Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.

Jisen Zhang; Xingtan Zhang; Haibao Tang; Qing Zhang; Xiuting Hua; Xiaokai Ma; Fan Zhu; Tyler Jones; Xinguang Zhu; John Bowers; Ching Man Wai; Chunfang Zheng; Yan Shi; Shuai Chen; Xiuming Xu; Jingjing Yue; David R. Nelson; Lixian Huang; Zhen Li; Huimin Xu; Dong Zhou; Yongjun Wang; Weichang Hu; Jishan Lin; Youjin Deng; Neha Pandey; Melina Mancini; Dessireé Zerpa; Julie K. Nguyen; Liming Wang; Liang Yu; Yinghui Xin; Liangfa Ge; Jie Arro; Jennifer O. Han; Setu Chakrabarty; Marija Pushko; Wenping Zhang; Yanhong Ma; Panpan Ma; Mingju Lv; Faming Chen; Guangyong Zheng; Jingsheng Xu; Zhenhui Yang; Fang Deng; Xuequn Chen; Zhenyang Liao; Xunxiao Zhang; Zhicong Lin; Hai Lin; Hansong Yan; Zheng Kuang; Weimin Zhong; Pingping Liang; Guofeng Wang; Yuan Yuan; Jiaxian Shi; Jinxiang Hou; Jingxian Lin; Jingjing Jin; Peijian Cao; Qiaochu Shen; Qing Jiang; Ping Zhou; Yaying Ma; Xiaodan Zhang; Rongrong Xu; Juan Liu; Yongmei Zhou; Haifeng Jia; Qing Ma; Rui Qi; Zhiliang Zhang; Jingping Fang; Hongkun Fang; Jinjin Song; Mengjuan Wang; Guangrui Dong; Gang Wang; Zheng Chen; Teng Ma; Hong Liu; Singha R. Dhungana; Sarah E. Huss; Xiping Yang; Anupma Sharma; Jhon H. Trujillo; Maria C. Martinez; Matthew Hudson; John J. Riascos; Mary Schuler; Li Qing Chen; David M. Braun; Lei Li; Qingyi Yu; Jianping Wang; Kai Wang; Michael C. Schatz; David Heckerman; Marie Anne Van Sluys; Glaucia Mendes Souza; Paul H. Moore; David Sankoff; Robert VanBuren; Andrew H. Paterson; Chifumi Nagai; Ray Ming

doi:10.1038/s41588-018-0237-2

Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.

Jisen Zhang^*, Xingtan Zhang, Haibao Tang, Qing Zhang, Xiuting Hua, Xiaokai Ma, Fan Zhu, Tyler Jones, Xinguang Zhu, John Bowers, Ching Man Wai, Chunfang Zheng, Yan Shi, Shuai Chen, Xiuming Xu, Jingjing Yue, David R. Nelson, Lixian Huang, Zhen Li, Huimin XuDong Zhou, Yongjun Wang, Weichang Hu, Jishan Lin, Youjin Deng, Neha Pandey, Melina Mancini, Dessireé Zerpa, Julie K. Nguyen, Liming Wang, Liang Yu, Yinghui Xin, Liangfa Ge, Jie Arro, Jennifer O. Han, Setu Chakrabarty, Marija Pushko, Wenping Zhang, Yanhong Ma, Panpan Ma, Mingju Lv, Faming Chen, Guangyong Zheng, Jingsheng Xu, Zhenhui Yang, Fang Deng, Xuequn Chen, Zhenyang Liao, Xunxiao Zhang, Zhicong Lin, Hai Lin, Hansong Yan, Zheng Kuang, Weimin Zhong, Pingping Liang, Guofeng Wang, Yuan Yuan, Jiaxian Shi, Jinxiang Hou, Jingxian Lin, Jingjing Jin, Peijian Cao, Qiaochu Shen, Qing Jiang, Ping Zhou, Yaying Ma, Xiaodan Zhang, Rongrong Xu, Juan Liu, Yongmei Zhou, Haifeng Jia, Qing Ma, Rui Qi, Zhiliang Zhang, Jingping Fang, Hongkun Fang, Jinjin Song, Mengjuan Wang, Guangrui Dong, Gang Wang, Zheng Chen, Teng Ma, Hong Liu, Singha R. Dhungana, Sarah E. Huss, Xiping Yang, Anupma Sharma, Jhon H. Trujillo, Maria C. Martinez, Matthew Hudson, John J. Riascos, Mary Schuler, Li Qing Chen, David M. Braun, Lei Li, Qingyi Yu, Jianping Wang, Kai Wang, Michael C. Schatz, David Heckerman, Marie Anne Van Sluys, Glaucia Mendes Souza, Paul H. Moore, David Sankoff, Robert VanBuren, Andrew H. Paterson, Chifumi Nagai, Ray Ming

