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

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.

Inference of Polyploid Origin and Inheritance Mode from Population Genomic Data.

Whole-genome duplications yield varied chromosomal pairing patterns, ranging from strictly bivalent to multivalent, resulting in disomic and polysomic inheritance modes. In the bivalent case, homeologous chromosomes form pairs, where in a multivalent pattern all copies are homologous and are therefore free to pair and recombine. As sufficient sequencing data is more readily available than high-quality cytological assessments of meiotic behavior or population genetic assessment of allelic segregation, especially for non-model organisms, bioinformatics approaches to infer origins and inheritance modes of polyploids using short-read sequencing data are attractive. Here we describe two such approaches, where the first is based on distributions of allelic read depth at heterozygous sites within an individual, as the expectations of such distributions are different for disomic and polysomic inheritance modes. The second approach is more laborious and based on a phylogenetic assessment of partially phased haplotypes of a polyploid in comparison to the closest diploid relatives. We discuss the sources of deviations from expected inheritance patterns, advantages and pitfalls of both methods, effects of mating types on the performance of the methods, and possible future developments.

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae.

Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self-compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae (Arabidopsis suecica, Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S-locus from one parental lineage was dominant over the functional S-locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.

Whole genome duplication in coast redwood (Sequoia sempervirens) and its implications for explaining the rarity of polyploidy in conifers.

Polyploidy is common and an important evolutionary factor in most land plant lineages, but it is rare in gymnosperms. Coast redwood (Sequoia sempervirens) is one of just two polyploid conifer species and the only hexaploid. Evidence from fossil guard cell size suggests that polyploidy in Sequoia dates to the Eocene. Numerous hypotheses about the mechanism of polyploidy and parental genome donors have been proposed, based primarily on morphological and cytological data, but it remains unclear how Sequoia became polyploid and why this lineage overcame an apparent gymnosperm barrier to whole-genome duplication (WGD). We sequenced transcriptomes and used phylogenetic inference, Bayesian concordance analysis and paralog age distributions to resolve relationships among gene copies in hexaploid coast redwood and close relatives. Our data show that hexaploidy in coast redwood is best explained by autopolyploidy or, if there was allopolyploidy, it happened within the Californian redwood clade. We found that duplicate genes have more similar sequences than expected, given the age of the inferred polyploidization. Conflict between molecular and fossil estimates of WGD can be explained if diploidization occurred very slowly following polyploidization. We extrapolate from this to suggest that the rarity of polyploidy in gymnosperms may be due to slow diploidization in this clade.