Robust Cytonuclear Coordination of Transcription in Nascent Arabidopsis thaliana Autopolyploids

Abstract

Polyploidy is hypothesized to cause dosage imbalances between the nucleus and the other genome-containing organelles (mitochondria and plastids), but the evidence for this is limited. We performed RNA-seq on Arabidopsis thaliana diploids and their derived autopolyploids to quantify the degree of inter-genome coordination of transcriptional responses to nuclear whole genome duplication in two different organs (sepals and rosette leaves). We show that nuclear and organellar genomes exhibit highly coordinated responses in both organs. First, organelle genome copy number increased in response to nuclear whole genome duplication (WGD), at least partially compensating for altered nuclear genome dosage. Second, transcriptional output of the different cellular compartments is tuned to maintain diploid-like levels of relative expression among interacting genes. In particular, plastid genes and nuclear genes whose products are plastid-targeted show coordinated down-regulation, such that their expression levels relative to each other remain constant across ploidy levels. Conversely, mitochondrial genes and nuclear genes with mitochondrial targeting show either constant or coordinated up-regulation of expression relative to other nuclear genes. Thus, cytonuclear coordination is robust to changes in nuclear ploidy level, with diploid-like balance in transcript abundances achieved within three generations after nuclear whole genome duplication.

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…The allopolyploid individuals will thus contain biparental nuclear chromosomes and uniparental organellar genome inherited from different species, potentially resulting in CNI [51]. Several mechanisms are hypothesized to maintain coordination between organellar and nuclear genomes (reviewed in [51]): down-regulating the expression of the nuclear genes targeted to organelles (of both nuclear genomes or by the preferential expression of the organellar donor), or up-regulating the expression of organellar genes [52]. The study of allopolyploidization influence on CN interactions has mostly been studied on the Rubisco-encoding genes that revealed that maternal genes were preferentially expressed (reviewed in [51]).…”

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

“…The discrepancies between the former two studies (performed in diploids) and the latter two (performed in polyploids) indicates that cytonuclear stoichiometry may be highly responsive to nuclear gene content. In support of that hypothesis, diverse polyploids appear to compensate for elevated nuclear ploidy with increased organelle genome copy number [40,214,[217][218][219][220]. Additional work investigating the immediate and evolved consequences of cytonuclear stoichiometry at the genomic, transcriptomic, proteomic, and organellar levels, especially by homoeologous pair analysis, will provide valuable insights into the unresolved question of how genome doubling can affect cellular energy production and homeostasis.…”

Autopolyploidy: an epigenetic macromutation

“…1A). There is often a global reduction in expression on a per‐genome basis, combined with differential effects on the regulation of particular classes of genes, notably those that are dosage sensitive (Hou et al, 2018; Coate et al, 2020; Song et al, 2020). Neither overall patterns of methylation nor proximity of transposable elements to genes appears to explain these genome‐wide or gene‐class‐specific phenomena, leaving chromatin folding in space and time (the 4D nucleome; Dekker et al, 2017) as a possible mechanism for coordinated responses of numerous unlinked genes.…”