^*Corresponding author for this work

Biochemistry and Molecular Genetics

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

506 Scopus citations

Abstract

Modern sugarcanes are polyploid interspecific hybrids, combining high sugar content from Saccharum officinarum with hardiness, disease resistance and ratooning of Saccharum spontaneum. Sequencing of a haploid S. spontaneum, AP85-441, facilitated the assembly of 32 pseudo-chromosomes comprising 8 homologous groups of 4 members each, bearing 35,525 genes with alleles defined. The reduction of basic chromosome number from 10 to 8 in S. spontaneum was caused by fissions of 2 ancestral chromosomes followed by translocations to 4 chromosomes. Surprisingly, 80% of nucleotide binding site-encoding genes associated with disease resistance are located in 4 rearranged chromosomes and 51% of those in rearranged regions. Resequencing of 64 S. spontaneum genomes identified balancing selection in rearranged regions, maintaining their diversity. Introgressed S. spontaneum chromosomes in modern sugarcanes are randomly distributed in AP85-441 genome, indicating random recombination among homologs in different S. spontaneum accessions. The allele-defined Saccharum genome offers new knowledge and resources to accelerate sugarcane improvement.

Original language	English (US)
Pages (from-to)	1565-1573
Number of pages	9
Journal	Nature Genetics
Volume	50
Issue number	11
DOIs	https://doi.org/10.1038/s41588-018-0237-2
State	Published - Nov 1 2018

Funding

We thank L. McHale for reviewing and commenting on the section on disease resistance genes. This project was supported by a startup fund from Fujian Agriculture and Forestry University to R.M., the International Consortium for Sugarcane Biotechnology (project #35, R.M.), the US Department of Energy (DOE; DE-SC0010686 to R.M.), the European Bioinformatics Institute (BP2012OO2J17 to R.M.), the US National Science Foundation Plant Genome Research Program (grant IOS-1025976 to D.M.B.), the 863 program (2013AA102604 to J.Z.), the Natural Science Foundation of China (31201260 to J.Z.), the Program for New Century Excellent Talents in Fujian Province (J.Z.), and the S\u00E3o Paulo Research Foundation (FAPESP; grants 2008/52146-0, 2012/51062-3 and 2014/50921-8 to G.M.S. and 2008/52074-8 to M.-A.V.S.). This work was funded in part by the DOE Center for Advanced Bioenergy and Bioproducts Innovation (US DOE, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC 18420 to M.H. and L.-Q.C.).

ASJC Scopus subject areas

Genetics

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10.1038/s41588-018-0237-2

Cite this

@article{54ee7c2f0ede45679a7853e4ccf9edeb,

title = "Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.",

abstract = "Modern sugarcanes are polyploid interspecific hybrids, combining high sugar content from Saccharum officinarum with hardiness, disease resistance and ratooning of Saccharum spontaneum. Sequencing of a haploid S. spontaneum, AP85-441, facilitated the assembly of 32 pseudo-chromosomes comprising 8 homologous groups of 4 members each, bearing 35,525 genes with alleles defined. The reduction of basic chromosome number from 10 to 8 in S. spontaneum was caused by fissions of 2 ancestral chromosomes followed by translocations to 4 chromosomes. Surprisingly, 80% of nucleotide binding site-encoding genes associated with disease resistance are located in 4 rearranged chromosomes and 51% of those in rearranged regions. Resequencing of 64 S. spontaneum genomes identified balancing selection in rearranged regions, maintaining their diversity. Introgressed S. spontaneum chromosomes in modern sugarcanes are randomly distributed in AP85-441 genome, indicating random recombination among homologs in different S. spontaneum accessions. The allele-defined Saccharum genome offers new knowledge and resources to accelerate sugarcane improvement.",

