Ploidy and Size at Multiple Scales in the Arabidopsis Sepal

Abstract

Ploidy and size phenomena are observed to be correlated across several biological scales, from subcellular to organismal. Two kinds of ploidy change can affect plants. Whole-genome multiplication increases ploidy in whole plants and is broadly associated with increases in cell and organism size. Endoreduplication increases ploidy in individual cells. Ploidy increase is strongly correlated with increased cell size and nuclear volume. Here, we investigate scaling relationships between ploidy and size by simultaneously quantifying nuclear size, cell size, and organ size in sepals from an isogenic series of diploid, tetraploid, and octoploid Arabidopsis thaliana plants, each of which contains an internal endopolyploidy series. We find that pavement cell size and transcriptome size increase linearly with whole-organism ploidy, but organ area increases more modestly due to a compensatory decrease in cell number. We observe that cell size and nuclear size are maintained at a constant ratio; the value of this constant is similar in diploid and tetraploid plants and slightly lower in octoploid plants. However, cell size is maintained in a mutant with reduced nuclear size, indicating that cell size is scaled to cell ploidy rather than to nuclear size. These results shed light on how size is regulated in plants and how cells and organisms of differing sizes are generated by ploidy change.

Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change InArabidopsis thaliana

“…or halved with a doubling or halving of the genome, and that most genes do not exhibit simple 1:1 gene dosage responses.Hou et al (2018) also observed slightly less than 1:1 increases in expression in a separate Arabidopsis ploidy series. Similar deviations from a simple 1:1 dosage response have been observed in leaf tissue of allotetraploid relatives of soybean(Coate and Doyle 2010), sepals of autotetraploid Arabidopsis(Robinson et al 2018), and leaves of allotetraploid Tolmiea(Visger 310 et al 2019). Non-linear transcriptional responses to changes in gene dosage have also been observed following small scale duplications.…”

“…RNA-seq libraries were generated for each sample from 1-2µg of extracted RNA. To enable estimation of mRNA transcriptome size per unit of DNA, each sample was spiked with ERCC Mix 1 in proportion to the DNA/RNA ratio determined above, as described in Robinson et al (2018). Libraries were generated using the Illumina TruSeq Stranded library prep kits.…”

“…Such decoupling is evident in response to polyploidy because not all genes show identical expression responses following duplication -whether measured at the level of transcript abundance (e.g. Pirrello et al (2018);Hou et al (2018);Guo et al (1996); Riddle et al (2006); Robinson et al (2018); Stupar et al (2007); Yu et al (2010), additional references in Doyle and Coate (2019)) or protein abundance (Birchler and Newton 1981;Yao et al 2011;Zhu et al 2012;Soltis et al 2016;55 Deng et al 2017;Wang et al 2017;Yan et al 2017). Consequently, WGD does not necessarily preserve protein dosage balance, and the extent to which dosage responses following WGD are coordinated amongst genes encoding interacting proteins is unknown.…”

The importance and prevalence of allopolyploidy in Aotearoa New Zealand

“…Nascent polyploids must adapt to an instantaneous increase in genomic material, with potential downstream consequences for cell regulatory functions. Such consequences are typically generated through non-proportional cellular expansion (Melaragno et al 1993;Robinson et al 2018), producing a stoichiometric imbalance between chromatin components and envelope proteins (Corredor et al 2005). This scaling relationship may be further observed at the organismal level, particularly in polyploid plants (the gigas effect) (Sattler et al 2016;Robinson et al 2018), or there may be a compensatory reduction in cell number that lessens the impact of increased cell size on organ size changes (Tsukaya 2008;Del Pozo and Ramirez-Parra 2014;Czesnick and Lenhard 2015).…”

“…Such consequences are typically generated through non-proportional cellular expansion (Melaragno et al 1993;Robinson et al 2018), producing a stoichiometric imbalance between chromatin components and envelope proteins (Corredor et al 2005). This scaling relationship may be further observed at the organismal level, particularly in polyploid plants (the gigas effect) (Sattler et al 2016;Robinson et al 2018), or there may be a compensatory reduction in cell number that lessens the impact of increased cell size on organ size changes (Tsukaya 2008;Del Pozo and Ramirez-Parra 2014;Czesnick and Lenhard 2015). Diploidisation, the process by which a polyploid genome returns to a state of diploidy, commonly follows ploidy elevation, suggesting that the challenges associated with whole genome duplication are often too complex to allow the establishment of the nascent polyploid species (Wolfe 2001;Leitch and Bennett 2004).…”