Lineage-Specific CYP80 Expansion and Benzylisoquinoline Alkaloid Diversity in Early-Diverging Eudicots.
Menispermum
benzylisoquinoline alkaloids
biosynthetic pathway
chemo-diversity
stereospecificity
Journal
Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569
Informations de publication
Date de publication:
13 Mar 2024
13 Mar 2024
Historique:
revised:
07
02
2024
received:
19
12
2023
medline:
13
3
2024
pubmed:
13
3
2024
entrez:
13
3
2024
Statut:
aheadofprint
Résumé
Menispermaceae species, as early-diverging eudicots, can synthesize valuable benzylisoquinoline alkaloids (BIAs) like bisbenzylisoquinoline alkaloids (bisBIAs) and sinomenines with a wide range of structural diversity. However, the evolutionary mechanisms responsible for their chemo-diversity are not well understood. Here, a chromosome-level genome assembly of Menispermum dauricum is presented and demonstrated the occurrence of two whole genome duplication (WGD) events that are shared by Ranunculales and specific to Menispermum, providing a model for understanding chromosomal evolution in early-diverging eudicots. The biosynthetic pathway for diverse BIAs in M. dauricum is reconstructed by analyzing the transcriptome and metabolome. Additionally, five catalytic enzymes - one norcoclaurine synthase (NCS) and four cytochrome P450 monooxygenases (CYP450s) - from M. dauricum are responsible for the formation of the skeleton, hydroxylated modification, and C-O/C-C phenol coupling of BIAs. Notably, a novel leaf-specific MdCYP80G10 enzyme that catalyzes C2'-C4a phenol coupling of (S)-reticuline into sinoacutine, the enantiomer of morphinan compounds, with predictable stereospecificity is discovered. Moreover, it is found that Menispermum-specific CYP80 gene expansion, as well as tissue-specific expression, has driven BIA diversity in Menispermaceae as compared to other Ranunculales species. This study sheds light on WGD occurrences in early-diverging eudicots and the evolution of diverse BIA biosynthesis.
Identifiants
pubmed: 38477432
doi: 10.1002/advs.202309990
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2309990Subventions
Organisme : National Key R&D Program of China
ID : 2023YFC3504800
Organisme : National Natural Science Foundation of China
ID : 82274037
Organisme : National Natural Science Foundation of China
ID : 82360754
Organisme : National Natural Science Foundation of China
ID : U23A20511
Organisme : Fundamental Research Funds for the Central public welfare research institutes
ID : ZZ16-YQ-047
Organisme : Fundamental Research Funds for the Central Universities
ID : 2572022DX06
Organisme : Heilongjiang Touyan Innovation Team Program (Tree Genetics and Breeding Innovation Team)
Informations de copyright
© 2024 The Authors. Advanced Science published by Wiley-VCH GmbH.
Références
D. K. Liscombe, B. P. Macleod, N. Loukanina, O. I. Nandi, P. J. Facchini, Phytochemistry 2005, 66, 1374.
P. J. Wiffen, B. Wee, S. Derry, R. F. Bell, R. A. Moore, Cochrane Database Syst. Rev. 2017, 7, CD012592.
H. Fan, S. T. He, P. Han, B. Hong, K. Liu, M. Li, S. Wang, Y. Tong, Adv Biol (Weinh) 2022, 6, e2200148.
C. S.-M. Atsushi Hijikata, Setsu Nakae, Masafumi Shionyu, Motonori Ota, Shigehiko Kanaya, Takatsugu Hirokawa, Shogo Nakajima, Koichi Watashi, Tsuyoshi Shirai, FEBS Open Bio. 2021, 12, 285.
C. Zhang, S. Zhang, J. Liao, Z. Gong, X. Chai, H. Lyu, Molecules 2022, 27.
K. Wang, Z. Zhang, J. Hang, J. Liu, F. Guo, Y. Ding, M. Li, Q. Nie, J. Lin, Y. Zhuo, L. Sun, X. Luo, Q. Zhong, C. Ye, C. Yun, Y. Zhang, J. Wang, R. Bao, Y. Pang, G. Wang, F. J. Gonzalez, X. Lei, J. Qiao, C. Jiang, Science 2023, 381, eadd5787.
