SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya

Jingjing Yue; Robert VanBuren; Juan Liu; Jingping Fang; Xingtan Zhang; Zhenyang Liao; Ching Man Wai; Xiuming Xu; Shuai Chen; Shengchen Zhang; Xiaokai Ma; Yaying Ma; Hongying Yu; Jing Lin; Ping Zhou; Yongji Huang; Ban Deng; Fang Deng; Xiaobing Zhao; Hansong Yan; Mahpara Fatima; Dessireé Zerpa-Catanho; Xiaodan Zhang; Zhicong Lin; Mei Yang; Nancy J. Chen; Eric Mora-Newcomer; Patricia Quesada-Rojas; Antonio Bogantes; Víctor M. Jiménez; Haibao Tang; Jisen Zhang; Ming Li Wang; Robert E. Paull; Qingyi Yu; Ray Ming

doi:10.1038/s41588-022-01068-1

SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya

Jingjing Yue, Robert VanBuren, Juan Liu, Jingping Fang, Xingtan Zhang, Zhenyang Liao, Ching Man Wai, Xiuming Xu, Shuai Chen, Shengchen Zhang, Xiaokai Ma, Yaying Ma, Hongying Yu, Jing Lin, Ping Zhou, Yongji Huang, Ban Deng, Fang Deng, Xiaobing Zhao, Hansong YanMahpara Fatima, Dessireé Zerpa-Catanho, Xiaodan Zhang, Zhicong Lin, Mei Yang, Nancy J. Chen, Eric Mora-Newcomer, Patricia Quesada-Rojas, Antonio Bogantes, Víctor M. Jiménez, Haibao Tang, Jisen Zhang, Ming Li Wang, Robert E. Paull, Qingyi Yu, Ray Ming^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

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

46 Scopus citations

Abstract

Transgenic papaya is widely publicized for controlling papaya ringspot virus. However, the impact of particle bombardment on the genome remains unknown. The transgenic SunUp and its progenitor Sunset genomes were assembled into 351.5 and 350.3 Mb in nine chromosomes, respectively. We identified a 1.64 Mb insertion containing three transgenic insertions in SunUp chromosome 5, consisting of 52 nuclear-plastid, 21 nuclear-mitochondrial and 1 nuclear genomic fragments. A 591.9 kb fragment in chromosome 5 was translocated into the 1.64 Mb insertion. We assembled a gapless 9.8 Mb hermaphrodite-specific region of the Y^h chromosome and its 6.0 Mb X counterpart. Resequencing 86 genomes revealed three distinct groups, validating their geographic origin and breeding history. We identified 147 selective sweeps and defined the essential role of zeta-carotene desaturase in carotenoid accumulation during domestication. Our findings elucidated the impact of particle bombardment and improved our understanding of sex chromosomes and domestication to expedite papaya improvement.

Original language	English (US)
Pages (from-to)	715-724
Number of pages	10
Journal	Nature Genetics
Volume	54
Issue number	5
DOIs	https://doi.org/10.1038/s41588-022-01068-1
State	Published - May 2022

Funding

This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y). This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y).

ASJC Scopus subject areas

Genetics

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Yue, J., VanBuren, R., Liu, J., Fang, J., Zhang, X., Liao, Z., Wai, C. M., Xu, X., Chen, S., Zhang, S., Ma, X., Ma, Y., Yu, H., Lin, J., Zhou, P., Huang, Y., Deng, B., Deng, F., Zhao, X., ... Ming, R. (2022). SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya. Nature Genetics, 54(5), 715-724. https://doi.org/10.1038/s41588-022-01068-1

@article{c88c6145e9604fcaa2e82ecb5f0459a3,

title = "SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya",

abstract = "Transgenic papaya is widely publicized for controlling papaya ringspot virus. However, the impact of particle bombardment on the genome remains unknown. The transgenic SunUp and its progenitor Sunset genomes were assembled into 351.5 and 350.3 Mb in nine chromosomes, respectively. We identified a 1.64 Mb insertion containing three transgenic insertions in SunUp chromosome 5, consisting of 52 nuclear-plastid, 21 nuclear-mitochondrial and 1 nuclear genomic fragments. A 591.9 kb fragment in chromosome 5 was translocated into the 1.64 Mb insertion. We assembled a gapless 9.8 Mb hermaphrodite-specific region of the Yh chromosome and its 6.0 Mb X counterpart. Resequencing 86 genomes revealed three distinct groups, validating their geographic origin and breeding history. We identified 147 selective sweeps and defined the essential role of zeta-carotene desaturase in carotenoid accumulation during domestication. Our findings elucidated the impact of particle bombardment and improved our understanding of sex chromosomes and domestication to expedite papaya improvement.",

author = "Jingjing Yue and Robert VanBuren and Juan Liu and Jingping Fang and Xingtan Zhang and Zhenyang Liao and Wai, {Ching Man} and Xiuming Xu and Shuai Chen and Shengchen Zhang and Xiaokai Ma and Yaying Ma and Hongying Yu and Jing Lin and Ping Zhou and Yongji Huang and Ban Deng and Fang Deng and Xiaobing Zhao and Hansong Yan and Mahpara Fatima and Dessire{\'e} Zerpa-Catanho and Xiaodan Zhang and Zhicong Lin and Mei Yang and Chen, {Nancy J.} and Eric Mora-Newcomer and Patricia Quesada-Rojas and Antonio Bogantes and Jim{\'e}nez, {V{\'i}ctor M.} and Haibao Tang and Jisen Zhang and Wang, {Ming Li} and Paull, {Robert E.} and Qingyi Yu and Ray Ming",

