Epitranscriptome changes triggered by ammonium nutrition regulate the proteome response of maritime pine roots

Epitranscriptome constitutes a gene expression checkpoint in all living organisms. Nitrogen is an essential element for plant growth and development that influences gene expression at different levels such as epigenome, transcriptome, proteome, and metabolome. Therefore, our hypothesis is that changes in the epitranscriptome may regulate nitrogen metabolism. In this study, epitranscriptomic modifications caused by ammonium nutrition were monitored in maritime pine roots using Oxford Nanopore Technology. Transcriptomic responses mainly affected transcripts involved in nitrogen and carbon metabolism, defense, hormone synthesis/signaling, and translation. Global detection of epitranscriptomic marks was performed to evaluate this posttranscriptional mechanism in un/treated seedlings. Increased N-6-methyladenosine (m(6)A) deposition in the 3'-UTR was observed in response to ammonium, which seems to be correlated with poly(A) lengths and changes in the relative abundance of the corresponding proteins. The results showed that m(6)A deposition and its dynamics seem to be important regulators of translation under ammonium nutrition. These findings suggest that protein translation is finely regulated through epitranscriptomic marks likely by changes in mRNA poly(A) length, transcript abundance and ribosome protein composition. An integration of multiomics data suggests that the epitranscriptome modulates responses to nutritional, developmental and environmental changes through buffering, filtering, and focusing the final products of gene expression.

Automated summary

Epitranscriptome serves as a checkpoint for gene expression in all living organisms, and nitrogen nutrition influences gene expression through epitranscriptomic modifications. This study revealed that increased m(6)A deposition in response to ammonium is correlated with mRNA poly(A) lengths and protein abundance. It was also found that the epitranscriptome finely regulates protein translation by modulating mRNA poly(A) length, transcript abundance, and ribosome protein composition. Integration of multiomics data suggests that the epitranscriptome modulates responses to nutritional, developmental, and environmental changes by buffering, filtering, and focusing the final products of gene expression.