DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 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 Laboratory (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. https://doi.org/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. https://doi.org/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. 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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 316 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons
journal, May 2007

  • Xu, Z.; Wang, H.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm286

Nuclear DNA content of some important plant species
journal, August 1991

  • Arumuganathan, K.; Earle, E. D.
  • Plant Molecular Biology Reporter, Vol. 9, Issue 3
  • DOI: 10.1007/BF02672069

PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006

  • Suyama, M.; Torrents, D.; Bork, P.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl315

Crassulacean Acid Metabolism: A Curiosity in Context
journal, June 1978


The map-based sequence of the rice genome
journal, August 2005


Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014


Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses
journal, January 2009


The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle
journal, February 2014

  • Wang, W.; Haberer, G.; Gundlach, H.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4311

LTR_STRUC: a novel search and identification program for LTR retrotransposons
journal, February 2003


Many or most genes in Arabidopsis transposed after the origin of the order Brassicales
journal, October 2008


Phosphoenolpyruvate Carboxykinase in Plants Exhibiting Crassulacean Acid Metabolism
journal, October 1973

  • Dittrich, P.; Campbell, Wilbur H.; Black, C. C.
  • Plant Physiology, Vol. 52, Issue 4
  • DOI: 10.1104/pp.52.4.357

Gene identification in novel eukaryotic genomes by self-training algorithm
journal, November 2005


Longli is not a Hybrid of Longan and Lychee as Revealed by Genome Size Analysis and Trichome Morphology
journal, November 2011


Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms
journal, February 2004

  • Nam, Jongmin; Kim, Joonyul; Lee, Shinyoung
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 7
  • DOI: 10.1073/pnas.0308430100

PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006

  • Suyama, M.; Torrents, D.; Bork, P.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl315

LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons
journal, May 2007

  • Xu, Z.; Wang, H.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm286

Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism
journal, January 2005

  • Holtum, Joseph A. M.; Smith, J. Andrew C.; Neuhaus, H. Ekkehard
  • Functional Plant Biology, Vol. 32, Issue 5
  • DOI: 10.1071/FP04189

Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae
journal, February 2014

  • Givnish, Thomas J.; Barfuss, Michael H. J.; Ee, Benjamin Van
  • Molecular Phylogenetics and Evolution, Vol. 71
  • DOI: 10.1016/j.ympev.2013.10.010

The banana (Musa acuminata) genome and the evolution of monocotyledonous plants
journal, July 2012

  • D’Hont, Angélique; Denoeud, France; Aury, Jean-Marc
  • Nature, Vol. 488, Issue 7410
  • DOI: 10.1038/nature11241

Longli is not a Hybrid of Longan and Lychee as Revealed by Genome Size Analysis and Trichome Morphology
journal, November 2011


Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple)
journal, June 2007

  • Antony, E.; Taybi, T.; Courbot, M.
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/ern077

Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids
journal, October 2008

  • Lyons, Eric; Pedersen, Brent; Kane, Josh
  • Plant Physiology, Vol. 148, Issue 4
  • DOI: 10.1104/pp.108.124867

Evolution along the crassulacean acid metabolism continuum
journal, January 2010

  • Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark
  • Functional Plant Biology, Vol. 37, Issue 11
  • DOI: 10.1071/FP10084

Nuclear DNA content of some important plant species
journal, November 1991

  • Arumuganathan, K.; Earle, E. D.
  • Plant Molecular Biology Reporter, Vol. 9, Issue 4
  • DOI: 10.1007/bf02672016

Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds
journal, July 2013

  • Singh, Rajinder; Ong-Abdullah, Meilina; Low, Eng-Ti Leslie
  • Nature, Vol. 500, Issue 7462
  • DOI: 10.1038/nature12309

De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera)
journal, May 2011

  • Al-Dous, Eman K.; George, Binu; Al-Mahmoud, Maryam E.
  • Nature Biotechnology, Vol. 29, Issue 6
  • DOI: 10.1038/nbt.1860

