The Capsella rubella genome and the genomic consequences of rapid mating system evolution

Journal name:
Nature Genetics
Volume:
45,
Pages:
831–835
Year published:
DOI:
doi:10.1038/ng.2669
Received
Accepted
Published online

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

Figures

  1. Genomic structures, chromosome painting and comparative genomic mapping in C. rubella, A. lyrata and A. thaliana.
    Figure 1: Genomic structures, chromosome painting and comparative genomic mapping in C. rubella, A. lyrata and A. thaliana.

    (a) Comparative genome structure and major chromosome landmarks in C. rubella (CR). The 24 ancestral genomic blocks are indicated by uppercase letters (A–X) and are colored according to their position on the eight chromosomes of the ancestral crucifer karyotype (ACK12). (b) Comparative chromosome painting of CR1 and CR2. Differentially labeled A. thaliana BAC contigs corresponding to the genomic blocks A, B, C, D and E were used as painting probes on the pachytene bivalents of CR1 and CR2. The true fluorescence signals were pseudocolored according to the color code used in a. The arrowheads indicate unpainted pericentromeric heterochromatin. Scale bars, 10 μm. (c,d) Comparative genome mapping of C. rubella with A. lyrata (AL; c) and A. thaliana (AT; d). The outer ring shows the percentage of the genomic window that comprises transposable elements, with a maximum at 60% coverage, the second ring shows gene density, and the inner ring shows orthologous regions between species on the basis of whole-genome alignment and orthologous chaining. Note that the A. lyrata, but not the C. rubella, assembly includes gaps for inferred centromeric heterochromatin. From synteny analyses of the three species, the approximate gene intervals contained within each block include: A/B, AT1G01010–AT1G36980; C, AT1G41830–AT1G56200; D, AT1G56210–AT1G64720; E, AT1G64790–AT1G80950; F, AT3G01070–AT3G25530; G, AT2G04039–AT2G07050; H, AT2G10870–AT2G20900; I, AT2G20920–AT2G26430; J, AT2G26670–AT2G48160; K, AT2G01060–AT2G04038; L, AT3G25545–AT3G32980; M/N, AT3G42170–AT3G63490; O, AT4G00026–AT4G05530; P, AT4G06534–AT4G12590; Q/R, AT5G01010–AT5G30510; S, AT5G32440–AT5G42110; T/U, AT4G12640–AT4G40100; V, AT5G42140–AT5G47760; W/X, AT5G47800–AT5G67640.

  2. Evolution of gene expression in selfing and outcrossing Capsella and comparisons to Arabidopsis.
    Figure 2: Evolution of gene expression in selfing and outcrossing Capsella and comparisons to Arabidopsis.

    Distribution of fold changes in gene expression in C. grandiflora relative to C. rubella (x axis) and A. lyrata relative to A. thaliana (y axis) at genes showing significant downregulation or significant upregulation in C. rubella.

  3. Polymorphism comparisons in C. rubella and C. grandiflora.
    Figure 3: Polymorphism comparisons in C. rubella and C. grandiflora.

    (a) Average pairwise differences (π) at nonsynonymous (nonsyn) and synonymous (syn) sites. Error bars indicate standard errors across all loci. Cr, C. rubella; Cg, C. grandiflora. (b) Ratio of nonsynonymous to synonymous polymorphisms at each derived frequency class using data subsampled to six chromosomes per species. N. paniculata was used as an outgroup to infer derived status. (c) Proportion of synonymous and nonsynonymous polymorphisms unique to each species, as well as shared and fixed differences. Simulated (sim) values are from forward computer simulations using the inferred demographic model and strength of selection on nonsynonymous sites (see main text). Obs, observed.

  4. Evolution of genome structure and transposable element abundance in Capsella and Arabidopsis.
    Figure 4: Evolution of genome structure and transposable element abundance in Capsella and Arabidopsis.

    (a) Slope of the physical positions in orthologous blocks between C. rubella and A. thaliana and A. lyrata. Ancestral orthologous blocks are labeled on the x axis (see Fig. 1). (b) Transposable element genomic coverage in the three species. LINE, long interspersed nucleotide repetitive elements; SINE, short interspersed nucleotide repetitive elements. (c) Distribution of the distances between transposable elements and their nearest protein-coding genes. (d) Age distribution of full-length LTR retrotransposons estimated using the rate of substitution between LTRs of individual insertions and assuming a substitution rate of 7 × 10−9 per bp per generation. MYA, million years ago.

