Dominance between self-incompatibility alleles determines the mating system of Capsella allopolyploids

Abstract

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 impede self-fertilization is controlled by two 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. Brassicaceae allopolyploid species are often self-compatible (SC) even when one of their parents is self-incompatible, but the causes of the loss of self-incompatibility (SI) in polyploid lineages have generally remained elusive. We used a series of synthetic hybrids obtained between self-fertilizing Capsella orientalis and outcrossing C. grandiflora to test whether the breakdown of SI in allopolyploid species, such as C. bursa-pastoris, could be explained by the dominance interactions between S-haplotypes inherited from the parental lineages. After establishing a database of reference S-allele sequences, we used RNA-sequencing data from young inflorescences to measure allele-specific expression of the SCR and SRK genes in diploid and tetraploid synthetic hybrids. We then compared the observed expression of SCR alleles with the predicted dominance relationship between S-haplotypes in pollen and with the seed set from autonomous self-fertilization in the synthetic hybrids. Our results formally establish that upon hybridization, the immediate effect on the mating system depends on the relative dominance between S-alleles inherited from the parental species. They illustrate that a detailed understanding of the genetic architecture of the control of SI is essential to predict the patterns of association between the mating system and changes in ploidy.

Molecular insights into self-incompatibility systems: From evolution to breeding

“…lyrata , and their predicted targets were as follows: class IV > class III > class II > class I ( Yasuda et al., 2021 ). Further analysis of interactions between sRNAs and their target sites in other SI species should provide more information on dominance–recessiveness mechanisms in Brassicaceae ( Fujii and Takayama, 2018 ; Duan et al., 2023 ).…”

Dominance modifiers at the Arabidopsis self-incompatibility locus retain proto-miRNA features and act through non-canonical pathways

“…This contrasts with the less complex dominance hierarchy of Brassica, where fewer allelic interactions are present, and a single functional sRNA molecule per precursor has been suggested to mediate all dominance relationships (7, 8). It is important to note that while we investigated a total of 15 S-alleles in this study, at least 43 are known to exist in A. halleri (15), and > 80 in the closely related Capsella grandiflora (22). Therefore, in this study we most likely underestimated the fraction of functional sRNAs in each precursor, since those that are non-functional in the allelic interactions explored here could potentially have a role in interactions that have not yet been characterized.…”