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

Tanja Slotte; Khaled M. Hazzouri; J. Arvid Ågren; Daniel Koenig; Florian Maumus; Ya Long Guo; Kim Steige; Adrian E. Platts; Juan S. Escobar; L. Killian Newman; Wei Wang; Terezie Mandáková; Emilio Vello; Lisa M. Smith; Stefan R. Henz; Joshua Steffen; Shohei Takuno; Yaniv Brandvain; Graham Coop; Peter Andolfatto; Tina T. Hu; Mathieu Blanchette; Richard M. Clark; Hadi Quesneville; Magnus Nordborg; Brandon S. Gaut; Martin A. Lysak; Jerry Jenkins; Jane Grimwood; Jarrod Chapman; Simon Prochnik; Shengqiang Shu; Daniel Rokhsar; Jeremy Schmutz; Detlef Weigel; Stephen I. Wright

doi:10.1038/ng.2669

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

Tanja Slotte, Khaled M. Hazzouri, J. Arvid Ågren, Daniel Koenig, Florian Maumus, Ya Long Guo, Kim Steige, Adrian E. Platts, Juan S. Escobar, L. Killian Newman, Wei Wang, Terezie Mandáková, Emilio Vello, Lisa M. Smith, Stefan R. Henz, Joshua Steffen, Shohei Takuno, Yaniv Brandvain, Graham Coop, Peter AndolfattoTina T. Hu, Mathieu Blanchette, Richard M. Clark, Hadi Quesneville, Magnus Nordborg, Brandon S. Gaut, Martin A. Lysak, Jerry Jenkins, Jane Grimwood, Jarrod Chapman, Simon Prochnik, Shengqiang Shu, Daniel Rokhsar, Jeremy Schmutz, Detlef Weigel, Stephen I. Wright

Plant and Microbial Biology

Research output: Contribution to journal › Article › peer-review

285 Scopus citations

Abstract

The shift from outcrossing to selfing is common in flowering plants, 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.

Original language	English (US)
Pages (from-to)	831-835
Number of pages	5
Journal	Nature Genetics
Volume	45
Issue number	7
DOIs	https://doi.org/10.1038/ng.2669
State	Published - Jul 2013

Bibliographical note

Funding Information:
The work conducted by the DoE JGI is supported by the Office of Science of the DoE under contract number DE-AC02-05CH11231. We thank J. Bergelson, J. Borevitz, A. Hall, C. Langley, K. Mayer, J. Nasrallah, B. Neuffer, Y. Van de Peer and O. Savolainen for contributing to the initial sequencing proposal submitted to the Community Sequencing Program at JGI. We also thank T. Bureau, D. Schoen, P. Harrison, J. Stinchcombe, A. Moses and E. Harmsen for their contributions to the Value-directed Evolutionary Genomics Initiative (VEGI) grant (Genome Quebec/Genome Canada), which funded C. grandiflora genomic and mRNA sequencing, and G. Coupland (Max Planck Institute for Plant Breeding Research) and colleagues for information on Arabis alpina repeats. The work was supported by the Max Planck Society (D.W.), the Genome Quebec and Genome Canada VEGI grant (S.I.W. and M.B.), the Natural Sciences and Engineering Research Council of Canada (NSERC) (S.I.W.), the Swedish Research Council (T.S.), the Carl Trygger and Erik Philip-Sörensen foundations (T.S.), National Science Foundation (NSF) grant 0929262 (J. Steffen and R.M.C.), the French National Research Agency (ANR-08-KBBE-012-02 to H.Q.), the Czech Science Foundation (excellence cluster P501/12/G090 to M.A.L.) and the European Regional Development Fund (CZ.1.05/1.1.00/02.0068 to M.A.L.). D.K. was supported by a Human Frontiers in Science Program Long-Term Fellowship, and G.C. was supported by the Alfred P. Sloan Foundation. Population genetics analyses were performed on resources provided by the Swedish National Infrastructure for Computing (SNIC) through the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under project b2012122. L.M.S. was supported by a European Community FP7 Marie Curie Fellowship (PIEF-GA-2008-221553) and an EMBO Long-Term fellowship.

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Slotte, T., Hazzouri, K. M., Ågren, J. A., Koenig, D., Maumus, F., Guo, Y. L., Steige, K., Platts, A. E., Escobar, J. S., Newman, L. K., Wang, W., Mandáková, T., Vello, E., Smith, L. M., Henz, S. R., Steffen, J., Takuno, S., Brandvain, Y., Coop, G., ... Wright, S. I. (2013). The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nature Genetics, 45(7), 831-835. https://doi.org/10.1038/ng.2669

