Genetic variation exists within Zea mays to influence unsustainable nitrogen cycling microbiome function

Abstract

Overuse of synthetic nitrogen fertilizers in agroecosystems causes environmental pollution and human harm at a global level. Nitrogenous fertilizers provide a short-lived benefit to crops in the agroecosystem, but stimulate microbially-mediated nitrification and denitrification, processes that result in N pollution, greenhouse gas (GHG) production, and reduced soil fertility. Recent advances in plant microbiome science suggest that plants can modulate the composition and activity of rhizosphere microbial communities. These rhizosphere communities act as an extended phenotype, primed by genetic variation in the plant host. Genetic variation in traits (e.g., plant secondary metabolites, root architecture, immune system, etc.) act as mechanistic selective agents on the composition of the microbiome. Here we attempted to determine whether genetic variation exists in Zea mays for the ability to influence the extended phenotype of rhizosphere soil microbiome composition and function. Specifically, we determined whether plants’ influence on soil nitrogen cycling activities was altered by plant genetics and thereby allowing it to be incorporated into breeding practices. To capture an extensive amount of genetic diversity within maize we sampled the rhizosphere microbiome of a germplasm chronosequence that included ex-PVP inbreds, hybrids, and teosinte (Z. mays ssp. mexicana and Z. mays ssp. parviglumis). We observed that potential N cycling processes were influenced by plant genetics. Teosinte and some hybrid genotypes supported microbial communities with lower potential nitrification and potential denitrification activity in the rhizosphere, while inbreds stimulated/did not inhibit these undesirable N-cycling activities. These potential differences translated to functional differences in N₂O production, with teosinte plots producing less GHG than maize plots. Furthermore, within these Zea cultivars we found that plant genetics explained a significant amount of variation in the microbiome, particularly among different nitrification and denitrification functional genes within the community. We found that potential nitrification, potential incomplete denitrification, and overall denitrification rates, but not abundance of N-cycling genes of rhizosphere soils were influenced by growth stage and plant genetics. Taken together, these results suggest that crop selection can lead to changes in root phenotypes that could suppress unsustainable N-cycling processes. Reintroducing stress-adapted and “wild” root characteristics into modern germplasm may be a way to manipulate soil microbiomes at both a composition and functional level to improve sustainability.