Root photosynthate allocation and root developmental stage interactively determine spatial patterns in the maize rhizosphere microbiota

The underlying mechanisms of microbiome assembly resulting in spatial patterns of the rhizosphere microbiota within individual root systems are not well understood. We hypothesised that the distribution of photosynthates in the root system is of central importance to shape the rhizosphere microbiota. Using maize, we analysed variation in the prokaryotic, fungal and protist communities in dependence on the spatial distribution of fresh photosynthates. We visualized fresh photosynthates in the root system by combining the non-invasive 3D imaging techniques radioactive 11CO2 labelling with subsequent positron emission tomography (PET) and magnetic resonance imaging (MRI). Imaging revealed a highly heterogeneous belowground distribution of photosynthates, with accumulations at root tips, most prominently at those of recently emerged crown roots. Guided by the images, we collected rhizosphere samples from different root sections and types with distinct photosynthate allocation patterns. Amplicon sequencing revealed that the community structure of prokaryotes, fungi and protists was influenced by root type/section and photosynthate allocation, individually as well as interactively. Heterogeneities at root tips were related to differences in photosynthate allocation, while differences between root types turned out to be the result of successive developments in the microbiota of a growing root system, also related to photosynthate allocation. Thus, root photosynthate allocation and root development jointly contribute to rhizosphere microbiota assembly.