Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change in Arabidopsis thaliana

Abstract

The gene balance hypothesis postulates that there is selection on gene copy number (gene dosage) to preserve the stoichiometric balance among interacting proteins. This presupposes that gene product abundance is governed by gene dosage and that gene dosage responses are consistent for interacting genes in a dosage-balance-sensitive network or complex. Gene dosage responses, however, have rarely been quantified, and the available data suggest that they are highly variable. We sequenced the transcriptomes of two synthetic autopolyploid accessions of Arabidopsis (Arabidopsis thaliana) and their diploid progenitors, as well as one natural tetraploid and its synthetic diploid produced via haploid induction, to estimate transcriptome size and dosage responses immediately following ploidy change. Similar to what has been observed in previous studies, overall transcriptome size does not exhibit a simple doubling in response to genome doubling, and individual gene dosage responses are highly variable in all three accessions, indicating that expression is not strictly coupled with gene dosage. Nonetheless, putatively dosage balance-sensitive gene groups (Gene Ontology terms, metabolic networks, gene families, and predicted interacting proteins) exhibit smaller and more coordinated dosage responses than do putatively dosage-insensitive gene groups, suggesting that constraints on dosage balance operate immediately following whole-genome duplication and that duplicate gene retention patterns are shaped by selection to preserve dosage balance.

Robust Cytonuclear Coordination of Transcription in Nascent Arabidopsis thaliana Autopolyploids

“…Second, the number and/or volume of chloroplasts per cell often increases with WGD [35,[40][41][42]. Increased plastid number per cell with WGD has been documented in maize, cotton, alfalfa (citations in [9]), and Glycine [43] among others [41].…”

“…The number of mitochondria per cell is also known to increase with cell size [44]. Given the correlation between WGD and cell size, therefore, the number of mitochondria per cell likely increases with ploidy as well [35].…”

“…Such relative measures report the fraction of total transcripts contributed by a given gene (i.e., transcript concentration; [31]), but do not, by themselves, allow inferences about absolute expression levels, such as transcripts per gene copy or transcripts per cell [31][32][33][34]. Total transcript abundance (transcriptome size) generally increases with ploidy [21,[31][32][33]35], meaning that the expression of individual genes could decrease in relative expression (e.g., TPM's, transcript concentrations), as observed for genes with plastid-targeting, while remaining constant or even increasing in absolute expression per gene or per cell.…”

Gene Dosage Balance Immediately following Whole-Genome Duplication in Arabidopsis

“…Although considerable interest exists in understanding the gene dosage responses, very little is known about the gene dosage response to immediate autopolyploidy. In new work, Song et al (2020) sought to determine the instantaneous effect of gene duplication in the absence of hybridization. Previous work by the authors showed that reciprocally retained genes in Glycine neoallopolyploids displayed a coordinated dosage response compared to non-reciprocally retained genes (Coate et al 2016).…”

“…However, the observed gene expression changes were confounded by the combination of WGD, hybridization, and 0.5 million years of evolution post-WGD. To avoid these confounding effects, Song et al (2020) used diploid/synthetic autotetraploid pairs of Arabidopsis thaliana ecotype C24 and Ws (colchicine-induced tetraploid of the same accessions) and a tetraploid/synthetic diploid pair of the ecotype Wa (diploid generated by Tailswap haploid induction).…”