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

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 ZhouWon 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

Plant Systems Biology

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

418 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 1 2015

Funding

We thank R. Kai and C. Mayo Riley for maintaining the pineapple plants and the collection of leaf tissues; M. Conway at Dole Plantation for assistance in time-course leaf sample collection; G. Sanewski for providing the MD2 pedigree; and M. Cushman for providing clarifying comments on the manuscript. This project is supported by funding from the Fujian Agriculture and Forestry University to R.M.; a USDA T-START grant through the University of Hawaii to Q.Y., R.M., P.H.M. and R.E.P.; and funding from the University of Illinois at Urbana-Champaign to R.M. H.T. is supported by the 100 Talent Plan award from the Fujian provincial government. Analyses of the pineapple genome are supported by the following funding sources: US National Science Foundation (NSF) Plant Genome Program grant 0922545 to R.M., P.H.M. and Q.Y. and NSF grant DBI-1401572 to R.V.; NSF grant IOS-1444567 to J.H.L.-M.; and US National Institutes of Health award R01-HG006677 and US NSF awards DBI-1350041 and DBI-1265383 to M.C.S. W.C.Y., H.-B.G., H.G., G.A.T., X.Y. and J.C.C. acknowledge support from the US Department of Energy, Office of Science, Genomic Science Program, under award DE-SC0008834.

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@article{afa6796ce9b64567a4f2b52e6dd14236,

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.",

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 Yun Zheng 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",

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doi = "10.1038/ng.3435",

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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, Zheng, Y, 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

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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 - Zheng, Yun

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 - 2015/12/1

Y1 - 2015/12/1

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.

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ER -

The pineapple genome and the evolution of CAM photosynthesis

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