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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.

Authors:
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  1. Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign School of Integrative Biology Joint Center for Genomics and Biotechnology, National Sugarcane Engineering Technology Research Center, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou (China)
  2. University of Illinois at Urbana-Champaign, Urbana, IL (United States)
  3. Hawaii Agriculture Research Center, Kunia, HI (United States)
  4. Chinese Academy of Sciences, Shanghai (China)
  5. Univ. of Georgia, Athens, GA (United States)
  6. Michigan State Univ., East Lansing, MI (United States)
  7. University of Ottawa, ON (Canada)
  8. University of Tennessee HSC, Memphis, TN (United States)
  9. Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou (China)
  10. Univ. of Missouri, Columbia, MO (United States)
  11. Univ. of Florida, Gainesville, FL (United States)
  12. Texas A&M AgriLife Research, Texas A&M University System, Dallas, TX (United States)
  13. Centro de Investigación de la Caña de Azúcar de Colombia (Cenicaña), Cali (Columbia)
  14. Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign School of Integrative Biology Joint Center for Genomics and Biotechnology, National Sugarcane Engineering Technology Research Center, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou (China); Univ. of Florida, Gainesville, FL (United States)
  15. Johns Hopkins Univ., Baltimore, MD (United States)
  16. Microsoft Research, Redmond, WA (United States)
  17. Universidade de São Paulo (Brazil)
  18. Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign School of Integrative Biology Joint Center for Genomics and Biotechnology, National Sugarcane Engineering Technology Research Center, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou (China); University of Illinois at Urbana-Champaign, Urbana, IL (United States)
Publication Date:
Research Org.:
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1478071
Grant/Contract Number:  
SC0018420; SC0010686
Resource Type:
Accepted Manuscript
Journal Name:
Nature Genetics
Additional Journal Information:
Journal Volume: 50; Journal ID: ISSN 1061-4036
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; Genomics; Plant Genetics; Sugarcane; Biofuels

