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; 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

doi:10.1038/ng.3435

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, 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

Fujian Agriculture and Forestry University
University of Illinois at Urbana-Champaign
Donald Danforth Plant Science Center
University of Arizona
Cold Spring Harbor Laboratory
Johns Hopkins University
Stony Brook University
University of Maryland
University of Georgia
State of Hawaii, Department of Agriculture
University of Hawai'i at Mānoa
Caris Life Sciences
Shenyang Northern Hospital
CAS - Shanghai Institute of Materia Medica
Sun Yat-Sen University
Fox Chase Cancer Center
University of Pennsylvania
University of Nevada, Reno
University of Ottawa
University of California at Berkeley
COFFEEADAPT
Institut de recherche pour le développement
University of Tennessee, Knoxville
University of Chinese Academy of Sciences
Texas A&M University
Youngstown State University
Baylor College of Medicine
University of Texas Southwestern Medical Center
University of North Carolina at Chapel Hill
The Children's Hospital of Philadelphia
Association for Molecular Pathology
University of Kentucky
University of Adelaide
National Taiwan University
Oak Ridge National Laboratory
United States Department of Agriculture
Oklahoma State University
University of Oxford

Research output: Contribution to journal › Article › peer-review

478 Scopus citations

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 C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

Original language	English
Pages (from-to)	1435-1442
Number of pages	8
Journal	Nature Genetics
Volume	47
Issue number	12
DOIs	https://doi.org/10.1038/ng.3435
State	Published - Dec 2015

Keywords

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

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@article{a04088b231154ba69234d19906d74b1d,

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. Pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.",

keywords = "Ananas/genetics, Chromosome Mapping, Epigenomics, Evolution, Molecular, Gene Expression Regulation, Plant, Gene Regulatory Networks, Genetic Markers, Genome, Plant, Genomics/methods, High-Throughput Nucleotide Sequencing/methods, Photosynthesis/physiology",

author = "Ray Ming and Robert VanBuren and Wai, \{Ching Man\} and Haibao Tang and Schatz, \{Michael C.\} and Bowers, \{John E.\} and Eric Lyons and Wang, \{Ming Li\} and Jung Chen and Eric Biggers and Jisen Zhang and Lixian Huang and Lingmao Zhang and Wenjing Miao and Jian Zhang and Zhangyao Ye and Chenyong Miao and Zhicong Lin and Hao Wang and Hongye Zhou and Yim, \{Won C.\} and Priest, \{Henry D.\} and Chunfang Zheng and Margaret Woodhouse and Edger, \{Patrick P.\} and Romain Guyot and Guo, \{Hao Bo\} and Hong Guo and Guangyong Zheng and Ratnesh Singh and Anupma Sharma and Xiangjia Min and Hayan Lee and James Gurtowski and Sedlazeck, \{Fritz J.\} and Alex Harkess and McKain, \{Michael R.\} and Zhenyang Liao and Jingping Fang and Juan Liu and Xiaodan Zhang and Qing Zhang and Weichang Hu and Yuan Qin and Kai Wang and Chen, \{Li Yu\} and Neil Shirley and Lin, \{Yann Rong\} and Liu, \{Li Yu\} and Hernandez, \{Alvaro G.\} and Wright, \{Chris L.\} and Vincent Bulone and Tuskan, \{Gerald A.\} and Katy Heath and Francis Zee and Moore, \{Paul H.\} and Ramanjulu Sunkar and Leebens-Mack, \{James H.\} and Todd Mockler and Bennetzen, \{Jeffrey L.\} and Michael Freeling and David Sankoff and Paterson, \{Andrew H.\} and Xinguang Zhu and Xiaohan Yang and Smith, \{J. Andrew C.\} and Cushman, \{John C.\} and Paull, \{Robert E.\} and Qingyi Yu",

year = "2015",

month = dec,

doi = "10.1038/ng.3435",

language = "English",

volume = "47",

pages = "1435--1442",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Research",