Genetics of Self-Incompatibility in the Monocot Genera, Ananas (Pineapple) and Gasteria
journal, May 1967


Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis
journal, September 2002

  • Michael, Todd P.; McClung, C. Robertson
  • Plant Physiology, Vol. 130, Issue 2
  • DOI: 10.1104/pp.004929

Gene identification in novel eukaryotic genomes by self-training algorithm
journal, November 2005


The Sorghum bicolor genome and the diversification of grasses
journal, January 2009

  • Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
  • Nature, Vol. 457, Issue 7229
  • DOI: 10.1038/nature07723

Sucrose transport across the vacuolar membrane of Ananas comosus
journal, January 2002

  • McRae, Shelley R.; Christopher, John T.; Smith, J. Andrew C.
  • Functional Plant Biology, Vol. 29, Issue 6
  • DOI: 10.1071/PP01227

Shared origins of a key enzyme during the evolution of C4 and CAM metabolism
journal, March 2014

  • Christin, Pascal-Antoine; Arakaki, Monica; Osborne, Colin P.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru087

Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs
journal, June 2010


InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


Abundance, Distribution, and Transcriptional Activity of Repetitive Elements in the Maize Genome
journal, September 2001


Integrated Syntenic and Phylogenomic Analyses Reveal an Ancient Genome Duplication in Monocots
journal, July 2014


Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012


Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules
journal, January 2008


Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

Screening synteny blocks in pairwise genome comparisons through integer programming
journal, April 2011


Adaptive seeds tame genomic sequence comparison
journal, January 2011


Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids
journal, December 2011

  • Woodhouse, Margaret R.; Tang, Haibao; Freeling, Michael
  • The Plant Cell, Vol. 23, Issue 12
  • DOI: 10.1105/tpc.111.093567

JBrowse: A next-generation genome browser
journal, July 2009

  • Skinner, M. E.; Uzilov, A. V.; Stein, L. D.
  • Genome Research, Vol. 19, Issue 9
  • DOI: 10.1101/gr.094607.109

The genome sequence of the orchid Phalaenopsis equestris
journal, November 2014

  • Cai, Jing; Liu, Xin; Vanneste, Kevin
  • Nature Genetics, Vol. 47, Issue 1
  • DOI: 10.1038/ng.3149

Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics
journal, May 2004

  • Paterson, A. H.; Bowers, J. E.; Chapman, B. A.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 26
  • DOI: 10.1073/pnas.0307901101

Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis
journal, September 2002

  • Michael, Todd P.; McClung, C. Robertson
  • Plant Physiology, Vol. 130, Issue 2
  • DOI: 10.1104/pp.004929

Crassulacean Acid Metabolism: A Curiosity in Context
journal, June 1978


Shared origins of a key enzyme during the evolution of C4 and CAM metabolism
journal, March 2014

  • Christin, Pascal-Antoine; Arakaki, Monica; Osborne, Colin P.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru087

The Development of C 4 Rice: Current Progress and Future Challenges
journal, June 2012

  • von Caemmerer, Susanne; Quick, W. Paul; Furbank, Robert T.
  • Science, Vol. 336, Issue 6089
  • DOI: 10.1126/science.1220177

Maintenance Carbon Cycle in Crassulacean Acid Metabolism Plant Leaves: Source and Compartmentation of Carbon for Nocturnal Malate Synthesis
journal, January 1985

  • Kenyon, William H.; Severson, Ray F.; Black, Clanton C.
  • Plant Physiology, Vol. 77, Issue 1
  • DOI: 10.1104/pp.77.1.183

MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes
journal, November 2007

  • Cantarel, B. L.; Korf, I.; Robb, S. M. C.
  • Genome Research, Vol. 18, Issue 1
  • DOI: 10.1101/gr.6743907

Letter to the editor
journal, January 2003


Origin and Domestication of Native Amazonian Crops
journal, January 2010

  • Clement, Charles; De Cristo-Araújo, Michelly; Coppens D’Eeckenbrugge, Geo
  • Diversity, Vol. 2, Issue 1
  • DOI: 10.3390/d2010072

InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world
journal, July 2015

  • Yang, Xiaohan; Cushman, John C.; Borland, Anne M.
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13393

Angiosperm genome comparisons reveal early polyploidy in the monocot lineage
journal, December 2009

  • Tang, H.; Bowers, J. E.; Wang, X.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 1
  • DOI: 10.1073/pnas.0908007107

Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.)
journal, January 2013


Angiosperm Responses to a Low-CO 2 World: CAM and C 4 Photosynthesis as Parallel Evolutionary Trajectories
journal, July 2012

  • Edwards, Erika J.; Ogburn, R. Matthew
  • International Journal of Plant Sciences, Vol. 173, Issue 6
  • DOI: 10.1086/666098

Nuclear DNA content of some important plant species
journal, November 1991

  • Arumuganathan, K.; Earle, E. D.
  • Plant Molecular Biology Reporter, Vol. 9, Issue 4
  • DOI: 10.1007/bf02672016

JBrowse: A next-generation genome browser
journal, July 2009

  • Skinner, M. E.; Uzilov, A. V.; Stein, L. D.
  • Genome Research, Vol. 19, Issue 9
  • DOI: 10.1101/gr.094607.109

Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments
journal, January 2008


A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity
journal, December 2014

  • Magallón, Susana; Gómez‐Acevedo, Sandra; Sánchez‐Reyes, Luna L.
  • New Phytologist, Vol. 207, Issue 2
  • DOI: 10.1111/nph.13264

Phosphoenolpyruvate Carboxykinase in Plants Exhibiting Crassulacean Acid Metabolism
journal, October 1973

  • Dittrich, P.; Campbell, Wilbur H.; Black, C. C.
  • Plant Physiology, Vol. 52, Issue 4
  • DOI: 10.1104/pp.52.4.357

DNA-binding specificities of plant transcription factors and their potential to define target genes
journal, January 2014

  • Franco-Zorrilla, José M.; López-Vidriero, Irene; Carrasco, José L.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 6
  • DOI: 10.1073/pnas.1316278111

Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

Works referencing / citing this record:

Ammonium intensifies CAM photosynthesis and counteracts drought effects by increasing malate transport and antioxidant capacity in Guzmania monostachia
journal, February 2018

  • Pereira, Paula Natália; Gaspar, Marília; Smith, J. Andrew C.
  • Journal of Experimental Botany, Vol. 69, Issue 8
  • DOI: 10.1093/jxb/ery054

A gene-rich fraction analysis of the Passiflora edulis genome reveals highly conserved microsyntenic regions with two related Malpighiales species
journal, August 2018

  • Munhoz, Carla Freitas; Costa, Zirlane Portugal; Cauz-Santos, Luiz Augusto
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-31330-8

The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017


The low-copy nuclear gene Agt1 as a novel DNA barcoding marker for Bromeliaceae
journal, March 2020


Correction to: Simple protoplast isolation system for gene expression and protein interaction studies in pineapple (Ananas comosus L.)
journal, December 2018


Genome-wide searches and molecular analyses highlight the unique evolutionary path of flavone synthase I (FNSI) in Apiaceae
journal, February 2018


Identification of microRNAs, phasiRNAs and Their Targets in Pineapple
journal, June 2016


Reconstructing the genome of the most recent common ancestor of flowering plants
journal, March 2017

  • Murat, Florent; Armero, Alix; Pont, Caroline
  • Nature Genetics, Vol. 49, Issue 4
  • DOI: 10.1038/ng.3813

The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017


Transcriptome Profiling of the Pineapple under Low Temperature to Facilitate Its Breeding for Cold Tolerance
journal, September 2016


Correction to: Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
journal, April 2019


CMIP: a software package capable of reconstructing genome-wide regulatory networks using gene expression data
journal, December 2016


Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)
journal, January 2019

  • Heyduk, Karolina; Hwang, Michelle; Albert, Victor
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.02000

