Dynamic changes in mRNA nucleocytoplasmic localization in the nitrate response of Arabidopsis roots

Abstract

Nitrate is a nutrient and signal that regulates gene expression. The nitrate response has been extensively characterized at the organism, organ, and cell-type-specific levels, but intracellular mRNA dynamics remain unexplored. To characterize nuclear and cytoplasmic transcriptome dynamics in response to nitrate, we performed a time-course expression analysis after nitrate treatment in isolated nuclei, cytoplasm, and whole roots. We identified 402 differentially localized transcripts (DLTs) in response to nitrate treatment. Induced DLT genes showed rapid and transient recruitment of the RNA polymerase II, together with an increase in the mRNA turnover rates. DLTs code for genes involved in metabolic processes, localization, and response to stimulus indicating DLTs include genes with relevant functions for the nitrate response that have not been previously identified. Using single-molecule RNA FISH, we observed early nuclear accumulation of the NITRATE REDUCTASE 1 (NIA1) transcripts in their transcription sites. We found that transcription of NIA1, a gene showing delayed cytoplasmic accumulation, is rapidly and transiently activated; however, its transcripts become unstable when they reach the cytoplasm. Our study reveals the dynamic localization of mRNAs between the nucleus and cytoplasm as an emerging feature in the temporal control of gene expression in response to nitrate treatment in Arabidopsis roots.Transcriptome analysis of nuclear and cytoplasmic fractions in response to nitrate revealed transcripts with specific subcellular localization, revealing a novel layer of gene regulation. The dynamic interplay between mRNA localization, synthesis, and decay is crucial for the adaptive response of Arabidopsis roots to nitrate.

Keywords

gene expression regulation; nitrate; RNA dynamics; subcellular localization

Published in

Plant, Cell and Environment
2024, volume: 47, number: 11, pages: 4227-4245
Publisher: WILEY

SLU Authors

• Fonseca Cárdenas, Alejandro

  • Department of Plant Biology, Swedish University of Agricultural Sciences
    
  • Millennium Institute Center for Genome Regulation (CRG)
  • Millennium Institute for Integrative Biology
  • Pontifical Catholic University of Chile

• Rosa, Stefanie

  • Department of Plant Biology, Swedish University of Agricultural Sciences
    

UKÄ Subject classification

Botany
Genetics and Genomics

Publication identifier

• DOI: https://doi.org/10.1111/pce.15018

Permanent link to this page (URI)

https://res.slu.se/id/publ/131200