Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Authors: FORSYTHE, EVAN - Colorado State University; GROVER, CORRINNE - Iowa State University; MILLER, EMMA - Iowa State University; CONOVER, JUSTIN - Iowa State University; ARICK II, MARK - Mississippi State University; CHAVARRO, M. CAROLINA - University Of Georgia; LEAL-BERTIOLI, SORAYA - University Of Georgia; PETERSON, DANIEL - Mississippi State University; SHARBROUGH, JOEL - New Mexico Institute Of Mining & Technology; WENDEL, JONATHAN - Iowa State University; SLOAN, DANIEL - Colorado State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/14/2022
Publication Date: 7/19/2022
Citation: Forsythe, E.S., Grover, C.E., Miller, E.R., Conover, J.L., Arick Ii, M.A., Chavarro, M.F., Leal-Bertioli, S.C., Peterson, D.G., Sharbrough, J., Wendel, J.F., Sloan, D.B. 2022. Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels. Proceedings of the National Academy of Sciences (PNAS). https://doi.org/10.1073/pnas.2204187119.
DOI: https://doi.org/10.1073/pnas.2204187119

Interpretive Summary: Plants cells must coordinate gene expression across three different genomic compartments (nuclear, chloroplast, and mitochondrial). Rampant nuclear genome duplication (polyploidy) across plant diversity may potentially disrupt this delicate balance. We performed genome-wide analyses of gene expression in related polyploids and diploids from four lineages of flowering plants. Despite the minimal gene content of chloroplast and mitochondrial genomes, their transcripts comprise most of the mRNA pool in leaf cells. This finding illustrates the extreme cytoplasmic-nuclear asymmetry in RNA expression that plants overcome to maintain balanced protein expression. Cytoplasmic-nuclear RNA expression ratios are similar across diverse functional gene classes and different ploidy levels, indicating that successfully established polyploids have compensated for perturbations in gene expression associated with nuclear genome doubling.

Technical Abstract: Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.