Revisiting the Central Dogma: the distinct roles of genome, methylation, transcription, and translation on protein expression in Arabidopsis thaliana
Authors: Zhong, Z., Bailey, M., Kim, Y.-I., Pesaran-Afsharyan, N., Parker, B., Arathoon, L., Li, X., Rundle, C. A., Behrens, A., Nedialkova, D. D., Slavov, G., Hassani-Pak, K., Lilley, K. S., Theodoulou, F. L., Mott, R.
The study combined long‑read whole‑genome assembly, multi‑omics profiling (DNA methylation, mRNA, ribosome‑associated transcripts, tRNA abundance, and protein levels) in two Arabidopsis thaliana accessions to evaluate how genomic information propagates through the Central Dogma. Codon usage in gene sequences emerged as the strongest predictor of both mRNA and protein abundance, while methylation, tRNA levels, and ribosome‑associated transcripts contributed little additional information under stable conditions.
The study used comparative transcriptomics to examine how Fusarium oxysporum isolates with different lifestyles on angiosperms regulate effector genes during infection of the non‑vascular liverwort Marchantia polymorpha. Core effector genes on fast core chromosomes are actively expressed in the bryophyte host, while lineage‑specific effectors linked to angiosperm pathogenicity are silent, and disruption of a compatibility‑associated core effector alters the expression of other core effectors, highlighting conserved fungal gene networks across plant lineages.
Phylogenetic analysis reveals that non‑seed plants, exemplified by the liverwort Marchantia polymorpha, possess a streamlined repertoire of cyclin and CDK genes, with only three cyclins active in a phase‑specific manner during vegetative development. Single‑cell RNA‑seq and fluorescent reporter assays, combined with functional overexpression studies, demonstrate the distinct, non‑redundant roles of MpCYCD;1, MpCYCA, and MpCYCB;1 in G1 entry, S‑phase progression, and G2/M transition, respectively.
Chromatin accessibility profiling and transcriptomics of Marchantia polymorpha heat‑shock transcription factor (HSF) mutants reveal that HSFA1 governs the placement of cis‑regulatory elements for heat‑induced gene activation, a mechanism conserved across plants, mice, and humans. Integrated gene regulatory network modeling identifies MpWRKY10 and MpABI5B as indirect regulators linking phenylpropanoid and stress pathways, while abscisic acid influences gene expression downstream of HSFA1 without broadly reshaping chromatin. A cross‑species, cross‑condition machine‑learning framework successfully predicts chromatin accessibility and expression, underscoring a conserved regulatory logic in stress responses.
The study performed a comprehensive computational analysis of the Arabidopsis thaliana proteome, classifying 48,359 proteins by melting temperature (Tm) and melting temperature index (TI) and linking thermal stability to amino acid composition, molecular mass, and codon usage. Machine‑learning and evolutionary analyses revealed that higher molecular mass and specific codon pairs correlate with higher Tm, and that gene duplication has driven the evolution of high‑Tm proteins, suggesting a genomic basis for stress resilience.
The study mapped the subcellular localization of isoprenoid biosynthetic enzymes in Marchantia polymorpha, confirming most predictions and identifying oil body cells as primary sites of terpene synthesis. Overexpression and CRISPR knockout of the ABC transporter ABCG1 revealed its essential role in retaining sesquiterpenes within oil bodies, while attempts to boost heterologous diterpene and triterpene production in oil bodies did not increase yields.