The Cycas genome and the early evolution of seed plants

Yang Liu; Sibo Wang; Linzhou Li; Ting Yang; Shanshan Dong; Tong Wei; Shengdan Wu; Yongbo Liu; Yiqing Gong; Xiuyan Feng; Jianchao Ma; Guanxiao Chang; Jinling Huang; Yong Yang; Hongli Wang; Min Liu; Yan Xu; Hongping Liang; Jin Yu; Yuqing Cai; Zhaowu Zhang; Yannan Fan; Weixue Mu; Sunil Kumar Sahu; Shuchun Liu; Xiaoan Lang; Leilei Yang; Na Li; Sadaf Habib; Yongqiong Yang; Anders J. Lindstrom; Pei Liang; Bernard Goffinet; Sumaira Zaman; Jill L. Wegrzyn; Dexiang Li; Jian Liu; Jie Cui; Eva C. Sonnenschein; Xiaobo Wang; Jue Ruan; Jia-Yu Xue; Zhu-Qing Shao; Chi Song; Guangyi Fan; Zhen Li; Liangsheng Zhang; Jianquan Liu; Zhong-Jian Liu; Yuannian Jiao; Xiao-Quan Wang; Hong Wu; Ertao Wang; Michael Lisby; Huanming Yang; Jian Wang; Xin Liu; Xun Xu; Nan Li; Pamela S. Soltis; Yves Van de Peer; Douglas E. Soltis; Xun Gong; Huan Liu; Shouzhou Zhang

doi:10.1038/s41477-022-01129-7

The Cycas genome and the early evolution of seed plants

Yang Liu^*, Sibo Wang, Linzhou Li, Ting Yang, Shanshan Dong, Tong Wei, Shengdan Wu, Yongbo Liu, Yiqing Gong, Xiuyan Feng, Jianchao Ma, Guanxiao Chang, Jinling Huang, Yong Yang, Hongli Wang, Min Liu, Yan Xu, Hongping Liang, Jin Yu, Yuqing CaiZhaowu Zhang, Yannan Fan, Weixue Mu, Sunil Kumar Sahu, Shuchun Liu, Xiaoan Lang, Leilei Yang, Na Li, Sadaf Habib, Yongqiong Yang, Anders J. Lindstrom, Pei Liang, Bernard Goffinet, Sumaira Zaman, Jill L. Wegrzyn, Dexiang Li, Jian Liu, Jie Cui, Eva C. Sonnenschein, Xiaobo Wang, Jue Ruan, Jia-Yu Xue, Zhu-Qing Shao, Chi Song, Guangyi Fan, Zhen Li, Liangsheng Zhang, Jianquan Liu, Zhong-Jian Liu, Yuannian Jiao, Xiao-Quan Wang, Hong Wu, Ertao Wang, Michael Lisby, Huanming Yang, Jian Wang, Xin Liu, Xun Xu, Nan Li, Pamela S. Soltis, Yves Van de Peer^*, Douglas E. Soltis^*, Xun Gong^*, Huan Liu^*, Shouzhou Zhang^*

^*Corresponding author for this work

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Abstract

Cycads represent one of the most ancient lineages of living seed plants. Identifying genomic features uniquely shared by cycads and other extant seed plants, but not non-seed-producing plants, may shed light on the origin of key innovations, as well as the early diversification of seed plants. Here, we report the 10.5-Gb reference genome of Cycas panzhihuaensis, complemented by the transcriptomes of 339 cycad species. Nuclear and plastid phylogenomic analyses strongly suggest that cycads and Ginkgo form a clade sister to all other living gymnosperms, in contrast to mitochondrial data, which place cycads alone in this position. We found evidence for an ancient whole-genome duplication in the common ancestor of extant gymnosperms. The Cycas genome contains four homologues of the fitD gene family that were likely acquired via horizontal gene transfer from fungi, and these genes confer herbivore resistance in cycads. The male-specific region of the Y chromosome of C. panzhihuaensis contains a MADS-box transcription factor expressed exclusively in male cones that is similar to a system reported in Ginkgo, suggesting that a sex determination mechanism controlled by MADS-box genes may have originated in the common ancestor of cycads and Ginkgo. The C. panzhihuaensis genome provides an important new resource of broad utility for biologists.

