Background Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties. Results Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments. Conclusions These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions.

BackgroundPlants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of these root-associated microbiotas is not well understood. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the US. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soil types.ResultsOur analysis showed that the secretion of BXs affected community composition of rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of the two genetic backgrounds was weaker than that of the presence or absence of BXs, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three soil types. Instead, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae, and enriched various plant pathogenic fungi in the roots.ConclusionsThese findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different field locations. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions.

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