Genome management and mismanagement—cell-level opportunities and challenges of whole-genome duplication

Abstract

Whole-genome duplication (WGD) doubles the DNA content in the nucleus and leads to polyploidy. In whole-organism polyploids, WGD has been implicated in adaptability and the evolution of increased genome complexity, but polyploidy can also arise in somatic cells of otherwise diploid plants and animals, where it plays important roles in development and likely environmental responses. As with whole organisms, WGD can also promote adaptability and diversity in proliferating cell lineages, although whether WGD is beneficial is clearly context-dependent. WGD is also sometimes associated with aging and disease and may be a facilitator of dangerous genetic and karyotypic diversity in tumorigenesis. Scaling changes can affect cell physiology, but problems associated with WGD in large part seem to arise from problems with chromosome segregation in polyploid cells. Here we discuss both the adaptive potential and problems associated with WGD, focusing primarily on cellular effects. We see value in recognizing polyploidy as a key player in generating diversity in development and cell lineage evolution, with intriguing parallels across kingdoms.

Genomic novelty and process-level convergence in adaptation to whole genome duplication

“…Given the shared challenges attendant to WGD in C. amara and A. arenosa 4,10,11 , we hypothesised at least partially convergent responses in these species. While we found obvious convergent recruitment at the level of inferred functional processes, we could detect no excess convergence at orthologous genes with our genome scanning approach.…”

“…Thus, they typically harbour four full genomes that are similar in all pairwise combinations 2 , resulting in a lack of pairing partner preferences at meiosis. This, combined with multiple crossover events per chromosome pair, can result in entanglements among three or more homologs at anaphase and mis-segregation or chromosome breakage, leading to aneuploidy [2][3][4] . Beyond this obvious challenge, WGD presents a suddenly transformed intracellular landscape to the conserved workings of the cell, such as altered ion homeostasis and a host of 'nucleotypic' factors revolving around cell size, volume, and cell cycle duration [4][5][6] .…”

“…In fact, with increased ploidy, genetic variability can be maintained in a masked state, with evidence of lineages acting as allelic sponges recruiting diverse alleles by gene flow across ploidies, and indeed, species 8,9 . Thus, while substantial opportunities may present for lineages that can adapt to a WGD state, clear challenges must be overcome to function as a polyploid 4,10,11 .…”

Picking up the Ball at the K/Pg Boundary: The Distribution of Ancient Polyploidies in the Plant Phylogenetic Tree as a Spandrel of Asexuality with Occasional Sex

“…happens (Yant and Bomblies, 2015). Diploidization is the adaptive process of evolving a balanced chromosomal set and alignment machinery that permit efficient segregation and assortment during meiosis.…”

Partial interfertility between independently originated populations of the neo-allopolyploid Mimulus peregrinus

“…In addition, postzygotic barriers between independently originated populations may evolve following the polyploidisation event. Polyploid and hybrid genomes can be highly dynamic often undergoing considerable change in gene content, gene expression, and chromosome structure and number in a few generations (Song et al 1995;Wendel 2000;Ozkan et al 2001;Tate et al 2006;Chester et al 2012;Buggs 2013;Hegarty et al 2013;Lafon-Placette and Kohler 2015;Soltis et al 2015;Yant and Bomblies 2015). These rapid genomic changes may result in postzygotic reproductive barriers that impede mating among independently originated populations after they come into secondary contact.…”