The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

Ray Ming; Shaobin Hou; Yun Feng; Qingyi Yu; Alexandre Dionne-Laporte; Jimmy H. Saw; Pavel Senin; Wei Wang; Benjamin V. Ly; Kanako L.T. Lewis; Steven L. Salzberg; Lu Feng; Meghan R. Jones; Rachel L. Skelton; Jan E. Murray; Cuixia Chen; Wubin Qian; Junguo Shen; Peng Du; Moriah Eustice; Eric Tong; Haibao Tang; Eric Lyons; Robert E. Paull; Todd P. Michael; Kerr Wall; Danny W. Rice; Henrik Albert; Ming Li Wang; Yun J. Zhu; Michael Schatz; Niranjan Nagarajan; Ricelle A. Acob; Peizhu Guan; Andrea Blas; Ching Man Wai; Christine M. Ackerman; Yan Ren; Chao Liu; Jianmei Wang; Jianping Wang; Jong Kuk Na; Eugene V. Shakirov; Brian Haas; Jyothi Thimmapuram; David Nelson; Xiyin Wang; John E. Bowers; Andrea R. Gschwend; Arthur L. Delcher; Ratnesh Singh; Jon Y. Suzuki; Savarni Tripathi; Kabi Neupane; Hairong Wei; Beth Irikura; Maya Paidi; Ning Jiang; Wenli Zhang; Gernot Presting; Aaron Windsor; Rafael Navajas-Pérez; Manuel J. Torres; F. Alex Feltus; Brad Porter; Yingjun Li; A. Max Burroughs; Ming Cheng Luo; Lei Liu; David A. Christopher; Stephen M. Mount; Paul H. Moore; Tak Sugimura; Jiming Jiang; Mary A. Schuler; Vikki Friedman; Thomas Mitchell-Olds; Dorothy E. Shippen; Claude W. Depamphilis; Jeffrey D. Palmer; Michael Freeling; Andrew H. Paterson; Dennis Gonsalves; Lei Wang; Maqsudul Alam

doi:10.1038/nature06856

The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

Ray Ming, Shaobin Hou, Yun Feng, Qingyi Yu, Alexandre Dionne-Laporte, Jimmy H. Saw, Pavel Senin, Wei Wang, Benjamin V. Ly, Kanako L.T. Lewis, Steven L. Salzberg, Lu Feng, Meghan R. Jones, Rachel L. Skelton, Jan E. Murray, Cuixia Chen, Wubin Qian, Junguo Shen, Peng Du, Moriah EusticeEric Tong, Haibao Tang, Eric Lyons, Robert E. Paull, Todd P. Michael, Kerr Wall, Danny W. Rice, Henrik Albert, Ming Li Wang, Yun J. Zhu, Michael Schatz, Niranjan Nagarajan, Ricelle A. Acob, Peizhu Guan, Andrea Blas, Ching Man Wai, Christine M. Ackerman, Yan Ren, Chao Liu, Jianmei Wang, Jianping Wang, Jong Kuk Na, Eugene V. Shakirov, Brian Haas, Jyothi Thimmapuram, David Nelson, Xiyin Wang, John E. Bowers, Andrea R. Gschwend, Arthur L. Delcher, Ratnesh Singh, Jon Y. Suzuki, Savarni Tripathi, Kabi Neupane, Hairong Wei, Beth Irikura, Maya Paidi, Ning Jiang, Wenli Zhang, Gernot Presting, Aaron Windsor, Rafael Navajas-Pérez, Manuel J. Torres, F. Alex Feltus, Brad Porter, Yingjun Li, A. Max Burroughs, Ming Cheng Luo, Lei Liu, David A. Christopher, Stephen M. Mount, Paul H. Moore, Tak Sugimura, Jiming Jiang, Mary A. Schuler, Vikki Friedman, Thomas Mitchell-Olds, Dorothy E. Shippen, Claude W. Depamphilis, Jeffrey D. Palmer, Michael Freeling, Andrew H. Paterson, Dennis Gonsalves, Lei Wang^*, Maqsudul Alam

