Locating the microbes along the maize root system under low nitrogen: a root phenotyping approach

Background and Aims. One major challenge in agriculture is the low nitrogen uptake efficiency (NUpE) of maize (Zea mays), which poses environmental and economic costs. The utility of root phenotypes to improve nitrogen uptake is an active research field which promises to be applicable to maize breeding aiming to reduce nitrogen losses from fertilizer application. However, synergies between root phenotypes and root microbes to favor environmental-friendly nitrogen cycling are less understood and explored. Methods. With the purpose of characterizing the spatial distribution of the prokaryotic microbiome composition and abundance in relation with root architecture and anatomy, we studied the microbiome of 4-week-old maize plants growing in 30 L mesocosms under reduced nitrogen inputs. Two sandy soil mixtures containing either agricultural or grassland soils were used, allowing for the root architecture and anatomy to be fully expressed. We destructively collected root and soil samples at different depths (0-20, 20-70, 70-150 cm), root classes (lateral, axial) and root types (seminal and nodal) at harvest, measured plant growth response to stress, and performed 16S rRNA gene metabarcoding of extracted DNA from bulk and rhizosphere soil, and root tissue. Key Results. Plants allocated roots to deeper soil strata under low-nitrogen conditions. All experimental factors were significant determinants of the prokaryotic ß-diversity, with soil mixture explaining around 40% of the variance, followed by bulk soil/rhizosphere/endosphere compartment (~12%), sampling point (~5%) and nitrogen stress (~2%). Lateral root branching density explained ~10% and of this variance in the rhizosphere and the endosphere. We report prokaryotic genera with increased or decreased relative abundance with depth, by soil-root compartment, root class, root types and root phenotypes under low nitrogen. Conclusions. The maize root microbiome varies by sampling point and depth, with different values of the root architectural phenotypes lateral root branching density and length, in a soil-mixture and nitrogen stress dependent fashion. The presented mesocosm are experimental systems useful to study maize root phenotypes in association with microbial communities in a system that allows for interactions with soil gradients, and clear soil-root compartmentalization.