Citation Formats

Zhang, Jisen, Zhang, Xingtan, Tang, Haibao, Zhang, Qing, Hua, Xiuting, Ma, Xiaokai, Zhu, Fan, Jones, Tyler, Zhu, Xinguang, Bowers, John, Wai, Ching Man, Zheng, Chunfang, Shi, Yan, Chen, Shuai, Xu, Xiuming, Yue, Jingjing, Nelson, David R., Huang, Lixian, Li, Zhen, Xu, Huimin, Zhou, Dong, Wang, Yongjun, Hu, Weichang, Lin, Jishan, Deng, Youjin, Pandey, Neha, Mancini, Melina, Zerpa, Dessireé, Nguyen, Julie K., Wang, Liming, Yu, Liang, Xin, Yinghui, Ge, Liangfa, Arro, Jie, Han, Jennifer O., Chakrabarty, Setu, Pushko, Marija, Zhang, Wenping, Ma, Yanhong, Ma, Panpan, Lv, Mingju, Chen, Faming, Zheng, Guangyong, Xu, Jingsheng, Yang, Zhenhui, Deng, Fang, Chen, Xuequn, Liao, Zhenyang, Zhang, Xunxiao, Lin, Zhicong, Lin, Hai, Yan, Hansong, Kuang, Zheng, Zhong, Weimin, Liang, Pingping, Wang, Guofeng, Yuan, Yuan, Shi, Jiaxian, Hou, Jinxiang, Lin, Jingxian, Jin, Jingjing, Cao, Peijian, Hou, Jinxiang, Jiang, Qing, Zhou, Ping, Ma, Yaying, Zhang, Xiaodan, Xu, Rongrong, Liu, Juan, Zhou, Yongmei, Jia, Haifeng, Ma, Qing, Qi, Rui, Zhang, Zhiliang, Fang, Jingping, Fang, Hongkun, Song, Jinjin, Wang, Mengjuan, Dong, Guangrui, Wang, Gang, Chen, Zheng, Ma, Teng, Liu, Hong, Dhungana, Singha R., Huss, Sarah E., Yang, Xiping, Sharma, Anupma, Trujillo, Jhon H., Martinez, Maria C., Hudson, Matthew, Riascos, John J., Schuler, Mary, Chen, Li-Qing, Braun, David M., Li, Lei, Yu, Qingyi, Wang, Jianping, Wang, Kai, Schatz, Michael C., Heckerman, David, Van Sluys, Marie-Anne, Souza, Glaucia Mendes, Moore, Paul H., Sankoff, David, VanBuren, Robert, Paterson, Andrew H., Nagai, Chifumi, and Ming, Ray. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.. United States: N. p., 2018. Web. doi:10.1038/s41588-018-0237-2.
Zhang, Jisen, Zhang, Xingtan, Tang, Haibao, Zhang, Qing, Hua, Xiuting, Ma, Xiaokai, Zhu, Fan, Jones, Tyler, Zhu, Xinguang, Bowers, John, Wai, Ching Man, Zheng, Chunfang, Shi, Yan, Chen, Shuai, Xu, Xiuming, Yue, Jingjing, Nelson, David R., Huang, Lixian, Li, Zhen, Xu, Huimin, Zhou, Dong, Wang, Yongjun, Hu, Weichang, Lin, Jishan, Deng, Youjin, Pandey, Neha, Mancini, Melina, Zerpa, Dessireé, Nguyen, Julie K., Wang, Liming, Yu, Liang, Xin, Yinghui, Ge, Liangfa, Arro, Jie, Han, Jennifer O., Chakrabarty, Setu, Pushko, Marija, Zhang, Wenping, Ma, Yanhong, Ma, Panpan, Lv, Mingju, Chen, Faming, Zheng, Guangyong, Xu, Jingsheng, Yang, Zhenhui, Deng, Fang, Chen, Xuequn, Liao, Zhenyang, Zhang, Xunxiao, Lin, Zhicong, Lin, Hai, Yan, Hansong, Kuang, Zheng, Zhong, Weimin, Liang, Pingping, Wang, Guofeng, Yuan, Yuan, Shi, Jiaxian, Hou, Jinxiang, Lin, Jingxian, Jin, Jingjing, Cao, Peijian, Hou, Jinxiang, Jiang, Qing, Zhou, Ping, Ma, Yaying, Zhang, Xiaodan, Xu, Rongrong, Liu, Juan, Zhou, Yongmei, Jia, Haifeng, Ma, Qing, Qi, Rui, Zhang, Zhiliang, Fang, Jingping, Fang, Hongkun, Song, Jinjin, Wang, Mengjuan, Dong, Guangrui, Wang, Gang, Chen, Zheng, Ma, Teng, Liu, Hong, Dhungana, Singha R., Huss, Sarah E., Yang, Xiping, Sharma, Anupma, Trujillo, Jhon H., Martinez, Maria C., Hudson, Matthew, Riascos, John J., Schuler, Mary, Chen, Li-Qing, Braun, David M., Li, Lei, Yu, Qingyi, Wang, Jianping, Wang, Kai, Schatz, Michael C., Heckerman, David, Van Sluys, Marie-Anne, Souza, Glaucia Mendes, Moore, Paul H., Sankoff, David, VanBuren, Robert, Paterson, Andrew H., Nagai, Chifumi, & Ming, Ray. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.. United States. doi:10.1038/s41588-018-0237-2.
Zhang, Jisen, Zhang, Xingtan, Tang, Haibao, Zhang, Qing, Hua, Xiuting, Ma, Xiaokai, Zhu, Fan, Jones, Tyler, Zhu, Xinguang, Bowers, John, Wai, Ching Man, Zheng, Chunfang, Shi, Yan, Chen, Shuai, Xu, Xiuming, Yue, Jingjing, Nelson, David R., Huang, Lixian, Li, Zhen, Xu, Huimin, Zhou, Dong, Wang, Yongjun, Hu, Weichang, Lin, Jishan, Deng, Youjin, Pandey, Neha, Mancini, Melina, Zerpa, Dessireé, Nguyen, Julie K., Wang, Liming, Yu, Liang, Xin, Yinghui, Ge, Liangfa, Arro, Jie, Han, Jennifer O., Chakrabarty, Setu, Pushko, Marija, Zhang, Wenping, Ma, Yanhong, Ma, Panpan, Lv, Mingju, Chen, Faming, Zheng, Guangyong, Xu, Jingsheng, Yang, Zhenhui, Deng, Fang, Chen, Xuequn, Liao, Zhenyang, Zhang, Xunxiao, Lin, Zhicong, Lin, Hai, Yan, Hansong, Kuang, Zheng, Zhong, Weimin, Liang, Pingping, Wang, Guofeng, Yuan, Yuan, Shi, Jiaxian, Hou, Jinxiang, Lin, Jingxian, Jin, Jingjing, Cao, Peijian, Hou, Jinxiang, Jiang, Qing, Zhou, Ping, Ma, Yaying, Zhang, Xiaodan, Xu, Rongrong, Liu, Juan, Zhou, Yongmei, Jia, Haifeng, Ma, Qing, Qi, Rui, Zhang, Zhiliang, Fang, Jingping, Fang, Hongkun, Song, Jinjin, Wang, Mengjuan, Dong, Guangrui, Wang, Gang, Chen, Zheng, Ma, Teng, Liu, Hong, Dhungana, Singha