The kinome of pineapple: catalog and insights into functions in crassulacean acid metabolism plants
journal, September 2018


AfAP2-1, An Age-Dependent Gene of Aechmea fasciata, Responds to Exogenous Ethylene Treatment
journal, February 2016

  • Lei, Ming; Li, Zhi-Ying; Wang, Jia-Bin
  • International Journal of Molecular Sciences, Vol. 17, Issue 3
  • DOI: 10.3390/ijms17030303

Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants
journal, February 2019


Genome-Wide Comparative Analysis of Microsatellites in Pineapple
journal, March 2016


Genome-Wide Classification and Evolutionary and Functional Analyses of the VQ Family
journal, April 2019


Independent origin of MIRNA genes controlling homologous target genes by partial inverted duplication of antisense‐transcribed sequences
journal, November 2019

  • Gramzow, Lydia; Lobbes, Dajana; Innard, Nathan
  • The Plant Journal, Vol. 101, Issue 2
  • DOI: 10.1111/tpj.14550

Secrets of succulence
journal, March 2017


CMIP: a software package capable of reconstructing genome-wide regulatory networks using gene expression data
journal, December 2016


Expression Profiles of Wuschel-Related Homeobox Gene Family in Pineapple (Ananas comosus L)
journal, November 2017


Identification and evolution of C4 photosynthetic pathway genes in plants
journal, March 2020


Circadian Regulation of the Plant Transcriptome Under Natural Conditions
journal, November 2019

  • Panter, Paige E.; Muranaka, Tomoaki; Cuitun-Coronado, David
  • Frontiers in Genetics, Vol. 10
  • DOI: 10.3389/fgene.2019.01239

Temporal and spatial transcriptomic and micro RNA dynamics of CAM photosynthesis in pineapple
journal, August 2017

  • Wai, Ching M.; VanBuren, Robert; Zhang, Jisen
  • The Plant Journal, Vol. 92, Issue 1
  • DOI: 10.1111/tpj.13630

The Peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity
journal, March 2017


Virus-induced gene silencing: empowering genetics in non-model organisms
journal, November 2018

  • Dommes, Anna B.; Gross, Thomas; Herbert, Denise B.
  • Journal of Experimental Botany, Vol. 70, Issue 3
  • DOI: 10.1093/jxb/ery411

A role for MIR828 in pineapple fruit development
journal, January 2020


Photosynthesis and salinity: are these mutually exclusive?
journal, March 2018


A role for MIR828 in pineapple fruit development
journal, January 2020


The Apostasia genome and the evolution of orchids
journal, September 2017

  • Zhang, Guo-Qiang; Liu, Ke-Wei; Li, Zhen
  • Nature, Vol. 549, Issue 7672
  • DOI: 10.1038/nature23897

Stout camphor tree genome fills gaps in understanding of flowering plant genome evolution
journal, January 2019


Simple protoplast isolation system for gene expression and protein interaction studies in pineapple (Ananas comosus L.)
journal, October 2018


Genome-Wide Analysis of the YABBY Transcription Factor Family in Pineapple and Functional Identification of AcYABBY4 Involvement in Salt Stress
journal, November 2019

  • Li, Zeyun; Li, Gang; Cai, Mingxing
  • International Journal of Molecular Sciences, Vol. 20, Issue 23
  • DOI: 10.3390/ijms20235863

The water lily genome and the early evolution of flowering plants
journal, December 2019


The asparagus genome sheds light on the origin and evolution of a young Y chromosome
journal, November 2017


Systematics of Vriesea (Bromeliaceae): phylogenetic relationships based on nuclear gene and partial plastome sequences
journal, December 2019

  • Machado, Talita Mota; Loiseau, Oriane; Paris, Margot
  • Botanical Journal of the Linnean Society, Vol. 192, Issue 4
  • DOI: 10.1093/botlinnean/boz102

Identification and characterization of pineapple leaf lncRNAs in crassulacean acid metabolism (CAM) photosynthesis pathway
journal, April 2019


