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Research Article

The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau

Xingquan Zeng, Hai Long, Zhuo Wang, Shancen Zhao, Yawei Tang, Zhiyong Huang, Yulin Wang, Qijun Xu, Likai Mao, Guangbing Deng, Xiaoming Yao, Xiangfeng Li, Lijun Bai, Hongjun Yuan, Zhifen Pan, Renjian Liu, Xin Chen, QiMei WangMu, Ming Chen, Lili Yu, Junjun Liang, DaWa DunZhu, Yuan Zheng, Shuiyang Yu, ZhaXi LuoBu, Xuanmin Guang, Jiang Li, Cao Deng, Wushu Hu, Chunhai Chen, XiongNu TaBa, Liyun Gao, Xiaodan Lv, Yuval Ben Abu, Xiaodong Fang, Eviatar Nevo, Maoqun Yu, Jun Wang, and Nyima Tashi
  1. aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
  2. bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
  3. cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
  4. dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
  5. eCollege of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China;
  6. fProjects and Physics Section, Sapir Academic College, D.N. Hof Ashkelon 79165, Israel;
  7. gInstitute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel;
  8. hBGI-Shenzhen, Shenzhen 518083, China;
  9. iDepartment of Biology, University of Copenhagen, Copenhagen 2200, Denmark; and
  10. jPrincess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21441, Saudi Arabia

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PNAS first published January 12, 2015; https://doi.org/10.1073/pnas.1423628112
Xingquan Zeng
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Hai Long
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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Zhuo Wang
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Shancen Zhao
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Yawei Tang
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Zhiyong Huang
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Yulin Wang
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Qijun Xu
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Likai Mao
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Guangbing Deng
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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Xiaoming Yao
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Xiangfeng Li
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
eCollege of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China;
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Lijun Bai
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Hongjun Yuan
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Zhifen Pan
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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Renjian Liu
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Xin Chen
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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QiMei WangMu
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Ming Chen
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Lili Yu
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Junjun Liang
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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DaWa DunZhu
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Yuan Zheng
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Shuiyang Yu
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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ZhaXi LuoBu
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Xuanmin Guang
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Jiang Li
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Cao Deng
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Wushu Hu
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Chunhai Chen
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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XiongNu TaBa
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Liyun Gao
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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Xiaodan Lv
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Yuval Ben Abu
fProjects and Physics Section, Sapir Academic College, D.N. Hof Ashkelon 79165, Israel;
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Xiaodong Fang
dBGI-Tech, BGI-Shenzhen, Shenzhen 518083, China;
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Eviatar Nevo
gInstitute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel;
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  • For correspondence: nima_zhaxi@sina.com nevo@research.haifa.ac.il yumaoqun@cib.ac.cn wangj@genomics.org.cn
Maoqun Yu
cChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, P. R. China;
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  • For correspondence: nima_zhaxi@sina.com nevo@research.haifa.ac.il yumaoqun@cib.ac.cn wangj@genomics.org.cn
Jun Wang
hBGI-Shenzhen, Shenzhen 518083, China;
iDepartment of Biology, University of Copenhagen, Copenhagen 2200, Denmark; and
jPrincess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21441, Saudi Arabia
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  • For correspondence: nima_zhaxi@sina.com nevo@research.haifa.ac.il yumaoqun@cib.ac.cn wangj@genomics.org.cn
Nyima Tashi
aTibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Tibet 850002, China;
bBarley Improvement and Yak Breeding Key Laboratory of Tibet Autonomous Region, Lhasa 850002, China;
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  • For correspondence: nima_zhaxi@sina.com nevo@research.haifa.ac.il yumaoqun@cib.ac.cn wangj@genomics.org.cn
  1. Contributed by Eviatar Nevo, December 11, 2014 (sent for review September 15, 2014)

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Significance

The draft genome of Tibetan hulless barley provides a robust framework to better understand Poaceae evolution and a substantial basis for functional genomics of crop species with a large genome. The expansion of stress-related gene families in Tibetan hulless barley implies that it could be considered as an invaluable gene resource aiding stress tolerance improvement in Triticeae crops. Genome resequencing revealed extensive genetic diversity in Tibetan barley germplasm and divergence to sequenced barley genomes from other geographical regions. Investigation of genome-wide selection footprints demonstrated an adaptive correlation of genes under selection with extensive stressful environmental variables. These results reveal insights into the adaptation of Tibetan hulless barley to harsh environments on the highland and will facilitate future genetic improvement of crops.

