Abstract
An analysis of over 10000 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 (4-70Mb/million years, 4-482bp/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.
Highlights
Polyploidy or whole-genome duplication (WGD) is prevalent amongst many vascular plant lineages and is a major driver of evolutionary novelty and speciation (Escudero and Wendel, 2020; Fox et al, 2020)
In order to explain the observation that most angiosperms have small genome sizes (GSs) despite (i) the high frequency of polyploidy, (ii) the small amounts of DNA predicted to be lost per generation following WGD (Figure 3) and (iii) the power of drift in driving GS divergence (Lynch and Conery, 2003), we need to establish where a strong selection pressure might act on GS or where processes might be triggered that indirectly lead to DNA loss
The only way to reconcile a role for photosynthesis, water use efficiency and/or N and P costs in acting as selection pressures driving genome downsizing is to assume that DNA loss is extensive and rapid in the early polyploid generations
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. 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). We 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.
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