Adaptation to whole genome duplication
Polyploid species and variants are important in evolution as well as agriculture. Many familiar cultivated plants, such as wheat, oats, potato, banana, cotton, sugar cane, and many more are polyploids. However, when polyploids first arise, they face substantial problems to their basic biology - particularly to the regular two-by-two segregation of chromosomes that occurs in meiosis and is essential for fertility. Other effects, such as changes in cell size and geometry are likely also important.
What does it take to be a stable polyploid? In plants, many species have ploidy variants, showing that evolution can overcome the problems facing new polyploids. But how does it do so? What changes are necessary?
Figure 1: Arabidopsis arenosa growing on a limestone outcrop in the Upper Danube Valley in Southwestern Germany.
Our model system is Arabidopsis arenosa, a close relative of the widely used molecular model plant, Arabidopsis thaliana. Unlike A. thaliana, A. arenosa is an obligate outcrosser and has extant diploid and autotetraploid populations (autotetraploids result from within-species genome duplications where all four chromosome copies remain homologous). We know now, from our biogeographic work, that A. arenosa tetraploids arose approximately 20,000 generations ago from a single ancestral diploid population (Arnold et al 2015). We also know from our own work (Yant et al. 2013; Higgins et al 2014) as well as prior work from other groups (e.g. Comai et al. 2003; Carvalho et al. 2010) that A. arenosa tetraploids are fertile and have stable meiotic chromosome segregation. This is coupled with a reduction in crossover number, which is associated in many autotetraploids with meiotic stability because it reduces the number of complex multivalent associations among chromosomes in meiosis that complicates segregation (Bomblies et al 2015; Bomblies & Madlung, 2014).
Figure 2: Metaphase spreads of diploid, tetraploid and colchicine-doubled "neotetraploid" A. arenosa. From such images we learn several important things: (1) the diploid has higher crossover rates than the tetraploid, (2) the tetraploid has more "rod" bivalents with terminally-located chiasmata, while the diploid has more centrally located chiasmata, and (3) a colchicine-doubled neotetraploid line shows extensive chromosome tangling associated with low fertility of these lines.
From artificially genome-doubling a diploid A. arenosa, however, we also know that the diploid genome is not sufficient to sustain tetraploid meiosis, showing that the stability of the natural tetraploid is likely an evolved phenotype (Yant et al 2013).
Figure 3: Genome scan result showing an example of a selective sweep signature spanning the ASY3 gene. Each dot shows frequency of a single polymorphism relative to the diploid - the peak in ASY3 indicates that this region carries a large number of derived changes that are at high frequency in the tetraploid relative to the diploid.
We undertook a genome resequencing scan of the tetraploid comparing it to the closest related diploids and identified regions of the genome that showed evidence of having been under selection specifically in the autotetraploid lineage (Yant et al 2013; Hollister et al 2012). 39 loci passed our most stringent filters and show clear evidence of derived alleles being under selection. Differentiation drops back to background very quickly, which makes identification of candidate genes easy. From our genome scan results, we hypothesise that several processes were important in polyploid adaptation - genes implicated in cell size regulation, cell growth, and particularly in core aspects of meiosis show evidence of selection. Interestingly, the meiosis genes with evidence of selection control a related set of phenotypes.
Figure 4: During meiosis, linear structures form between the sister chromatids called axes. These then become lateral elements as the synaptonemal complex forms between homologs. These structures form the context for chromosome pairing and recombination, which occurs via the maturation of recombination nodules (brown elipses). The proteins under selection in A. arenosa are all key components of these processes, hinting that their modulation may be important for stabilizing tetraploid meiosis, perhaps by altering the dynamics of crossover maturation.
We are currently following up several different genes, focusing in particular on the stabilisation of meiosis in the tetraploid lineage. We are particularly focused on understanding how the meiosis genes we identified in our scan for selection may have changed function and how this might contribute to the meiotic stability of the tetraploid lineage. These genes all play roles in axis and SC formation This involves functional follow-up using genetic and transgenic lines, coupled with detailed cytological study. For this we are working with collaborators Chris Franklin (University of Birmingham), and James Higgins (University of Leicester).
Another important question is what traits are under selection in independent polyploidy events. This is primarily work being carried out in collaborator Levi Yant's lab (JIC) who recently obtained an ERC starting grant to do this work.
Arnold, B., Kim, S-T., Bomblies, K. (2015) Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Mol Biol Evol 32: 1382-1395.
Bomblies, K., Jones, G.H., Franklin, F.C.H., Zickler, D., Kleckner, N. The challenge of evolving stable polyploidy: could interference play a central role? Invited review, Chromosoma [AOP].
Bomblies, K., Madlung, A. (2014) Polyploidy in the Arabidopsis genus. Invited review. Chromosome Research 22: 117-134.
Carvalho A, Delgado M, Barao A, Frescatada M, Ribeiro E, Pikaard CS, Viegas W, Neves N (2010) Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex Plant Reprod 23: 29–37.
Comai L, Tyagi AP, Lysak MA (2003) FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res 11: 217-226.
Higgins, J.D., Wright, K.M., Bomblies, K., Franklin, F. C. H. (2014) Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Invited contribution. Frontiers in Plant Science. 4: 546.
Hollister, J., Arnold, B., Svedin, E., Xue, K. Dilkes, B., Bomblies, K. (2012) Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genetics 8: e1003093.
Yant, L., Hollister, J., Wright, K.M., Arnold, B.J., Higgins, J.D., Franklin, F.C.H., Bomblies, K. (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Current Biology 23: 2151-2156.