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Phytoalexins play a crucial role in plant immunity. However, the mechanism of how phytoalexin is primed by beneficial microorganisms against broad‐spectrum pathogens remains elusive. This study showed that Bacillus cereus AR156 could trigger ISR against broad‐spectrum disease. RNA‐sequencing and camalexin content assays showed that AR156‐triggered ISR can prime the accumulation of camalexin synthesis and secretion‐related genes. Moreover, it was found that AR156‐triggered ISR elevates camalexin accumulation by increasing the expression of camalexin synthesis genes upon pathogen infection. We observed that the priming of camalexin accumulation by AR156 was abolished in cyp71a13 and pad3 mutants. Further investigations reveal that in the wrky33 mutant, the ability of AR156 to prime camalexin accumulation is abolished, and the mediated ISR against the three pathogens is significantly compromised. Furthermore, PEN3 and PDR12, acting as camalexin transporters, participate in AR156‐induced ISR against broad‐spectrum pathogens differently. In addition, salicylic acid and JA/ET signalling pathways participate in AR156‐primed camalexin synthesis to resist pathogens in different forms depending on the pathogen. In summary, B. cereus AR156 triggers ISR against Botrytis cinerea, Pst DC3000 and Phytophthora capsici by priming camalexin synthesis. Our study provides deeper insights into the significant role of camalexin for AR156‐induced ISR against broad‐spectrum pathogens. Summary statement: Beneficial rhizobacterium AR156 triggered ISR by enhancing camalexin accumulation in Arabidopsis, with WRKY33 acting as a positive regulator. PEN3 and PDR12 are involved in AR156‐induced ISR. Salicylic acid and JA/ET signalling pathways participate in AR156‐primed camalexin synthesis to resist various pathogens. [ABSTRACT FROM AUTHOR]

[Display omitted] • Bacillus amyloliquefaciens HSSN09 with antagonistic effect on FON was isolated. • B. amyloliquefaciens HSSN09 could effectively control watermelon Fusarium wilt and promote the growth of watermelon seedlings. • Tacrolimus has a very obvious antifungal effect and can be used to control watermelon Fusarium wilt. • Tacrolimus was also able to stimulate the growth of watermelon seedlings. • Tacrolimus or its analogs may play a role as a pleiotropic factor in B. amyloliquefaciens HSSN09 biological control. Watermelon Fusarium wilt caused by Fusarium oxysporum f. sp. niveum (FON) is one of the most devastating diseases in watermelon production. Biological control approaches are efficient and environmentally-friendly, thus have aroused broad interest. However, only a few biocontrol factors/molecules have been characterized due to varied genomes and diversified secreted secondary metabolites of biocontrol microorganisms. We report the screen and identification of a Bacillus amyloliquefaciens strain HSSN09 with high antagonism to FON and watermelon growth promotion capacity. B. amyloliquefaciens HSSN09 and its secondary metabolites showed inhibition on FON mycelial growth, spore formation and spore germination. Metabolomes of the highly antagonistic strain B. amyloliquefaciens HSSN09, medium antagonistic strain B. amyloliquefaciens FGW53, weakly antagonistic strain B. subtilis JC03 and non-antagonistic strain B. cereus FGW109 were compared with LC-MS/MS. By antagonistic assay, tacrolimus was screened out among the 531 molecules that appeared in the sequencing results of HSSN09 metabolome but not in that of the non-antagonistic strain without significant inhibition on the growth of FON. Among the four tested Bacillus strains, tacrolimus analogue was only observed in the supernatant of HSSN09 by HPLC and MALDI-TOF-MS. We further confirmed the ability of tacrolimus to suppress FON and promote watermelon seedling growth. [ABSTRACT FROM AUTHOR]