note = "Funding Information: This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y). Funding Information: This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y). Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2022",

month = may,

doi = "10.1038/s41588-022-01068-1",

language = "English (US)",

volume = "54",

pages = "715--724",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Research",

number = "5",

}

Yue, J, VanBuren, R, Liu, J, Fang, J, Zhang, X, Liao, Z, Wai, CM, Xu, X, Chen, S, Zhang, S, Ma, X, Ma, Y, Yu, H, Lin, J, Zhou, P, Huang, Y, Deng, B, Deng, F, Zhao, X, Yan, H, Fatima, M, Zerpa-Catanho, D, Zhang, X, Lin, Z, Yang, M, Chen, NJ, Mora-Newcomer, E, Quesada-Rojas, P, Bogantes, A, Jiménez, VM, Tang, H, Zhang, J, Wang, ML, Paull, RE, Yu, Q & Ming, R 2022, 'SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya', Nature Genetics, vol. 54, no. 5, pp. 715-724. https://doi.org/10.1038/s41588-022-01068-1

TY - JOUR

T1 - SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya

AU - Yue, Jingjing

AU - VanBuren, Robert

AU - Liu, Juan

AU - Fang, Jingping

AU - Zhang, Xingtan

AU - Liao, Zhenyang

AU - Wai, Ching Man

AU - Xu, Xiuming

AU - Chen, Shuai

AU - Zhang, Shengchen

AU - Ma, Xiaokai

AU - Ma, Yaying

AU - Yu, Hongying

AU - Lin, Jing

AU - Zhou, Ping

AU - Huang, Yongji

AU - Deng, Ban

AU - Deng, Fang

AU - Zhao, Xiaobing

AU - Yan, Hansong

AU - Fatima, Mahpara

AU - Zerpa-Catanho, Dessireé

AU - Zhang, Xiaodan

AU - Lin, Zhicong

AU - Yang, Mei

AU - Chen, Nancy J.

AU - Mora-Newcomer, Eric

AU - Quesada-Rojas, Patricia

AU - Bogantes, Antonio

AU - Jiménez, Víctor M.

AU - Tang, Haibao

AU - Zhang, Jisen

AU - Wang, Ming Li

AU - Paull, Robert E.

AU - Yu, Qingyi

AU - Ming, Ray

N1 - Funding Information: This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y). Funding Information: This work was supported by US National Science Foundation (NSF) Plant Genome Research Program Award (DBI-1546890 to R.M.), National Natural Science Foundation of China grants (31701889 to J.Y.) and Natural Science Foundation of Fujian Province grants (2018J01601 to J.Y. and 2018J01604 to Xingtan Zhang). The Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2020091A to J.Y). Publisher Copyright: © 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2022/5

Y1 - 2022/5

N2 - Transgenic papaya is widely publicized for controlling papaya ringspot virus. However, the impact of particle bombardment on the genome remains unknown. The transgenic SunUp and its progenitor Sunset genomes were assembled into 351.5 and 350.3 Mb in nine chromosomes, respectively. We identified a 1.64 Mb insertion containing three transgenic insertions in SunUp chromosome 5, consisting of 52 nuclear-plastid, 21 nuclear-mitochondrial and 1 nuclear genomic fragments. A 591.9 kb fragment in chromosome 5 was translocated into the 1.64 Mb insertion. We assembled a gapless 9.8 Mb hermaphrodite-specific region of the Yh chromosome and its 6.0 Mb X counterpart. Resequencing 86 genomes revealed three distinct groups, validating their geographic origin and breeding history. We identified 147 selective sweeps and defined the essential role of zeta-carotene desaturase in carotenoid accumulation during domestication. Our findings elucidated the impact of particle bombardment and improved our understanding of sex chromosomes and domestication to expedite papaya improvement.

AB - Transgenic papaya is widely publicized for controlling papaya ringspot virus. However, the impact of particle bombardment on the genome remains unknown. The transgenic SunUp and its progenitor Sunset genomes were assembled into 351.5 and 350.3 Mb in nine chromosomes, respectively. We identified a 1.64 Mb insertion containing three transgenic insertions in SunUp chromosome 5, consisting of 52 nuclear-plastid, 21 nuclear-mitochondrial and 1 nuclear genomic fragments. A 591.9 kb fragment in chromosome 5 was translocated into the 1.64 Mb insertion. We assembled a gapless 9.8 Mb hermaphrodite-specific region of the Yh chromosome and its 6.0 Mb X counterpart. Resequencing 86 genomes revealed three distinct groups, validating their geographic origin and breeding history. We identified 147 selective sweeps and defined the essential role of zeta-carotene desaturase in carotenoid accumulation during domestication. Our findings elucidated the impact of particle bombardment and improved our understanding of sex chromosomes and domestication to expedite papaya improvement.

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U2 - 10.1038/s41588-022-01068-1

DO - 10.1038/s41588-022-01068-1

M3 - Article

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AN - SCOPUS:85129831599

SN - 1061-4036

VL - 54

SP - 715

EP - 724

JO - Nature Genetics

JF - Nature Genetics

IS - 5

ER -

SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya

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