^*Corresponding author for this work

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

871 Scopus citations

Abstract

Papaya, a fruit crop cultivated in tropical and subtropical regions, is known for its nutritional benefits and medicinal applications. Here we report a 3× draft genome sequence of 'SunUp' papaya, the first commercial virus-resistant transgenic fruit tree to be sequenced. The papaya genome is three times the size of the Arabidopsis genome, but contains fewer genes, including significantly fewer disease-resistance gene analogues. Comparison of the five sequenced genomes suggests a minimal angiosperm gene set of 13,311. A lack of recent genome duplication, atypical of other angiosperm genomes sequenced so far, may account for the smaller papaya gene number in most functional groups. Nonetheless, striking amplifications in gene number within particular functional groups suggest roles in the evolution of tree-like habit, deposition and remobilization of starch reserves, attraction of seed dispersal agents, and adaptation to tropical daylengths. Transgenesis at three locations is closely associated with chloroplast insertions into the nuclear genome, and with topoisomerase I recognition sites. Papaya offers numerous advantages as a system for fruit-tree functional genomics, and this draft genome sequence provides the foundation for revealing the basis of Carica's distinguishing morpho-physiological, medicinal and nutritional properties.

Original language	English (US)
Pages (from-to)	991-996
Number of pages	6
Journal	Nature
Volume	452
Issue number	7190
DOIs	https://doi.org/10.1038/nature06856
State	Published - Apr 24 2008
Externally published	Yes

Funding

Acknowledgements We thank X. Wan, J. Saito and A. Young at the University of Hawaii for technical assistance; C. Detter at the DOE Joint Genome Institute; F. MacKenzie, O. Veatch and T. Uhm at the Hawaii Agriculture Research Center; L. Li, W. Teng, Y. Wu, Y. Yang, C. Zhou, N. Wang, P. Wang and D. Fei at the Tianjin Biochip Corporation, Tianjin Economic-Technological Development Area, Tianjin; and R. Herdes, L. Diebold, R. Kim, A. Hernandez, S. Ali and L. Bynum at the University of Illinois at Urbana-Champaign. This papaya genome-sequencing project was given support by the University of Hawaii and the US Department of Defense grant number W81XWH0520013 to M.A., the Maui High Performance Computing Center to M.A., the Hawaii Agriculture Research Center to R.M. and Q.Y., and Nankai University, China, to L.W. Other support to the papaya genome project included the United States Department of Agriculture T-STAR program; a United States Department of Agriculture\u2013Agricultural Research Service cooperative agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center; the University of Illinois; the National Science Foundation Plant Genome Research Program; and Tianjin Municipal Special Fund for Science and Technology Innovation Grant 05FZZDSH00800. We thank P. Englert, former chancellor of the University of Hawaii, for initial infrastructure support of the research.

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10.1038/nature06856

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Ming, R., Hou, S., Feng, Y., Yu, Q., Dionne-Laporte, A., Saw, J. H., Senin, P., Wang, W., Ly, B. V., Lewis, K. L. T., Salzberg, S. L., Feng, L., Jones, M. R., Skelton, R. L., Murray, J. E., Chen, C., Qian, W., Shen, J., Du, P., ... Alam, M. (2008). The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature, 452(7190), 991-996. https://doi.org/10.1038/nature06856

@article{22892d87bb6d4186912fbebf3b7c479e,

title = "The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)",

abstract = "Papaya, a fruit crop cultivated in tropical and subtropical regions, is known for its nutritional benefits and medicinal applications. Here we report a 3× draft genome sequence of 'SunUp' papaya, the first commercial virus-resistant transgenic fruit tree to be sequenced. The papaya genome is three times the size of the Arabidopsis genome, but contains fewer genes, including significantly fewer disease-resistance gene analogues. Comparison of the five sequenced genomes suggests a minimal angiosperm gene set of 13,311. A lack of recent genome duplication, atypical of other angiosperm genomes sequenced so far, may account for the smaller papaya gene number in most functional groups. Nonetheless, striking amplifications in gene number within particular functional groups suggest roles in the evolution of tree-like habit, deposition and remobilization of starch reserves, attraction of seed dispersal agents, and adaptation to tropical daylengths. Transgenesis at three locations is closely associated with chloroplast insertions into the nuclear genome, and with topoisomerase I recognition sites. Papaya offers numerous advantages as a system for fruit-tree functional genomics, and this draft genome sequence provides the foundation for revealing the basis of Carica's distinguishing morpho-physiological, medicinal and nutritional properties.",

