A Galbonolide-producing Streptomyces reconfigures the plant root microbiota by activating salicylate-dependent defence metabolism
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Streptomyces sp. AgN23 is an epiphytic rhizobacterium that establishes in the Arabidopsis rhizosphere by activating plant immune responses. This activity depends on the secretion of polyketide galbonolides, which inhibit host inositol phosphoceramide synthase (IPCS) and thereby perturb sphingolipid homeostasis. However, the downstream signalling events linking IPCS inhibition to AgN23 enrichment in the rhizosphere remain unclear. Here, we show that AgN23 activates ethylene- and salicylic acid-dependent immune signalling, leading to coordinated stimulation of phenylalanine- and tryptophan-derived secondary metabolism. Using Arabidopsis mutants defective in these pathways, we show that these metabolites mitigate AgN23-induced root growth inhibition. We further show that the npr1 mutant is strongly compromised in AgN23-triggered secondary metabolic responses, resulting in reduced rhizosphere colonization by AgN23. By comparing rhizosphere microbiota from wild-type and npr1 plants, we distinguished direct AgN23 effects linked to intermicrobial competition from indirect effects mediated by host metabolic activation. In particular, AgN23 colonization occurred at the expense of several Streptomycetaceae ASVs and coincided with changes in bacterial and fungal taxa belonging to Flavobacteriaceae and Mucoromycota . Together, these findings define a mechanistic framework in which Streptomyces AgN23 interacts with NPR1-dependent signalling to reprogram root metabolism and rhizosphere community structure, notably through the production of specialized metabolites such as galbonolides.
HIGHLIGHTS
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AgN23 root activity requires functional salicylate and ethylene signalling, but not jasmonate signalling.
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Salicylate pathway activation supports AgN23 rhizosphere colonization.
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AgN23 induces phenylalanine- and tryptophan-derived secondary metabolites that alleviate root growth inhibition.
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AgN23 reprogramming of the rhizosphere microbiota largely relies on NPR1 mediated responses to the Streptomyces .
SIGNIFICANCE
Plant roots interact with diverse microbial communities that support nutrition and enhance resilience to abiotic and biotic stresses. Engineering these communities is increasingly viewed as a key strategy for sustainable crop production. Beneficial microbes are often recruited through root exudation in a plant-driven “cry for help” process, yet the molecular mechanisms guiding this selective assembly remain incompletely understood. Here, we show that Streptomyces AgN23, a beneficial soil bacterium that produces antimicrobial and plant defence elicitor compounds such as galbonolides, exploits host immune signalling to establish itself in the rhizosphere and remodel the surrounding microbiota. AgN23 activates ethylene- and salicylic acid-dependent pathways in Arabidopsis , requiring the key signalling components EIN2 and NPR1, respectively. This immune activation triggers coordinated reprogramming of root metabolism that facilitates AgN23 growth, while also promoting phenylalanine- and tryptophan-derived secondary metabolites that mitigate root growth inhibition triggered by AgN23. By manipulating host metabolic outputs, AgN23 influences the composition of the root-associated community and secures its ecological niche. Given that Streptomyces species are consistently enriched in plants exposed to pathogens or drought, our findings support a model in which stress-associated Streptomyces leverage plant signalling hubs to thrive in the rhizosphere and participate in the assembly of a protective microbiota.
Abstract Figure
Graphical abstractModel summarizing how galbonolides secreted by Streptomyces AgN23 activate ethylene and salicylic acid signalling pathways in Arabidopsis , leading to a coordinated reprogramming of root metabolism that supports AgN23 development in the rhizosphere and reshapes the resident microbiota. Galbonolide-induced responses require the phytohormone signalling components EIN2 and NPR1. NPR1 is required to induce the biosynthesis and rhizosphere release of exudates that promote AgN23 growth. In parallel, Streptomyces -triggered production of phenylalanine- and tryptophan-derived secondary metabolites mitigates root growth inhibition and contributes to rhizosphere microbiota restructuring.
