Biochemistry, Biophysics and Molecular Biology Publications Biochemistry, Biophysics and Molecular Biology 3-18-2020 The honeysuckle genome provides insight into the molecular mechanism of carotenoid metabolism underlying dynamic flower coloration Xiangdong Pu Chinese Academy of Medical Sciences & Peking Union Medical College Zhen Li Ghent University Ya Tian Chinese Academy of Medical Sciences & Peking Union Medical College Ranran Gao Chinese Academy of Medical Sciences & Peking Union Medical College Lijun Hao Chinese Academy of Medical Sciences & Peking Union Medical College See next page for additional authors Follow this and additional works at: https://lib.dr.iastate.edu/bbmb_ag_pubs Part of the Biochemistry, Biophysics, and Structural Biology Commons, Genetics and Genomics Commons, and the Plant Sciences Commons The complete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ bbmb_ag_pubs/262. For information on how to cite this item, please visit http://lib.dr.iastate.edu/howtocite.html. This Article is brought to you for free and open access by the Biochemistry, Biophysics and Molecular Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Biochemistry, Biophysics and Molecular Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. The honeysuckle genome provides insight into the molecular mechanism of carotenoid metabolism underlying dynamic flower coloration Abstract Lonicera japonica is a wide-spread member of the Caprifoliaceae (honeysuckle) family utilized in traditional medical practices. This twining vine honeysuckle is also a much-sought ornamental, in part due to its dynamic flower coloration, which changes from white to gold during development. The molecular mechanism underlying dynamic flower coloration in L. japonica was elucidated by integrating whole genome sequencing, transcriptomic analysis, and biochemical assays. Here, we report a chromosome-level genome assembly of L. japonica, comprising nine pseudochromosomes with a total size of 843.2 Mb. We also provide evidence for a whole genome duplication event in the lineage leading to L. japonica, which occurred after its divergence from Dipsacales and Asterales. Moreover, gene expression analysis not only revealed correlated expression of the relevant biosynthetic genes with carotenoid accumulation, but also suggested a role for carotenoid degradation in L. japonica’s dynamic flower coloration. The variation of flower color is consistent with not only the observed carotenoid accumulation pattern, but also with the release of volatile apocarotenoids that presumably serve as pollinator attractants. Beyond novel insights into the evolution and dynamics of flower coloration, the high-quality L. japonica genome sequence also provides a foundation for molecular breeding to improve desired characteristics. Keywords Caprifoliaceae (honeysuckle), Lonicera japonica, genome, flower coloration, carotenoids, carotenoid cleavage dioxygenase (CCD) Disciplines Biochemistry, Biophysics, and Structural Biology | Genetics and Genomics | Plant Sciences Comments This is the peer reviewed version of the following article: Pu, Xiangdong, Zhen Li, Ya Tian, Ranran Gao, Lijun Hao, Yating Hu, Chunnian He et al. "The honeysuckle genome provides insight into the molecular mechanism of carotenoid metabolism underlying dynamic flower coloration." New Phytologist (2020), which has been published in final form at DOI: 10.1111/nph.16552. This article may be used for non- commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. Authors Xiangdong Pu, Zhen Li, Ya Tian, Ranran Gao, Lijun Hao, Yating Hu, Chunnian He, Wei Sun, Meimei Xu, Reuben J. Peters, Yves Van de Peer, Zhichao Xu, and Jingyuan Song This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/bbmb_ag_pubs/262 DR WEI SUN (Orcid ID : 0000-0001-5675-0466) PROF. REUBEN PETERS (Orcid ID : 0000-0003-4691-8477) PROF. JINGYUAN SONG (Orcid ID : 0000-0002-0892-035X) Article type : - Regular Manuscript The honeysuckle genome provides insight into the molecular mechanism of carotenoid metabolism underlying dynamic flower coloration Xiangdong Pua, Zhen Lib,c, Ya Tiana, Ranran Gaoa, Lijun Haoa, Yating Hua, Chunnian Hea,d, Wei Sune, Meimei Xuf, Reuben J. Petersf, Yves Van de Peerb,c,g,h, Zhichao Xua,d*, Jingyuan Songa,d,i* a Key Lab of Chinese Medicine Resources Conservation, State Administration of Traditional Chinese Medicine of the People’s Republic of China, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing 100193, China b Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium c Center for Plant Systems Biology, VIB, 9052, Ghent, Belgium d Engineering Research Center of Chinese Medicine Resource, Ministry of Education, Beijing 100193, China e Key Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, China Academy of Chinese Medical Sciences, Institute of Chinese Materia Medica, Beijing 100700, China f Roy J. Carver Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA, 50011-1079, USA g Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria 0028, South Africa h College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China i Yunnan Branch, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences, Peking Union Medical College, Jinghong 666100, China This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differencesAccepted Article between this version and the Version of Record. Please cite this article as doi: 10.1111/NPH.16552 This article is protected by copyright. All rights reserved *Corresponding Authors: Jingyuan Song: [email protected], 86-10-57833199; Zhichao Xu: [email protected], 86-10-57833199. Received: 30 January 2020 Accepted: 12 March 2020 ORCID: Xiangdong Pu: 0000-0002-0892-035X; Zhen Li: 0000-0001-8920-9270; Ranran Gao: 0000-0002-7164-0289; Chunnian He: 0000-0003-3659-7833; Wei Sun: 0000-0001-5675-0466; Reuben J. Peter: 0000-0003-4691-8477; Yves Van de Peer: 0000-0003-4327-3730; Zhichao Xu: 0000-0003-1753-5602; Jingyuan Song: 0000-0003- 2733-0416. Accepted Article This article is protected by copyright. All rights reserved Summary Lonicera japonica is a wide-spread member of the Caprifoliaceae (honeysuckle) family utilized in traditional medical practices. This twining vine honeysuckle is also a much-sought ornamental, in part due to its dynamic flower coloration, which changes from white to gold during development. The molecular mechanism underlying dynamic flower coloration in L. japonica was elucidated by integrating whole genome sequencing, transcriptomic analysis, and biochemical assays. Here, we report a chromosome-level genome assembly of L. japonica, comprising nine pseudo- chromosomes with a total size of 843.2 Mb. We also provide evidence for a whole genome duplication event in the lineage leading to L. japonica, which occurred after its divergence from Dipsacales and Asterales. Moreover, gene expression analysis not only revealed correlated expression of the relevant biosynthetic genes with carotenoid accumulation, but also suggested a role for carotenoid degradation in L. japonica’s dynamic flower coloration. The variation of flower color is consistent with not only the observed carotenoid accumulation pattern, but also with the release of volatile apocarotenoids that presumably serve as pollinator attractants. Beyond novel insights into the evolution and dynamics of flower coloration, the high-quality L. japonica genome sequence also provides a foundation for molecular breeding to improve desired characteristics. Key words: Caprifoliaceae (honeysuckle), Lonicera japonica, genome, flower coloration, carotenoids, carotenoid cleavage dioxygenase (CCD) Accepted Article This article is protected by copyright. All rights reserved Introduction Caprifoliaceae (the honeysuckle family) contains more than 800 species, including vines, shrubs, and small trees. A representative species of this family is Lonicera japonica, a perennial, evergreen, twining vine cultivated worldwide as an ornamental plant owing to its numerous, sweet-smelling, double-tongued flowers. L. japonica is known as golden-and-silver honeysuckle because its flowers change color, from white to gold, during their development (Figure 1A). Medicinal uses for this species are recorded in the pharmacopeia of China, Japan, and the United States (Schierenbeck, 2004; He et al., 2013). For thousands of years, L. japonica dried flower buds have been used in traditional Chinese medicine to treat fever and influenza, and the annual market for these dried flower buds is approximately 10 million kilograms, with sales of more than 2 billion yuan (CNY) in China (Shang et al., 2011). In addition, L. japonica is an important antiviral used to treat the SARS coronavirus (Wu et al., 2004; Liu et al., 2006; Shang et al., 2011; He et al., 2013), influenza A viruses (Zhou et al., 2015), the H1N1 flu virus (Ko et al., 2006), and Enterovirus 71 (Li et al., 2018a). It has further value as a component of healthy