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The Genome of Magnolia Biondii Pamp. Provides Insights Into the Evolution of Magnoliales and Biosynthesis of Terpenoids

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The Genome of Magnolia Biondii Pamp. Provides Insights Into the Evolution of Magnoliales and Biosynthesis of Terpenoids The genome of Magnolia biondii Pamp. provides insights into the evolution of Magnoliales and biosynthesis of terpenoids Dong, Shanshan; Liu, Min; Liu, Yang; Chen, Fei; Yang, Ting; Chen, Lu; Zhang, Xingtan; Guo, Xing; Fang, Dongming; Li, Linzhou; Deng, Tian; Yao, Zhangxiu; Lang, Xiaoan; Gong, Yiqing; Wu, Ernest; Wang, Yaling; Shen, Yamei; Gong, Xun; Liu, Huan; Zhang, Shouzhou Published in: Horticulture Research DOI: 10.1038/s41438-021-00471-9 Publication date: 2021 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Dong, S., Liu, M., Liu, Y., Chen, F., Yang, T., Chen, L., Zhang, X., Guo, X., Fang, D., Li, L., Deng, T., Yao, Z., Lang, X., Gong, Y., Wu, E., Wang, Y., Shen, Y., Gong, X., Liu, H., & Zhang, S. (2021). The genome of Magnolia biondii Pamp. provides insights into the evolution of Magnoliales and biosynthesis of terpenoids. Horticulture Research, 8, [38]. https://doi.org/10.1038/s41438-021-00471-9 Download date: 29. sep.. 2021 Dong et al. Horticulture Research (2021) 8:38 Horticulture Research https://doi.org/10.1038/s41438-021-00471-9 www.nature.com/hortres ARTICLE Open Access ThegenomeofMagnolia biondii Pamp. provides insights into the evolution of Magnoliales and biosynthesis of terpenoids Shanshan Dong1,MinLiu2,YangLiu1,2, Fei Chen3,TingYang2,LuChen1,XingtanZhang4,XingGuo2, Dongming Fang2,LinzhouLi 2,TianDeng1,ZhangxiuYao1,XiaoanLang1, Yiqing Gong1,ErnestWu5, Yaling Wang6, Yamei Shen7, Xun Gong8,HuanLiu 2,9 and Shouzhou Zhang 1 Abstract Magnolia biondii Pamp. (Magnoliaceae, magnoliids) is a phylogenetically, economically, and medicinally important ornamental tree species widely grown and cultivated in the north-temperate regions of China. Determining the genome sequence of M. biondii would help resolve the phylogenetic uncertainty of magnoliids and improve the understanding of individual trait evolution within the Magnolia genus. We assembled a chromosome-level reference genome of M. biondii using ~67, ~175, and ~154 Gb of raw DNA sequences generated via Pacific Biosciences single- molecule real-time sequencing, 10X Genomics Chromium, and Hi-C scaffolding strategies, respectively. The final genome assembly was ~2.22 Gb, with a contig N50 value of 269.11 kb and a BUSCO complete gene percentage of 91.90%. Approximately 89.17% of the genome was organized into 19 chromosomes, resulting in a scaffold N50 of 92.86 Mb. The genome contained 47,547 protein-coding genes, accounting for 23.47% of the genome length, whereas 66.48% of the genome length consisted of repetitive elements. We confirmed a WGD event that occurred very close to 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; the time of the split between the Magnoliales and Laurales. Functional enrichment of the Magnolia-specific and expanded gene families highlighted genes involved in the biosynthesis of secondary metabolites, plant–pathogen interactions, and responses to stimuli, which may improve the ecological fitness and biological adaptability of the lineage. Phylogenomic analyses revealed a sister relationship of magnoliids and Chloranthaceae, which are sister to a clade comprising monocots and eudicots. The genome sequence of M. biondii could lead to trait improvement, germplasm conservation, and evolutionary studies on the rapid radiation of early angiosperms. Introduction temperate and tropical regions of Southeast Asia, and the The family Magnoliaceae Juss., with more than others are distributed in the Americas, from temperate 300 species1 worldwide, comprises two genera, Lirioden- southeast North America through Central America to dron L., which includes only two species, and Magnolia L., Brazil3, forming disjunct distribution patterns4. which includes the others2. Approximately 80% of all Magnolia is a member of the magnoliids, which con- extant Magnoliaceae species are distributed in the stitutes one of the earliest assemblages of flowering plants (angiosperms) and occupies a pivotal position in the phylogeny of angiosperms5. After the early divergence of Correspondence: Huan Liu ([email protected])or angiosperms (Amborellales, Austrobaileyales, and Nym- Shouzhou Zhang ([email protected]) 1Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical phaeales), the rapid radiation of five lineages of mesan- Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, China giosperms (magnoliids, Chloranthaceae, Ceratophyllum, 2 State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen monocots, and eudicots) occurred within a very short 518083, China 6 Full list of author information is available at the end of the article time frame of < 5MYA , leading to unresolved/ These authors contributed equally: Shanshan Dong, Min Liu © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Dong et al. Horticulture Research (2021) 8:38 Page 2 of 13 controversial phylogenetic relationships among some antimicrobial, analgesic, blood pressure-decreasing, and lineages of mesangiosperms5. To date, of the 323 genome anti-allergic effects25. Modern phytochemical studies have sequences available for angiosperm species7, mostly those characterized the chemical constituents of volatile oils26, of plants with agronomic value, genomes are available for lignin27, and alkaloids28 from different parts of M. biondii only five magnoliids: black pepper8, avocado9, soursop10, plants. Volatile oils contain a rich array of terpenoids, stout camphor tree11, and Liriodendron chinense12. Phy- among which the main ingredients include 1,8-cineole, logenomic analyses based on these genomic data have led β-pinene, α-terpineol, and camphor25. These terpenoids to controversial taxonomic placements of magnoliids. are synthesized by terpene synthase (TPS), which belongs Specifically, magnoliids are resolved as sister to eudicots, to the TPS gene family. In this study, we sequenced and with relatively strong support11, which is consistent with assembled the reference genome of M. biondii using the results of a phylotranscriptomic analysis of 92 strep- PacBio long read, 10X Genomics Chromium, and Hi-C tophytes13 and 20 representative angiosperms14. Alter- scaffolding strategies. The ~2.22 Gb genome sequence of natively, magnoliids are resolved as sister to eudicots and M. biondii represents the largest genome assembled to – monocots, with weak support8 10,12, which is in agree- date for early-diverging magnoliids. This genome will ment with the large-scale plastome phylogenomic analysis support future studies on floral evolution and the bio- – of land plants, Viridiplantae, and angiosperms15 17.As synthesis of the primary and secondary metabolites phylogenetic inferences rely heavily on the sampling of unique to the species and will be an essential resource for lineages and genes, as well as analytical methods5, these understanding rapid changes that took place throughout controversial taxonomic placements of magnoliids rela- the phylogenetic backbone of angiosperms. Finally, this tive to monocots and eudicots need to be further exam- information could be used to further improve genome- ined with more genomic data from magnoliids. assisted cultivation and conservation efforts of Magnolia. Magnolia species are usually cross-pollinated with precocious pistils, resulting in a very short pollination Materials and methods period. Many species of this genus have relatively low Plant materials, DNA extractions, and sequencing rates of pollen and seed germination18, as well as low Fresh leaves and flower materials were collected from a production of fruits and seeds, which leads to difficult 21-year-old M. biondii tree (a cultivated variety) at three – regeneration of natural populations in nature19 21. Exa- developmental stages planted in the Xi’an Botanical cerbated by native habitat loss due to logging and agri- Garden, Xi’an, China. The specimen (voucher number: culture, approximately 48% of all Magnolia species are Zhang 201801M) has been deposited in the Herbarium of threatened in the wild1. Conservation of the germplasm Fairy Lake Botanical Garden, Shenzhen, China. Total resources of Magnolia has many economic and ecological genomic DNA was extracted from fresh young leaves of values. Most of the Magnolia species are excellent orna- M. biondii using the modified cetyltrimethylammonium mental tree species22 due to their attractive flowers with bromide (CTAB) method29. The quality and quantity of sweet fragrances and erect tree shape with graceful foli- the DNA samples were evaluated using a NanoDrop™ age, as is the case for M. denudata, M. liliiflora, and M. One UV-Vis spectrophotometer (Thermo Fisher Scien- ® grandiflora. Magnolia species also contain a rich array of tific, USA) and a Qubit
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