author = "Jisen Zhang and Xingtan Zhang and Haibao Tang and Qing Zhang and Xiuting Hua and Xiaokai Ma and Fan Zhu and Tyler Jones and Xinguang Zhu and John Bowers and Wai, {Ching Man} and Chunfang Zheng and Yan Shi and Shuai Chen and Xiuming Xu and Jingjing Yue and Nelson, {David R.} and Lixian Huang and Zhen Li and Huimin Xu and Dong Zhou and Yongjun Wang and Weichang Hu and Jishan Lin and Youjin Deng and Neha Pandey and Melina Mancini and Dessire{\'e} Zerpa and Nguyen, {Julie K.} and Liming Wang and Liang Yu and Yinghui Xin and Liangfa Ge and Jie Arro and Han, {Jennifer O.} and Setu Chakrabarty and Marija Pushko and Wenping Zhang and Yanhong Ma and Panpan Ma and Mingju Lv and Faming Chen and Guangyong Zheng and Jingsheng Xu and Zhenhui Yang and Fang Deng and Xuequn Chen and Zhenyang Liao and Xunxiao Zhang and Zhicong Lin and Hai Lin and Hansong Yan and Zheng Kuang and Weimin Zhong and Pingping Liang and Guofeng Wang and Yuan Yuan and Jiaxian Shi and Jinxiang Hou and Jingxian Lin and Jingjing Jin and Peijian Cao and Qiaochu Shen and Qing Jiang and Ping Zhou and Yaying Ma and Xiaodan Zhang and Rongrong Xu and Juan Liu and Yongmei Zhou and Haifeng Jia and Qing Ma and Rui Qi and Zhiliang Zhang and Jingping Fang and Hongkun Fang and Jinjin Song and Mengjuan Wang and Guangrui Dong and Gang Wang and Zheng Chen and Teng Ma and Hong Liu and Dhungana, {Singha R.} and Huss, {Sarah E.} and Xiping Yang and Anupma Sharma and Trujillo, {Jhon H.} and Martinez, {Maria C.} and Matthew Hudson and Riascos, {John J.} and Mary Schuler and Chen, {Li Qing} and Braun, {David M.} and Lei Li and Qingyi Yu and Jianping Wang and Kai Wang and Schatz, {Michael C.} and David Heckerman and {Van Sluys}, {Marie Anne} and Souza, {Glaucia Mendes} and Moore, {Paul H.} and David Sankoff and Robert VanBuren and Paterson, {Andrew H.} and Chifumi Nagai and Ray Ming",

note = "Funding Information: We thank L. McHale for reviewing and commenting on the section on disease resistance genes. This project was supported by a startup fund from Fujian Agriculture and Forestry University to R.M., the International Consortium for Sugarcane Biotechnology (project #35, R.M.), the US Department of Energy (DOE; DE-SC0010686 to R.M.), the European Bioinformatics Institute (BP2012OO2J17 to R.M.), the US National Science Foundation Plant Genome Research Program (grant IOS-1025976 to D.M.B.), the 863 program (2013AA102604 to J.Z.), the Natural Science Foundation of China (31201260 to J.Z.), the Program for New Century Excellent Talents in Fujian Province (J.Z.), and the S{\~a}o Paulo Research Foundation (FAPESP; grants 2008/52146-0, 2012/51062-3 and 2014/50921-8 to G.M.S. and 2008/52074-8 to M.-A.V.S.). This work was funded in part by the DOE Center for Advanced Bioenergy and Bioproducts Innovation (US DOE, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC 18420 to M.H. and L.-Q.C.). Publisher Copyright: {\textcopyright} 2018, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2018",

month = nov,

day = "1",

doi = "10.1038/s41588-018-0237-2",

language = "English (US)",

volume = "50",

pages = "1565--1573",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Research",

