and MP.

Data availability

Raw sequencing data with appropriate metadata are available in the NCBI Gene Expression Omnibus (GEO) repository under accession number GSE108421. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD038074.

Conflict of interests

None declared.

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