Unlocking BABA-induced resistance in tomato: a comprehensive multi-omics analysis sheds light on enhanced plant defense mechanisms
image: Overlap between genes induced by BABA and genes induced in selected plants with altered amino acid homeostasis.
Credit: Horticulture Research
Plants have always been susceptible to various environmental stresses and attacks by pests and pathogens. Over time, they have evolved multiple defense mechanisms to repel potential attackers. However, the basal immune responses typically only slow down the colonisation of pathogens, ultimately leading to significant global losses in plant production caused by fungi, oomycetes, bacteria, insects, and nematodes. Fortunately, when exposed to micro-beassociated molecular patterns (MAMPs) or specific chemical compounds, plants can enter a state of enhanced defence through "defense initiation". Defence priming can activate multigenic defence mechanisms, conferring relatively durable resistance. One of the most effective priming agents is the non-protein amino acid β-aminobutyric acid (BABA), which protects various plant species against a wide range of stresses. BABA is an endogenous stress metabolite ,which induces resistance through the action of several hormones, including salicylic acid (SA), jasmonic acid (JA), abscisic acid (ABA) and ethylene (ET). As tomato is an important crop globally, it is of great significance to gain insight into the molecular basis of BABA-induced resistance in tomato.
In April 2023, Horticulture Research published a research paper entitled by “BABA-induced pathogen resistance: a multi-omics analysis of the tomato response reveals a hyper-receptive status involving ethylene ”.
To understand the protective effect of BABA on tomato plants against various pathogens, plants were treated with 10 mM BABA and then exposed to biotrophic Oidium neolycopersici, hemibiotrophic Phytophthora parasitica, and necrotrophic Botrytis cinerea. The results showed that BABA treatment significantly reduced the sporulation of O. neolycopersici and the spreading of P. parasitica but had no effect on B. cinerea. Subsequently, transcriptomic and proteomic analyses were performed 24h and 48h after BABA treatment. RNA sequencing identified 24,562 genes, of which 1,523 genes were differentially expressed. The proteome analysis identified 1,808 protein groups and 319 differentially expressed proteins. As with the transcriptome, far more proteins were up-regulated (67%) than down-regulated (33%) after BABA treatment, but the correlation between proteins and transcripts changes was only about 10%. These results suggest that BABA treatment leads to extensive reprogramming of cellular processes in tomato. By comparing different RNA-seq data, it was found that almost 50% of the BABA-upregulated genes were also differentially regulated during MAMPs-triggered immunity (MTI), suggesting that BABA treatment exhibits common features with MTI. They also compared the set of BABA-upregulated genes with the set of genes upregulated in transcriptomics studies performed on tomato plants subjected to temperature, salinity stress, and infected by the fungus Stemphylium lycopersici and the FIRE. It was found that 50% of the BABA upregulated genes overlapped only with the set of genes up-regulated by abiotic stresses, confirming BABA primarily acts as a stress factor in tomato plants.
Researchers further performed KEGG and Gene Ontology (GO) term analysis to investigate the molecular mechanisms underlying the BABA stress response. The results showed a significant enrichment of genes related to the JA and ET signaling pathways. Moreover, both ET and JA accumulated in tomato plants during the first few hours after BABA treatment. Accordingly, the specific genes crucial for ET and JA biosynthesis were upregulated post-BABA treatment. There was no significant enrichment of genes related to the phytohormone SA, but rather a slight decline in SA levels in BABA-treated leaves. Additionally, BABA treatment did not significantly influence genes associated with ABA signaling. Therefore, the BABA stress response is mainly orchestrated via ET and JA signalling. Combined analysis of transcriptome and proteome revealed that protein kinases play an important role in the BABA stress response. Notably, the study also found BABA treatment induced the upregulation of 130 TF genes, including ERF, WRKY, MYB, and NAC families, which play essential roles in regulating stress responses in plants. By comparing of the BABA-upregulated RLPs/WRKY, ERF, and MYB genes with recent RNA-Seq results for tomato plants under biotic and abiotic stress, it was confirmed that the pattern of upregulation induced by BABA is significantly more similar to that for abiotic stress than that for biotic stress. Lastly, amino acid metabolism was explored in BABA-treated plants. Following BABA treatment, a notable increase in the levels of the enzymes, such as GlnRS, Glu and GABA. BABA-induced changes also affected nitrogen metabolism and the phenylpropanoid pathway. Despite the extensive change in the transcriptomic levels, there was no observed increase in polyamine levels, suggesting that agmatine serves some other metabolic purpose in BABA-treated tomatoes.
In conclusion, this study revealed that BABA triggers a primed state in plants, enhancing their defense responses against pathogens. BABA-induced resistance (BABA-IR) in tomatoes was mapped by integrating changes in metabolites with transcriptome and proteome data (Figure 1). This understanding can potentially revolutionize pathogen resistance strategies in crops, improving agricultural practices and yields.
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References
Authors
Martina Zapletalová1,2,†, Corinne Rancurel1,†, Benoit Industri1, Marc Bardin3, Kevin Le Brigand4, Philippe Nicot3, Virginie Magnone4, Aurélie Seassau1, Pascal Barbry4, David Potěšil5, Zbyněk Zdráhal5, Michel Ponchet1 and Jan Lochman2, *
†co-first authors who equally contributed to the work
Affiliations
1. UMRInstitut Sophia Agrobiotech INRAE 1355, CNRS 6254, Université Côte d’Azur, 400, Route des Chappes, 06903 Sophia Antipolis, France
2. Department of Biochemistry, Faculty of Science, Masaryk University, Kotlárská 2, 61137 Brno, Czech Republic
3. Unité 407 Pathologie végétale, INRAE, Domaine Saint-Maurice, 84143 Montfavet cedex, France
4. UMRInstitut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur, CNRS 7275, 660 Route des Lucioles 06560 Valbonne, France
5. Central European Institute of Technology, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
About Jan Lochman
He is an associate professor in the Department of Biochemistry at Masaryk University. His current research is focusing on identifying changes in glutamatergic pathways specific for sporadic form of Alzheimer's disease in human astrocytes and understand molecular pathogenesis of diseases through advanced DNA technologies.