J. M. Hagel, P. J. Facchini, Plant Cell Physiol. 2013, 54, 647.
M. R. P. Mehran Dastmalchi, Jeremy S. Morris, Peter Facchini, Phytochem. Rev. 2018, 17, 249.
I. M. M.-P. Aparna Singh, Peter J. Facchini, Phytochem. Rev. 2019, 18, 1457.
L. Pei, B. Wang, J. Ye, X. Hu, L. Fu, K. Li, Z. Ni, Z. Wang, Y. Wei, L. Shi, Y. Zhang, X. Bai, M. Jiang, S. Wang, C. Ma, S. Li, K. Liu, W. Li, B. Cong, Horticulture Research 2021, 8.
X. Deng, L. Zhao, T. Fang, Y. Xiong, C. Ogutu, D. Yang, S. Vimolmangkang, Y. Liu, Y. Han, Hortic. Res. 2018, 5, 29.
Q. Chen, J. Zhang, W. Zhang, Z. Chen, J. Sep. Sci. 2013, 36, 341.
Z. H.-y. Wan Jun-mei, L. Quan-wen, Chinese Journal of Pharmaceutical Analysis 2005.
H. H. Pauli, T. M. Kutchan, Plant J. 1998, 13, 793.
V. K. Nguyen, K. G. M. Kou, Org. Biomol. Chem. 2021, 19, 7535.
A. Gesell, M. Rolf, J. Ziegler, M. L. Diaz Chavez, F. C. Huang, T. M. Kutchan, J. Biol. Chem. 2009, 284, 24432.
K. I. Nobuhiro Ikezawa, Fumihiko Sato, J. Biol. Chem. 2008, 283, 8810.
J. T. Payne, T. R. Valentic, C. D. Smolke, Proc Natl Acad Sci U S A 2021, 118.
R. Stadler, M. H. Zenk, J. Biol. Chem. 1993, 268, 823.
M. E. Pyne, N. D. Gold, V. J. J. Martin, Metab. Eng. 2023, 77, 162.
Q. Li, S. Ramasamy, P. Singh, J. M. Hagel, S. M. Dunemann, X. Chen, R. Chen, L. Yu, J. E. Tucker, P. J. Facchini, S. Yeaman, Nat. Commun. 2020, 11, 1190.
L. Guo, T. Winzer, X. Yang, Y. Li, Z. Ning, Z. He, R. Teodor, Y. Lu, T. A. Bowser, I. A. Graham, K. Ye, Science 2018, 362, 343.
X. Yang, S. Gao, L. Guo, B. Wang, Y. Jia, J. Zhou, Y. Che, P. Jia, J. Lin, T. Xu, J. Sun, K. Ye, Nat. Commun. 2021, 12, 6030.
D.-x. Chen, Y. Pan, Y. Wang, Y.-Z. Cui, Y.-J. Zhang, R.-y. Mo, X.-l. Wu, J. Tan, J. Zhang, L.-a. Guo, X. Zhao, W. Jiang, T.-l. Sun, X.-D. Hu, L.-y. Li, Horticulture Research 2021, 8.
Y. Liu, B. Wang, S. Shu, Z. Li, C. Song, D. Liu, Y. Niu, J. Liu, J. Zhang, H. Liu, Z. Hu, B. Huang, X. Liu, W. Liu, L. Jiang, M. M. Alami, Y. Zhou, Y. Ma, X. He, Y. Yang, T. Zhang, H. Hu, M. S. Barker, S. Chen, X. Wang, J. Nie, Nat. Commun. 2021, 12, 3276.
Z. Xu, Z. Li, F. Ren, R. Gao, Z. Wang, J. Zhang, T. Zhao, X. Ma, X. Pu, T. Xin, S. Rombauts, W. Sun, Y. Van de Peer, S. Chen, J. Song, Plant J. 2022, 111, 217.
