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. 2022 Jul 30;10(8):1547.
doi: 10.3390/microorganisms10081547.

New Insights into Bacillus-Primed Plant Responses to a Necrotrophic Pathogen Derived from the Tomato- Botrytis Pathosystem

Paloma Morales  1 , Máximo González  2   3 , Ricardo Salvatierra-Martínez  2 , Michael Araya  4 , Enrique Ostria-Gallardo  2 , Alexandra Stoll  2   3
Affiliations

New Insights into Bacillus-Primed Plant Responses to a Necrotrophic Pathogen Derived from the Tomato- Botrytis Pathosystem

Paloma Morales et al. Microorganisms. .

Abstract

Induced systemic resistance (ISR) is one of the most studied mechanisms of plant−microbe interaction and is considered a very promising alternative for integrated pest management programs. In our study, we explored the plant defense response induced by Bacillus velezensis BBC047 in relation to its application before or after Botrytis cinerea infection of tomato plants. The inoculation of BBC047 did not considerably alter the gene expression of the tomato tissues, whereas infection with B. cinerea in BBC047-primed plants induced expression of LRR and NBS-LRR receptors, which are highly related to the ISR response. As expected, B. cinerea infection generated molecular patterns typical of a defense response to pathogen infection as the overexpression of pathogenesis-related proteins (PRs) in leaflets distant to the point of infection. The curative treatment (P + F + B) allowed us to gain insights into plant response to an inverted priming. In this treatment, B. cinerea caused the m tissue damage, extending nearly entirely across the entire infected leaves. Additionally, genes generally associated with early SAR response (<16 h) were overexpressed, and apparently, the beneficial strain was not perceived as such. Therefore, we infer that the plant defense to the curative treatment represents a higher degree of biological stress triggered by the incorporation of strain BBC047 as second arriving microorganism. We highlight the importance the phytosanitary status of plants prior to inoculation of beneficial microorganism for the biocontrol of pathogens.

Keywords: ISR; PGPR; biocontrol; priming; resistance induction.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Gnotobiotic resistance induction assay with strain BBC047 in tomato plants infected with Botrytis cinerea. Six treatments are displayed: control bacteria (CB), control plants (CP), plant + bacterial treatment (P + B); priming treatment (P + B + F), where BBC047 was inoculated 24 h before B. cinerea infection; curative treatment (P + F + B), where tomato plants were infected with B. cinerea and, 24 h later, were inoculated with BBC047; and infection control (P + F), where tomato plants were infected with B. cinerea only.
Figure 2
Figure 2
Effect of tomato root–Bacillus interaction on B. cinerea infection and surfactin C production. (a) Phenotype of representative leaflets per treatment infected with B. cinerea. (b) Adjusted surfactin C production in the four bacterial treatments normalized by the log of the colony-forming units (cfu) per milliliter of medium (cfu/mL) at 24 h. Different letters above the bars represent significant differences between the treatments according to the Tukey test (p < 0.05); n = 3 (three pooled replicates from three individuals each).
Figure 3
Figure 3
Differential gene expression (DGE) analysis by self-organizing map (SOM) and heat map. (a) SOM analysis with six nodes representing unique gene expression patterns in each treatment. In the box plots, lines and horizontal bars represent median, minimum and maximum of gene expression values, respectively. (b) Heat map developed from DGE analysis of gene expression of the four treatments, including SOM clustering identification.
Figure 4
Figure 4
Gene ontology (GO) term enrichment analysis of differential gene expression in the four most informative nodes (N) from SOM analysis. Gene function and relative gene enrichment represent response in the plant in N2-overexpressed genes in the curative treatment (P + F + B), N4-downregulated genes in the curative treatment, N3-overexpressed genes in the infection treatment (P + F) and N6-overexpressed genes in the priming treatment (P + B + F).
Figure 5
Figure 5
Schematic representation of the “plant–bacteria–fungi” pathosystem evaluated in this study. (Top): gene expression profile in P + F and P + F + B at 24 h after B. cinerea infection. A set of pathogenesis-related proteins is activated (left); however, the incorporation of BBC047 into the system (right) generates the worst damage in tissues expressed as genes related to SAR signals, as well as lignin biosynthesis and programed cell death. (Bottom): comparison of molecular response in the P + B and P + B + F treatments. Although few genes were differentially expressed between CP and P + B treatments, the incorporation of B. cinerea induced receptor-like kinases, NBS-LRR, transcription factors and related genes to antioxidant systems. Blue represents expressed genes, and red represents repressed genes.
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