Genome duplication effects on functional traits and fitness are genetic context and species dependent: studies of synthetic polyploid Fragaria

Abstract

Premise Divergence in functional traits and adaptive responses to environmental change underlies the ecological advantage of polyploid plants in the wild. While established polyploids may benefit from combined outcomes of genome doubling, hybridization, and polyploidy‐enabled adaptive evolution, whether genome doubling alone can drive ecological divergence or whether the outcome is genetically variable remains less clear. Methods Using synthetic, colchicine‐induced, autotetraploid (4x) plants derived from self‐pollinated diploid (2x) seeds, and their colchicine‐treated but unconverted diploid (2x.nc) full sibs from two diploid wild strawberry taxa (Fragaria vesca subsp. vesca and F. vesca subsp. bracteata), we examined the effects of genome doubling on functional traits, heat stress tolerance, and fitness components across taxa and maternal families (i.e., genetic families) within taxa. Results Comparisons between 2x and 2x.nc plants indicated a negligible effect of colchicine treatment on functional traits. Genome doubling increased stomatal length and decreased stomatal density, specific leaf area, and leaf vein density, recapitulating patterns observed in wild polyploid Fragaria. Trichome density, heat stress tolerance, and relative growth rate were not significantly affected by genome doubling. Although clonal reproduction was reduced in response to genome doubling, this effect was strongly genetic‐family dependent. Conclusions The results suggest that genome doubling during incipient speciation alone can generate ecological divergence and variation among genetic lineages. This response potentially allows for rapid short‐term evolutionary adaptation and fuels genomic diversity and independent origins of polyploidy.

Changes in ploidy affect vascular allometry and hydraulic function in Mangifera indica trees

“…Traditionally, agriculture and horticulture have benefited from the use of natural or artificial polyploid genotypes with increased tolerance to stresses such as salinity or drought. Herbaceous polyploid genotypes with these characteristics are present in species with genera of agronomic interest, such as Fragaria (Wei et al., 2019, 2020), Lycopersicum (Tal and Gardi, 1976) or Raphanus (Pei et al., 2019), but also in genera with ornamental species such as Chamaenerion (Maherali et al., 2009), Phlox (Vyas et al., 2007) or Saxifraga (Decanter et al., 2020). Comparatively, polyploidy is less frequent in woody species (Meyers and Levin, 2006), but some results in woody plants point to the capacity of tetraploids to retain more water, such as in seedlings of Betula (Li et al., 1996), and plants of Lonicera (Li et al., 2009) or Populus (Xu et al., 2018).…”

Evolutionary dynamics of genome size in a radiation of woody plants

“…Polyploids can achieve faster climatic niche differentiation than their diploid progenitors, possibly facilitating polyploid speciation (Baniaga et al, 2020). In comparisons of diploids and chemically induced polyploids of the same species, polyploids showed changes in physiologically‐relevant cellular traits, such as vein density, but did not exhibit concomitant changes in ecologically relevant responses, such as heat stress response or growth rate (Wei et al, 2020). In previous studies, increases in genome size have been correlated with slower growth rate (Cavalier‐Smith, 1978; Sharpe et al, 2012; Müller et al, 2019), which could in turn limit plants with large genomes from colonizing stressful or seasonal environments with short growing seasons where fast growth is required (Knight et al, 2005; Qiu et al, 2019).…”

Plant–environment interactions from the lens of plant stress, reproduction, and mutualisms

“…The authors expanded on previous work that identified the role of the mutant phyA in the BOG response by identifying a new mutant, sig6, which like phyA, allowed for greening after treatment that should have induced BOG. Finally, Wei et al (2020) examined the types and patterns of trait changes that may occur when genomes double, which can allow for rapid evolutionary adaptation to new and stressful environments. Using synthetic Fragaria polyploids, they show that genome doubling alters traits such as stomatal length and density, as well as specific leaf area and vein density.…”