The BOY NAMED SUE Quantitative Trait Locus Confers Increased Meiotic Stability to an Adapted Natural Allopolyploid of Arabidopsis

Abstract

Whole-genome duplication resulting from polyploidy is ubiquitous in the evolutionary history of plant species. Yet, polyploids must overcome the meiotic challenge of pairing, recombining, and segregating more than two sets of chromosomes. Using genomic sequencing of synthetic and natural allopolyploids of Arabidopsis thaliana and Arabidopsis arenosa, we determined that dosage variation and chromosomal translocations consistent with homoeologous pairing were more frequent in the synthetic allopolyploids. To test the role of structural chromosomal differentiation versus genetic regulation of meiotic pairing, we performed sequenced-based, high-density genetic mapping in F2 hybrids between synthetic and natural lines. This F2 population displayed frequent dosage variation and deleterious homoeologous recombination. The genetic map derived from this population provided no indication of structural evolution of the genome of the natural allopolyploid Arabidopsis suecica, compared with its predicted parents. The F2 population displayed variation in meiotic regularity and pollen viability that correlated with a single quantitative trait locus, which we named BOY NAMED SUE, and whose beneficial allele was contributed by A. suecica. This demonstrates that an additive, gain-of-function allele contributes to meiotic stability and fertility in a recently established allopolyploid and provides an Arabidopsis system to decipher evolutionary and molecular mechanisms of meiotic regularity in polyploids.

Evolution of the BBAA Component of Bread Wheat during Its History at the Allohexaploid Level

“…Together, the karyotyping data suggested that the property of karyotype stability that evolved in allohexaploid bread wheat is maintained in its extracted BBAA component. This is in line with recent findings in the genetic control of meiotic regularity in an adapted natural allopolyploid of Arabidopsis thaliana, in the sense that the controlling genetic factor(s) exerts its effect irrespective of altered genetic backgrounds (Henry et al, 2014). Therefore, it appears that different genes or pathways have evolved to serve the purpose of karyotype stabilization by similar mechanisms in different allopolyploid species.…”

“…Karyotype stability is usually a hallmark of established allopolyploid species (Comai, 2005;Hollister et al, 2012;Yant et al, 2013;Bomblies and Madlung, 2014;Henry et al, 2014). Although exceptions to this general rule have been documented recently in Brassica (Xiong et al, 2011) and Tragopogon (Chester et al, 2012), in which both structural chromosomal rearrangements and aneuploidy are abundant and even transgenerationally persistent, stabilized euploidy has selective advantages over aneuploid individuals in the long run.…”

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

“…Bomblies and colleagues proved that the tetraploid was not preadapted to diploidize and identified most or all of the over 40 loci that must mutate during diploidization (Yant et al, 2013). Comai and colleagues (Henry et al, 2014) identified a single naturally occurring allele in the wild, recent allotetraploid Arabidopsis suecica that increases the meiotic stability of the synthetic (not diploidized) allopolyploid, but diploidization is not complete. Diploidization is best seen as a multistep, mutation-fueled adaptation that might benefit from an environment of very relaxed selection that supports experimentation and absorbs massive failure.…”

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

“…Reduced viability or fertility in some F2 genotypes is well documented in homoploid hybrids (Grant 1966;Rieseberg et al 1996;Burke et al 1998;Burke and Arnold 2001), but less is known about how the fitness of allopolyploid taxa changes across early generations (Grant 1971;Comai et al 2000;Madlung et al 2005;Henry et al 2014). Artificially created allopolyploids often suffer from low fertility and viability and display phenotypic instability (Madlung et al 2005).…”

“…Again, in the allopolyploid A. suecica, F2s between natural and synthetic lines display variation in pollen viability. This variation is associated with the stability of meiosis in F2s and correlates with segregation at a single quantitative trait locus (BOY NAMED SUE) (Henry et al 2014). Natural allelic variation for genes controlling meiotic stability are well studied in autopolyploids (Yant et al 2013;Wright et al 2015) and in a few allopolyploids (Hollister 2015).…”