Root-exuded secondary metabolites can alleviate negative plant-soil feedbacks

Abstract

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 if and how benzoxazinoids, a class of dominant secondary metabolites that are exuded into the soil by maize and other cereals, help plants to resist negative plant-soil feedbacks. We find that three out of five tested crop species suppress maize performance relative to the mean across species. This effect is partially alleviated by the plant's capacity to produce benzoxazinoids. Soil complementation of benzoxazinoid-deficient mutants with purified benzoxazinoids is sufficient to restore the protective effect. Sterilization and reinoculation experiments suggest that benzoxazinoid-mediated protection acts via changes in soil microbes. Substantial variation of the protective effect between experiments and soil types illustrates that the magnitude of the protective effect of benzoxazinoids against negative plant-soil feedbacks is context dependent. In summary, our study demonstrates that plant secondary metabolites can confer resistance to negative plant-soil feedbacks. These findings expand the functional repertoire of plant secondary metabolites, reveal a mechanism by which plants can resist suppressive soils, and may represent a promising avenue to stabilize plant performance in crop rotations in the future.

A trait‐based framework linking the soil metabolome to plant–soil feedbacks

“…More recently, Gfeller et al (2023b) showed that wheat plants grown in the field on soil conditioned by a maize genotype capable of releasing root benzoxazinoids had more reproductive tillers, leading to higher grain yield. Root-emitted benzoxazinoids have also been shown to increase maize resistance to negative PSF (Gfeller et al, 2023a). These studies demonstrate the important role of the soil biota and belowground chemical interactions in mediating PSF.…”

Soil chemical and microbial gradients determine accumulation of root‐exuded secondary metabolites and plant–soil feedbacks in the field

“…Plant–soil feedbacks are well known to depend on the environmental context, the responsible mechanisms are, however, only partly understood (Gfeller, Thönen, et al, 2023; van der Putten et al, 2013; Smith‐Ramesh & Reynolds, 2017). Plant nutrient supply, for example, can influence the outcome of plant–soil feedbacks in crops and wild plants (Kos et al, 2015a; Kuerban et al, 2022).…”

“…They are long known to be involved in allelopathy and defence against insects and pathogens (Niemeyer, 2009; Schandry & Becker, 2020). More recently, they have been shown to alleviate plant growth‐suppressive effects provoked by preceding plants (Gfeller, Thönen, et al, 2023). They can also chelate iron and aluminium (Hu, Mateo, et al, 2018; Zhao et al, 2019; Zhou et al, 2018).…”

Getting to the root of divergent outcomes in the modulation of plant–soil feedbacks by benzoxazinoids

“…This process may also feedback to shape the microbial community by influencing the accessibility of iron to rhizosphere microbes. DIMBOA is in turn degraded to MBOA (3), which is the most abundant benzoxazinoid in the maize rhizosphere due to its greater stability (Hu et al, 2018;Gfeller et al, 2024, this issue of New Phytologist, pp. 2575-2588.…”

“…1). In a paper published in this issue of New Phytologist, Gfeller et al (2024;2575-2588 demonstrate that the production of benzoxazinoids can protect maize plants from heterospecific PSFs associated with several cover crops commonly grown in rotation with maize (Gfeller et al).…”