6 research outputs found

    Benzoxazinoids: a model for the repeated evolution of specialized metabolite biosynthesis in plants

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    Specialized metabolites are critical for plant interactions with the environment. While many metabolites are lineage-specific, independent evolution has led to identical compounds arising in distant taxa. Benzoxazinoids (BXD) exemplify this, occurring sporadically across angiosperms. Initially characterized in Zea mays (Poaceae - monocots), BXD serve as defense compounds, allelochemicals, and phytosiderophores. However, BXD biosynthesis in eudicots remained largely unknown. Through metabolomic and transcriptomic analyses, we uncovered BXD biosynthesis in three eudicot families: Acanthaceae, Lamiaceae, and Ranunculaceae. Although the biosynthetic pathways involve analogous reactions, the enzymes involved belong to distinct classes, distinct cytochrome P450 and UDP-glucosyltransferase families, as well as independently evolved 2-oxoglutarate-dependent dioxygenases, and O-methyltransferases. Phylogenetic analysis showed that BXD biosynthetic pathway evolved independently in Poaceae, Acanthaceae, Lamiaceae and Ranunculaceae. We further identified, in core eudicots, a pseudoenzyme, TSB-like, that mediates indole production by allosterically activating the tryptophan synthase α-subunit. TSB-like is a paralog of the canonical tryptophan synthase β-subunit, but lacks tryptophan biosynthetic activity. This pseudoenzyme is involved in the production of indole for BXD biosynthesis but its wider expression profile suggests a broader role in indole biosynthesis in core eudicots also for defense and pollinator attraction. Additionally, Z. mays exudes high levels of BXD in the soil, which result in the accumulation of the antimicrobial benzoxazolinone MBOA. The root-associated microbiota of Z. mays is enriched with bacteria strains able of catabolizing and metabolizing MBOA to the allelopathic aminophenol AMPO. We identified a N-acyl homoserine lactonase that catalyzes the conversion of MBOA to AMPO, enabling the adaptation of Z. mays root-associated bacteria to BXD

    The lactonase BxdA mediates metabolic specialisation of maize root bacteria to benzoxazinoids.

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    Root exudates contain specialised metabolites that shape the plant's root microbiome. How host-specific microbes cope with these bioactive compounds, and how this ability affects root microbiomes, remains largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound in the maize rhizosphere MBOA (6-methoxybenzoxazolin-2(3H)-one) and formed AMPO (2-amino-7-methoxy-phenoxazin-3-one). AMPO forming bacteria were enriched in the rhizosphere of benzoxazinoid-producing maize and could use MBOA as carbon source. We identified a gene cluster associated with AMPO formation in microbacteria. The first gene in this cluster, bxdA encodes a lactonase that converts MBOA to AMPO in vitro. A deletion mutant of the homologous bxdA genes in the genus Sphingobium, did not form AMPO nor was it able to use MBOA as a carbon source. BxdA was identified in different genera of maize root bacteria. Here we show that plant-specialised metabolites select for metabolisation-competent root bacteria. BxdA represents a benzoxazinoid metabolisation gene whose carriers successfully colonize the maize rhizosphere and thereby shape the plant's chemical environmental footprint

    The lactonase BxdA mediates metabolic adaptation of maize root bacteria to benzoxazinoids

    No full text
    Root exudates contain secondary metabolites that affect the plant’s root microbiome. How microbes cope with these bioactive compounds, and how this ability shapes root microbiomes remain largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound (6-methoxy-benzoxazolin-2-one, MBOA) in the maize rhizosphere to 2-amino-7-methoxyphenoxazin-3-one (AMPO). By contrast, bacteria isolated from Arabidopsis, which does not produce benzoxazinoids, were unable to metabolise MBOA. Among Microbacteria strains, this differential metabolisation allowed to identify a conserved gene cluster containing the lactonase bxdA. BxdA converts MBOA to AMPO in vitro and we show that this capacity provided bacteria a growth benefit under carbon-limiting conditions. Together these results reveal that maize root bacteria - through BxdA - are metabolically adapted to the benzoxazinoids of their host. We propose that metabolic adaptation to plant-specialised compounds shapes root bacterial communities across the plant kingdom

    The lactonase BxdA mediates metabolic specialisation of maize root bacteria to benzoxazinoids

    No full text
    Root exudates contain specialised metabolites that shape the plant’s root microbiome. How host-specific microbes cope with these bioactive compounds, and how this ability affects root microbiomes, remains largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound in the maize rhizosphere MBOA (6-methoxybenzoxazolin-2(3H)-one) and formed AMPO (2-amino-7-methoxy-phenoxazin-3-one). AMPO forming bacteria were enriched in the rhizosphere of benzoxazinoid-producing maize and could use MBOA as carbon source. We identified a gene cluster associated with AMPO formation in microbacteria. The first gene in this cluster, bxdA encodes a lactonase that converts MBOA to AMPO in vitro. A deletion mutant of the homologous bxdA genes in the genus Sphingobium, did not form AMPO nor was it able to use MBOA as a carbon source. BxdA was identified in different genera of maize root bacteria. Here we show that plant-specialised metabolites select for metabolisation-competent root bacteria. BxdA represents a benzoxazinoid metabolisation gene whose carriers successfully colonize the maize rhizosphere and thereby shape the plant’s chemical environmental footprint
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