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.
At a glance
- The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274–284 (2002).
- Self fertilization and population variability in the higher plants. Am. Nat. 91, 337–354 (1957).
- The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009). &
- Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11, 685–690 (2001). &
- Mutational meltdowns in sexual populations. Evolution 49, 1067–1080 (1995). , &
- The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92–94 (2010). et al.
- The evolution of selfing in Arabidopsis thaliana. Science 317, 1070–1072 (2007). et al.
- Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc. Natl. Acad. Sci. USA 106, 5246–5251 (2009). et al.
- Recent speciation associated with the evolution of selfing in Capsella. Proc. Natl. Acad. Sci. USA 106, 5241–5245 (2009). et al.
- Contrasting demographic history and population structure in Capsella rubella and Capsella grandiflora, two closely related species with different mating systems. Mol. Ecol. 20, 3306–3320 (2011). , , , &
- Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66, 1360–1374 (2012). , , , &
- The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11, 535–542 (2006). , &
- Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 107, 6100–6105 (2010). et al.
- An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64, 2855–2872 (2010). et al.
- Mating system and recombination affect molecular evolution in four Triticeae species. Genet. Res. (Camb.) 90, 97–109 (2008). et al.
- Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19, 1407–1420 (2002). , &
- Transposon dynamics and the breeding system. Genetica 107, 139–148 (1999). &
- The evolution of self-regulated transposition of transposable elements. Genetics 112, 359–383 (1986). &
- The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476–481 (2011). et al.
- Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc. Natl. Acad. Sci. USA 108, 2322–2327 (2011). et al.
- Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13, 91–96 (2003). et al.
- Independent FLC mutations as causes of flowering time variation in Arabidopsis thaliana and Capsella rubella. Genetics 192, 729–739 (2012). , , , &
- Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186 (2012). et al.
- Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666 (2003). et al.
- Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990). , , , &
- Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7 (suppl. 1), S10.1–S10.12 (2006). , , &
- Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005). &
- Computational inference of homologous gene structures in the human genome. Genome Res. 11, 803–816 (2001). , &
- How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53, 661–673 (2008). &
- Improved Pairwise Alignment of Genomic DNA. PhD thesis, Penn. State Univ. (2007).
- Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl. Acad. Sci. USA 100, 11484–11489 (2003). , , , &
- Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009). et al.
- Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011). et al.
- Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012). et al.
- Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936–939 (2011). &
- Considering transposable element diversification in de novo annotation approaches. PLoS ONE 6, e16526 (2011). , , &
- LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18 (2008). , &
- MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
- EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000). , &
- Analysis of plant meiotic chromosomes by chromosome painting. Methods Mol. Biol 990, 13–24 (2013). &
- Supplementary Text and Figures (3 MB)
Supplementary Figures 1–11, Supplementary Tables 1–16 and Supplementary Note