  5. Estimates of transposable element copy number and expression in C. rubella and C. grandiflora.
    Figure 5: Estimates of transposable element copy number and expression in C. rubella and C. grandiflora.

    (a) Numbers of insertion sites identified using read mapping of paired-end Illumina genomic data (using Popoolation TE) in two C. rubella accessions and two C. grandiflora accessions. SINE/LINE, SINE and LINE. (b) Mean and standard error of the proportion of RNA-seq transcripts mapping to transposable elements. (c) Distribution of transposable element insertions along chromosome 1 in two C. rubella accessions and two C. grandiflora accessions.

Accession codes

Primary accessions

BioProject

Gene Expression Omnibus

NCBI Reference Sequence

Sequence Read Archive

References

  1. Barrett, S.C.H. The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274284 (2002).
  2. Stebbins, G.L. Self fertilization and population variability in the higher plants. Am. Nat. 91, 337354 (1957).
  3. Charlesworth, D. & Willis, J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783796 (2009).
  4. Charlesworth, D. & Wright, S.I. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11, 685690 (2001).
  5. Lynch, M., Conery, J. & Burger, R. Mutational meltdowns in sexual populations. Evolution 49, 10671080 (1995).
  6. Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 9294 (2010).
  7. Tang, C. et al. The evolution of selfing in Arabidopsis thaliana. Science 317, 10701072 (2007).
  8. Guo, Y.L. 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, 52465251 (2009).
  9. Foxe, J.P. et al. Recent speciation associated with the evolution of selfing in Capsella. Proc. Natl. Acad. Sci. USA 106, 52415245 (2009).
  10. St Onge, K.R., Kallman, T., Slotte, T., Lascoux, M. & Palme, A.E. Contrasting demographic history and population structure in Capsella rubella and Capsella grandiflora, two closely related species with different mating systems. Mol. Ecol. 20, 33063320 (2011).
  11. Slotte, T., Hazzouri, K.M., Stern, D., Andolfatto, P. & Wright, S.I. Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66, 13601374 (2012).
  12. Schranz, M.E., Lysak, M.A. & Mitchell-Olds, T. The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11, 535542 (2006).
  13. Ye, Q. et al. Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 107, 61006105 (2010).
  14. Escobar, J.S. et al. An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64, 28552872 (2010).
  15. Haudry, A. et al. Mating system and recombination affect molecular evolution in four Triticeae species. Genet. Res. (Camb.) 90, 97109 (2008).
  16. Wright, S.I., Lauga, B. & Charlesworth, D. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19, 14071420 (2002).
  17. Wright, S.I. & Schoen, D.J. Transposon dynamics and the breeding system. Genetica 107, 139148 (1999).
  18. Charlesworth, B. & Langley, C.H. The evolution of self-regulated transposition of transposable elements. Genetics 112, 359383 (1986).
  19. Hu, T.T. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476481 (2011).
  20. Hollister, J.D. et al. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc. Natl. Acad. Sci. USA 108, 23222327 (2011).
  21. Jaffe, D.B. et al. Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13, 9196 (2003).
  22. Guo, Y.L., Todesco, M., Hagmann, J., Das, S. & Weigel, D. Independent FLC mutations as causes of flowering time variation in Arabidopsis thaliana and Capsella rubella. Genetics 192, 729739 (2012).
  23. Goodstein, D.M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178D1186 (2012).
  24. Haas, B.J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 56545666 (2003).
  25. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403410 (1990).
  26. Solovyev, V., Kosarev, P., Seledsov, I. & Vorobyev, D. Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7 (suppl. 1), S10.1S10.12 (2006).
  27. Slater, G.S. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).
  28. Yeh, R.F., Lim, L.P. & Burge, C.B. Computational inference of homologous gene structures in the human genome. Genome Res. 11, 803816 (2001).
  29. Lyons, E. & Freeling, M. How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53, 661673 (2008).
  30. Harris, R.S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Penn. State Univ. (2007).
  31. Kent, W.J., Baertsch, R., Hinrichs, A., Miller, W. & Haussler, D. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl. Acad. Sci. USA 100, 1148411489 (2003).
  32. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 16391645 (2009).
  33. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419423 (2011).
  34. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562578 (2012).
  35. Lunter, G. & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936939 (2011).
  36. Flutre, T., Duprat, E., Feuillet, C. & Quesneville, H. Considering transposable element diversification in de novo annotation approaches. PLoS ONE 6, e16526 (2011).
  37. Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18 (2008).
  38. Edgar, R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
  39. Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276277 (2000).
  40. Lysak, M.A. & Mandáková, T. Analysis of plant meiotic chromosomes by chromosome painting. Methods Mol. Biol 990, 1324 (2013).

