Near-Gapless and Haplotype-Resolved Capsella Genomes Enable Investigation into Genomic Consequences of Mating System Shifts

Abstract

The shift from outcrossing to self-fertilization is a common evolutionary transition in flowering plants. The genus Capsella, comprising the obligate outcrosser C. grandiflora and two self-fertile species, C. rubella and C. orientalis, provides a powerful system to explore genomic consequences of mating system shifts. Despite its utility, existing genomic resources in Capsella are fragmented, incomplete, and particularly deficient in repetitive genomic regions, hindering the study of transposable element (TE) dynamics and gene annotation. Here, we present high-quality, chromosome-scale, near-gapless genome assemblies for C. grandiflora, C. rubella, and C. orientalis. Leveraging these improved genomes, we created high-quality genomic resources for the Capsella genus by performing comprehensive, de novo annotations of protein-coding genes and TEs. Comparative genomic analysis among these species reveals differences in TE abundance, position, and production of small RNAs. These resources provide an unprecedented opportunity to explore how mating system transitions influence genome architecture, TE behavior, and gene evolution. This research also developed a static online platform for Capsella genomic resources, Capsella Database (CapBase, www.capsella.uk), to support community use of these resources. Our findings advance understanding of the genomic impacts of selfing and establish a robust foundation for future research into genomics, epigenomics, and evolutionary biology within Capsella and related plant systems. Significance statementThe Capsella species are model plants for investigating the genomic impacts of the shift from outcrossing to self-fertilization. However, genomic resources for these species remain poor. In this study, we created high-quality genome assemblies and annotations for three Capsella species, performed comparative genomic analysis among these genomes, and constructed the first Capsella online genomic database, CapBase (www.capsella.uk). These outputs provide a valuable foundation for studying plant genome dynamics following the evolution of self-fertilization.