number = "11",

}

Zhang, J, Zhang, X, Tang, H, Zhang, Q, Hua, X, Ma, X, Zhu, F, Jones, T, Zhu, X, Bowers, J, Wai, CM, Zheng, C, Shi, Y, Chen, S, Xu, X, Yue, J, Nelson, DR, Huang, L, Li, Z, Xu, H, Zhou, D, Wang, Y, Hu, W, Lin, J, Deng, Y, Pandey, N, Mancini, M, Zerpa, D, Nguyen, JK, Wang, L, Yu, L, Xin, Y, Ge, L, Arro, J, Han, JO, Chakrabarty, S, Pushko, M, Zhang, W, Ma, Y, Ma, P, Lv, M, Chen, F, Zheng, G, Xu, J, Yang, Z, Deng, F, Chen, X, Liao, Z, Zhang, X, Lin, Z, Lin, H, Yan, H, Kuang, Z, Zhong, W, Liang, P, Wang, G, Yuan, Y, Shi, J, Hou, J, Lin, J, Jin, J, Cao, P, Shen, Q, Jiang, Q, Zhou, P, Ma, Y, Zhang, X, Xu, R, Liu, J, Zhou, Y, Jia, H, Ma, Q, Qi, R, Zhang, Z, Fang, J, Fang, H, Song, J, Wang, M, Dong, G, Wang, G, Chen, Z, Ma, T, Liu, H, Dhungana, SR, Huss, SE, Yang, X, Sharma, A, Trujillo, JH, Martinez, MC, Hudson, M, Riascos, JJ, Schuler, M, Chen, LQ, Braun, DM, Li, L, Yu, Q, Wang, J, Wang, K, Schatz, MC, Heckerman, D, Van Sluys, MA, Souza, GM, Moore, PH, Sankoff, D, VanBuren, R, Paterson, AH, Nagai, C & Ming, R 2018, 'Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.', Nature Genetics, vol. 50, no. 11, pp. 1565-1573. https://doi.org/10.1038/s41588-018-0237-2

TY - JOUR

T1 - Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.

AU - Zhang, Jisen

AU - Zhang, Xingtan

AU - Tang, Haibao

AU - Zhang, Qing

AU - Hua, Xiuting

AU - Ma, Xiaokai

AU - Zhu, Fan

AU - Jones, Tyler

AU - Zhu, Xinguang

AU - Bowers, John

AU - Wai, Ching Man

AU - Zheng, Chunfang

AU - Shi, Yan

AU - Chen, Shuai

AU - Xu, Xiuming

AU - Yue, Jingjing

AU - Nelson, David R.

AU - Huang, Lixian

AU - Li, Zhen

AU - Xu, Huimin

AU - Zhou, Dong

AU - Wang, Yongjun

AU - Hu, Weichang

AU - Lin, Jishan

AU - Deng, Youjin

AU - Pandey, Neha

AU - Mancini, Melina

AU - Zerpa, Dessireé

AU - Nguyen, Julie K.

AU - Wang, Liming

AU - Yu, Liang

AU - Xin, Yinghui

AU - Ge, Liangfa

AU - Arro, Jie

AU - Han, Jennifer O.

AU - Chakrabarty, Setu

AU - Pushko, Marija

AU - Zhang, Wenping

AU - Ma, Yanhong

AU - Ma, Panpan

AU - Lv, Mingju

AU - Chen, Faming

AU - Zheng, Guangyong

AU - Xu, Jingsheng

AU - Yang, Zhenhui

AU - Deng, Fang

AU - Chen, Xuequn

AU - Liao, Zhenyang

AU - Zhang, Xunxiao

AU - Lin, Zhicong

AU - Lin, Hai

AU - Yan, Hansong

AU - Kuang, Zheng

AU - Zhong, Weimin

AU - Liang, Pingping

AU - Wang, Guofeng

AU - Yuan, Yuan

AU - Shi, Jiaxian

AU - Hou, Jinxiang

AU - Lin, Jingxian

AU - Jin, Jingjing

AU - Cao, Peijian

AU - Shen, Qiaochu

AU - Jiang, Qing

AU - Zhou, Ping

AU - Ma, Yaying

AU - Zhang, Xiaodan

AU - Xu, Rongrong

AU - Liu, Juan

AU - Zhou, Yongmei

AU - Jia, Haifeng

AU - Ma, Qing

AU - Qi, Rui

AU - Zhang, Zhiliang

AU - Fang, Jingping

AU - Fang, Hongkun

AU - Song, Jinjin

AU - Wang, Mengjuan

AU - Dong, Guangrui

AU - Wang, Gang

AU - Chen, Zheng

AU - Ma, Teng

AU - Liu, Hong

AU - Dhungana, Singha R.

AU - Huss, Sarah E.

AU - Yang, Xiping

AU - Sharma, Anupma

AU - Trujillo, Jhon H.

AU - Martinez, Maria C.

