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

Authors: TRAUBENIK, SOLEDAD - National University Of Laplata; REYNOSO, MAURICIO - National University Of Laplata; HOBECKER, KAREN - National University Of Laplata; LANCIA, MARCOS - National University Of La Plata; HUMMEL, MAUREEN - University Of California; Rosen, Benjamin - Ben; TOWN, CHRISTOPHER - National University Of Laplata; BAILEY-SERRES, JULIA - University Of California; BLANCO, FLAVIO - National University Of Laplata; ZANETTI, MARIA - National University Of Laplata

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/10/2019
Publication Date: 2/20/2020
Citation: Traubenik, S., Reynoso, M.A., Hobecker, K.V., Lancia, M., Hummel, M., Rosen, B.D., Town, C., Bailey-Serres, J., Blanco, F.F., Zanetti, M.E. 2020. Reprogramming of root cells during nitrogen-fixing symbiosis involves dynamic polysome association of coding and non-coding RNAs. The Plant Cell. 32:352-373. https://doi.org/10.1105/tpc.19.00647.
DOI: https://doi.org/10.1105/tpc.19.00647

Interpretive Summary: The nitrogen-fixing endosymbiosis is an agronomical important plant-microbe interaction with implications in food security. Successful establishment of this interaction requires a reprogramming of differentiated plant cells for endosymbiosis, which is controlled at multiple regulatory levels. Our results show that both protein-coding and non-coding RNAs, including long non-coding RNAs and small RNA precursors, are subjected to uncoupled regulation at transcriptional and translation level during nitrogen-fixing symbiosis. In addition, co-transcriptional processing, such as alternative splicing and alternative polyadenilation, also influences the landscape of transcripts that will recruited to the translational machinery, contributing to shape the physiological and morphological changes that occur during the symbiotic process. One of the differentially translated transcripts encoding a protein involved in mRNA decay and posttranscriptional gene silencing proved to exert an important function in cell division and differentiation during nodule development. Altogether, this study highlights the functional relevance and selectivity of translational regulatory mechanisms for the reprogramming of root cells for symbiosis, providing a comprehensive view of the different levels of gene regulation that operate in the specific cell types engaged in symbiosis.

Technical Abstract: mRNA translation mediates developmental and adaptive responses in plants, but the impact of this level of regulation in the reprogramming of root cells for symbiosis have remained unexplored. We show that adjustments in the translatome are poorly correlated with changes in the transcriptome, and identified RNAs with altered translational status, some of which exhibit cell-specific regulation during symbiosis. Transcript variants regulated at the translational level are enriched in chromatin remodeling, transcriptional regulation and mRNA stability. Silencing of SUPERKILLER 3, a component of the complex involved in 3´ to 5´ mRNA degradation, proved that this approach contributes to identify genes with key functions in nodule development. Association of long non-coding RNAs with the translational machinery is also modulated during symbiosis, such as an alternative polyadenilated variant of the trans-acting RNA 3 that modulates tasiRNA biogenesis upon infection. Our results provide new insights into the translational reprogramming of gene expression during symbiosis.