RESUMO
The shift from outcrossing to self-fertilization is one of the main evolutionary transitions in plants and has broad effects on evolutionary trajectories. In Brassicaceae, the ability to inhibit self-fertilization is controlled by 2 genes, SCR and SRK, tightly linked within the S-locus. A series of small non-coding RNAs also encoded within the S-locus regulates the transcriptional activity of SCR alleles, resulting in a linear dominance hierarchy between them. In Brassicaceae, natural allopolyploid species are often self-compatible (SC) even when one of the progenitor species is self-incompatible, but the reason why polyploid lineages tend to lose self-incompatibility (SI) and the timing of the loss of SI (immediately after ancestral hybridization between the progenitor species, or at a later stage after the formation of allopolyploid lineages) have generally remained elusive. We used a series of synthetic diploid and tetraploid hybrids obtained between self-fertilizing Capsella orientalis and outcrossing Capsella grandiflora to test whether the breakdown of SI could be observed immediately after hybridization, and whether the occurrence of SC phenotypes could be explained by the dominance interactions between S-haplotypes inherited from the parental lineages. We used RNA-sequencing data from young inflorescences to measure allele-specific expression of the SCR gene and infer dominance interactions in the synthetic hybrids. We then evaluated the seed set from autonomous self-pollination in the synthetic hybrids. Our results demonstrate that self-compatibility of the hybrids depends on the relative dominance between S-alleles inherited from the parental species, confirming that SI can be lost instantaneously upon formation of the ancestral allopolyploid lineage. They also confirm that the epigenetic regulation that controls dominance interactions between S-alleles can function between subgenomes in allopolyploids. Together, our results illustrate how a detailed knowledge of the mechanisms controlling SI can illuminate our understanding of the patterns of co-variation between the mating system and changes in ploidy.
RESUMO
In flowering plants, outcrossing is commonly ensured by self-incompatibility (SI) systems. These can be homomorphic (typically with many different allelic specificities) or can accompany flower heteromorphism (mostly with just two specificities and corresponding floral types). The SI system of the Oleaceae family is unusual, with the long-term maintenance of only two specificities but often without flower morphology differences. To elucidate the genomic architecture and molecular basis of this SI system, we obtained chromosome-scale genome assemblies of Phillyrea angustifolia individuals and related them to a genetic map. The S-locus region proved to have a segregating 543-kb indel unique to one specificity, suggesting a hemizygous region, as observed in all distylous systems so far studied at the genomic level. Only one of the predicted genes in this indel region is found in the olive tree, Olea europaea, genome, also within a segregating indel. We describe complete association between the presence/absence of this gene and the SI types determined for individuals of seven distantly related Oleaceae species. This gene is predicted to be involved in catabolism of the gibberellic acid (GA) hormone, and experimental manipulation of GA levels in developing buds modified the male and female SI responses of the two specificities in different ways. Our results provide a unique example of a homomorphic SI system, where a single conserved gibberellin-related gene in a hemizygous indel underlies the long-term maintenance of two groups of reproductive compatibility.