X. Liu, Y. Liu, P. Huang, Y. Ma, Z. Qing, Q. Tang, H. Cao, P. Cheng, Y. Zheng, Z. Yuan, Y. Zhou, J. Liu, Z. Tang, Y. Zhuo, Y. Zhang, L. Yu, J. Huang, P. Yang, Q. Peng, J. Zhang, W. Jiang, Z. Zhang, K. Lin, D. K. Ro, X. Chen, X. Xiong, Y. Shang, S. Huang, J. Zeng, Mol. Plant 2017, 10, 975.
Z. Y. Wang, Y. Li, P. C. Sun, M. J. Zhu, D. D. Wang, Z. Q. Lu, H. Y. Hu, R. P. Xu, J. Zhang, J. X. Ma, J. Q. Liu, Y. Z. Yang, Bmc. Biology 2022, 20.
I. M. Menendez-Perdomo, P. J. Facchini, Molecules 2018, 23.
O. Bayazeid, F. N. Yalcin, Med. Chem. Res. 2021, 30, 574.
X. Xu, D. Wang, Front Plant Sci 2020, 11, 600354.
T. Arias, D. M. Riano-Pachon, V. S. Di Stilio, Appl Plant Sci 2021, 9, e11407.
D. L. Filiault, E. S. Ballerini, T. Mandakova, G. Akoz, N. J. Derieg, J. Schmutz, J. Jenkins, J. Grimwood, S. Shu, R. D. Hayes, U. Hellsten, K. Barry, J. Yan, S. Mihaltcheva, M. Karafiatova, V. Nizhynska, E. M. Kramer, M. A. Lysak, S. A. Hodges, M. Nordborg, Elife 2018, 7.
Y. Yao, J. Gu, Y. Luo, Y. Wang, Y. Pang, G. Shen, B. Guo, Synth. Syst. Biotechnol. 2022, 7, 1095.
Y. Sun, T. Deng, A. Zhang, M. J. Moore, J. B. Landis, N. Lin, H. Zhang, X. Zhang, J. Huang, X. Zhang, H. Sun, H. Wang, iScience 2020, 23, 101124.
S. Zhong, B. Li, W. Chen, L. Wang, J. Guan, Q. Wang, Z. Yang, H. Yang, X. Wang, X. Yu, P. Fu, H. Liu, C. Chen, F. Tan, T. Ren, J. Shen, P. Luo, Plant J. 2022, 112, 1316.
Y. Jiao, J. Leebens-Mack, S. Ayyampalayam, J. E. Bowers, M. R. McKain, J. McNeal, M. Rolf, D. R. Ruzicka, E. Wafula, N. J. Wickett, X. Wu, Y. Zhang, J. Wang, Y. Zhang, E. J. Carpenter, M. K. Deyholos, T. M. Kutchan, A. S. Chanderbali, P. S. Soltis, D. W. Stevenson, R. McCombie, J. C. Pires, G. K. Wong, D. E. Soltis, C. W. Depamphilis, Genome Biol. 2012, 13, R3.
G. Akoz, M. Nordborg, Genome Biol. 2019, 20, 256.
T. Shi, J. Chen, Genome Biol. 2020, 21, 295.
T. Shi, R. S. Rahmani, P. F. Gugger, M. Wang, H. Li, Y. Zhang, Z. Li, Q. Wang, Y. Van de Peer, K. Marchal, J. Chen, Mol. Biol. Evol. 2020, 37, 2394.
G. Aköz, M. Nordborg, Genome Biol. 2020, 21, 297.
S. C. Farrow, J. M. Hagel, G. A. Beaudoin, D. C. Burns, P. J. Facchini, Nat. Chem. Biol. 2015, 11, 728.
T. Winzer, M. Kern, A. J. King, T. R. Larson, R. I. Teodor, S. L. Donninger, Y. Li, A. A. Dowle, J. Cartwright, R. Bates, D. Ashford, J. Thomas, C. Walker, T. A. Bowser, I. A. Graham, Science 2015, 349, 309.
D. H. R. Barton, T. Cohen, in World Scientific Series in 20th Century Chemistry, WORLD SCIENTIFIC / IMPERIAL COLLEGE PRESS, Vol. 6, 1957.
