By changing soil properties, plants can modify their growth environment. Although the soil microbiota is known to play a key role in the resulting plant-soil feedbacks, the proximal mechanisms underlying this phenomenon remain unknown. We found that benzoxazinoids, a class of defensive secondary metabolites that are released by roots of cereals such as wheat and maize, alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next plant generation. Complementation experiments demonstrate that the benzoxazinoid breakdown product 6-methoxy-benzoxazolin-2-one (MBOA), which accumulates in the soil during the conditioning phase, is both sufficient and necessary to trigger the observed phenotypic changes. Sterilization, fungal and bacterial profiling and complementation experiments reveal that MBOA acts indirectly by altering root-associated microbiota. Our results reveal a mechanism by which plants determine the composition of rhizosphere microbiota, plant performance and plant-herbivore interactions of the next generation.

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.

Phosphorus (P) crop fertilization requires optimal management to avoid the waste of a nonrenewable resource and water pollution, but current methods for assessing soil phyto-available P and plant P requirements are not sufficiently precise to meet this goal. The objectives of the present study were to (1) evaluate the effect of long-term P fertilization on the grain yield of winter wheat, maize, and rapeseed, (2) validate or establish models of critical shoot P concentration (P C ) based on relationships of shoot P concentration with either shoot biomass or shoot nitrogen (N) concentration, and (3) assess both plantbased and soil-based diagnostic tools for managing P fertilization. A long-term field experiment with contrasted P fertilizer treatments, established in 1971 by Agroscope in Changins (Switzerland), was used to measure the shoot biomass and P concentration of winter wheat in 2011, maize in 2012, and rapeseed in 2014 weekly during the growing period and the grain yield at harvest. Soil available P in the 0-0.20 m soil layer was assessed by three chemical extractions: ammonium acetate EDTA (P-AAE), sodium bicarbonate (P-NaHCO 3 ), and CO 2 -saturated water (P-CO 2 ). Long-term P fertilization increased soil available P extracted by P-CO 2 (? 24%), P-AAE (? 200%), and P-NaHCO 3 (? 155%), shoot growth and grain yield by 8.4% and 26.2% for winter wheat and rapeseed respectively but had no effect on maize. The relationships between P C and shoot biomass or N concentration were described respectively by allometric and linear models (R 2 [ 0.85, n = 21, 28 and 32 for winter wheat, maize and rapeseed respectively; slope P values for linear models \ 0.05). The P Cshoot N concentration model (slope: 0.083, intercept: 0.88) for winter wheat confirmed results from previous studies and can be used for calculating the P nutrition index. For the three soil available P indicators, threshold values needed to achieve 95% of the maximum yield for the three crops were less than those currently used in the official fertilization guidelines in Switzerland. Our results obtained after 44 years of contrasted P fertilization confirm the relationship between P C and shoot N concentration for grain crops and the need to revise P fertilizer recommendations based on currently used soil P tests.