Transition to Self-compatibility Associated With Dominant S-allele in a Diploid Siberian Progenitor of Allotetraploid Arabidopsis kamchatica Revealed by Arabidopsis lyrata Genomes

Abstract

A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here, we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid Arabidopsis kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to ∼90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

Keywords: Arabidopsis kamchatica; Arabidopsis lyrata; S-locus; allopolyploidy; self-compatibility.

Fig. 1.

Segregating large structural variants in Arabidopsis lyrata. (A) Eleven large inversions between North American MN47 v1 and both Siberian NT1 A. lyrata and the Arabidopsis arenosa subgenome of Arabidopsis suecica are not observed between NT1 and A. suecica (supplementary table S2, Supplementary Material online), suggesting these inversions are likely artifacts in the MN47 v1 assembly. (B) Segregating inversions in A. lyrata observed following reassembly by long reads and manual curation using Hi-C data of the North American MN47 genome and its alignment to the Siberian NT1 A. lyrata genome. Five inversions unique to MN47 (the longest being ∼2.4 Mb in size) are highlighted.

Fig. 2.

S-locus structure of the Siberian NT1 selfing Arabidopsis lyrata population. (A) Phylogenetic tree of SCR proteins reveals clustering of NT1 SCR (green) and AhS12. (B) Comparison of the S-locus region of the A. lyrata NT1 genome assembly with the Arabidopsis halleri S12 haplotype (Durand et al. 2014). Links between S-loci are colored according to the Blast scores from highest (blue) to lowest (gray). SCR, SRK, and flanking U-box and ARK3 genes have green, orange, and purple borders, respectively. SRK gene appears to be completely absent from the S-locus of the NT1 A. lyrata selfing accession. The only Blast hit to SRK is a spurious hit to ARK3 as they both encode receptor-like serine/threonine kinases. (C) Protein sequence alignment of S-locus SCR genes from A. halleri and A. lyrata, including NT1. One of the eight conserved cysteines important for structural integrity has been lost from the NT1 SCR protein.

Fig. 3.

(A) Map of short-read sequenced Siberian Arabidopsis lyrata (circles) and Arabidopsis kamchatica (triangles). Live A. lyrata accessions names start with NT, herbarium sample names start with MW, a previously published sample of A. lyrata has been assigned the SRR and DRR prefix, and A. kamchatica samples start with SAMD. Colors indicate heterozygosity per sample, calculated by the percent of heterozygous sites. (B) Network depiction of Nei's D between individuals shows that selfing A. lyrata is genetically closer to A. kamchatica than the outcrossing populations. Whereas the network is drawn as unrooted, an outgroup accession provides context for interpretation. Individual genetic distances are also shown as heatmap in supplementary figure S14, Supplementary Material online. (C) Neighbor-joining tree of Siberian A. lyrata accessions with heterozygosity and genotyped SCR and SRK alleles. (D) Best-fit demographic model of divergence, a bottleneck in selfers, and asymmetric migration between selfing and outcrossing lineages, with parameter estimate for divergence time. T_DIV, time of divergence between selfing and outcrossing lineage (origin of selfing); Ne_ANC, effective population size of ancestor lineage; Ne_POP1, effective population size of selfing lineage; Ne_POP2, effective population size of outcrossing lineage; T_BOT, time of bottleneck in selfing lineage; Nm₁₂ and Nm₂₁, the number of migrants between selfing and outcrossing lineages. Further values are reported in table 1. Point estimates and confidence intervals are reported in table 1; point estimates for all tested models are reported in supplementary table S4, Supplementary Material online.

Fig. 4.

(A) Self-pollinated F1 progeny (F1.1-1) resulting from a cross between a self-incompatible (shown in B) ♀ TE10.3-2 Arabidopsis lyrata accession and ♂ NT1 self-compatible A. lyrata accession shows pollen tube growth (yellow arrow) and dominance of self-compatibility in the F1 generation. (B) Self-pollinated self-incompatible A. lyrata accession TE10.3-2 (used as the maternal plant in A shows no pollen tube growth, demonstrating its self-incompatibility. (C) The geographical distribution of Arabidopsis kamchatica S-haplotypes shows a strong population structure across the species range. Circles are individual accessions, with S-haplogroups indicated by colors of pie slices. Arabidopsis halleri orthologous S-haplogroups are mentioned in the parenthesis next to the A. kamchatica S-haplogroups (AkS-A-E). Circle outline indicates either previously published data (grey) or newly reported accessions (black). A. kamchatica occurrences from the Global Biodiversity Information Facility (GBIF) are indicated by transparent grey dots.