Evolutionary history and structure of nuclear matrix constituent proteins, the plant analogues of lamins
journal, March 2019

  • Ciska, Malgorzata; Hikida, Riku; Masuda, Kiyoshi
  • Journal of Experimental Botany, Vol. 70, Issue 10
  • DOI: 10.1093/jxb/erz102

Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants
journal, February 2019


Widespread lateral gene transfer among grasses
journal, April 2021

  • Hibdige, Samuel G. S.; Raimondeau, Pauline; Christin, Pascal‐Antoine
  • New Phytologist, Vol. 230, Issue 6
  • DOI: 10.1111/nph.17328

Genome-Wide Identification and Expression, Protein–Protein Interaction and Evolutionary Analysis of the Seed Plant-Specific BIG GRAIN and BIG GRAIN LIKE Gene Family
journal, October 2017

  • Mishra, Bhuwaneshwar S.; Jamsheer K., Muhammed; Singh, Dhriti
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01812

Molecular foundations of chilling-tolerance of modern maize
journal, February 2016


Think tank: water relations of Bromeliaceae in their evolutionary context
journal, April 2016

  • Males, Jamie
  • Botanical Journal of the Linnean Society, Vol. 181, Issue 3
  • DOI: 10.1111/boj.12423

Inference of Gene Regulatory Network Uncovers the Linkage between Circadian Clock and Crassulacean Acid Metabolism in Kalanchoë fedtschenkoi
journal, August 2021

  • Moseley, Robert C.; Motta, Francis; Tuskan, Gerald A.
  • Cells, Vol. 10, Issue 9
  • DOI: 10.3390/cells10092217

Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album
journal, June 2019


Comparative Analysis of GC Content Variations in Plant Genomes
journal, April 2016


Advances in and perspectives on evolution in Bromeliaceae
journal, June 2016

  • Palma-Silva, Clarisse; Leal, Barbara S. S.; Chaves, Cleber J. N.
  • Botanical Journal of the Linnean Society, Vol. 181, Issue 3
  • DOI: 10.1111/boj.12431

Identification, Characterization and Expression Profiles of Dof Transcription Factors in Pineapple (Ananas comosus L)
journal, April 2018


The evolutionary significance of polyploidy
journal, May 2017

  • Van de Peer, Yves; Mizrachi, Eshchar; Marchal, Kathleen
  • Nature Reviews Genetics, Vol. 18, Issue 7
  • DOI: 10.1038/nrg.2017.26

The Gastrodia elata genome provides insights into plant adaptation to heterotrophy
journal, April 2018


Analysis of MADS-box genes revealed modified flowering gene network and diurnal expression in pineapple
journal, January 2020


Agave angustifolia albino plantlets lose stomatal physiology function by changing the development of the stomatal complex due to a molecular disruption
journal, January 2020

  • Sara, Hernández-Castellano; René, Garruña-Hernández; Rosa, Us-Camas
  • Molecular Genetics and Genomics, Vol. 295, Issue 3
  • DOI: 10.1007/s00438-019-01643-y

Integrated DNA methylome and transcriptome analysis reveals the ethylene-induced flowering pathway genes in pineapple
journal, December 2017


A phylogenomic assessment of ancient polyploidy and genome evolution across the Poales
journal, March 2016

  • McKain, Michael R.; Tang, Haibao; McNeal, Joel R.
  • Genome Biology and Evolution
  • DOI: 10.1093/gbe/evw060

A gene-rich fraction analysis of the Passiflora edulis genome reveals highly conserved microsyntenic regions with two related Malpighiales species
journal, August 2018

  • Munhoz, Carla Freitas; Costa, Zirlane Portugal; Cauz-Santos, Luiz Augusto
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-31330-8

Draft Genomes of Two Artocarpus Plants, Jackfruit (A. heterophyllus) and Breadfruit (A. altilis)
journal, December 2019


Mikania micrantha genome provides insights into the molecular mechanism of rapid growth
journal, January 2020


Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway
journal, April 2016

  • Zhang, Liangsheng; Chen, Fei; Zhang, Guo-Qiang
  • The Plant Journal, Vol. 86, Issue 2
  • DOI: 10.1111/tpj.13159

The distance and median problems in the single-cut-or-join model with single-gene duplications
journal, May 2020

  • Mane, Aniket C.; Lafond, Manuel; Feijao, Pedro C.
  • Algorithms for Molecular Biology, Vol. 15, Issue 1
  • DOI: 10.1186/s13015-020-00169-y

PGD: Pineapple Genomics Database
journal, September 2018


New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics
journal, November 2018


Paleogenomics: reconstruction of plant evolutionary trajectories from modern and ancient DNA
journal, February 2019


Ancient Polyploidy and Genome Evolution in Palms
journal, April 2019

  • Barrett, Craig F.; McKain, Michael R.; Sinn, Brandon T.
  • Genome Biology and Evolution, Vol. 11, Issue 5
  • DOI: 10.1093/gbe/evz092

Histological evaluation of pineapple transgenic plants following 8 years of field growth
journal, January 2020


DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.)
journal, January 2020


Economic importance, taxonomic representation and scientific priority as drivers of genome sequencing projects
journal, November 2016

  • Vallée, Geneviève C.; Muñoz, Daniella Santos; Sankoff, David
  • BMC Genomics, Vol. 17, Issue S10
  • DOI: 10.1186/s12864-016-3100-9

Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album
journal, June 2019


New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics
journal, November 2018


Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants
journal, September 2019

  • Yang, Xiaohan; Liu, Degao; Tschaplinski, Timothy J.
  • Journal of Experimental Botany, Vol. 70, Issue 22
  • DOI: 10.1093/jxb/erz408

Secrets of succulence
text, January 2017


Interaction between the Circadian Clock and Regulators of Heat Stress Responses in Plants
journal, February 2020


Developing naturally stress-resistant crops for a sustainable agriculture
journal, November 2018


Elucidating and mining the Tulipa and Lilium transcriptomes
journal, July 2016

  • Moreno-Pachon, Natalia M.; Leeggangers, Hendrika A. C. F.; Nijveen, Harm
  • Plant Molecular Biology, Vol. 92, Issue 3
  • DOI: 10.1007/s11103-016-0508-1

Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm)
journal, June 2017


Genome Wide Identification and Expression Profiles of TALE Genes in Pineapple (Ananas comosus L)
journal, June 2019


Genome-Wide Identification and Expression Profile Analysis of WRKY Family Genes in the Autopolyploid Saccharum spontaneum
journal, December 2019

  • Li, Zhen; Hua, Xiuting; Zhong, Weiming
  • Plant and Cell Physiology, Vol. 61, Issue 3
  • DOI: 10.1093/pcp/pcz227

Comparative genomics revealed the gene evolution and functional divergence of magnesium transporter families in Saccharum
journal, January 2019


Mikania micrantha genome provides insights into the molecular mechanism of rapid growth
journal, January 2020


The bracteatus pineapple genome and domestication of clonally propagated crops
journal, September 2019


Ancient Polyploidy and Genome Evolution in Palms
journal, April 2019

  • Barrett, Craig F.; McKain, Michael R.; Sinn, Brandon T.
  • Genome Biology and Evolution, Vol. 11, Issue 5
  • DOI: 10.1093/gbe/evz092

The genetics of convergent evolution: insights from plant photosynthesis
journal, March 2019

  • Heyduk, Karolina; Moreno-Villena, Jose J.; Gilman, Ian S.
  • Nature Reviews Genetics, Vol. 20, Issue 8
  • DOI: 10.1038/s41576-019-0107-5

Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing of Spirodela
journal, September 2019

  • An, Dong; Zhou, Yong; Li, Changsheng
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 38
  • DOI: 10.1073/pnas.1910401116

Genome-Wide Analysis of the YABBY Transcription Factor Family in Pineapple and Functional Identification of AcYABBY4 Involvement in Salt Stress
journal, November 2019

