| Summary: | <i>Bacillus velezensis</i> manifests robust biocontrol activity against fungal plant pathogens; however, its antiviral activity has rarely been investigated. <i>Bacillus velezensis</i> strain PEA1 was isolated, characterized, and evaluated for antifungal and antiviral activities against <i>Fusarium oxysporum</i> MT270445 and cucumber mosaic virus (CMV) MN594112. Our findings proved that strain PEA1 had intense antagonist activity against <i>F.</i><i>oxysporum</i>. Under greenhouse conditions, the antiviral activities (protective, curative, and inactivation) of PEA1-culture filtrate (CF) on <i>Datura stramonium</i> plants were assayed, using a half-leaf method. The inactivation treatment exhibited the highest inhibition rate (97.56%) and the most considerable reduction of <i>CMV-CP</i> accumulation levels (2.1-fold) in PEA1-CF-treated plants when compared with untreated plants (26.9-fold). Furthermore, PEA1-CF induced systemic resistance with significantly elevated transcriptional levels of <i>PAL</i>, <i>CHS</i>, <i>HQT</i>, <i>PR-1</i>, and <i>POD</i> genes in <i>D</i>. <i>stramonium</i> leaves after all treatments. Gas chromatography‒mass spectrometry analysis showed that pyrrolo[1,2-a]pyrazine-1,4-dione is the main compound in the PEA1-CF ethyl acetate extract, which may act as an elicitor molecule that induces plant systemic resistance and inhibits both fungal growth and viral replication. Consequently, <i>B. velezensis</i> can be considered as a potential source for the production of bioactive compounds for the management of plant diseases. To our knowledge, this is the first report of the antiviral activity of <i>B</i>. <i>velezensis</i> against plant viral infection.
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