number = "12",

}

Ming, R, VanBuren, R, Wai, CM, Tang, H, Schatz, MC, Bowers, JE, Lyons, E, Wang, ML, Chen, J, Biggers, E, Zhang, J, Huang, L, Zhang, L, Miao, W, Zhang, J, Ye, Z, Miao, C, Lin, Z, Wang, H, Zhou, H, Yim, WC, Priest, HD, Zheng, C, Woodhouse, M, Edger, PP, Guyot, R, Guo, HB, Guo, H, Zheng, G, Singh, R, Sharma, A, Min, X, Lee, H, Gurtowski, J, Sedlazeck, FJ, Harkess, A, McKain, MR, Liao, Z, Fang, J, Liu, J, Zhang, X, Zhang, Q, Hu, W, Qin, Y, Wang, K, Chen, LY, Shirley, N, Lin, YR, Liu, LY, Hernandez, AG, Wright, CL, Bulone, V, Tuskan, GA, Heath, K, Zee, F, Moore, PH, Sunkar, R, Leebens-Mack, JH, Mockler, T, Bennetzen, JL, Freeling, M, Sankoff, D, Paterson, AH, Zhu, X, Yang, X, Smith, JAC, Cushman, JC, Paull, RE & Yu, Q 2015, 'The pineapple genome and the evolution of CAM photosynthesis', Nature Genetics, vol. 47, no. 12, pp. 1435-1442. https://doi.org/10.1038/ng.3435

TY - JOUR

T1 - The pineapple genome and the evolution of CAM photosynthesis

AU - Ming, Ray

AU - VanBuren, Robert

AU - Wai, Ching Man

AU - Tang, Haibao

AU - Schatz, Michael C.

AU - Bowers, John E.

AU - Lyons, Eric

AU - Wang, Ming Li

AU - Chen, Jung

AU - Biggers, Eric

AU - Zhang, Jisen

AU - Huang, Lixian

AU - Zhang, Lingmao

AU - Miao, Wenjing

AU - Zhang, Jian

AU - Ye, Zhangyao

AU - Miao, Chenyong

AU - Lin, Zhicong

AU - Wang, Hao

AU - Zhou, Hongye

AU - Yim, Won C.

AU - Priest, Henry D.

AU - Zheng, Chunfang

AU - Woodhouse, Margaret

AU - Edger, Patrick P.

AU - Guyot, Romain

AU - Guo, Hao Bo

AU - Guo, Hong

AU - Zheng, Guangyong

AU - Singh, Ratnesh

AU - Sharma, Anupma

AU - Min, Xiangjia

AU - Lee, Hayan

AU - Gurtowski, James

AU - Sedlazeck, Fritz J.

AU - Harkess, Alex

AU - McKain, Michael R.

AU - Liao, Zhenyang

AU - Fang, Jingping

AU - Liu, Juan

AU - Zhang, Xiaodan

AU - Zhang, Qing

AU - Hu, Weichang

AU - Qin, Yuan

AU - Wang, Kai

AU - Chen, Li Yu

AU - Shirley, Neil

AU - Lin, Yann Rong

AU - Liu, Li Yu

AU - Hernandez, Alvaro G.

AU - Wright, Chris L.

AU - Bulone, Vincent

AU - Tuskan, Gerald A.

AU - Heath, Katy

AU - Zee, Francis

AU - Moore, Paul H.

AU - Sunkar, Ramanjulu

AU - Leebens-Mack, James H.

AU - Mockler, Todd

AU - Bennetzen, Jeffrey L.

AU - Freeling, Michael

AU - Sankoff, David

AU - Paterson, Andrew H.

AU - Zhu, Xinguang

AU - Yang, Xiaohan

AU - Smith, J. Andrew C.

AU - Cushman, John C.

AU - Paull, Robert E.

AU - Yu, Qingyi

PY - 2015/12

Y1 - 2015/12

N2 - 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 C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

AB - 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 C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

KW - Ananas/genetics

KW - Chromosome Mapping

KW - Epigenomics

KW - Evolution, Molecular

KW - Gene Expression Regulation, Plant

KW - Gene Regulatory Networks

KW - Genetic Markers

KW - Genome, Plant

KW - Genomics/methods

KW - High-Throughput Nucleotide Sequencing/methods

KW - Photosynthesis/physiology

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U2 - 10.1038/ng.3435

DO - 10.1038/ng.3435

M3 - Article

C2 - 26523774

SN - 1061-4036

VL - 47

SP - 1435

EP - 1442

JO - Nature Genetics

JF - Nature Genetics

IS - 12

ER -

The pineapple genome and the evolution of CAM photosynthesis

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Keywords

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