  • Li, Zeyun; Li, Gang; Cai, Mingxing
  • International Journal of Molecular Sciences, Vol. 20, Issue 23
  • DOI: 10.3390/ijms20235863

The water lily genome and the early evolution of flowering plants
journal, December 2019


The Gastrodia elata genome provides insights into plant adaptation to heterotrophy
journal, April 2018


Evolutionary history and structure of nuclear matrix constituent proteins, the plant analogues of lamins
journal, March 2019

  • Ciska, Malgorzata; Hikida, Riku; Masuda, Kiyoshi
  • Journal of Experimental Botany, Vol. 70, Issue 10
  • DOI: 10.1093/jxb/erz102

Undervalued potential of crassulacean acid metabolism for current and future agricultural production
journal, June 2019

  • Davis, Sarah C.; Simpson, June; Gil-Vega, Katia del Carmen
  • Journal of Experimental Botany, Vol. 70, Issue 22
  • DOI: 10.1093/jxb/erz223

Expansin gene loss is a common occurrence during adaptation to an aquatic environment
journal, November 2019

  • Hepler, Nathan K.; Bowman, Alexa; Carey, Robert E.
  • The Plant Journal, Vol. 101, Issue 3
  • DOI: 10.1111/tpj.14572

Model-Based Detection of Whole-Genome Duplications in a Phylogeny
journal, May 2020

  • Zwaenepoel, Arthur; Van de Peer, Yves
  • Molecular Biology and Evolution, Vol. 37, Issue 9
  • DOI: 10.1093/molbev/msaa111

Chromosome-level genome assembly, annotation and evolutionary analysis of the ornamental plant Asparagus setaceus
journal, April 2020


Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
journal, August 2018


Diurnal Cycling Transcription Factors of Pineapple Revealed by Genome-Wide Annotation and Global Transcriptomic Analysis
journal, August 2017

  • Sharma, Anupma; Wai, Ching Man; Ming, Ray
  • Genome Biology and Evolution, Vol. 9, Issue 9
  • DOI: 10.1093/gbe/evx161

The Peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity
journal, March 2017


A first glimpse at genes important to the Azolla–Nostoc symbiosis
journal, January 2019


Ecophysiology of constitutive and facultative CAM photosynthesis
journal, February 2019


Phylogenetic relationships among Ananas and related taxa (Bromelioideae, Bromeliaceae) based on nuclear, plastid and AFLP data
journal, May 2018

  • Matuszak-Renger, Sabine; Paule, Juraj; Heller, Sascha
  • Plant Systematics and Evolution, Vol. 304, Issue 7
  • DOI: 10.1007/s00606-018-1514-3

Genomic Survey, Characterization, and Expression Profile Analysis of the SBP Genes in Pineapple (Ananas comosus L.)
journal, January 2017

  • Ali, Hina; Liu, Yanhui; Azam, Syed Muhammad
  • International Journal of Genomics, Vol. 2017
  • DOI: 10.1155/2017/1032846

The role of cis-elements in the evolution of crassulacean acid metabolism photosynthesis
journal, January 2020


Draft Genomes of Two Artocarpus Plants, Jackfruit (A. heterophyllus) and Breadfruit (A. altilis)
journal, December 2019


Floral Transcriptomes in Woodland Strawberry Uncover Developing Receptacle and Anther Gene Networks
journal, May 2014

  • Hollender, Courtney A.; Kang, Chunying; Darwish, Omar
  • Plant Physiology, Vol. 165, Issue 3
  • DOI: 10.1104/pp.114.237529

The asparagus genome sheds light on the origin and evolution of a young Y chromosome
journal, November 2017


RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum
journal, November 2018


Revisiting ancestral polyploidy in plants
journal, July 2017

  • Ruprecht, Colin; Lohaus, Rolf; Vanneste, Kevin
  • Science Advances, Vol. 3, Issue 7
  • DOI: 10.1126/sciadv.1603195