Download references

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada.

    • Tanja Slotte,
    • Khaled M Hazzouri,
    • J Arvid Ågren,
    • Juan S Escobar,
    • L Killian Newman,
    • Wei Wang &
    • Stephen I Wright
  2. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

    • Tanja Slotte &
    • Kim Steige
  3. Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

    • Tanja Slotte
  4. Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates.

    • Khaled M Hazzouri
  5. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.

    • Daniel Koenig,
    • Lisa M Smith,
    • Stefan R Henz &
    • Detlef Weigel
  6. Unité de Recherche en Génomique-Info, Institut Scientifique de Recherche Agronomique (INRA) Centre de Versailles-Grignon, Versailles, France.

    • Florian Maumus &
    • Hadi Quesneville
  7. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.

    • Ya-Long Guo
  8. Department of Biology, McGill University, Montreal, Quebec, Canada.

    • Adrian E Platts &
    • Emilio Vello
  9. Laboratory of Plant Cytogenomics, Central European Institute of Technology (CEITEC), Masaryk University, Brno, Czech Republic.

    • Terezie Mandáková &
    • Martin A Lysak
  10. Department of Biology, University of Utah, Salt Lake City, Utah, USA.

    • Joshua Steffen &
    • Richard M Clark
  11. Department of Natural Sciences, Colby-Sawyer College, New London, New Hampshire, USA.

    • Joshua Steffen
  12. Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, California, USA.

    • Shohei Takuno &
    • Brandon S Gaut
  13. Department of Plant Sciences, University of California Davis, Davis, California, USA.

    • Shohei Takuno
  14. Department of Evolution and Ecology, University of California Davis, Davis, California, USA.

    • Yaniv Brandvain &
    • Graham Coop
  15. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, USA.

    • Peter Andolfatto &
    • Tina T Hu
  16. The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USA.

    • Peter Andolfatto &
    • Tina T Hu
  17. School of Computer Science, McGill University, Montreal, Quebec, Canada.

    • Mathieu Blanchette
  18. Gregor Mendel Institute, Austrian Academy of Science, Vienna, Austria.

    • Magnus Nordborg
  19. HudsonAlpha Institute of Biotechnology, Huntsville, Alabama, USA.

    • Jerry Jenkins,
    • Jane Grimwood &
    • Jeremy Schmutz
  20. US Department of Energy (DoE), Joint Genome Institute (JGI), Walnut Creek, California, USA.

    • Jarrod Chapman,
    • Simon Prochnik,
    • Shengqiang Shu,
    • Daniel Rokhsar &
    • Jeremy Schmutz
  21. The Center for Integrative Genomics, University of California Berkeley, Berkeley, California, USA.

    • Daniel Rokhsar
  22. Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario, Canada.

    • Stephen I Wright

Contributions

B.S.G., M.N., J. Schmutz, T.S., D.R., D.W. and S.I.W. conceived and designed the study. Y.-L.G., K.M.H., D.K., J. Steffen and T.S. prepared samples for sequencing. J.J. and J. Schmutz conducted de novo assembly of C. rubella. Y.-L.G., S.R.H., S.P., D.R. and S.S. performed genome annotation. J.G. led the data collection of BAC-end and clone sequencing. P.A., K.M.H., T.T.H., T.S. and S.I.W. conducted genetic mapping analysis. J.A.Å., Y.-L.G., D.K., F.M., H.Q. and W.W. performed the transposon analysis. Y.B., G.C., J.S.E., K.M.H., L.K.N., K.S., T.S. and S.I.W. conducted population genetic analysis. R.M.C., J. Steffen, L.M.S., K.M.H. and A.E.P. conducted the RNA sequence and expression analysis. M.B. and A.E.P. conducted de novo assembly of N. paniculata and whole-genome alignments. J.C. led the de novo assembly of C. grandiflora. A.E.P., S.T. and E.V. conducted comparative genomic analysis. T.M. and M.A.L. conducted FISH and chromosome painting. B.S.G., M.N., T.S., D.W. and S.I.W. wrote the paper with contributions from all authors.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Text and Figures (3 MB)

    Supplementary Figures 1–11, Supplementary Tables 1–16 and Supplementary Note

Additional data