Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae).

The breakdown of self-incompatibility (SI) in angiosperms is one of the most commonly observed evolutionary transitions. While multiple examples of SI breakdown have been documented in natural populations, there is strikingly little evidence of stable within-population polymorphism with both inbreeding (self-compatible) and outcrossing (self-incompatible) individuals. This absence of breeding system polymorphism corroborates theoretical expectations that predict that in/outbreeding polymorphism is possible only under very restricted conditions. However, theory also predicts that a diallelic sporophytic SI system should facilitate the maintenance of such polymorphism. We tested this prediction by studying the breeding system of Ligustrum vulgare L., an insect-pollinated hermaphroditic species of the Oleaceae family. Using stigma tests with controlled pollination and paternity assignment of open-pollinated progenies, we confirmed the existence of two self-incompatibility groups in this species. We also demonstrated the occurrence of self-compatible individuals in different populations of Western Europe arising from a mutation affecting the functioning of the pollen component of SI. Our results show that the observed low frequency of self-compatible individuals in natural populations is compatible with theoretical predictions only if inbreeding depression is very high.

The homomorphic self-incompatibility system in Oleaceae is controlled by a hemizygous genomic region expressing a gibberellin pathway gene.

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.

Base-Pairing Requirements for Small RNA-Mediated Gene Silencing of Recessive Self-Incompatibility Alleles in Arabidopsis halleri.

Small noncoding RNAs are central regulators of genome activity and stability. Their regulatory function typically involves sequence similarity with their target sites, but understanding the criteria by which they specifically recognize and regulate their targets across the genome remains a major challenge in the field, especially in the face of the diversity of silencing pathways involved. The dominance hierarchy among self-incompatibility alleles in Brassicaceae is controlled by interactions between a highly diversified set of small noncoding RNAs produced by dominant S-alleles and their corresponding target sites on recessive S-alleles. By controlled crosses, we created numerous heterozygous combinations of S-alleles in Arabidopsis halleri and developed an real-time quantitative PCR assay to compare allele-specific transcript levels for the pollen determinant of self-incompatibility (SCR). This provides the unique opportunity to evaluate the precise base-pairing requirements for effective transcriptional regulation of this target gene. We found strong transcriptional silencing of recessive SCR alleles in all heterozygote combinations examined. A simple threshold model of base pairing for the small RNA-target interaction captures most of the variation in SCR transcript levels. For a subset of S-alleles, we also measured allele-specific transcript levels of the determinant of pistil specificity (SRK), and found sharply distinct expression dynamics throughout flower development between SCR and SRK In contrast to SCR, both SRK alleles were expressed at similar levels in the heterozygote genotypes examined, suggesting no transcriptional control of dominance for this gene. We discuss the implications for the evolutionary processes associated with the origin and maintenance of the dominance hierarchy among self-incompatibility alleles.

Genomic Analyses Yield Markers for Identifying Agronomically Important Genes in Potato.

Wild potato species have substantial phenotypic and physiological diversity. Here, we report a comprehensive assessment of wild and cultivated potato species based on genomic analyses of 201 accessions of Solanum section Petota. We sequenced the genomes of these 201 accessions and identified 6 487 006 high-quality single nucleotide polymorphisms (SNPs) from 167 accessions in clade 4 of Solanum section Petota, including 146 wild and 21 cultivated diploid potato accessions with a broad geographic distribution. Genome-wide genetic variation analysis showed that the diversity of wild potatoes is higher than that of cultivated potatoes, and much higher genetic diversity in the agronomically important disease resistance genes was observed in wild potatoes. Furthermore, by exploiting information about known quantitative trait loci (QTL), we identified 609 genes under selection, including those correlated with the loss of bitterness in tubers and those involved in tuberization, two major domesticated traits of potato. Phylogenetic analyses revealed a north-south division of all species in clade 4, not just those in the S. brevicaule complex, and further supported S. candolleanum as the progenitor of cultivated potato and the monophyletic origin of cultivated potato in southern Peru. In addition, we analyzed the genome of S. candolleanum and identified 529 genes lost in cultivated potato. Collectively, the molecular markers generated in this study provide a valuable resource for the identification of agronomically important genes useful for potato breeding.