Linking spatial patterns of the rhizosphere microbiota with photosynthate dynamics in maize roots

Abstract

The rhizosphere serves as the boundary layer between plant roots and soil, enabling nutrient and water uptake while facilitating interactions with microorganisms through rhizodeposition. Despite its importance for plant health, the spatiotemporal dynamics of rhizodeposition and their effect on microbial community assembly in the rhizosphere remain poorly understood, particularly in functionally complex root systems. To bridge this gap, we investigated how spatial patterns of photosynthate distribution impact the assembly of prokaryotic, fungal, and cercozoan rhizosphere microbiomes in the maize rhizosphere. <br/> Firstly, we explored small-scale spatial variation in the prokaryotic community within the maize rhizosphere, rhizoplane and endosphere. By combining the non-invasive root system monitoring technique magnetic resonance imaging (MRI) with 16S rRNA amplicon sequencing, we identified spatial patterns in prokaryotic diversity and community structure that varied sequentially across root types, along root longitudinal sections, as well as with root growth rates and root age. The consistency of these patterns across three different soil textures suggested the presence of conserved mechanisms governing microbiome spatial organization. <br/> Secondly, we linked the spatial patterns of the rhizosphere microbiota to root photosynthate distribution. By labeling fresh photosynthates with the radioactive isotope ¹¹C and visualizing allocation via positron emission tomography (PET) and MRI, we found that photosynthate distribution is highly heterogeneous, varying between root types, along the root axis, and over time, with pronounced accumulations at young crown root tips. Corresponding labeling with and quantification of the stable isotope ¹³C in root tissue and the rhizosphere revealed similar patterns, implying that root-internal photosynthate levels regulate rhizodeposition. Amplicon sequencing confirmed that these heterogeneities significantly shape prokaryotic, fungal and cercozoan rhizosphere communities, fueling colonization differences between root types and sections. Variability at root tips arose from heterogeneous photosynthate allocation and priority effects, while microbial patterns at root bases reflected succession during root maturation and shifting photosynthate distribution. Using DNA stable isotope probing (DNA-SIP), we identified prokaryotic, fungal and cercozoan consumers of ¹³C-labeled photosynthates and found that specific consumer taxa profited in distinct regions with varying photosynthate allocation. This indicates that photosynthate heterogeneities, along with root architectural traits, drive microhabitat formation and thus niche differentiation, as well as microbial food web establishment in the complex root system of maize. <br/> Overall, our findings highlight the critical role of spatially heterogeneous photosynthate allocation in shaping the rhizosphere microbiome. This introduces a new mechanism governing microbial colonization of the rhizosphere but also deepens our understanding of spatiotemporal rhizosphere organization, paving the way for future strategies to enhance plant health and resilience.