Meiotic adaptation to genome duplication in Arabidopsis arenosa

Abstract

Whole genome duplication (WGD) is a major factor in the evolution of multicellular eukaryotes, yet by doubling the number of homologs, WGD severely challenges reliable chromosome segregation, a process conserved across kingdoms. Despite this, numerous genome-duplicated (polyploid) species persist in nature, indicating early problems can be overcome. Little is known about which genes are involved--only one has been molecularly characterized. To gain new insights into the molecular basis of adaptation to polyploidy, we investigated genome-wide patterns of differentiation between natural diploids and tetraploids of Arabidopsis arenosa, an outcrossing relative of A. thaliana. We first show that diploids are not preadapted to polyploid meiosis. We then use a genome scanning approach to show that although polymorphism is extensively shared across ploidy levels, there is strong ploidy-specific differentiation in 39 regions spanning 44 genes. These are discrete, mostly single-gene peaks of sharply elevated differentiation. Among these peaks are eight meiosis genes whose encoded proteins coordinate a specific subset of early meiotic functions, suggesting these genes comprise a polygenic solution to WGD-associated chromosome segregation challenges. Our findings indicate that even conserved meiotic processes can be capable of nimble evolutionary shifts when required.

Figure 1. Chromosome spreads and map locations

(A) DAPI-stained meiotic chromosome spreads. Left column shows chromosome counts, middle column, diakinesis, and right column, metaphase I. Top row shows diploid A. arenosa. Somatic chromosome counts are as expected (2N=16) and associations are bivalents. Second row shows a natural tetraploid. Chromosome count (2N=32) in somatic cells (left). Middle and right panels show bivalent associations. Bottom row shows neo-tetraploid A. arenosa. Somatic chromosome counts (left) confirmed tetraploidy (2N=32). Extensive multivalent formation and fine ectopic inter-chromosomal connections (examples indicated by arrows) are evident at diakinesis and metaphase I. (B) Map of populations. Tetraploid populations are indicated with closed circles and diploids with open circles.

Figure 2. Diversity and differentiation of meiosis genes relative to genome-wide patterns

Genome-wide values for 100 SNP windows for F_ST (A), CLR Score (B), and Diversity/Differentiation residuals (C). X-axes are linear, indicate means, and outlier meiosis genes are labeled. (D) Nucleotide diversity of 100 SNP windows in tetraploids plotted against differentiation between ploidies. Heavy line shows linear regression and lighter line, 1% cutoff. Red dots represent 100 SNP windows in meiosis genes with extreme outliers labeled. Note: each gene can have multiple hits as it can have multiple 100 SNP windows. (E) CLR Score vs Diversity/Differentiation Residual for all windows. Dotted lines indicate 0.5% cutoffs. Meiosis genes are indicated in respective quadrants.

Figure 3. Most differentiated regions and examples of differentiation in two sweep candidates

(A) Differentiated regions (vertical lines), with meiosis genes labeled. ZYP1 consists of tandem duplicates, ZYP1a and ZYP1b. (B) Two example differentiated regions in meiosis genes. Dots represent polymorphic SNPs. X-axis gives chromosome location. Y-axis shows degree of differentiation calculated by subtracting diploid from tetraploid allele frequency. Short gaps are regions in which reads did not align due to repeat masking, high intergenic polymorphism, or deletions in A. arenosa relative to A. lyrata. These were verified with alignment of an A. arenosa de novo assembly and paired end read information.