Soil iron drives beneficial maize microbiome feedbacks inrotations with wheat

Abstract

BackgroundPlants change their surrounding soil microbiome by root exudates and such conditioned microbiomes impact the performance of the present as well as the next plant generation as for example in crop rotations. The big challenge is that such microbiome feedbacks are highly context-dependent, i.e. they vary in strength and direction dependent on the local soil environment - of which the driving factor(s) remain unknown. Including maize in crop rotations involves benzoxazinoids (BXs), which are exuded from roots and alter the soil microbiome, which in turn affects growth and defence of the following crop. ResultsHere, we grew wild-type and BX-depleted maize in the field to differentially condition their soil microbiome and we found varying feedbacks on wheat performance dependent on the local physicochemical soil parameters. Using multivariate, correlation and modelling approaches and including additional data from two previous field experiments, we identified plant-available (PA) iron to explain BX-dependent microbiome feedbacks on wheat. The BX-conditioned soil microbiome caused wheat to grow taller at low levels of soil PA-iron but smaller at high levels. This finding was generalized testing these maize microbiome feedbacks on the model plant Arabidopsis thaliana using soil batches containing different levels of iron. Consistent with wheat, a significant inverse relationship between soil PA-iron levels and plant growth was found. This relationship was experimentally validated with Arabidopsis grown at low levels of soil iron where iron supplementation abolished the beneficial feedback of the BX-conditioned soil microbiome. ConclusionTogether these findings revealed that beneficial microbiome feedbacks occur at low levels of plant-available iron, i.e. when plants grow in a suboptimal soil, but they are lost when plants are nutritionally well supported. These results underscore the importance of iron availability in soil for beneficial microbial feedbacks on plant growth and predict agronomic benefits of incorporating maize in crop rotations on low iron soils.