Plant secondary metabolite-dependent plant-soil feedbacks can improve crop yield in the field

Abstract

Plant secondary metabolites that are released into the rhizosphere alter biotic and abiotic soil properties, which in turn affect the performance of other plants. How such plant-soil feedbacks affect agricultural productivity and food quality in crop rotations is unknown. Here, we assessed the impact of maize benzoxazinoids on the performance, yield and food quality of three winter wheat varieties in a two-year field experiment. Following maize cultivation, we detected benzoxazinoid-dependent chemical and microbial fingerprints in the soil. The chemical fingerprint was still visible during wheat growth, while the microbial fingerprint was no longer detected. Benzoxazinoid soil conditioning by wild-type maize led to increased wheat emergence, tillering, growth and biomass compared to soil conditioning by bx1 mutant plants. Weed cover remained unaffected, while insect damage decreased in a subset of varieties. Wheat yield was increased by over 4% without reduction in grain quality across variety. This improvement was directly associated with increased germination and tillering. Taken together, our experiments demonstrate that plant secondary metabolites can increase yield via plant-soil feedbacks under agronomically realistic conditions. If this phenomenon holds across different soils and environmental conditions, optimizing plant root exudation could be a powerful, genetically tractable strategy to enhance crop yields without additional inputs.

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

“…We had originally discovered benzoxazinoid-dependent and microbe-driven feedbacks on plant performance in controlled conditions 11 and recently, we show that they also operate in field conditions increasing wheat yield in certain soils 38 . The latter suggest that microbial feedbacks are agriculturally relevant and highlights that plant specialised metabolites present a strong tool for leveraging microbiome functions.…”

“…The finding that AMPO-forming bacteria were less abundant in the wheat root microbiomes may appear surprising but is consistent with the MBOA levels in the rhizosphere of this wheat variety. More than 10x less MBOA (~5 ng/mL) was found in the rhizosphere of CH Claro compared to maize (~60 ng/mL) 38 . Hence, we think that the much lower levels of MBOA in the rhizosphere of CH Claro resulted in a much lower selection of AMPO formers.…”

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

“…In our work, we find that one single group of secondary metabolites controlled by one single gene (Bx1) determines the resistance of maize against negative plant-soil feedbacks. Given that the same metabolites can increase agricultural productivity of the following crop (Gfeller et al, 2022), this makes the genes involved in biosynthesis and exudation of such metabolites a potential breeding target for superior crop rotations. Many maize lines already produce substantial amounts of benzoxazinoids in their roots, but substantial genetic variation is commonly observed (Handrick et al, 2016).…”

“…Benzoxazinoids extracted from soils and the purified benzoxazinoid mixture from germinated maize kernels were analysis as described before (Gfeller et al, 2022). In short, an Acquity UHPLC system coupled to a G2-XS QTOF mass spectrometer equipped with an electrospray source and piloted by the software MassLynx 4.1 (Waters AG, Baden-Dättwil, Switzerland) was used.…”

“…For benzoxazinoids and flavones these changes were linked to the performance of succeeding conspecific plants (Hu et al, 2018b;Yu et al, 2021). Through plant-soil feedbacks, the trait of benzoxazinoid exudation in maize also affects wheat performance under controlled conditions and improves wheat yield under field conditions (Cadot et al, 2021a;Gfeller et al, 2022). Considering that benzoxazinoids can structure the rhizosphere microbiome of maize already at the seedling stage (Cotton et al, 2019;Kudjordjie et al, 2019), that benzoxazinoids can act fungistatic against soil pathogens (Wilkes et al, 1999;Martyniuk et al, 2006), and that benzoxazinoids can attract a Pseudomonas putida strain that potentially induces plant resistance (Neal et al, 2012;Neal & Ton, 2013), we hypothesize that they could also increase crop rotation stability by alleviating negative plant-soil feedbacks.…”