- Population genomics
- Evolution of meiosis
- Gene network evolution
- Mechanisms of habitat adaptation and morphological evolution
Evolution of meiosis in Arabidopsis arenosa
Plants are quite adept at doubling their genome content through whole genome duplication. This can occur through hybridization of diverged genomes (allopolyploidy) or through doubling within a species such that all four homologs of each chromosome are roughly equivalent (autopolyploidy). Polyploidy is likely a very important force in plant evolution and speciation, but the proteins involved in stabilizing chromosome segregation in polyploids after they form, and how they might change in function remains largely mysterious.
What is the problem with doubling a genome? Consider meiosis - this fine-tuned machinery has been perfected over eons to separate pairs of homologous chromosomes. So what happens when suddenly four homologs are present? Often, it turns out, sorting all these extra copies is challenging. Work with artificially induced or young natural autopolyploids in an extensive body of literature suggests that diploid meiotic machinery is not usually well equipped for a chromosome duplicated situation and meiotic abnormalities, aneuploid gamete formation and low fertility can result. We now know A. arenosa is no exception - here too doubled diploid genotypes show meiotic abnormalities not observed in the evolved tetraploid (see Figure below from our collaborators, James Higgins and Chris Franklin).
The figure above shows metaphase I chromosome spreads from (A) diploid A. arenosa, (B) the natural autotetraploid with arrowhead indicating one unpaired univalent, and (C) a newly generated confirmed tetraploid made by treating diploid A. arenosa with colchicine. The colchicine doubled line has messy chromosome organization at metaphase I with some multivalent associations evident (bottom of panel). This suggests that the diploids are not "pre-adapted" to well organized meiosis as tetraploids. (These images were taken by James Higgins at the University of Birmingham, UK).
Established autopolyploids, however, are abundant in nature and are usually meiotically stable. In general these species have cytologically diploid-like chromosome behavior at meiosis, but the chromosomes may still associate randomly (so there are four alleles segregating at each locus instead of two). This is also true of A. arenosa, which shows regular, diploid-like chromosome pairing in meiotic metaphase I, albeit with apprently fewer chiasmata than diploids. How does this work? How do chromosomes with no partner preferences "know" to only pair with one other partner? What changes occured at the molecular level to cytologically diploidize meiosis and prevent multivalent formation in established A. arenosa?
To begin addressing how polyploid meiosis might stabilize, we undertook a genome scan for selection in tetraploid A. arenosa, and for divergence between diploid and tetraploid A. arenosa. We sequenced 16 tetraploid and 8 diploid individuals to ask whether there are signatures in the genome indicative of adaptation to whole genome duplication. Comparing the genomes of diploids and tetraploids, has been a fruitful collaboration with Levi Yant.
The image above shows the output from one of our genome scans (see Yant et al 2013). It shows divergence between diploid and tetraploid A. arenosa for 100 SNP windows. Peaks of divergence are evident, and one of them, noted here, is ASY3, a meiosis gene with one of the strongest peaks genome-wide.
The image above shows two examples of the very strong peaks we've found in our genome scan (soon to be published; Yant et al 2013). The dots are single SNPs - both of these genes are strongly differentiated between diploids and tetraploids, and both are important for events in early meiosis. For ASY3 at least, it is clear the peak itself lies in the coding region and not the promoter.
Our initial genome scans have revealed interesting candidate genes that may have been involved in either the initial formation of the tetraploids or in their subsequent meiotic stabilization (Hollister et al 2012; Yant et al 2013). We are following these up with molecular studies using genetic and cytogenetic approaches to gain molecular insight into autotetraploid meiosis. This is primarily the work of Kevin Wright, an NRSA postdoctoral fellow in the lab. Currently we are focusing mostly on early events in prophase I of meiosis. In one case, we already know that a genetic variant common in tetraploids but very rare in diploids is critical for successful meiosis: tetraploids homozygous for the diploid-like allele show extensive meiotic abnormalities that appear similar to those we see in colchicine-doubled diploids.
We are also investigating the molecular evolution and population genetics of several candidate genes that we know are differentiated between diploid and tetraploid A. arenosa. These have confirmed that the selective sweeps we have seen evidence of are very strong, and very discrete (they accompany just single genes, and sometimes even just part of a gene).
Relevant Publications from our lab:
- Yant, L.*, Hollister, J. D.*, Wright, K. M., Arnold, B. J., Higgins, J. D., Franklin, F. C. H. and Bomblies, K. (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Current Biology. Vol 23, pp. 2151-2156. * = contributed equally.
- Hunter, B.*, Wright, K. M.* and Bomblies, K. (2013) Short read sequencing in studies of natural variation and adaptation. Curr Op Plant Biol. Vol 16, pp. 85-91. * = contributed equally.
- Hollister, J., Arnold, B., Svedin, E., Xue, K., Dilkes, B. and Bomblies, K. (2012) Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genetics, 8(12): e1003093.