Single-cell resolution transcriptome atlases of soybean root organs reveal new regulatory programs controlling the nodulation process

Abstract The soybean root system is complex. In addition to being composed of various cell types, the soybean root system is also composed of the nodule, an organ in which mutualistic symbiosis with the nitrogen-fixing bacterium Bradyrhizobium diazoefficiens occurs. Notably, the soybean root nodule is characterized by a central infection zone where the atmospheric nitrogen is fixed and assimilated by the symbiont, resulting from the close cooperation between the plant cell and the bacteria. To date, the cellular complexity of the soybean root and nodule has not been characterized. Applying single nucleus RNA-seq technology, we characterized the transcriptomic signature of the soybean root and nodule cell types and revealed the existence of different sub-populations of B. diazoefficiens-infected cells in the soybean nodule including those actively involved or not in nitrogen fixation. The mining of the single cell-resolution atlas also helped reevaluate the role of known and identified new genes controlling the nodulation process. For instance, we functionally characterized the role of a new microdomain-associated GmFWL3 protein in the soybean nodule. Our study reveals the unique cellular complexity of the soybean nodule and helps redefine the concept of cell types when focusing on the infection zone of the nodule.