Genome downsizing after polyploidy: mechanisms, rates and selection pressures

Abstract

SUMMARY An analysis of over 10 000 plant genome sizes (GSs) indicates that most species have smaller genomes than expected given the incidence of polyploidy in their ancestries, suggesting selection for genome downsizing. However, comparing ancestral GS with the incidence of ancestral polyploidy suggests that the rate of DNA loss following polyploidy is likely to have been very low (4–70 Mb/million years, 4–482 bp/generation). This poses a problem. How might such small DNA losses be visible to selection, overcome the power of genetic drift and drive genome downsizing? Here we explore that problem, focussing on the role that double‐strand break (DSB) repair pathways (non‐homologous end joining and homologous recombination) may have played. We also explore two hypotheses that could explain how selection might favour genome downsizing following polyploidy: to reduce (i) nitrogen (N) and phosphate (P) costs associated with nucleic acid synthesis in the nucleus and the transcriptome and (ii) the impact of scaling effects of GS on cell size, which influences CO2 uptake and water loss. We explore the hypothesis that losses of DNA must be fastest in early polyploid generations. Alternatively, if DNA loss is a more continuous process over evolutionary time, then we propose it is a byproduct of selection elsewhere, such as limiting the damaging activity of repetitive DNA. If so, then the impact of GS on photosynthesis, water use efficiency and/or nutrient costs at the nucleus level may be emergent properties, which have advantages, but not ones that could have been selected for over generational timescales.

Genomic and Meiotic Changes Accompanying Polyploidization

“…Genome sizes of polyploids are typically smaller than expected, suggesting that genome downsizing is a common readjustment in the diploidization process [ 261 ]. The loss of genetic material is a non-random process.…”

Karyotype and genome size variation in white-flowered Eranthis sect. Shibateranthis (Ranunculaceae)

“…It is known that the size and shape of homologous chromosomes may change in the course of the diploidization process following polyploidization, i.e., due to the genome downsizing. Repetitive DNA sequences, both non-coding and coding, gene duplicates may be eliminated from the genome, resulting in changes in the karyotype parameters (Leitch and Bennett 2004;Mandáková and Lysak 2018;Wang et al 2021).…”

Chromosome Number, Ploidy Level, and Nuclear DNA Content in 23 Species of Echeveria (Crassulaceae)

“…Although a positive significant correlation was observed between ploidy level and chromosome number, a negative significant correlation between ploidy level and the 1C x -value was observed. The decrease in the monoploid genome size as polyploidy level increases is a process known as genome downsizing [ 77 ] and can be explained as a strategy for the reduction in the number of chromosomes and a significant loss of both, repetitive sequences and duplicated genes related to the diploidization process [ 65 , 67 ]. Wang et al [ 77 ] propose that genome downsizing may be a byproduct of various processes that give rise to smaller genomes, which could offer a selective advantage as an emergent property.…”

“…The decrease in the monoploid genome size as polyploidy level increases is a process known as genome downsizing [ 77 ] and can be explained as a strategy for the reduction in the number of chromosomes and a significant loss of both, repetitive sequences and duplicated genes related to the diploidization process [ 65 , 67 ]. Wang et al [ 77 ] propose that genome downsizing may be a byproduct of various processes that give rise to smaller genomes, which could offer a selective advantage as an emergent property. As Wendel [ 67 ] has mention, angiosperms history includes many multiple events of polyploidy and reduction in chromosome numbers through massive rearrangement, which cause the reduction in genome size [ 65 , 78 ].…”