Dynamic genome evolution in a model fern

D. Blaine Marchant; Guang Chen; Shengguan Cai; Fei Chen; Peter Schafran; Jerry Jenkins; Shengqiang Shu; Chris Plott; Jenell Webber; John T. Lovell; Guifen He; Laura Sandor; Melissa Williams; Shanmugam Rajasekar; Adam Healey; Kerrie Barry; Yinwen Zhang; Emily Sessa; Rijan R. Dhakal; Paul G. Wolf; Alex Harkess; Fay-Wei Li; Clemens Roessner; Annette Becker; Lydia Gramzow; Dawei Xue; Yuhuan Wu; Tao Tong; Yuanyuan Wang; Fei Dai; Shuijin Hua; Hua Wang; Shengchun Xu; Fei Xu; Honglang Duan; Guenter Theissen; Michael R. McKain; Zheng Li; Michael T. W.) McKibben; Michael S. Barker; Robert J. Schmitz; Dennis W. Stevenson; Cecilia Zumajo-Cardona; Barbara A. Ambrose; James H. Leebens-Mack; Jane Grimwood; Jeremy Schmutz; Pamela S. Soltis; Douglas E. Soltis; Zhong-Hua Chen

doi:10.1038/s41477-022-01226-7

Dynamic genome evolution in a model fern

D. Blaine Marchant
, Guang Chen
, Shengguan Cai
, Fei Chen
, Peter Schafran
, Jerry Jenkins
, Shengqiang Shu
, Chris Plott
, Jenell Webber
, John T. Lovell
, Guifen He
, Laura Sandor
, Melissa Williams
, Shanmugam Rajasekar
, Adam Healey
, Kerrie Barry
, Yinwen Zhang
, Emily Sessa
, Rijan R. Dhakal
, Paul G. Wolf

Alex Harkess, Fay-Wei Li, Clemens Roessner, Annette Becker, Lydia Gramzow, Dawei Xue, Yuhuan Wu, Tao Tong, Yuanyuan Wang, Fei Dai, Shuijin Hua, Hua Wang, Shengchun Xu, Fei Xu, Honglang Duan, Guenter Theissen, Michael R. McKain, Zheng Li, Michael T. W.) McKibben, Michael S. Barker, Robert J. Schmitz, Dennis W. Stevenson, Cecilia Zumajo-Cardona, Barbara A. Ambrose, James H. Leebens-Mack, Jane Grimwood, Jeremy Schmutz, Pamela S. Soltis, Douglas E. Soltis, Zhong-Hua Chen

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

154 Citations (Scopus)

Abstract

The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii. The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology.

Original language	English
Pages (from-to)	1038-1051
Number of pages	14
Journal	Nature Plants
Volume	8
Issue number	9
DOIs	https://doi.org/10.1038/s41477-022-01226-7
Publication status	Published - Sept 2021

Bibliographical note

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© 2022, The Author(s).

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10.1038/s41477-022-01226-7

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@article{b0eea306682a4c24b70e98d631255539,

title = "Dynamic genome evolution in a model fern",

abstract = "The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii. The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology.",

author = "Marchant, \{D. Blaine\} and Guang Chen and Shengguan Cai and Fei Chen and Peter Schafran and Jerry Jenkins and Shengqiang Shu and Chris Plott and Jenell Webber and Lovell, \{John T.\} and Guifen He and Laura Sandor and Melissa Williams and Shanmugam Rajasekar and Adam Healey and Kerrie Barry and Yinwen Zhang and Emily Sessa and Dhakal, \{Rijan R.\} and Wolf, \{Paul G.\} and Alex Harkess and Fay-Wei Li and Clemens Roessner and Annette Becker and Lydia Gramzow and Dawei Xue and Yuhuan Wu and Tao Tong and Yuanyuan Wang and Fei Dai and Shuijin Hua and Hua Wang and Shengchun Xu and Fei Xu and Honglang Duan and Guenter Theissen and McKain, \{Michael R.\} and Zheng Li and McKibben, \{Michael T. W.)\} and Barker, \{Michael S.\} and Schmitz, \{Robert J.\} and Stevenson, \{Dennis W.\} and Cecilia Zumajo-Cardona and Ambrose, \{Barbara A.\} and Leebens-Mack, \{James H.\} and Jane Grimwood and Jeremy Schmutz and Soltis, \{Pamela S.\} and Soltis, \{Douglas E.\} and Zhong-Hua Chen",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2021",

