Streptomycetes are Gram-positive actinobacteria largely represented in the plant root microbiota. The genetic determinants involved in the adaption of Streptomyces in the rhizosphere environment are mostly unknown but can rely on the ability to release phytohormones, degrade plant cell-wall polysaccharides and produce specialised metabolites notably involved in microbial competition. Here we sequenced the genome of the rhizospheric and plant defence-stimulating strain Streptomyces sp. AgN23. We found out that it belongs to the soil and plant root dwelling S. violaceusniger clade. The genome annotation of AgN23 revealed the genetic potential of the bacterium to degrade plant cell wall with a large repertoire of carbohydrate degrading enzymes, to synthesise auxin, a major regulator of plant development, and to produce antimicrobials (rustmicin, mediomycin, niphimycin, nigericin) and plant bioactive compounds (nigericin, echosides, elaiophylin) through a set of biosynthetic gene clusters. We also found that these genomic features are well-conserved among members of the S. violaceusniger clade. In addition, AgN23 display original events of biosynthetic gene clusters acquisitions and losses which may account for its interaction with plants. Taken together, our work supports the hypothesis that evolution of large conserved hydrolytic enzymes directed against plant polymers and specialised metabolites repertoires can mediate the adaptation of S. violaceusniger strains to the rhizopsheric ecological niches.