Derived alleles of two axis proteins affect meiotic traits in autotetraploid Arabidopsis arenosa

Abstract

Polyploidy, which results from whole genome duplication (WGD), has shaped the long-term evolution of eukaryotic genomes in all kingdoms. Polyploidy is also implicated in adaptation, domestication, and speciation. Yet when WGD newly occurs, the resulting neopolyploids face numerous challenges. A particularly pernicious problem is the segregation of multiple chromosome copies in meiosis. Evolution can overcome this challenge, likely through modification of chromosome pairing and recombination to prevent deleterious multivalent chromosome associations, but the molecular basis of this remains mysterious. We study mechanisms underlying evolutionary stabilization of polyploid meiosis using Arabidopsis arenosa, a relative of A. thaliana with natural diploid and meiotically stable autotetraploid populations. Here we investigate the effects of ancestral (diploid) versus derived (tetraploid) alleles of two genes, ASY1 and ASY3, that were among several meiosis genes under selection in the tetraploid lineage. These genes encode interacting proteins critical for formation of meiotic chromosome axes, long linear multiprotein structures that form along sister chromatids in meiosis and are essential for recombination, chromosome segregation, and fertility. We show that derived alleles of both genes are associated with changes in meiosis, including reduced formation of multichromosome associations, reduced axis length, and a tendency to more rod-shaped bivalents in metaphase I. Thus, we conclude that ASY1 and ASY3 are components of a larger multigenic solution to polyploid meiosis in which individual genes have subtle effects. Our results are relevant for understanding polyploid evolution and more generally for understanding how meiotic traits can evolve when faced with challenges.

Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution

“…Prevention of non-homologous pairing between subgenomes in allohexaploid bread wheat is facilitated by the major qualitative effect Ph1 locus (Sears, 1976;Feldman, 1993;Griffiths et al, 2006;Bhullar et al, 2014), for which the molecular mechanism is still not completely characterized, but which may involve suppression of CDK2-like activity to result in chromatin modifications (Greer et al, 2012) as well as the presence of an additional copy of a meiotic ZIP4 gene (Rey et al, 2017). By contrast, at least eight meiosis genes have been implicated in genomic stabilization of autotetraploid Arabidopsis arenosa (Yant et al, 2013), with two of these genes (ASY1 and ASY3) later found to directly reduce multivalent formation and chiasma number, as expected (Morgan et al, 2020). Triticum and Aradidopsis represent the two best-characterized models for meiotic regulation in polyploids to date (reviewed by Cifuentes et al, 2010;Lloyd and Bomblies, 2016).…”

Varietal variation and chromosome behaviour during meiosis in Solanum tuberosum

“…We observed such pairing partner switches in the late zygotene/pachytene-like stage in tetraploid potato varieties. These switches could be confirmed and visualised in greater detail using structured illumination microscopy, which has been applied in the established autotetraploid, A. arenosa (Morgan et al 2020 ). In addition, we have observed large foci of ASY1 and ZYP1 proteins, which are similar to those described previously in yeast as polycomplexes (Sym and Roeder 1995 ; Henderson and Keeney 2004 ), and also observed in hexaploid wheat ph1b mutants (Boden et al 2009 ), and in A. arenosa grown at high temperature (Morgan et al 2017 ).…”

“…We found a clear preference for bivalent pairing of chromosomes in autotetraploid varieties, accompanied by a reduction in the CO frequency per bivalent compared with the diploid variety. Finally, given the important role of the chromosome axis and synaptonemal complex in stabilising meiosis in autopolyploids (Hollister et al 2012 ; Bomblies et al 2016 ; Morgan et al 2020 ), we immunolocalised two of the key axis proteins, ASY1 and ZYP1, and found that polymerisation and/or maintenance of the axis may be compromised in the tetraploid varieties.…”

“…Meanwhile, class II COs are interference independent (Copenhaver et al 2002 ). Comparatively less is known about how meiosis adapts to the polyploid state, though more recently, Arabidopsis species have provided an ideal model for studying the additional complexities in meiosis introduced by polyploidy (Lloyd and Bomblies 2016 ; Morgan et al 2020 ).…”

A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata

“…Recently ASY1 and ASY3 have been shown to have an effect in stabilising autotetraploid A . arenosa [ 29 ], but thus far, no formal confirmation of an association between meiotic stabilisation has been attributed to these evolved alleles in tetraploid A . lyrata .…”