Nuclear–cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number

• Published in: The Plant journal : for cell and molecular biology 2021-10, Vol.108 (1), p.219-230
• Main Authors: Fernandes Gyorfy, Matheus, Miller, Emma R., Conover, Justin L., Grover, Corrinne E., Wendel, Jonathan F., Sloan, Daniel B., Sharbrough, Joel
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis arenosa; Arabidopsis suecica; Arabidopsis thaliana; Cell Nucleus - genetics; Chloroplast; Chloroplasts - genetics; Copy number; cytonuclear interactions; Cytoplasm - genetics; Diploids; Diploidy; DNA Copy Number Variations; Gene Duplication; Gene expression; Genome, Plant - genetics; Genome, Plastid - genetics; Genomes; Mitochondria; Mitochondria - genetics; Nuclei (cytology); Plant cells; Plastids; Plastids - genetics; Polyploidy; Progenitor cells; Reproduction (copying); Stoichiometry; Triticum - genetics; Triticum aestivum; Triticum turgidum; whole genome duplications
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15436

SUMMARY The plant genome is partitioned across three distinct subcellular compartments: the nucleus, mitochondria, and plastids. Successful coordination of gene expression among these organellar genomes and the nuclear genome is critical for plant function and fitness. Whole genome duplication (WGD) events in the nucleus have played a major role in the diversification of land plants and are expected to perturb the relative copy number (stoichiometry) of nuclear, mitochondrial, and plastid genomes. Thus, elucidating the mechanisms whereby plant cells respond to the cytonuclear stoichiometric imbalance that follows WGDs represents an important yet underexplored question in understanding the evolutionary consequences of genome doubling. We used droplet digital PCR to investigate the relationship between nuclear and organellar genome copy numbers in allopolyploids and their diploid progenitors in both wheat and Arabidopsis. Polyploids exhibit elevated organellar genome copy numbers per cell, largely preserving the cytonuclear stoichiometry observed in diploids despite the change in nuclear genome copy number. To investigate the timescale over which cytonuclear stoichiometry may respond to WGD, we also estimated the organellar genome copy number in Arabidopsis synthetic autopolyploids and in a haploid‐induced diploid line. We observed corresponding changes in organellar genome copy number in these laboratory‐generated lines, indicating that at least some of the cellular response to cytonuclear stoichiometric imbalance is immediate following WGD. We conclude that increases in organellar genome copy numbers represent a common response to polyploidization, suggesting that maintenance of cytonuclear stoichiometry is an important component in establishing polyploid lineages. Significance Statement Whole genome duplications (WGDs) have the potential to alter the stoichiometric balance between nuclear and organellar genomes. We used two separate diploid‐polyploid complexes to show that plant cells with WGD exhibit elevated mitochondrial and plastid genome copy numbers, both immediately in lab‐generated lines and in natural polyploids.