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Title: The pineapple genome and the evolution of CAM photosynthesis

Abstract

Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ρ duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Lastly, we found pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

Authors:
 [1];  [2];  [1]; ORCiD logo [3];  [4];  [5];  [6];  [7];  [8];  [4];  [9];  [9];  [9];  [9];  [9];  [9];  [9];  [9];  [5];  [5] more »;  [10];  [11];  [12];  [13];  [13];  [14];  [15];  [15];  [16]; ORCiD logo [17];  [17];  [18];  [19];  [4];  [4];  [4];  [5];  [11];  [9];  [9];  [9];  [9];  [9];  [9];  [9];  [9];  [9];  [20];  [21];  [21];  [22];  [22];  [20];  [23];  [24];  [25];  [7];  [26];  [5]; ORCiD logo [11];  [5];  [13];  [12];  [27];  [16];  [23]; ORCiD logo [28];  [10];  [8];  [17] « less
  1. Fujian Agriculture and Forestry Univ., Fuzhou (China); Univ. of Illinois, Urbana-Champaign, IL (United States). School of Integrative Biology Joint Center for Genomics and Biotechnology; Fujian Agriculture and Forestry Univ., Fuzhou (China). Fujian-Taiwan Joint Center for Ecological Control of Crop Pests; Univ. of Illinois, Urbana-Champaign, IL (United States). Dept. of Plant Biology
  2. Fujian Agriculture and Forestry Univ., Fuzhou (China); Univ. of Illinois, Urbana-Champaign, IL (United States). School of Integrative Biology Joint Center for Genomics and Biotechnology; Fujian Agriculture and Forestry Univ., Fuzhou (China). Fujian-Taiwan Joint Center for Ecological Control of Crop Pests; Univ. of Illinois, Urbana-Champaign, IL (United States). Dept. of Plant Biology; Donald Danforth Plant Science Center, St. Louis, MO (United States)
  3. Fujian Agriculture and Forestry Univ., Fuzhou (China); Univ. of Illinois, Urbana-Champaign, IL (United States). School of Integrative Biology Joint Center for Genomics and Biotechnology; Fujian Agriculture and Forestry Univ., Fuzhou (China). Fujian-Taiwan Joint Center for Ecological Control of Crop Pests; Univ. of Arizona, Tucson, AZ (United States). iPlant Collaborative
  4. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (United States)
  5. Univ. of Georgia, Athens, GA (United States). Dept. of Plant Biology
  6. Univ. of Arizona, Tucson, AZ (United States). iPlant Collaborative
  7. Hawaii Agriculture Research Center, Kunia, HI (United States)
  8. Univ. of Hawaii, Honolulu, HI (United States). Dept. of Tropical Plant and Soil Sciences
  9. Fujian Agriculture and Forestry Univ., Fuzhou (China); Univ. of Illinois, Urbana-Champaign, IL (United States). School of Integrative Biology Joint Center for Genomics and Biotechnology; Fujian Agriculture and Forestry Univ., Fuzhou (China). Fujian-Taiwan Joint Center for Ecological Control of Crop Pests
  10. Univ. of Nevada, Reno, NV (United States). Dept. of Biochemistry and Molecular Biology
  11. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  12. Univ. of Ottawa, Ottawa, ON (Canada). Dept. of Mathematics and Statistics
  13. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  14. Inst. of Research for Development, Diversity and Adaptation of Plants Development, Montpellier (France)
  15. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry and Cellular and Molecular Biology
  16. Chinese Academy of Sciences - Max Planck Gesellschaft Partner Inst. for Computational Biology (CAS-MPG), Shanghai (China); Chinese Academy of Sciences (CAS), Shanghai (China). Shanghai Inst. for Biological Sciences
  17. Texas A&M Univ. System, Dallas, TX (United States). Dept. of Plant Pathology and Microbiology
  18. Youngstown State Univ., OH (United States). Dept. of Biological Sciences
  19. Kunming Univ. of Science and Technology, Kunming (China)
  20. Univ. of Adelaide, SA (Australia). Waite Campus Urrbrae, School of Agriculture, Food and Wine
  21. National Taiwan Univ., Taipei (Taiwan). Dept. of Agronomy
  22. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States). W.M. Keck Center
  23. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  24. Univ. of Illinois, Urbana-Champaign, IL (United States). Dept. of Plant Biology
  25. US Dept. of Agriculture - Agricultural Research Service (USDA-ARS)., Hilo, HI (United States). Pacific Basin Agricultural Research Center
  26. Oklahoma State Univ., Stillwater, OK (United States). Dept. of Biochemistry and Molecular Biology
  27. Univ. of Georgia, Athens, GA (United States). Plant Genome Mapping Lab.
  28. Univ. of Oxford (United Kingdom). Dept. of Plant Sciences
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1293938
Alternate Identifier(s):
OSTI ID: 1319239
Grant/Contract Number:  
SC0008834; 0922545; DBI-1401572; IOS-1444567; R01-HG006677; DBI-1350041; DBI-1265383; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Nature Genetics
Additional Journal Information:
Journal Volume: 47; Journal Issue: 12; Journal ID: ISSN 1061-4036
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; DNA sequencing; Genomics; Plant genetics