AU - Hudson, Matthew

AU - Riascos, John J.

AU - Schuler, Mary

AU - Chen, Li Qing

AU - Braun, David M.

AU - Li, Lei

AU - Yu, Qingyi

AU - Wang, Jianping

AU - Wang, Kai

AU - Schatz, Michael C.

AU - Heckerman, David

AU - Van Sluys, Marie Anne

AU - Souza, Glaucia Mendes

AU - Moore, Paul H.

AU - Sankoff, David

AU - VanBuren, Robert

AU - Paterson, Andrew H.

AU - Nagai, Chifumi

AU - Ming, Ray

N1 - Funding Information: We thank L. McHale for reviewing and commenting on the section on disease resistance genes. This project was supported by a startup fund from Fujian Agriculture and Forestry University to R.M., the International Consortium for Sugarcane Biotechnology (project #35, R.M.), the US Department of Energy (DOE; DE-SC0010686 to R.M.), the European Bioinformatics Institute (BP2012OO2J17 to R.M.), the US National Science Foundation Plant Genome Research Program (grant IOS-1025976 to D.M.B.), the 863 program (2013AA102604 to J.Z.), the Natural Science Foundation of China (31201260 to J.Z.), the Program for New Century Excellent Talents in Fujian Province (J.Z.), and the São Paulo Research Foundation (FAPESP; grants 2008/52146-0, 2012/51062-3 and 2014/50921-8 to G.M.S. and 2008/52074-8 to M.-A.V.S.). This work was funded in part by the DOE Center for Advanced Bioenergy and Bioproducts Innovation (US DOE, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC 18420 to M.H. and L.-Q.C.). Publisher Copyright: © 2018, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2018/11/1

Y1 - 2018/11/1

N2 - Modern sugarcanes are polyploid interspecific hybrids, combining high sugar content from Saccharum officinarum with hardiness, disease resistance and ratooning of Saccharum spontaneum. Sequencing of a haploid S. spontaneum, AP85-441, facilitated the assembly of 32 pseudo-chromosomes comprising 8 homologous groups of 4 members each, bearing 35,525 genes with alleles defined. The reduction of basic chromosome number from 10 to 8 in S. spontaneum was caused by fissions of 2 ancestral chromosomes followed by translocations to 4 chromosomes. Surprisingly, 80% of nucleotide binding site-encoding genes associated with disease resistance are located in 4 rearranged chromosomes and 51% of those in rearranged regions. Resequencing of 64 S. spontaneum genomes identified balancing selection in rearranged regions, maintaining their diversity. Introgressed S. spontaneum chromosomes in modern sugarcanes are randomly distributed in AP85-441 genome, indicating random recombination among homologs in different S. spontaneum accessions. The allele-defined Saccharum genome offers new knowledge and resources to accelerate sugarcane improvement.

AB - Modern sugarcanes are polyploid interspecific hybrids, combining high sugar content from Saccharum officinarum with hardiness, disease resistance and ratooning of Saccharum spontaneum. Sequencing of a haploid S. spontaneum, AP85-441, facilitated the assembly of 32 pseudo-chromosomes comprising 8 homologous groups of 4 members each, bearing 35,525 genes with alleles defined. The reduction of basic chromosome number from 10 to 8 in S. spontaneum was caused by fissions of 2 ancestral chromosomes followed by translocations to 4 chromosomes. Surprisingly, 80% of nucleotide binding site-encoding genes associated with disease resistance are located in 4 rearranged chromosomes and 51% of those in rearranged regions. Resequencing of 64 S. spontaneum genomes identified balancing selection in rearranged regions, maintaining their diversity. Introgressed S. spontaneum chromosomes in modern sugarcanes are randomly distributed in AP85-441 genome, indicating random recombination among homologs in different S. spontaneum accessions. The allele-defined Saccharum genome offers new knowledge and resources to accelerate sugarcane improvement.

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UR - http://www.scopus.com/inward/citedby.url?scp=85054572121&partnerID=8YFLogxK

U2 - 10.1038/s41588-018-0237-2

DO - 10.1038/s41588-018-0237-2

M3 - Article

C2 - 30297971

AN - SCOPUS:85054572121

SN - 1061-4036

VL - 50

SP - 1565

EP - 1573

JO - Nature Genetics

JF - Nature Genetics

IS - 11

ER -

Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.

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