Original language	English
Journal	Nature Plants
Volume	8
Issue number	4
Pages (from-to)	389-401
Number of pages	13
ISSN	2055-026X
DOIs	https://doi.org/10.1038/s41477-022-01129-7
Publication status	Published - 2022

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@article{684018849199400b82a3fc1b3c9cf584,

title = "The Cycas genome and the early evolution of seed plants",

abstract = "Cycads represent one of the most ancient lineages of living seed plants. Identifying genomic features uniquely shared by cycads and other extant seed plants, but not non-seed-producing plants, may shed light on the origin of key innovations, as well as the early diversification of seed plants. Here, we report the 10.5-Gb reference genome of Cycas panzhihuaensis, complemented by the transcriptomes of 339 cycad species. Nuclear and plastid phylogenomic analyses strongly suggest that cycads and Ginkgo form a clade sister to all other living gymnosperms, in contrast to mitochondrial data, which place cycads alone in this position. We found evidence for an ancient whole-genome duplication in the common ancestor of extant gymnosperms. The Cycas genome contains four homologues of the fitD gene family that were likely acquired via horizontal gene transfer from fungi, and these genes confer herbivore resistance in cycads. The male-specific region of the Y chromosome of C. panzhihuaensis contains a MADS-box transcription factor expressed exclusively in male cones that is similar to a system reported in Ginkgo, suggesting that a sex determination mechanism controlled by MADS-box genes may have originated in the common ancestor of cycads and Ginkgo. The C. panzhihuaensis genome provides an important new resource of broad utility for biologists.",

author = "Yang Liu and Sibo Wang and Linzhou Li and Ting Yang and Shanshan Dong and Tong Wei and Shengdan Wu and Yongbo Liu and Yiqing Gong and Xiuyan Feng and Jianchao Ma and Guanxiao Chang and Jinling Huang and Yong Yang and Hongli Wang and Min Liu and Yan Xu and Hongping Liang and Jin Yu and Yuqing Cai and Zhaowu Zhang and Yannan Fan and Weixue Mu and Sahu, {Sunil Kumar} and Shuchun Liu and Xiaoan Lang and Leilei Yang and Na Li and Sadaf Habib and Yongqiong Yang and Lindstrom, {Anders J.} and Pei Liang and Bernard Goffinet and Sumaira Zaman and Wegrzyn, {Jill L.} and Dexiang Li and Jian Liu and Jie Cui and Sonnenschein, {Eva C.} and Xiaobo Wang and Jue Ruan and Jia-Yu Xue and Zhu-Qing Shao and Chi Song and Guangyi Fan and Zhen Li and Liangsheng Zhang and Jianquan Liu and Zhong-Jian Liu and Yuannian Jiao and Xiao-Quan Wang and Hong Wu and Ertao Wang and Michael Lisby and Huanming Yang and Jian Wang and Xin Liu and Xun Xu and Nan Li and Soltis, {Pamela S.} and {Van de Peer}, Yves and Soltis, {Douglas E.} and Xun Gong and Huan Liu and Shouzhou Zhang",

year = "2022",

doi = "10.1038/s41477-022-01129-7",

language = "English",

volume = "8",

pages = "389--401",

journal = "Nature Plants",

issn = "2055-026X",

publisher = "Nature Publishing Group",

number = "4",

}

Liu, Y, Wang, S, Li, L, Yang, T, Dong, S, Wei, T, Wu, S, Liu, Y, Gong, Y, Feng, X, Ma, J, Chang, G, Huang, J, Yang, Y, Wang, H, Liu, M, Xu, Y, Liang, H, Yu, J, Cai, Y, Zhang, Z, Fan, Y, Mu, W, Sahu, SK, Liu, S, Lang, X, Yang, L, Li, N, Habib, S, Yang, Y, Lindstrom, AJ, Liang, P, Goffinet, B, Zaman, S, Wegrzyn, JL, Li, D, Liu, J, Cui, J, Sonnenschein, EC, Wang, X, Ruan, J, Xue, J-Y, Shao, Z-Q, Song, C, Fan, G, Li, Z, Zhang, L, Liu, J, Liu, Z-J, Jiao, Y, Wang, X-Q, Wu, H, Wang, E, Lisby, M, Yang, H, Wang, J, Liu, X, Xu, X, Li, N, Soltis, PS, Van de Peer, Y, Soltis, DE, Gong, X, Liu, H & Zhang, S 2022, 'The Cycas genome and the early evolution of seed plants', Nature Plants, vol. 8, no. 4, pp. 389-401. https://doi.org/10.1038/s41477-022-01129-7

