Learning to tango with four (or more): the molecular basis of adaptation to polyploid meiosis

Abstract

Polyploidy, which arises from genome duplication, has occurred throughout the history of eukaryotes, though it is especially common in plants. The resulting increased size, heterozygosity, and complexity of the genome can be an evolutionary opportunity, facilitating diversification, adaptation and the evolution of functional novelty. On the other hand, when they first arise, polyploids face a number of challenges, one of the biggest being the meiotic pairing, recombination and segregation of the suddenly more than two copies of each chromosome, which can limit their fertility. Both for developing polyploidy as a crop improvement tool (which holds great promise due to the high and lasting multi-stress resilience of polyploids), as well as for our basic understanding of meiosis and plant evolution, we need to know both the specific nature of the challenges polyploids face, as well as how they can be overcome in evolution. In recent years there has been a dramatic uptick in our understanding of the molecular basis of polyploid adaptations to meiotic challenges, and that is the focus of this review.

Desynapsis in potato is caused byStMSH4mutant alleles and leads to either highly uniform unreduced pollen or sterility

“…In this context, reducing MSH4 dosage seems to help stabilising allopolyploid meiosis by favouring homologous chromosomes as recombination partner. Contrary to allopolyploids, the stabilization of meiosis in autopolyploids, such as S. tuberosum , does not rely on recombination partner choice but on avoiding multivalent formation, in particular the combination of trivalent and univalent (Bomblies 2022). This can be mediated by increasing crossover interference strength and ultimately decreasing crossovers number to a minimum of one per pair (Morgan et al 2021).…”

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

“…Homoeologous exchanges have long been recognized as an engine of phenotypic diversity and novelty in newly formed polyploids (Pires et al 2004; Gaeta et al 2007; Xiong et al 2011; Rousseau-Guetin et al 2017; Stein et al 2017; Leal-Bertioli et al 2018; Lloyd et al 2018; Mason and Wendel 2020; Ferreira de Carvalho et al 2021, Wu et al 2021; Bomblies 2022). Our analysis of genomic rearrangements and homoeologous exchanges in resynthesized B. napus confirmed at higher resolution the extensive rearrangements in these lines (Gaeta et al 2007; Xiong et al 2011).…”

“…This new avenue of investigation may help further examine evolution and epistasis as well as selection and divergence among paralogs (Qi et al 2021; Conover and Wendel, 2022; Kwon et al 2022), and spur further integration of methods and data across phylogenomics, comparative and population genomics, and network biology (Renny-Byfield et al 2017; Blischak et al 2018). Such work can enhance plant breeding efforts by providing a strengthened evolutionary understanding of the consequences of gene duplications, gene balance, and subgenome dominance (Rodriguez-Leal et al 2017; Bird et al 2018; Salman-Minkov et al 2016; Turner-Hissong et al 2020; Bayer et al 2021; Bomblies 2022).…”

“…This effect is driven by the merger of evolutionarily diverged genomes, which frequently results in remodeling of epigenetic markers (Madlung et al, 2001; Edger et al, 2017; Bird et al, 2021), alterations in gene regulation (Chen, 2007), and activation of transposable elements (Vicient and Casacuberta, 2012). Importantly, there is also a continuum of polyploidy as parental genomes within and among species can vary in evolutionary distance and subsequent genome evolution blurs the distinction between autopolyploidy and allopolyploidy (Stebbins 1947; Leal-Bertioli et al 2018; Mason and Wendel 2020; Blischak et al 2022; Bomblies 2022). Subgenome expression dominance has been defined in terms of a subgenome possessing a greater amount of dominantly expressed homoeologs and has been identified in many allopolyploid species, including maize (Schnable et al 2011) Mimulus peregrinus (Edger et al 2017), garden strawberry (Edger et al 2019), Brassica rapa (Cheng et al 2012; Cheng et al 2016), and a population of resynthesized Brassica napus (Bird et al 2021).…”

“…This effect is driven by the merger of evolutionarily diverged genomes, which frequently results in remodeling of epigenetic markers (Madlung et al, 2001;Edger et al, 2017;Bird et al, 2021), alterations in gene regulation (Chen, 2007), and activation of transposable elements (Vicient and Casacuberta, 2012). Importantly, there is also a continuum of polyploidy as parental genomes within and among species can vary in evolutionary distance and subsequent genome evolution blurs the distinction between autopolyploidy and allopolyploidy (Stebbins 1947;Leal-Bertioli et al 2018;Mason and Wendel 2020;Blischak et al 2022;Bomblies 2022).…”