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

doi:10.1038/s41588-019-0506-8

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 HwaShu 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^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

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

68 Scopus citations

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.

Original language	English (US)
Pages (from-to)	1549-1558
Number of pages	10
Journal	Nature Genetics
Volume	51
Issue number	10
DOIs	https://doi.org/10.1038/s41588-019-0506-8
State	Published - Oct 1 2019

Funding

This work was supported by the Department of Science and Technology of Fujian Province (grant no. 2016NZ0001-1), the National Natural Science Foundation of China grants (nos. U1605212 to Y.Q., 31628013 to Q.Y. and 31701874 to X.Z.), the Fuzhou Science and Technology project (grant no. 2017-N-33 to X.Z.), the Distinguished Young Scholars Fund in Fujian Agriculture and Forestry University (grant no. xjq201609 to L.Y.C.), the National Science Foundation grants (nos. DBI-1401572 to R.V. and DBI-1350041 to M.C.S.), the US National Institutes of Health (grant no. R01-HG006677 to M.C.S.), the NSF Plant Genome grants (nos. 0607123 and 043707-01 to J.L.B. and IOS-1546218 to M.D.P.), Zegar Family Foundation Grant (no. A16-0051-001 to M.D.P.) and the Swiss National Science Foundation grant (no. CRSII3_147630 to C.L.). We thank W. Till, D. Wegmann and D. Bartholomew for helpful discussions and J. Lin for assistance with data submission.

ASJC Scopus subject areas

Genetics

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10.1038/s41588-019-0506-8

Cite this

Chen, L. Y., VanBuren, R., Paris, M., Zhou, H., Zhang, X., Wai, C. M., Yan, H., Chen, S., Alonge, M., Ramakrishnan, S., Liao, Z., Liu, J., Lin, J., Yue, J., Fatima, M., Lin, Z., Zhang, J., Huang, L., Wang, H., ... Ming, R. (2019). The bracteatus pineapple genome and domestication of clonally propagated crops. Nature Genetics, 51(10), 1549-1558. https://doi.org/10.1038/s41588-019-0506-8

@article{36aa7a1b529042d5b92b02a05463c9f7,

title = "The bracteatus pineapple genome and domestication of clonally propagated crops",

abstract = "Domestication of clonally propagated crops such as pineapple from South America was hypothesized to be a {\textquoteleft}one-step operation{\textquoteright}. 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 {\textquoteleft}Smooth Cayenne{\textquoteright} and {\textquoteleft}Queen{\textquoteright} exhibited ancient and recent admixture, while {\textquoteleft}Singapore Spanish{\textquoteright} 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.",

author = "Chen, {Li Yu} and Robert VanBuren and Margot Paris and Hongye Zhou and Xingtan Zhang and Wai, {Ching Man} and Hansong Yan and Shuai Chen and Michael Alonge and Srividya Ramakrishnan and Zhenyang Liao and Juan Liu and Jishan Lin and Jingjing Yue and Mahpara Fatima and Zhicong Lin and Jisen Zhang and Lixian Huang and Hao Wang and Hwa, {Teh Yang} and Kao, {Shu Min} and Choi, {Jae Young} and Anupma Sharma and Jian Song and Lulu Wang and Yim, {Won C.} and Cushman, {John C.} and Paull, {Robert E.} and Tracie Matsumoto and Yuan Qin and Qingsong Wu and Jianping Wang and Qingyi Yu and Jun Wu and Shaoling Zhang and Peter Boches and Tung, {Chih Wei} and Wang, {Ming Li} and {Coppens d{\textquoteright}Eeckenbrugge}, Geo and Sanewski, {Garth M.} and Purugganan, {Michael D.} and Schatz, {Michael C.} and Bennetzen, {Jeffrey L.} and Christian Lexer and Ray Ming",

note = "Funding Information: This work was supported by the Department of Science and Technology of Fujian Province (grant no. 2016NZ0001-1), the National Natural Science Foundation of China grants (nos. U1605212 to Y.Q., 31628013 to Q.Y. and 31701874 to X.Z.), the Fuzhou Science and Technology project (grant no. 2017-N-33 to X.Z.), the Distinguished Young Scholars Fund in Fujian Agriculture and Forestry University (grant no. xjq201609 to L.Y.C.), the National Science Foundation grants (nos. DBI-1401572 to R.V. and DBI-1350041 to M.C.S.), the US National Institutes of Health (grant no. R01-HG006677 to M.C.S.), the NSF Plant Genome grants (nos. 0607123 and 043707-01 to J.L.B. and IOS-1546218 to M.D.P.), Zegar Family Foundation Grant (no. A16-0051-001 to M.D.P.) and the Swiss National Science Foundation grant (no. CRSII3_147630 to C.L.). We thank W. Till, D. Wegmann and D. Bartholomew for helpful discussions and J. Lin for assistance with data submission. Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = oct,

