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 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 spanning decades suggests that diploid meiotic machinery is not usually well equipped for this 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.

 

But established autopolyploids 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 behavior. How does this work? How do chromosomes with no partner preferences "know" to only pair with one partner? What changes occured at the molecular level to cytologically diploidize meiosis and prevent multivalent formation in established A. arenosa?

 

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. We are following up these with molecular studies, and in parallel also initiating a genetic mapping experiment for meiotic stability. This project will provide a molecular characterization of autotetraploid meiosis. Currently we are focusing mostly on early events in meiosis - things that occur in zygotene and pachytene to ensure regular meiosis. 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.

 

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).