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Nature genetics
Dec, 2015;47 (12): 1435-42.

The pineapple genome and the evolution of CAM photosynthesis.

Ray Ming, Robert VanBuren, Ching Man Wai, Haibao Tang, Michael C Schatz, John E Bowers, Eric Lyons, Ming-Li Wang, Jung Chen, Eric Biggers, Jisen Zhang, Lixian Huang, Lingmao Zhang, Wenjing Miao, Jian Zhang, Zhangyao Ye, Chenyong Miao, Zhicong Lin, Hao Wang, Hongye Zhou, Won C Yim, Henry D Priest, Chunfang Zheng, Margaret Woodhouse, Patrick P Edger, Romain Guyot, Hao-Bo Guo, Hong Guo, Guangyong Zheng, Ratnesh Singh, Anupma Sharma, Xiangjia Min, Yun Zheng, Hayan Lee, James Gurtowski, Fritz J Sedlazeck, Alex Harkess, Michael R McKain, Zhenyang Liao, Jingping Fang, Juan Liu, Xiaodan Zhang, Qing Zhang, Weichang Hu, Yuan Qin, Kai Wang, Li-Yu Chen, Neil Shirley, Yann-Rong Lin, Li-Yu Liu, Alvaro G Hernandez, Chris L Wright, Vincent Bulone, Gerald A Tuskan, Katy Heath, Francis Zee, Paul H Moore, Ramanjulu Sunkar, James H Leebens-Mack, Todd Mockler, Jeffrey L Bennetzen, Michael Freeling, David Sankoff, Andrew H Paterson, Xinguang Zhu, Xiaohan Yang, J Andrew C Smith, John C Cushman, Robert E Paull, Qingyi Yu
Author Information
  1. Ray Ming: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  2. Robert VanBuren: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  3. Ching Man Wai: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  4. Haibao Tang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  5. Michael C Schatz: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
  6. John E Bowers: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  7. Eric Lyons: iPlant Collaborative/University of Arizona, Tucson, Arizona, USA.
  8. Ming-Li Wang: Hawaii Agriculture Research Center, Kunia, Hawaii, USA.
  9. Jung Chen: Department of Tropical Plant and Soil Sciences, University of Hawaii, Honolulu, Hawaii, USA.
  10. Eric Biggers: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
  11. Jisen Zhang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  12. Lixian Huang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  13. Lingmao Zhang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  14. Wenjing Miao: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  15. Jian Zhang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  16. Zhangyao Ye: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  17. Chenyong Miao: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  18. Zhicong Lin: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  19. Hao Wang: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  20. Hongye Zhou: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  21. Won C Yim: Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada, USA.
  22. Henry D Priest: Donald Danforth Plant Science Center, St. Louis, Missouri, USA.
  23. Chunfang Zheng: Department of Mathematics and Statistics, University of Ottawa, Ottawa, Ontario, Canada.
  24. Margaret Woodhouse: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USA.
  25. Patrick P Edger: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USA.
  26. Romain Guyot: Institut de Recherche pour le Développement, Diversité Adaptation et Développement des Plantes, Montpellier, France.
  27. Hao-Bo Guo: Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, Tennessee, USA.
  28. Hong Guo: Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, Tennessee, USA.
  29. Guangyong Zheng: Key Laboratory of Computational Biology, Chinese Academy of Sciences-Max Planck Gesellschaft Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
  30. Ratnesh Singh: Texas A&M AgriLife Research, Department of Plant Pathology and Microbiology, Texas A&M University System, Dallas, Texas, USA. ORCID
  31. Anupma Sharma: Texas A&M AgriLife Research, Department of Plant Pathology and Microbiology, Texas A&M University System, Dallas, Texas, USA.
  32. Xiangjia Min: Department of Biological Sciences, Youngstown State University, Youngstown, Ohio, USA.
  33. Yun Zheng: Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming, China.
  34. Hayan Lee: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
  35. James Gurtowski: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
  36. Fritz J Sedlazeck: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
  37. Alex Harkess: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  38. Michael R McKain: Donald Danforth Plant Science Center, St. Louis, Missouri, USA.
  39. Zhenyang Liao: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  40. Jingping Fang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  41. Juan Liu: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  42. Xiaodan Zhang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  43. Qing Zhang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  44. Weichang Hu: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  45. Yuan Qin: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  46. Kai Wang: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  47. Li-Yu Chen: Fujian Agriculture and Forestry University and University of Illinois at Urbana-Champaign-School of Integrative Biology Joint Center for Genomics and Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
  48. Neil Shirley: Australian Research Council (ARC) Centre of Excellence in Plant Cell Walls, School of Agriculture, Food and Wine, University of Adelaide, Waite Campus Urrbrae, Adelaide, South Australia, Australia.
  49. Yann-Rong Lin: Department of Agronomy, National Taiwan University, Taipei, Taiwan.
  50. Li-Yu Liu: Department of Agronomy, National Taiwan University, Taipei, Taiwan.
  51. Alvaro G Hernandez: W.M. Keck Center, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
  52. Chris L Wright: W.M. Keck Center, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
  53. Vincent Bulone: Australian Research Council (ARC) Centre of Excellence in Plant Cell Walls, School of Agriculture, Food and Wine, University of Adelaide, Waite Campus Urrbrae, Adelaide, South Australia, Australia.
  54. Gerald A Tuskan: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
  55. Katy Heath: Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
  56. Francis Zee: US Department of Agriculture-Agricultural Research Service (USDA-ARS), Pacific Basin Agricultural Research Center, Hilo, Hawaii, USA.
  57. Paul H Moore: Hawaii Agriculture Research Center, Kunia, Hawaii, USA.
  58. Ramanjulu Sunkar: Department of Biochemistry and Molecular Biology, Noble Research Center, Oklahoma State University, Stillwater, Oklahoma, USA.
  59. James H Leebens-Mack: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  60. Todd Mockler: Donald Danforth Plant Science Center, St. Louis, Missouri, USA. ORCID
  61. Jeffrey L Bennetzen: Department of Plant Biology, University of Georgia, Athens, Georgia, USA.
  62. Michael Freeling: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USA.
  63. David Sankoff: Department of Mathematics and Statistics, University of Ottawa, Ottawa, Ontario, Canada.
  64. Andrew H Paterson: Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia, USA.
  65. Xinguang Zhu: Key Laboratory of Computational Biology, Chinese Academy of Sciences-Max Planck Gesellschaft Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
  66. Xiaohan Yang: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
  67. J Andrew C Smith: Department of Plant Sciences, University of Oxford, Oxford, UK. ORCID
  68. John C Cushman: Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada, USA.
  69. Robert E Paull: Department of Tropical Plant and Soil Sciences, University of Hawaii, Honolulu, Hawaii, USA.
  70. Qingyi Yu: Texas A&M AgriLife Research, Department of Plant Pathology and Microbiology, Texas A&M University System, Dallas, Texas, USA.
PMID: 26523774 DOI: 10.1038/ng.3435

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. 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.

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Grants

  1. R01 HG006677/NHGRI NIH HHS
  2. R01-HG006677/NHGRI NIH HHS

MeSH Term

Ananas
Chromosome Mapping
Epigenomics
Evolution, Molecular
Gene Expression Regulation, Plant
Gene Regulatory Networks
Genetic Markers
Genome, Plant
Genomics
High-Throughput Nucleotide Sequencing
Photosynthesis

Chemicals

Genetic Markers
Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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