author = "Ray Ming and Shaobin Hou and Yun Feng and Qingyi Yu and Alexandre Dionne-Laporte and Saw, {Jimmy H.} and Pavel Senin and Wei Wang and Ly, {Benjamin V.} and Lewis, {Kanako L.T.} and Salzberg, {Steven L.} and Lu Feng and Jones, {Meghan R.} and Skelton, {Rachel L.} and Murray, {Jan E.} and Cuixia Chen and Wubin Qian and Junguo Shen and Peng Du and Moriah Eustice and Eric Tong and Haibao Tang and Eric Lyons and Paull, {Robert E.} and Michael, {Todd P.} and Kerr Wall and Rice, {Danny W.} and Henrik Albert and Wang, {Ming Li} and Zhu, {Yun J.} and Michael Schatz and Niranjan Nagarajan and Acob, {Ricelle A.} and Peizhu Guan and Andrea Blas and Wai, {Ching Man} and Ackerman, {Christine M.} and Yan Ren and Chao Liu and Jianmei Wang and Jianping Wang and Na, {Jong Kuk} and Shakirov, {Eugene V.} and Brian Haas and Jyothi Thimmapuram and David Nelson and Xiyin Wang and Bowers, {John E.} and Gschwend, {Andrea R.} and Delcher, {Arthur L.} and Ratnesh Singh and Suzuki, {Jon Y.} and Savarni Tripathi and Kabi Neupane and Hairong Wei and Beth Irikura and Maya Paidi and Ning Jiang and Wenli Zhang and Gernot Presting and Aaron Windsor and Rafael Navajas-P{\'e}rez and Torres, {Manuel J.} and Feltus, {F. Alex} and Brad Porter and Yingjun Li and Burroughs, {A. Max} and Luo, {Ming Cheng} and Lei Liu and Christopher, {David A.} and Mount, {Stephen M.} and Moore, {Paul H.} and Tak Sugimura and Jiming Jiang and Schuler, {Mary A.} and Vikki Friedman and Thomas Mitchell-Olds and Shippen, {Dorothy E.} and Depamphilis, {Claude W.} and Palmer, {Jeffrey D.} and Michael Freeling and Paterson, {Andrew H.} and Dennis Gonsalves and Lei Wang and Maqsudul Alam",

note = "Funding Information: Acknowledgements We thank X. Wan, J. Saito and A. Young at the University of Hawaii for technical assistance; C. Detter at the DOE Joint Genome Institute; F. MacKenzie, O. Veatch and T. Uhm at the Hawaii Agriculture Research Center; L. Li, W. Teng, Y. Wu, Y. Yang, C. Zhou, N. Wang, P. Wang and D. Fei at the Tianjin Biochip Corporation, Tianjin Economic-Technological Development Area, Tianjin; and R. Herdes, L. Diebold, R. Kim, A. Hernandez, S. Ali and L. Bynum at the University of Illinois at Urbana-Champaign. This papaya genome-sequencing project was given support by the University of Hawaii and the US Department of Defense grant number W81XWH0520013 to M.A., the Maui High Performance Computing Center to M.A., the Hawaii Agriculture Research Center to R.M. and Q.Y., and Nankai University, China, to L.W. Other support to the papaya genome project included the United States Department of Agriculture T-STAR program; a United States Department of Agriculture–Agricultural Research Service cooperative agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center; the University of Illinois; the National Science Foundation Plant Genome Research Program; and Tianjin Municipal Special Fund for Science and Technology Innovation Grant 05FZZDSH00800. We thank P. Englert, former chancellor of the University of Hawaii, for initial infrastructure support of the research.",