Slotte, T, Hazzouri, KM, Ågren, JA, Koenig, D, Maumus, F, Guo, YL, Steige, K, Platts, AE, Escobar, JS, Newman, LK, Wang, W, Mandáková, T, Vello, E, Smith, LM, Henz, SR, Steffen, J, Takuno, S, Brandvain, Y, Coop, G, Andolfatto, P, Hu, TT, Blanchette, M, Clark, RM, Quesneville, H, Nordborg, M, Gaut, BS, Lysak, MA, Jenkins, J, Grimwood, J, Chapman, J, Prochnik, S, Shu, S, Rokhsar, D, Schmutz, J, Weigel, D & Wright, SI 2013, 'The Capsella rubella genome and the genomic consequences of rapid mating system evolution', Nature Genetics, vol. 45, no. 7, pp. 831-835. https://doi.org/10.1038/ng.2669

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title = "The Capsella rubella genome and the genomic consequences of rapid mating system evolution",

abstract = "The shift from outcrossing to selfing is common in flowering plants, 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.",

author = "Tanja Slotte and Hazzouri, {Khaled M.} and {\AA}gren, {J. Arvid} and Daniel Koenig and Florian Maumus and Guo, {Ya Long} and Kim Steige and Platts, {Adrian E.} and Escobar, {Juan S.} and Newman, {L. Killian} and Wei Wang and Terezie Mand{\'a}kov{\'a} and Emilio Vello and Smith, {Lisa M.} and Henz, {Stefan R.} and Joshua Steffen and Shohei Takuno and Yaniv Brandvain and Graham Coop and Peter Andolfatto and Hu, {Tina T.} and Mathieu Blanchette and Clark, {Richard M.} and Hadi Quesneville and Magnus Nordborg and Gaut, {Brandon S.} and Lysak, {Martin A.} and Jerry Jenkins and Jane Grimwood and Jarrod Chapman and Simon Prochnik and Shengqiang Shu and Daniel Rokhsar and Jeremy Schmutz and Detlef Weigel and Wright, {Stephen I.}",

note = "Funding Information: The work conducted by the DoE JGI is supported by the Office of Science of the DoE under contract number DE-AC02-05CH11231. We thank J. Bergelson, J. Borevitz, A. Hall, C. Langley, K. Mayer, J. Nasrallah, B. Neuffer, Y. Van de Peer and O. Savolainen for contributing to the initial sequencing proposal submitted to the Community Sequencing Program at JGI. We also thank T. Bureau, D. Schoen, P. Harrison, J. Stinchcombe, A. Moses and E. Harmsen for their contributions to the Value-directed Evolutionary Genomics Initiative (VEGI) grant (Genome Quebec/Genome Canada), which funded C. grandiflora genomic and mRNA sequencing, and G. Coupland (Max Planck Institute for Plant Breeding Research) and colleagues for information on Arabis alpina repeats. The work was supported by the Max Planck Society (D.W.), the Genome Quebec and Genome Canada VEGI grant (S.I.W. and M.B.), the Natural Sciences and Engineering Research Council of Canada (NSERC) (S.I.W.), the Swedish Research Council (T.S.), the Carl Trygger and Erik Philip-S{\"o}rensen foundations (T.S.), National Science Foundation (NSF) grant 0929262 (J. Steffen and R.M.C.), the French National Research Agency (ANR-08-KBBE-012-02 to H.Q.), the Czech Science Foundation (excellence cluster P501/12/G090 to M.A.L.) and the European Regional Development Fund (CZ.1.05/1.1.00/02.0068 to M.A.L.). D.K. was supported by a Human Frontiers in Science Program Long-Term Fellowship, and G.C. was supported by the Alfred P. Sloan Foundation. Population genetics analyses were performed on resources provided by the Swedish National Infrastructure for Computing (SNIC) through the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under project b2012122. L.M.S. was supported by a European Community FP7 Marie Curie Fellowship (PIEF-GA-2008-221553) and an EMBO Long-Term fellowship.",

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month = jul,

doi = "10.1038/ng.2669",

language = "English (US)",

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T1 - The Capsella rubella genome and the genomic consequences of rapid mating system evolution

AU - Slotte, Tanja

AU - Hazzouri, Khaled M.

AU - Ågren, J. Arvid

AU - Koenig, Daniel

AU - Maumus, Florian

AU - Guo, Ya Long

AU - Steige, Kim

AU - Platts, Adrian E.

AU - Escobar, Juan S.

AU - Newman, L. Killian

AU - Wang, Wei

AU - Mandáková, Terezie

AU - Vello, Emilio

AU - Smith, Lisa M.

AU - Henz, Stefan R.

AU - Steffen, Joshua

AU - Takuno, Shohei

AU - Brandvain, Yaniv

AU - Coop, Graham

AU - Andolfatto, Peter

AU - Hu, Tina T.

AU - Blanchette, Mathieu

AU - Clark, Richard M.

AU - Quesneville, Hadi

AU - Nordborg, Magnus

AU - Gaut, Brandon S.

AU - Lysak, Martin A.

AU - Jenkins, Jerry

AU - Grimwood, Jane

AU - Chapman, Jarrod

AU - Prochnik, Simon

AU - Shu, Shengqiang

AU - Rokhsar, Daniel

AU - Schmutz, Jeremy

AU - Weigel, Detlef

AU - Wright, Stephen I.

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

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