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Nature genetics
10, 2019;51 (10): 1549-1558.

The bracteatus pineapple genome and domestication of clonally propagated crops.

Li-Yu Chen, Robert VanBuren, Margot Paris, Hongye Zhou, Xingtan Zhang, Ching Man Wai, Hansong Yan, Shuai Chen, Michael Alonge, Srividya Ramakrishnan, Zhenyang Liao, Juan Liu, Jishan Lin, Jingjing Yue, Mahpara Fatima, Zhicong Lin, Jisen Zhang, Lixian Huang, Hao Wang, Teh-Yang Hwa, Shu-Min Kao, Jae Young Choi, Anupma Sharma, Jian Song, Lulu Wang, Won C Yim, John C Cushman, Robert E Paull, Tracie Matsumoto, Yuan Qin, Qingsong Wu, Jianping Wang, Qingyi Yu, Jun Wu, Shaoling Zhang, Peter Boches, Chih-Wei Tung, Ming-Li Wang, Geo Coppens d'Eeckenbrugge, Garth M Sanewski, Michael D Purugganan, Michael C Schatz, Jeffrey L Bennetzen, Christian Lexer, Ray Ming
Author Information
  1. Li-Yu Chen: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  2. Robert VanBuren: Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
  3. Margot Paris: Department of Biology, University of Fribourg, Fribourg, Switzerland.
  4. Hongye Zhou: Department of Genetics, University of Georgia, Athens, GA, USA. ORCID
  5. Xingtan Zhang: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  6. Ching Man Wai: Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA. ORCID
  7. Hansong Yan: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  8. Shuai Chen: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  9. Michael Alonge: Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA.
  10. Srividya Ramakrishnan: Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA.
  11. Zhenyang Liao: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  12. Juan Liu: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  13. Jishan Lin: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  14. Jingjing Yue: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  15. Mahpara Fatima: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  16. Zhicong Lin: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  17. Jisen Zhang: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  18. Lixian Huang: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  19. Hao Wang: Department of Genetics, University of Georgia, Athens, GA, USA.
  20. Teh-Yang Hwa: Department of Agronomy, National Taiwan University, Taipei, ROC.
  21. Shu-Min Kao: Department of Agronomy, National Taiwan University, Taipei, ROC.
  22. Jae Young Choi: Department of Biology, Center for Genomics and Systems Biology, New York University, NY, New York, USA. ORCID
  23. Anupma Sharma: Texas A&M AgriLife Research, Texas A&M University System, Dallas, TX, USA.
  24. Jian Song: Department of Agronomy, University of Florida, Gainesville, FL, USA.
  25. Lulu Wang: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  26. Won C Yim: Department of Biochemistry and Molecular Biology, MS330, University of Nevada, Reno, NV, USA. ORCID
  27. John C Cushman: Department of Biochemistry and Molecular Biology, MS330, University of Nevada, Reno, NV, USA.
  28. Robert E Paull: Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, Honolulu, HI, USA.
  29. Tracie Matsumoto: USDA-ARS, Pacific Basin Agricultural Research Center, Hilo, HI, USA.
  30. Yuan Qin: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
  31. Qingsong Wu: South Subtropical Crops Research Institute, CATAS, Zhanjiang, China.
  32. Jianping Wang: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  33. Qingyi Yu: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  34. Jun Wu: Centre of Pear Engineering Technology Research, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, China.
  35. Shaoling Zhang: Centre of Pear Engineering Technology Research, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, China.
  36. Peter Boches: USDA-ARS, Pacific Basin Agricultural Research Center, Hilo, HI, USA.
  37. Chih-Wei Tung: Department of Agronomy, National Taiwan University, Taipei, ROC.
  38. Ming-Li Wang: Hawaii Agriculture Research Center, Kunia, HI, USA.
  39. Geo Coppens d'Eeckenbrugge: Centre de Coopération Internationale en Recherche Agronomique pour le Développement, UMR AGAP, Montpellier, France.
  40. Garth M Sanewski: Queensland Department of Agriculture and Fisheries, Nambour, Queensland, Australia.
  41. Michael D Purugganan: Department of Biology, Center for Genomics and Systems Biology, New York University, NY, New York, USA. ORCID
  42. Michael C Schatz: Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA.
  43. Jeffrey L Bennetzen: Department of Genetics, University of Georgia, Athens, GA, USA. maize@uga.edu.
  44. Christian Lexer: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria. christian.lexer@univie.ac.at. ORCID
  45. Ray Ming: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China. rayming@illinois.edu. ORCID
PMID: 31570895 DOI: 10.1038/s41588-019-0506-8

Abstract

Domestication of clonally propagated crops such as pineapple from South America was hypothesized to be a 'one-step operation'. We sequenced the genome of Ananas comosus var. bracteatus CB5 and assembled 513 Mb into 25 chromosomes with 29,412 genes. Comparison of the genomes of CB5, F153 and MD2 elucidated the genomic basis of fiber production, color formation, sugar accumulation and fruit maturation. We also resequenced 89 Ananas genomes. Cultivars 'Smooth Cayenne' and 'Queen' exhibited ancient and recent admixture, while 'Singapore Spanish' supported a one-step operation of domestication. We identified 25 selective sweeps, including a strong sweep containing a pair of tandemly duplicated bromelain inhibitors. Four candidate genes for self-incompatibility were linked in F153, but were not functional in self-compatible CB5. Our findings support the coexistence of sexual recombination and a one-step operation in the domestication of clonally propagated crops. This work guides the exploration of sexual and asexual domestication trajectories in other clonally propagated crops.

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MeSH Term

Ananas
Bromelains
Crops, Agricultural
Domestication
Gene Expression Regulation, Plant
Genome, Plant
Phenotype
Plant Proteins
Plants, Genetically Modified
Population Dynamics
Quantitative Trait, Heritable
Sugars

Chemicals

Plant Proteins
Sugars
Bromelains
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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