Root‐exuded benzoxazinoids can alleviate negative plant–soil feedbacks

Abstract

Summary Plants can suppress the growth of other plants by modifying soil properties. These negative plant–soil feedbacks are often species‐specific, suggesting that some plants possess resistance strategies. However, the underlying mechanisms remain largely unknown. Here, we investigated whether benzoxazinoids, a class of dominant secondary metabolites that are exuded into the soil by maize and other cereals, allow maize plants to cope with plant–soil feedbacks. We find that three out of five tested crop species reduce maize (Zea mays L.) performance via negative plant–soil feedbacks relative to the mean across species. This effect is partially alleviated by the capacity of maize plants to produce benzoxazinoids. Soil complementation with purified benzoxazinoids restores the protective effect for benzoxazinoid‐deficient mutants. Sterilization and reinoculation experiments suggest that benzoxazinoid‐mediated protection acts via changes in soil biota. Substantial variation of the protective effect between experiments and soil types illustrates context dependency. In conclusion, exuded plant secondary metabolites allow plants to cope with plant–soil feedbacks. These findings expand the functional repertoire of plant secondary metabolites and reveal a mechanism by which plants can resist negative effects of soil feedbacks. The uncovered phenomenon may represent a promising avenue to stabilize plant performance in crop rotations.

Root-exuded specialized metabolites reduce arsenic toxicity in maize

“…The crystallized benzoxazinoids were dissolved in MilliQ water and complemented to the mutant every 3 d, with a total amount of 1.6 mg of benzoxazinoids per pot per week. This amount corresponds to physiologically relevant doses used in previously published work ( 28 , 32 ), as determined by Gfeller et al 2023 ( 53 ).…”

“…Thus, these findings are not in support of a major role of the soil microbiota in the observed phenotype. Further experiments could focus on testing this hypothesis and investigating the role of soil microbial communities and dynamics in more detail, for instance though sterilization and complementation approaches ( 28 , 53 ).…”

Neighbour-induced changes in root exudation patterns of buckwheat results in altered root architecture of redroot pigweed

“…Species-specific soil chemical legacies also affect the vegetation composition and dynamics through plant-soil feedback effects 74 . Studies show that negative feedback in wheat result in the release of secondary metabolites of the family of the benzoxazinoids 75 . However, more information is needed to suggest that this is what is specifically happening, and further studies would be needed to assess persistence of metabolites within the substrate, the next generation of plants, and consequence of this possible feedback.…”