Abstract

The Tibetan hulless barley (Hordeum vulgare L. var. nudum), also called “Qingke” in Chinese and “Ne” in Tibetan, is the staple food for Tibetans and an important livestock feed in the Tibetan Plateau. The diploid nature and adaptation to diverse environments of the highland give it unique resources for genetic research and crop improvement. Here we produced a 3.89-Gb draft assembly of Tibetan hulless barley with 36,151 predicted protein-coding genes. Comparative analyses revealed the divergence times and synteny between barley and other representative Poaceae genomes. The expansion of the gene family related to stress responses was found in Tibetan hulless barley. Resequencing of 10 barley accessions uncovered high levels of genetic variation in Tibetan wild barley and genetic divergence between Tibetan and non-Tibetan barley genomes. Selective sweep analyses demonstrate adaptive correlations of genes under selection with extensive environmental variables. Our results not only construct a genomic framework for crop improvement but also provide evolutionary insights of highland adaptation of Tibetan hulless barley.

  • Tibetan hulless barley
  • Triticeae evolution
  • genetic diversity
  • adaptation
  • selective sweep

Footnotes

  • ↵1X.Z., H.L., Z.W., S.Z., Y.T., Z.H., and Y.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: nima_zhaxi{at}sina.com, nevo{at}research.haifa.ac.il, yumaoqun{at}cib.ac.cn, or wangj{at}genomics.org.cn.
  • Author contributions: M.Y., J.W., and N.T. designed research; X.Z., H.L., Y.T., Y.W., Q.X., H.Y., R.L., Q.W., D.D., Z.L., X.T., and L.G. performed research; L.B. and X. Lv coordinated the project; H.L., Z.W., S.Z., Z.H., L.M., G.D., X.Y., X. Li, L.B., Z.P., X.C., M.C., L.Y., J. Liang, Y.Z., S.Y., X.G., J. Li, C.D., W.H., C.C., X. Lv, Y.B.A., X.F., and E.N. analyzed data; and H.L., S.Z., Z.H., E.N., and N.T. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive, www.ncbi.nlm.nih.gov/sra (accession no. SRA201388).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1423628112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Tibetan barley genome reveals highland adaption
Xingquan Zeng, Hai Long, Zhuo Wang, Shancen Zhao, Yawei Tang, Zhiyong Huang, Yulin Wang, Qijun Xu, Likai Mao, Guangbing Deng, Xiaoming Yao, Xiangfeng Li, Lijun Bai, Hongjun Yuan, Zhifen Pan, Renjian Liu, Xin Chen, QiMei WangMu, Ming Chen, Lili Yu, Junjun Liang, DaWa DunZhu, Yuan Zheng, Shuiyang Yu, ZhaXi LuoBu, Xuanmin Guang, Jiang Li, Cao Deng, Wushu Hu, Chunhai Chen, XiongNu TaBa, Liyun Gao, Xiaodan Lv, Yuval Ben Abu, Xiaodong Fang, Eviatar Nevo, Maoqun Yu, Jun Wang, Nyima Tashi
Proceedings of the National Academy of Sciences Jan 2015, 201423628; DOI: 10.1073/pnas.1423628112

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Tibetan barley genome reveals highland adaption
Xingquan Zeng, Hai Long, Zhuo Wang, Shancen Zhao, Yawei Tang, Zhiyong Huang, Yulin Wang, Qijun Xu, Likai Mao, Guangbing Deng, Xiaoming Yao, Xiangfeng Li, Lijun Bai, Hongjun Yuan, Zhifen Pan, Renjian Liu, Xin Chen, QiMei WangMu, Ming Chen, Lili Yu, Junjun Liang, DaWa DunZhu, Yuan Zheng, Shuiyang Yu, ZhaXi LuoBu, Xuanmin Guang, Jiang Li, Cao Deng, Wushu Hu, Chunhai Chen, XiongNu TaBa, Liyun Gao, Xiaodan Lv, Yuval Ben Abu, Xiaodong Fang, Eviatar Nevo, Maoqun Yu, Jun Wang, Nyima Tashi
Proceedings of the National Academy of Sciences Jan 2015, 201423628; DOI: 10.1073/pnas.1423628112
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