day = "1",

doi = "10.1038/s41588-019-0506-8",

language = "English (US)",

volume = "51",

pages = "1549--1558",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Research",

number = "10",

}

Chen, LY, VanBuren, R, Paris, M, Zhou, H, Zhang, X, Wai, CM, Yan, H, Chen, S, Alonge, M, Ramakrishnan, S, Liao, Z, Liu, J, Lin, J, Yue, J, Fatima, M, Lin, Z, Zhang, J, Huang, L, Wang, H, Hwa, TY, Kao, SM, Choi, JY, Sharma, A, Song, J, Wang, L, Yim, WC, Cushman, JC, Paull, RE, Matsumoto, T, Qin, Y, Wu, Q, Wang, J, Yu, Q, Wu, J, Zhang, S, Boches, P, Tung, CW, Wang, ML, Coppens d’Eeckenbrugge, G, Sanewski, GM, Purugganan, MD, Schatz, MC, Bennetzen, JL, Lexer, C & Ming, R 2019, 'The bracteatus pineapple genome and domestication of clonally propagated crops', Nature Genetics, vol. 51, no. 10, pp. 1549-1558. https://doi.org/10.1038/s41588-019-0506-8

TY - JOUR

T1 - The bracteatus pineapple genome and domestication of clonally propagated crops

AU - Chen, Li Yu

AU - VanBuren, Robert

AU - Paris, Margot

AU - Zhou, Hongye

AU - Zhang, Xingtan

AU - Wai, Ching Man

AU - Yan, Hansong

AU - Chen, Shuai

AU - Alonge, Michael

AU - Ramakrishnan, Srividya

AU - Liao, Zhenyang

AU - Liu, Juan

AU - Lin, Jishan

AU - Yue, Jingjing

AU - Fatima, Mahpara

AU - Lin, Zhicong

AU - Zhang, Jisen

AU - Huang, Lixian

AU - Wang, Hao

AU - Hwa, Teh Yang

AU - Kao, Shu Min

AU - Choi, Jae Young

AU - Sharma, Anupma

AU - Song, Jian

AU - Wang, Lulu

AU - Yim, Won C.

AU - Cushman, John C.

AU - Paull, Robert E.

AU - Matsumoto, Tracie

AU - Qin, Yuan

AU - Wu, Qingsong

AU - Wang, Jianping

AU - Yu, Qingyi

AU - Wu, Jun

AU - Zhang, Shaoling

AU - Boches, Peter

AU - Tung, Chih Wei

AU - Wang, Ming Li

AU - Coppens d’Eeckenbrugge, Geo

AU - Sanewski, Garth M.

AU - Purugganan, Michael D.

AU - Schatz, Michael C.

AU - Bennetzen, Jeffrey L.

AU - Lexer, Christian

AU - Ming, Ray

N1 - Funding Information: This work was supported by the Department of Science and Technology of Fujian Province (grant no. 2016NZ0001-1), the National Natural Science Foundation of China grants (nos. U1605212 to Y.Q., 31628013 to Q.Y. and 31701874 to X.Z.), the Fuzhou Science and Technology project (grant no. 2017-N-33 to X.Z.), the Distinguished Young Scholars Fund in Fujian Agriculture and Forestry University (grant no. xjq201609 to L.Y.C.), the National Science Foundation grants (nos. DBI-1401572 to R.V. and DBI-1350041 to M.C.S.), the US National Institutes of Health (grant no. R01-HG006677 to M.C.S.), the NSF Plant Genome grants (nos. 0607123 and 043707-01 to J.L.B. and IOS-1546218 to M.D.P.), Zegar Family Foundation Grant (no. A16-0051-001 to M.D.P.) and the Swiss National Science Foundation grant (no. CRSII3_147630 to C.L.). We thank W. Till, D. Wegmann and D. Bartholomew for helpful discussions and J. Lin for assistance with data submission. Publisher Copyright: © 2019, The Author(s).

PY - 2019/10/1

Y1 - 2019/10/1

N2 - 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.

AB - 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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U2 - 10.1038/s41588-019-0506-8

DO - 10.1038/s41588-019-0506-8

M3 - Article

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AN - SCOPUS:85074201385

SN - 1061-4036

VL - 51

SP - 1549

EP - 1558

JO - Nature Genetics

JF - Nature Genetics

IS - 10

ER -

The bracteatus pineapple genome and domestication of clonally propagated crops

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