Reprogramming of root cells during nitrogen-fixing symbiosis involves dynamic polysome association of coding and non-coding RNAs

Translational control is a widespread mechanism that allows the cell to rapidly modulate gene expression in order to provide flexibility and adaptability to eukaryotic organisms. We applied TRAP (Translating Ribosome Affinity Purification) combined with RNA sequencing to characterize translational regulation of mRNAs at early stages of the nitrogen-fixing symbiosis established between Medicago truncatula and Sinorhizobium meliloti. Our analysis revealed a poor correlation between transcriptional and translational changes and identified hundreds of regulated protein-coding and long non-coding RNAs (lncRNAs), some of which are regulated in specific cell-types. We demonstrated that a short variant of the lncRNA TAS3 increased its association to the translational machinery in response to rhizobia. Functional analysis revealed that this short variant of TAS3 might act as a target mimic that capture miR390, contributing to reduce tasiARFs production and modulating nodule formation and rhizobial infection. The analysis of alternative transcript variants identified a translationally up-regulated mRNA encoding the subunit 3 of the SUPERKILLER complex (SKI3), which participates in mRNA decay. Knock-down of SKI3 decreased nodule initiation and development, as well as the survival of bacteria within nodules. Our results highlight the importance of translational control and mRNA decay pathways for the successful establishment of the nitrogen-fixing symbiosis.