Citation Formats

Ming, Ray, VanBuren, Robert, Wai, Ching Man, Tang, Haibao, Schatz, Michael C., Bowers, John E., Lyons, Eric, Wang, Ming-Li, Chen, Jung, Biggers, Eric, Zhang, Jisen, Huang, Lixian, Zhang, Lingmao, Miao, Wenjing, Zhang, Jian, Ye, Zhangyao, Miao, Chenyong, Lin, Zhicong, Wang, Hao, Zhou, Hongye, Yim, Won C., Priest, Henry D., Zheng, Chunfang, Woodhouse, Margaret, Edger, Patrick P., Guyot, Romain, Guo, Hao-Bo, Guo, Hong, Zheng, Guangyong, Singh, Ratnesh, Sharma, Anupma, Min, Xiangjia, Zheng, Yun, Lee, Hayan, Gurtowski, James, Sedlazeck, Fritz J., Harkess, Alex, McKain, Michael R., Liao, Zhenyang, Fang, Jingping, Liu, Juan, Zhang, Xiaodan, Zhang, Qing, Hu, Weichang, Qin, Yuan, Wang, Kai, Chen, Li-Yu, Shirley, Neil, Lin, Yann-Rong, Liu, Li-Yu, Hernandez, Alvaro G., Wright, Chris L., Bulone, Vincent, Tuskan, Gerald A., Heath, Katy, Zee, Francis, Moore, Paul H., Sunkar, Ramanjulu, Leebens-Mack, James H., Mockler, Todd, Bennetzen, Jeffrey L., Freeling, Michael, Sankoff, David, Paterson, Andrew H., Zhu, Xinguang, Yang, Xiaohan, Smith, J. Andrew C., Cushman, John C., Paull, Robert E., and Yu, Qingyi. The pineapple genome and the evolution of CAM photosynthesis. United States: N. p., 2015. Web. doi:10.1038/ng.3435.
Ming, Ray, VanBuren, Robert, Wai, Ching Man, Tang, Haibao, Schatz, Michael C., Bowers, John E., Lyons, Eric, Wang, Ming-Li, Chen, Jung, Biggers, Eric, Zhang, Jisen, Huang, Lixian, Zhang, Lingmao, Miao, Wenjing, Zhang, Jian, Ye, Zhangyao, Miao, Chenyong, Lin, Zhicong, Wang, Hao, Zhou, Hongye, Yim, Won C., Priest, Henry D., Zheng, Chunfang, Woodhouse, Margaret, Edger, Patrick P., Guyot, Romain, Guo, Hao-Bo, Guo, Hong, Zheng, Guangyong, Singh, Ratnesh, Sharma, Anupma, Min, Xiangjia, Zheng, Yun, Lee, Hayan, Gurtowski, James, Sedlazeck, Fritz J., Harkess, Alex, McKain, Michael R., Liao, Zhenyang, Fang, Jingping, Liu, Juan, Zhang, Xiaodan, Zhang, Qing, Hu, Weichang, Qin, Yuan, Wang, Kai, Chen, Li-Yu, Shirley, Neil, Lin, Yann-Rong, Liu, Li-Yu, Hernandez, Alvaro G., Wright, Chris L., Bulone, Vincent, Tuskan, Gerald A., Heath, Katy, Zee, Francis, Moore, Paul H., Sunkar, Ramanjulu, Leebens-Mack, James H., Mockler, Todd, Bennetzen, Jeffrey L., Freeling, Michael, Sankoff, David, Paterson, Andrew H., Zhu, Xinguang, Yang, Xiaohan, Smith, J. Andrew C., Cushman, John C., Paull, Robert E., & Yu, Qingyi. The pineapple genome and the evolution of CAM photosynthesis. United States. doi:10.1038/ng.3435.