month = sep,

doi = "10.1038/s41477-022-01226-7",

language = "English",

volume = "8",

pages = "1038--1051",

journal = "Nature Plants",

issn = "2055-0278",

publisher = "Nature Research",

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Marchant, DB, Chen, G, Cai, S, Chen, F, Schafran, P, Jenkins, J, Shu, S, Plott, C, Webber, J, Lovell, JT, He, G, Sandor, L, Williams, M, Rajasekar, S, Healey, A, Barry, K, Zhang, Y, Sessa, E, Dhakal, RR, Wolf, PG, Harkess, A, Li, F-W, Roessner, C, Becker, A, Gramzow, L, Xue, D, Wu, Y, Tong, T, Wang, Y, Dai, F, Hua, S, Wang, H, Xu, S, Xu, F, Duan, H, Theissen, G, McKain, MR, Li, Z, McKibben, MTW, Barker, MS, Schmitz, RJ, Stevenson, DW, Zumajo-Cardona, C, Ambrose, BA, Leebens-Mack, JH, Grimwood, J, Schmutz, J, Soltis, PS, Soltis, DE & Chen, Z-H 2021, 'Dynamic genome evolution in a model fern', Nature Plants, vol. 8, no. 9, pp. 1038-1051. https://doi.org/10.1038/s41477-022-01226-7

TY - JOUR

T1 - Dynamic genome evolution in a model fern

AU - Marchant, D. Blaine

AU - Chen, Guang

AU - Cai, Shengguan

AU - Chen, Fei

AU - Schafran, Peter

AU - Jenkins, Jerry

AU - Shu, Shengqiang

AU - Plott, Chris

AU - Webber, Jenell

AU - Lovell, John T.

AU - He, Guifen

AU - Sandor, Laura

AU - Williams, Melissa

AU - Rajasekar, Shanmugam

AU - Healey, Adam

AU - Barry, Kerrie

AU - Zhang, Yinwen

AU - Sessa, Emily

AU - Dhakal, Rijan R.

AU - Wolf, Paul G.

AU - Harkess, Alex

AU - Li, Fay-Wei

AU - Roessner, Clemens

AU - Becker, Annette

AU - Gramzow, Lydia

AU - Xue, Dawei

AU - Wu, Yuhuan

AU - Tong, Tao

AU - Wang, Yuanyuan

AU - Dai, Fei

AU - Hua, Shuijin

AU - Wang, Hua

AU - Xu, Shengchun

AU - Xu, Fei

AU - Duan, Honglang

AU - Theissen, Guenter

AU - McKain, Michael R.

AU - Li, Zheng

AU - McKibben, Michael T. W.)

AU - Barker, Michael S.

AU - Schmitz, Robert J.

AU - Stevenson, Dennis W.

AU - Zumajo-Cardona, Cecilia

AU - Ambrose, Barbara A.

AU - Leebens-Mack, James H.

AU - Grimwood, Jane

AU - Schmutz, Jeremy

AU - Soltis, Pamela S.

AU - Soltis, Douglas E.

AU - Chen, Zhong-Hua

PY - 2021/9

Y1 - 2021/9

N2 - The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii. The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology.

AB - The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii. The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology.

UR - https://hdl.handle.net/1959.7/uws:67752

U2 - 10.1038/s41477-022-01226-7

DO - 10.1038/s41477-022-01226-7

M3 - Article

C2 - 36050461

SN - 2055-0278

SN - 2055-026X

VL - 8

SP - 1038

EP - 1051

JO - Nature Plants

JF - Nature Plants

IS - 9

ER -

Dynamic genome evolution in a model fern

Abstract

Bibliographical note

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