year = "2008",

month = apr,

day = "24",

doi = "10.1038/nature06856",

language = "English (US)",

volume = "452",

pages = "991--996",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7190",

}

Ming, R, Hou, S, Feng, Y, Yu, Q, Dionne-Laporte, A, Saw, JH, Senin, P, Wang, W, Ly, BV, Lewis, KLT, Salzberg, SL, Feng, L, Jones, MR, Skelton, RL, Murray, JE, Chen, C, Qian, W, Shen, J, Du, P, Eustice, M, Tong, E, Tang, H, Lyons, E, Paull, RE, Michael, TP, Wall, K, Rice, DW, Albert, H, Wang, ML, Zhu, YJ, Schatz, M, Nagarajan, N, Acob, RA, Guan, P, Blas, A, Wai, CM, Ackerman, CM, Ren, Y, Liu, C, Wang, J, Wang, J, Na, JK, Shakirov, EV, Haas, B, Thimmapuram, J, Nelson, D, Wang, X, Bowers, JE, Gschwend, AR, Delcher, AL, Singh, R, Suzuki, JY, Tripathi, S, Neupane, K, Wei, H, Irikura, B, Paidi, M, Jiang, N, Zhang, W, Presting, G, Windsor, A, Navajas-Pérez, R, Torres, MJ, Feltus, FA, Porter, B, Li, Y, Burroughs, AM, Luo, MC, Liu, L, Christopher, DA, Mount, SM, Moore, PH, Sugimura, T, Jiang, J, Schuler, MA, Friedman, V, Mitchell-Olds, T, Shippen, DE, Depamphilis, CW, Palmer, JD, Freeling, M, Paterson, AH, Gonsalves, D, Wang, L & Alam, M 2008, 'The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)', Nature, vol. 452, no. 7190, pp. 991-996. https://doi.org/10.1038/nature06856

TY - JOUR

T1 - The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

AU - Ming, Ray

AU - Hou, Shaobin

AU - Feng, Yun

AU - Yu, Qingyi

AU - Dionne-Laporte, Alexandre

AU - Saw, Jimmy H.

AU - Senin, Pavel

AU - Wang, Wei

AU - Ly, Benjamin V.

AU - Lewis, Kanako L.T.

AU - Salzberg, Steven L.

AU - Feng, Lu

AU - Jones, Meghan R.

AU - Skelton, Rachel L.

AU - Murray, Jan E.

AU - Chen, Cuixia

AU - Qian, Wubin

AU - Shen, Junguo

AU - Du, Peng

AU - Eustice, Moriah

AU - Tong, Eric

AU - Tang, Haibao

AU - Lyons, Eric

AU - Paull, Robert E.

AU - Michael, Todd P.

AU - Wall, Kerr

AU - Rice, Danny W.

AU - Albert, Henrik

AU - Wang, Ming Li

AU - Zhu, Yun J.

AU - Schatz, Michael

AU - Nagarajan, Niranjan

AU - Acob, Ricelle A.

AU - Guan, Peizhu

AU - Blas, Andrea

AU - Wai, Ching Man

AU - Ackerman, Christine M.

AU - Ren, Yan

AU - Liu, Chao

AU - Wang, Jianmei

AU - Wang, Jianping

AU - Na, Jong Kuk

AU - Shakirov, Eugene V.

AU - Haas, Brian

AU - Thimmapuram, Jyothi

AU - Nelson, David

AU - Wang, Xiyin

AU - Bowers, John E.

AU - Gschwend, Andrea R.

AU - Delcher, Arthur L.

AU - Singh, Ratnesh

AU - Suzuki, Jon Y.

AU - Tripathi, Savarni

AU - Neupane, Kabi

AU - Wei, Hairong

AU - Irikura, Beth

AU - Paidi, Maya

AU - Jiang, Ning

AU - Zhang, Wenli

AU - Presting, Gernot

AU - Windsor, Aaron

AU - Navajas-Pérez, Rafael

AU - Torres, Manuel J.

AU - Feltus, F. Alex

AU - Porter, Brad

AU - Li, Yingjun

AU - Burroughs, A. Max

AU - Luo, Ming Cheng

AU - Liu, Lei

AU - Christopher, David A.

AU - Mount, Stephen M.

AU - Moore, Paul H.

AU - Sugimura, Tak

AU - Jiang, Jiming

AU - Schuler, Mary A.

AU - Friedman, Vikki

AU - Mitchell-Olds, Thomas

AU - Shippen, Dorothy E.

AU - Depamphilis, Claude W.

AU - Palmer, Jeffrey D.

AU - Freeling, Michael

AU - Paterson, Andrew H.