R., Huss, Sarah E., Yang, Xiping, Sharma, Anupma, Trujillo, Jhon H., Martinez, Maria C., Hudson, Matthew, Riascos, John J., Schuler, Mary, Chen, Li-Qing, Braun, David M., Li, Lei, Yu, Qingyi, Wang, Jianping, Wang, Kai, Schatz, Michael C., Heckerman, David, Van Sluys, Marie-Anne, Souza, Glaucia Mendes, Moore, Paul H., Sankoff, David, VanBuren, Robert, Paterson, Andrew H., Nagai, Chifumi, and Ming, Ray. Mon . "Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.". United States. doi:10.1038/s41588-018-0237-2. https://www.osti.gov/servlets/purl/1478071.
@article{osti_1478071,
title = {Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.},
author = {Zhang, Jisen and Zhang, Xingtan and Tang, Haibao and Zhang, Qing and Hua, Xiuting and Ma, Xiaokai and Zhu, Fan and Jones, Tyler and Zhu, Xinguang and Bowers, John and Wai, Ching Man and Zheng, Chunfang and Shi, Yan and Chen, Shuai and Xu, Xiuming and Yue, Jingjing and Nelson, David R. and Huang, Lixian and Li, Zhen and Xu, Huimin and Zhou, Dong and Wang, Yongjun and Hu, Weichang and Lin, Jishan and Deng, Youjin and Pandey, Neha and Mancini, Melina and Zerpa, Dessireé and Nguyen, Julie K. and Wang, Liming and Yu, Liang and Xin, Yinghui and Ge, Liangfa and Arro, Jie and Han, Jennifer O. and Chakrabarty, Setu and Pushko, Marija and Zhang, Wenping and Ma, Yanhong and Ma, Panpan and Lv, Mingju and Chen, Faming and Zheng, Guangyong and Xu, Jingsheng and Yang, Zhenhui and Deng, Fang and Chen, Xuequn and Liao, Zhenyang and Zhang, Xunxiao and Lin, Zhicong and Lin, Hai and Yan, Hansong and Kuang, Zheng and Zhong, Weimin and Liang, Pingping and Wang, Guofeng and Yuan, Yuan and Shi, Jiaxian and Hou, Jinxiang and Lin, Jingxian and Jin, Jingjing and Cao, Peijian and Hou, Jinxiang and Jiang, Qing and Zhou, Ping and Ma, Yaying and Zhang, Xiaodan and Xu, Rongrong and Liu, Juan and Zhou, Yongmei and Jia, Haifeng and Ma, Qing and Qi, Rui and Zhang, Zhiliang and Fang, Jingping and Fang, Hongkun and Song, Jinjin and Wang, Mengjuan and Dong, Guangrui and Wang, Gang and Chen, Zheng and Ma, Teng and Liu, Hong and Dhungana, Singha R. and Huss, Sarah E. and Yang, Xiping and Sharma, Anupma and Trujillo, Jhon H. and Martinez, Maria C. and Hudson, Matthew and Riascos, John J. and Schuler, Mary and Chen, Li-Qing and Braun, David M. and Li, Lei and Yu, Qingyi and Wang, Jianping and Wang, Kai and Schatz, Michael C. and Heckerman, David and Van Sluys, Marie-Anne and Souza, Glaucia Mendes and Moore, Paul H. and Sankoff, David and VanBuren, Robert and Paterson, Andrew H. and Nagai, Chifumi and Ming, Ray},
abstractNote = {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.},
doi = {10.1038/s41588-018-0237-2},
journal = {Nature Genetics},
number = ,
volume = 50,
place = {United States},
year = {2018},
month = {10}
}

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MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons
journal, December 2017


The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection
journal, September 2016

  • Yang, Jinghua; Liu, Dongyuan; Wang, Xiaowu
  • Nature Genetics, Vol. 48, Issue 10
  • DOI: 10.1038/ng.3657

Wild emmer genome architecture and diversity elucidate wheat evolution and domestication
journal, July 2017


The Sequence Alignment/Map format and SAMtools
journal, June 2009


Understanding mechanisms of novel gene expression in polyploids
journal, March 2003


Current perspectives on the regulation of whole-plant carbohydrate partitioning
journal, April 2010


De Novo Plant Genome Assembly Based on Chromatin Interactions: A Case Study of Arabidopsis thaliana
journal, March 2015


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

The three 'C' s of chromosome conformation capture: controls, controls, controls
journal, December 2005


SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011


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    Common metabolic networks contribute to carbon sink strength of sorghum internodes: implications for bioenergy improvement
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