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The distinct roles of genome, methylation, transcription, and translation on protein expression in Arabidopsis thaliana resolve the Central Dogma’s information flow

Zhong, Z; Bailey, M; Kim, YI; Afsharyan, NP; Parker, B; Arathoon, L; Li, X; ... Mott, R; + view all (2025) The distinct roles of genome, methylation, transcription, and translation on protein expression in Arabidopsis thaliana resolve the Central Dogma’s information flow. Genome Biology , 26 , Article 319. 10.1186/s13059-025-03741-0. Green open access

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Abstract

BACKGROUND: We investigate the flow of genetic information from DNA to RNA to protein as described by the Central Dogma in molecular biology, to determine the impact of intermediate genomic levels on plant protein expression. RESULTS: We perform genomic profiling of rosette leaves in two Arabidopsis accessions, Col-0 and Can-0, and assemble their genomes using long reads and chromatin interaction data. We measure gene and protein expression in biological replicates grown in a controlled environment, also measuring CpG methylation, ribosome-associated transcript levels, and tRNA abundance. Each omic level is highly reproducible between biological replicates and between accessions despite their ~1% sequence divergence; the single best predictor of any level in one accession is the corresponding level in the other. Within each accession, gene codon frequencies accurately model both mRNA and protein expression. The effects of a codon on mRNA and protein expression are highly correlated but independent of genome-wide codon frequencies or tRNA levels which instead match genome-wide amino acid frequencies. Ribosome-associated transcripts closely track mRNA levels. CONCLUSIONS: DNA codon frequencies and mRNA expression levels are the main predictors of protein abundance. In the absence of environmental perturbation neither gene-body methylation, tRNA abundance nor ribosome-associated transcript levels add appreciable information. The impact of constitutive gene-body methylation is mostly explained by gene codon composition. tRNA abundance tracks overall amino acid demand. However, genetic differences between accessions associate with differential gene-body methylation by inflating differential expression variation. Our data show that the dogma holds only if both sequence and abundance information in mRNA are considered.

Type: Article
Title: The distinct roles of genome, methylation, transcription, and translation on protein expression in Arabidopsis thaliana resolve the Central Dogma’s information flow
Location: England
Open access status: An open access version is available from UCL Discovery
DOI: 10.1186/s13059-025-03741-0
Publisher version: https://doi.org/10.1186/s13059-025-03741-0
Language: English
Additional information: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Keywords: Gene-body methylation, Mim-tRNAseq, RNAseq, Ribosome-associated expression, Gene expression, Protein expression, Data-independent acquisition, Genome assembly, Chromatin interaction, Long reads, Central Dogma
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10215582
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