B. R. Lichman, G. T. Godden, C. R. Buell, Curr. Opin. Plant Biol. 2020, 55, 74.
Y. Wang, F. Chen, Y. Ma, T. Zhang, P. Sun, M. Lan, F. Li, W. Fang, Hortic. Res. 2021, 8, 176.
F. Denoeud, L. Carretero-Paulet, A. Dereeper, G. Droc, R. Guyot, M. Pietrella, C. Zheng, A. Alberti, F. Anthony, G. Aprea, J. M. Aury, P. Bento, M. Bernard, S. Bocs, C. Campa, A. Cenci, M. C. Combes, D. Crouzillat, C. Da Silva, L. Daddiego, F. De Bellis, S. Dussert, O. Garsmeur, T. Gayraud, V. Guignon, K. Jahn, V. Jamilloux, T. Joet, K. Labadie, T. Lan, et al., Science 2014, 345, 1181.
Z. Xu, X. Pu, R. Gao, O. C. Demurtas, S. J. Fleck, M. Richter, C. He, A. Ji, W. Sun, J. Kong, K. Hu, F. Ren, J. Song, Z. Wang, T. Gao, C. Xiong, H. Yu, T. Xin, V. A. Albert, G. Giuliano, S. Chen, J. Song, BMC Biol. 2020, 18, 63.
W. Sun, Q. Yin, H. Wan, C. Xiong, C. Xie, X. Meng, C. Wang, R. Gao, W. Chen, Z. Xie, Z. Xue, H. Yao, P. Sun, X. Xie, Z. Hu, D. Nelson, Z. Xu, X. Sun, S. Chen, Preprint from Research Square 2022.
D. J. Kliebenstein, V. M. Lambrix, M. Reichelt, J. Gershenzon, T. Mitchell-Olds, The Plant Cell 2001, 13, 681.
A. M. Takos, C. Knudsen, D. Lai, R. Kannangara, L. Mikkelsen, M. S. Motawia, C. E. Olsen, S. Sato, S. Tabata, K. Jørgensen, B. L. Møller, F. Rook, The Plant Journal 2011, 68, 273.
Y. Wang, H. Zhang, H. C. Ri, Z. An, X. Wang, J. N. Zhou, D. Zheng, H. Wu, P. Wang, J. Yang, D. K. Liu, D. Zhang, W. C. Tsai, Z. Xue, Z. Xu, P. Zhang, Z. J. Liu, H. Shen, Y. Li, Nat. Commun. 2022, 13, 2224.
Z. Yang, X. Li, L. Yang, S. Peng, W. Song, Y. Lin, G. Xiang, Y. Li, S. Ye, C. Ma, J. Miao, G. Zhang, W. Chen, S. Yang, Y. Dong, Plant Commun 2023, 4, 100591.
T. Winzer, V. Gazda, Z. He, F. Kaminski, M. Kern, T. R. Larson, Y. Li, F. Meade, R. Teodor, F. E. Vaistij, C. Walker, T. A. Bowser, I. A. Graham, Science 2012, 336, 1704.
X. Y. Shilin Chen, Jianping Han, Wei Sun, Hui Yao, Jingyuan Song, Xiwen Li, Journal of Pharmaceutical Analysis 2023, 13, 431.
E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, J. Dekker, Science 2009, 326, 289.
H. Cheng, G. T. Concepcion, X. Feng, H. Zhang, H. Li, Nat. Methods 2021, 18, 170.
F. A. Simao, R. M. Waterhouse, P. Ioannidis, E. V. Kriventseva, E. M. Zdobnov, Bioinformatics 2015, 31, 3210.
X. Zhang, S. Zhang, Q. Zhao, R. Ming, H. Tang, Nat. Plants 2019, 5, 833.
M. Tarailo-Graovac, N. Chen, Curr. Protoc. Bioinformatics 2009, 4, 10.
M. G. Grabherr, B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, X. Adiconis, L. Fan, R. Raychowdhury, Q. Zeng, Z. Chen, E. Mauceli, N. Hacohen, A. Gnirke, N. Rhind, F. di Palma, B. W. Birren, C. Nusbaum, K. Lindblad-Toh, N. Friedman, A. Regev, Nat. Biotechnol. 2011, 29, 644.
B. L. Cantarel, I. Korf, S. M. Robb, G. Parra, E. Ross, B. Moore, C. Holt, A. Sanchez Alvarado, M. Yandell, Genome Res. 2008, 18, 188.