Ming, Ray, VanBuren, Robert, Wai, Ching Man, Tang, Haibao, Schatz, Michael C., Bowers, John E., Lyons, Eric, Wang, Ming-Li, Chen, Jung, Biggers, Eric, Zhang, Jisen, Huang, Lixian, Zhang, Lingmao, Miao, Wenjing, Zhang, Jian, Ye, Zhangyao, Miao, Chenyong, Lin, Zhicong, Wang, Hao, Zhou, Hongye, Yim, Won C., Priest, Henry D., Zheng, Chunfang, Woodhouse, Margaret, Edger, Patrick P., Guyot, Romain, Guo, Hao-Bo, Guo, Hong, Zheng, Guangyong, Singh, Ratnesh, Sharma, Anupma, Min, Xiangjia, Zheng, Yun, Lee, Hayan, Gurtowski, James, Sedlazeck, Fritz J., Harkess, Alex, McKain, Michael R., Liao, Zhenyang, Fang, Jingping, Liu, Juan, Zhang, Xiaodan, Zhang, Qing, Hu, Weichang, Qin, Yuan, Wang, Kai, Chen, Li-Yu, Shirley, Neil, Lin, Yann-Rong, Liu, Li-Yu, Hernandez, Alvaro G., Wright, Chris L., Bulone, Vincent, Tuskan, Gerald A., Heath, Katy, Zee, Francis, Moore, Paul H., Sunkar, Ramanjulu, Leebens-Mack, James H., Mockler, Todd, Bennetzen, Jeffrey L., Freeling, Michael, Sankoff, David, Paterson, Andrew H., Zhu, Xinguang, Yang, Xiaohan, Smith, J. Andrew C., Cushman, John C., Paull, Robert E., and Yu, Qingyi. Mon . "The pineapple genome and the evolution of CAM photosynthesis". United States. doi:10.1038/ng.3435. https://www.osti.gov/servlets/purl/1293938.
@article{osti_1293938,
title = {The pineapple genome and the evolution of CAM photosynthesis},
author = {Ming, Ray and VanBuren, Robert and Wai, Ching Man and Tang, Haibao and Schatz, Michael C. and Bowers, John E. and Lyons, Eric and Wang, Ming-Li and Chen, Jung and Biggers, Eric and Zhang, Jisen and Huang, Lixian and Zhang, Lingmao and Miao, Wenjing and Zhang, Jian and Ye, Zhangyao and Miao, Chenyong and Lin, Zhicong and Wang, Hao and Zhou, Hongye and Yim, Won C. and Priest, Henry D. and Zheng, Chunfang and Woodhouse, Margaret and Edger, Patrick P. and Guyot, Romain and Guo, Hao-Bo and Guo, Hong and Zheng, Guangyong and Singh, Ratnesh and Sharma, Anupma and Min, Xiangjia and Zheng, Yun and Lee, Hayan and Gurtowski, James and Sedlazeck, Fritz J. and Harkess, Alex and McKain, Michael R. and Liao, Zhenyang and Fang, Jingping and Liu, Juan and Zhang, Xiaodan and Zhang, Qing and Hu, Weichang and Qin, Yuan and Wang, Kai and Chen, Li-Yu and Shirley, Neil and Lin, Yann-Rong and Liu, Li-Yu and Hernandez, Alvaro G. and Wright, Chris L. and Bulone, Vincent and Tuskan, Gerald A. and Heath, Katy and Zee, Francis and Moore, Paul H. and Sunkar, Ramanjulu and Leebens-Mack, James H. and Mockler, Todd and Bennetzen, Jeffrey L. and Freeling, Michael and Sankoff, David and Paterson, Andrew H. and Zhu, Xinguang and Yang, Xiaohan and Smith, J. Andrew C. and Cushman, John C. and Paull, Robert E. and Yu, Qingyi},
abstractNote = {Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ρ duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Lastly, we found pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.},
doi = {10.1038/ng.3435},
journal = {Nature Genetics},
number = 12,
volume = 47,
place = {United States},
year = {2015},
month = {11}
}

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