TY - JOUR

T1 - The Cycas genome and the early evolution of seed plants

AU - Liu, Yang

AU - Wang, Sibo

AU - Li, Linzhou

AU - Yang, Ting

AU - Dong, Shanshan

AU - Wei, Tong

AU - Wu, Shengdan

AU - Liu, Yongbo

AU - Gong, Yiqing

AU - Feng, Xiuyan

AU - Ma, Jianchao

AU - Chang, Guanxiao

AU - Huang, Jinling

AU - Yang, Yong

AU - Wang, Hongli

AU - Liu, Min

AU - Xu, Yan

AU - Liang, Hongping

AU - Yu, Jin

AU - Cai, Yuqing

AU - Zhang, Zhaowu

AU - Fan, Yannan

AU - Mu, Weixue

AU - Sahu, Sunil Kumar

AU - Liu, Shuchun

AU - Lang, Xiaoan

AU - Yang, Leilei

AU - Li, Na

AU - Habib, Sadaf

AU - Yang, Yongqiong

AU - Lindstrom, Anders J.

AU - Liang, Pei

AU - Goffinet, Bernard

AU - Zaman, Sumaira

AU - Wegrzyn, Jill L.

AU - Li, Dexiang

AU - Liu, Jian

AU - Cui, Jie

AU - Sonnenschein, Eva C.

AU - Wang, Xiaobo

AU - Ruan, Jue

AU - Xue, Jia-Yu

AU - Shao, Zhu-Qing

AU - Song, Chi

AU - Fan, Guangyi

AU - Li, Zhen

AU - Zhang, Liangsheng

AU - Liu, Jianquan

AU - Liu, Zhong-Jian

AU - Jiao, Yuannian

AU - Wang, Xiao-Quan

AU - Wu, Hong

AU - Wang, Ertao

AU - Lisby, Michael

AU - Yang, Huanming

AU - Wang, Jian

AU - Liu, Xin

AU - Xu, Xun

AU - Li, Nan

AU - Soltis, Pamela S.

AU - Van de Peer, Yves

AU - Soltis, Douglas E.

AU - Gong, Xun

AU - Liu, Huan

AU - Zhang, Shouzhou

PY - 2022

Y1 - 2022

N2 - Cycads represent one of the most ancient lineages of living seed plants. Identifying genomic features uniquely shared by cycads and other extant seed plants, but not non-seed-producing plants, may shed light on the origin of key innovations, as well as the early diversification of seed plants. Here, we report the 10.5-Gb reference genome of Cycas panzhihuaensis, complemented by the transcriptomes of 339 cycad species. Nuclear and plastid phylogenomic analyses strongly suggest that cycads and Ginkgo form a clade sister to all other living gymnosperms, in contrast to mitochondrial data, which place cycads alone in this position. We found evidence for an ancient whole-genome duplication in the common ancestor of extant gymnosperms. The Cycas genome contains four homologues of the fitD gene family that were likely acquired via horizontal gene transfer from fungi, and these genes confer herbivore resistance in cycads. The male-specific region of the Y chromosome of C. panzhihuaensis contains a MADS-box transcription factor expressed exclusively in male cones that is similar to a system reported in Ginkgo, suggesting that a sex determination mechanism controlled by MADS-box genes may have originated in the common ancestor of cycads and Ginkgo. The C. panzhihuaensis genome provides an important new resource of broad utility for biologists.

AB - Cycads represent one of the most ancient lineages of living seed plants. Identifying genomic features uniquely shared by cycads and other extant seed plants, but not non-seed-producing plants, may shed light on the origin of key innovations, as well as the early diversification of seed plants. Here, we report the 10.5-Gb reference genome of Cycas panzhihuaensis, complemented by the transcriptomes of 339 cycad species. Nuclear and plastid phylogenomic analyses strongly suggest that cycads and Ginkgo form a clade sister to all other living gymnosperms, in contrast to mitochondrial data, which place cycads alone in this position. We found evidence for an ancient whole-genome duplication in the common ancestor of extant gymnosperms. The Cycas genome contains four homologues of the fitD gene family that were likely acquired via horizontal gene transfer from fungi, and these genes confer herbivore resistance in cycads. The male-specific region of the Y chromosome of C. panzhihuaensis contains a MADS-box transcription factor expressed exclusively in male cones that is similar to a system reported in Ginkgo, suggesting that a sex determination mechanism controlled by MADS-box genes may have originated in the common ancestor of cycads and Ginkgo. The C. panzhihuaensis genome provides an important new resource of broad utility for biologists.

U2 - 10.1038/s41477-022-01129-7

DO - 10.1038/s41477-022-01129-7

M3 - Journal article

C2 - 35437001

SN - 2055-026X

VL - 8

SP - 389

EP - 401

JO - Nature Plants

JF - Nature Plants

IS - 4

ER -

The Cycas genome and the early evolution of seed plants

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