M. Stanke, O. Keller, I. Gunduz, A. Hayes, S. Waack, B. Morgenstern, Nucleic Acids Res. 2006, 34, W435.
D. Kim, B. Langmead, S. L. Salzberg, Nat. Methods 2015, 12, 357.
B. Zhang, S. Horvath, Stat. Appl. Genet. Mol. Biol. 2005, 4, 17.
D. M. Emms, S. Kelly, Genome Biol. 2019, 20, 238.
O. Jaillon, J. M. Aury, B. Noel, A. Policriti, C. Clepet, A. Casagrande, N. Choisne, S. Aubourg, N. Vitulo, C. Jubin, A. Vezzi, F. Legeai, P. Hugueney, C. Dasilva, D. Horner, E. Mica, D. Jublot, J. Poulain, C. Bruyere, A. Billault, B. Segurens, M. Gouyvenoux, E. Ugarte, F. Cattonaro, V. Anthouard, V. Vico, C. Del Fabbro, M. Alaux, G. Di Gaspero, V. Dumas, et al., Nature 2007, 449, 463.
R. Ming, R. VanBuren, Y. Liu, M. Yang, Y. Han, L. T. Li, Q. Zhang, M. J. Kim, M. C. Schatz, M. Campbell, J. Li, J. E. Bowers, H. Tang, E. Lyons, A. A. Ferguson, G. Narzisi, D. R. Nelson, C. E. Blaby-Haas, A. R. Gschwend, Y. Jiao, J. P. Der, F. Zeng, J. Han, X. J. Min, K. A. Hudson, R. Singh, A. K. Grennan, S. J. Karpowicz, J. R. Watling, K. Ito, et al., Genome Biol. 2013, 14, R41.
K. Hori, Y. Yamada, R. Purwanto, Y. Minakuchi, A. Toyoda, H. Hirakawa, F. Sato, Plant Cell Physiol. 2018, 59, 222.
P. Amborella Genome, Science 2013, 342, 1241089.
K. Katoh, D. M. Standley, Mol. Biol. Evol. 2013, 30, 772.
S. Capella-Gutierrez, J. M. Silla-Martinez, T. Gabaldon, Bioinformatics 2009, 25, 1972.
A. Stamatakis, Bioinformatics 2006, 22, 2688.
Z. Yang, Mol. Biol. Evol. 2007, 24, 1586.
F. K. Mendes, D. Vanderpool, B. Fulton, M. W. Hahn, Bioinformatics 2021, 36, 5516.
P. Sun, B. Jiao, Y. Yang, L. Shan, T. Li, X. Li, Z. Xi, X. Wang, J. Liu, Mol. Plant 2022, 15, 1841.
A. Zwaenepoel, Y. Van de Peer, Bioinformatics 2019, 35, 2153.
S. Proost, J. Fostier, D. De Witte, B. Dhoedt, P. Demeester, Y. Van de Peer, K. Vandepoele, Nucleic Acids Res. 2012, 40, e11.
C. Sensalari, S. Maere, R. Lohaus, Bioinformatics 2022, 38, 530.
C. Zhang, M. Rabiee, E. Sayyari, S. Mirarab, BMC Bioinformatics 2018, 19, 153.
H. Minami, E. Dubouzet, K. Iwasa, F. Sato, J. Biol. Chem. 2007, 282, 6274.
K. Katoh, K. Misawa, K. Kuma, T. Miyata, Nucleic Acids Res. 2002, 30, 3059.
B. Q. Minh, H. A. Schmidt, O. Chernomor, D. Schrempf, M. D. Woodhams, A. von Haeseler, R. Lanfear, Mol. Biol. Evol. 2020, 37, 1530.
C. C. Hansen, D. R. Nelson, B. L. Moller, D. Werck-Reichhart, Mol. Plant 2021, 14, 1244.
Z. Wang, Y. Li, P. Sun, M. Zhu, D. Wang, Z. Lu, H. Hu, R. Xu, J. Zhang, J. Ma, J. Liu, Y. Yang, BMC Biol. 2022, 20, 216.