The shift from outcrossing to selfing is common in flowering plants1,2, but the genomic consequences and the speed at which they emerge remain poorly understood. An excellent model for understanding the evolution of self fertilization is provided by Capsella rubella, which became self compatible <200,000 years ago. We report a C. rubella reference genome sequence and compare RNA expression and polymorphism patterns between C. rubella and its outcrossing progenitor Capsella grandiflora. We found a clear shift in the expression of genes associated with flowering phenotypes, similar to that seen in Arabidopsis, in which self fertilization evolved about 1 million years ago. Comparisons of the two Capsella species showed evidence of rapid genome-wide relaxation of purifying selection in C. rubella without a concomitant change in transposable element abundance. Overall we document that the transition to selfing may be typified by parallel shifts in gene expression, along with a measurable reduction of purifying selection.

Gene family size variation is an important mechanism that shapes the natural variation for adaptation in various species. Despite its importance, the pattern of gene family size variation in green plants is still not well understood. In particular, the evolutionary pattern of genes and gene families remains unknown in the model plant Arabidopsis thaliana in the context of green plants. In this study, eight representative genomes of green plants are sampled to study gene family evolution and characterize the origination of A. thaliana genes, respectively. Four important insights gained are that: (i) the rate of gene gains and losses is about 0.001359 per gene every million years, similar to the rate in yeast, Drosophila, and mammals; (ii) some gene families evolved rapidly with extreme expansions or contractions, and 2745 gene families present in all the eight species represent the ‘core’ proteome of green plants; (iii) 70% of A. thaliana genes could be traced back to 450 million years ago; and (iv) intriguingly, A. thaliana genes with early origination are under stronger purifying selection and more conserved. In summary, the present study provides genome‐wide insights into evolutionary history and mechanisms of genes and gene families in green plants and especially in A. thaliana.

Capsella rubella is an inbreeding annual forb closely related to Arabidopsis thaliana, a model species widely used for studying natural variation in adaptive traits such as flowering time. Although mutations in dozens of genes can affect flowering of A. thaliana in the laboratory, only a handful of such genes vary in natural populations. Chief among these are FRIGIDA (FRI) and FLOWERING LOCUS C (FLC). Common and rare FRI mutations along with rare FLC mutations explain a large fraction of flowering-time variation in A. thaliana. Here we document flowering time under different conditions in 20 C. rubella accessions from across the species’ range. Similar to A. thaliana, vernalization, long photoperiods and elevated ambient temperature generally promote flowering. In this collection of C. rubella accessions, we did not find any obvious loss-of-function FRI alleles. Using mapping-by-sequencing with two strains that have contrasting flowering behaviors, we identified a splice-site mutation in FLC as the likely cause of early flowering in accession 1408. However, other similarly early C. rubella accessions did not share this mutation. We conclude that the genetic basis of flowering-time variation in C. rubella is complex, despite this very young species having undergone an extreme genetic bottleneck when it split from C. grandiflora a few tens of thousands of years ago.

Plants, like animals, use several lines of defense against pathogen attack. Prominent among genes that confer disease resistance are those encoding nucleotide-binding site-leucine-rich repeat (NB-LRR) proteins. Likely due to selection pressures caused by pathogens, NB-LRR genes are the most variable gene family in plants, but there appear to be species-specific limits to the number of NB-LRR genes in a genome. Allelic diversity within an individual is also increased by obligatory outcrossing, which leads to genome-wide heterozygosity. In this study, we compared the NB-LRR gene complement of the selfer Arabidopsis thaliana and its outcrossing close relative Arabidopsis lyrata. We then complemented and contrasted the interspecific patterns with studies of NB-LRR diversity within A. thaliana. Three important insights are as follows: (1) that both species have similar numbers of NB-LRR genes; (2) that loci with single NB-LRR genes are less variable than tandem arrays; and (3) that presence-absence polymorphisms within A. thaliana are not strongly correlated with the presence or absence of orthologs in A. lyrata. Although A. thaliana individuals are mostly homozygous and thus potentially less likely to suffer from aberrant interaction of NB-LRR proteins with newly introduced alleles, the number of NB-LRR genes is similar to that in A. lyrata. In intraspecific and interspecific comparisons, NB-LRR genes are also more variable than receptor-like protein genes. Finally, in contrast to Drosophila, there is a clearly positive relationship between interspecific divergence and intraspecific polymorphisms.

The S locus, a single polymorphic locus, is responsible for self-incompatibility (SI) in the Brassicaceae family and many related plant families. Despite its importance, our knowledge of S-locus evolution is largely restricted to the causal genes encoding the S-locus receptor kinase (SRK) receptor and S-locus cysteine-rich protein (SCR) ligand of the SI system. Here, we present high-quality sequences of the genomic region of six S-locus haplotypes: Arabidopsis (Arabidopsis thaliana; one haplotype), Arabidopsis lyrata (four haplotypes), and Capsella rubella (one haplotype). We compared these with reference S-locus haplotypes of the self-compatible Arabidopsis and its SI congener A. lyrata. We subsequently reconstructed the likely genomic organization of the S locus in the most recent common ancestor of Arabidopsis and Capsella. As previously reported, the two SI-determining genes, SCR and SRK, showed a pattern of coevolution. In addition, consistent with previous studies, we found that duplication, gene conversion, and positive selection have been important factors in the evolution of these two genes and appear to contribute to the generation of new recognition specificities. Intriguingly, the inactive pseudo-S-locus haplotype in the self-compatible species C. rubella is likely to be an old S-locus haplotype that only very recently became fixed when C. rubella split off from its SI ancestor, Capsella grandiflora.