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Driven by climate change, Fusarium ear rot (FER) caused by Fusarium verticillioides occurs frequently in maize worldwide. In parallel, legislative regulations and increasing environmental awareness have spurred research on alternative FER biocontrol strategies. A promising group of bacterial control agents is Streptomyces species due to their metabolic versatility. However, insights into the molecular modes of action of these biocontrol agents are often lacking. This study aims at unraveling the biocontrol efficacy of Streptomyces rhizobacterial strains against F. verticillioides. We first assessed the direct antagonism of four Streptomyces strains ST02, ST03, ST07, and ST08. Then, a profile of 16 genes associated with intrinsic plant defense signaling was assessed in maize plants. Both in vitro and in vivo data showed that the biocontrol strain ST03 perfectly suppressed the growth of F. verticillioides. High inhibition efficacy was also observed for extracellular compounds in the supernatant secreted by this strain. Especially, for maize cobs, the biocontrol strain ST03 not only inhibited the proliferation of F. verticillioides but also significantly repressed fungal fumonisin production 7 days after inoculation. On maize plants, the direct antagonism was confirmed by a significant reduction of the fungal DNA level in soils when co-applied with F. verticillioides and strain ST03. In terms of its action on plants, strain ST03 induced downregulation of auxin responsive genes (AUX1 , ARF1 , and ARF2) and gibberellic acid (GA)-related gene AN1 even in the absence of F. verticillioides at early time points. In leaves, the biocontrol strain induced the expression of genes related to salicylic acid (SA), and 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA)-mediated pathways, and pathogenesis-related proteins in the presence or absence of the pathogen. Interestingly, the biocontrol strain significantly promoted plant growth even in the presence of F. verticillioides. All of which demonstrated that the Streptomyces strain ST03 is a promising FER biocontrol and a growth-promoting candidate. Streptomyces strains promote plant growth and induce resistance against Fusarium verticillioides via transient regulation of auxin signaling and archetypal defense pathways in plants. [ABSTRACT FROM AUTHOR]