AU - Gonsalves, Dennis

AU - Wang, Lei

AU - Alam, Maqsudul

N1 - Funding Information: Acknowledgements We thank X. Wan, J. Saito and A. Young at the University of Hawaii for technical assistance; C. Detter at the DOE Joint Genome Institute; F. MacKenzie, O. Veatch and T. Uhm at the Hawaii Agriculture Research Center; L. Li, W. Teng, Y. Wu, Y. Yang, C. Zhou, N. Wang, P. Wang and D. Fei at the Tianjin Biochip Corporation, Tianjin Economic-Technological Development Area, Tianjin; and R. Herdes, L. Diebold, R. Kim, A. Hernandez, S. Ali and L. Bynum at the University of Illinois at Urbana-Champaign. This papaya genome-sequencing project was given support by the University of Hawaii and the US Department of Defense grant number W81XWH0520013 to M.A., the Maui High Performance Computing Center to M.A., the Hawaii Agriculture Research Center to R.M. and Q.Y., and Nankai University, China, to L.W. Other support to the papaya genome project included the United States Department of Agriculture T-STAR program; a United States Department of Agriculture–Agricultural Research Service cooperative agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center; the University of Illinois; the National Science Foundation Plant Genome Research Program; and Tianjin Municipal Special Fund for Science and Technology Innovation Grant 05FZZDSH00800. We thank P. Englert, former chancellor of the University of Hawaii, for initial infrastructure support of the research.

PY - 2008/4/24

Y1 - 2008/4/24

N2 - Papaya, a fruit crop cultivated in tropical and subtropical regions, is known for its nutritional benefits and medicinal applications. Here we report a 3× draft genome sequence of 'SunUp' papaya, the first commercial virus-resistant transgenic fruit tree to be sequenced. The papaya genome is three times the size of the Arabidopsis genome, but contains fewer genes, including significantly fewer disease-resistance gene analogues. Comparison of the five sequenced genomes suggests a minimal angiosperm gene set of 13,311. A lack of recent genome duplication, atypical of other angiosperm genomes sequenced so far, may account for the smaller papaya gene number in most functional groups. Nonetheless, striking amplifications in gene number within particular functional groups suggest roles in the evolution of tree-like habit, deposition and remobilization of starch reserves, attraction of seed dispersal agents, and adaptation to tropical daylengths. Transgenesis at three locations is closely associated with chloroplast insertions into the nuclear genome, and with topoisomerase I recognition sites. Papaya offers numerous advantages as a system for fruit-tree functional genomics, and this draft genome sequence provides the foundation for revealing the basis of Carica's distinguishing morpho-physiological, medicinal and nutritional properties.

AB - Papaya, a fruit crop cultivated in tropical and subtropical regions, is known for its nutritional benefits and medicinal applications. Here we report a 3× draft genome sequence of 'SunUp' papaya, the first commercial virus-resistant transgenic fruit tree to be sequenced. The papaya genome is three times the size of the Arabidopsis genome, but contains fewer genes, including significantly fewer disease-resistance gene analogues. Comparison of the five sequenced genomes suggests a minimal angiosperm gene set of 13,311. A lack of recent genome duplication, atypical of other angiosperm genomes sequenced so far, may account for the smaller papaya gene number in most functional groups. Nonetheless, striking amplifications in gene number within particular functional groups suggest roles in the evolution of tree-like habit, deposition and remobilization of starch reserves, attraction of seed dispersal agents, and adaptation to tropical daylengths. Transgenesis at three locations is closely associated with chloroplast insertions into the nuclear genome, and with topoisomerase I recognition sites. Papaya offers numerous advantages as a system for fruit-tree functional genomics, and this draft genome sequence provides the foundation for revealing the basis of Carica's distinguishing morpho-physiological, medicinal and nutritional properties.

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UR - http://www.scopus.com/inward/citedby.url?scp=42949157236&partnerID=8YFLogxK

U2 - 10.1038/nature06856

DO - 10.1038/nature06856

M3 - Article

C2 - 18432245

AN - SCOPUS:42949157236

SN - 0028-0836

VL - 452

SP - 991

EP - 996

JO - Nature

JF - Nature

IS - 7190

ER -

The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

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