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The Apostasia Genome and the Evolution of Orchids

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The Apostasia Genome and the Evolution of Orchids There are amendments to this paper OPEN LETTER doi:10.1038/nature23897 The Apostasia genome and the evolution of orchids Guo-Qiang Zhang1*, Ke-Wei Liu1*, Zhen Li2,3*, Rolf Lohaus2,3*, Yu-Yun Hsiao4,5*, Shan-Ce Niu1,6, Jie-Yu Wang1,7, Yao-Cheng Lin2,3†, Qing Xu1, Li-Jun Chen1, Kouki Yoshida8, Sumire Fujiwara9, Zhi-Wen Wang10, Yong-Qiang Zhang1, Nobutaka Mitsuda9, Meina Wang1, Guo-Hui Liu1, Lorenzo Pecoraro1, Hui-Xia Huang1, Xin-Ju Xiao1, Min Lin1, Xin-Yi Wu1, Wan-Lin Wu1,4, You-Yi Chen4,5, Song-Bin Chang4,5, Shingo Sakamoto9, Masaru Ohme-Takagi9,11, Masafumi Yagi12, Si-Jin Zeng1,7, Ching-Yu Shen13, Chuan-Ming Yeh11, Yi-Bo Luo6, Wen-Chieh Tsai4,5,13, Yves Van de Peer2,3,14 & Zhong-Jian Liu1,7,15,16 Constituting approximately 10% of flowering plant species, orchids those of other Orchidaceae subfamilies, which have three sepals, three (Orchidaceae) display unique flower morphologies, possess an ­petals (of which one has specialized to form the labellum), and stamens extraordinary diversity in lifestyle, and have successfully colonized and pistil fused into a more complex gynostemium (Extended Data almost every habitat on Earth1–3. Here we report the draft genome Fig. 1b), but are similar to those of some species of Hypoxidaceae sequence of Apostasia shenzhenica4, a representative of one of two (a sister family to Orchidaceae, in the order Asparagales). genera that form a sister lineage to the rest of the Orchidaceae, We sequenced the A. shenzhenica genome using a ­combination providing a reference for inferring the genome content and of ­different approaches; the total length of the final assembly was structure of the most recent common ancestor of all extant orchids 349 Mb (see Methods and Supplementary Tables 1–4). We ­confidently and improving our understanding of their origins and evolution. annotated 21,841 protein-coding genes, of which 20,202 (92.50%) In addition, we present transcriptome data for representatives of were supported­ by transcriptome data (Supplementary Fig. 1 Vanilloideae, Cypripedioideae and Orchidoideae, and novel third- and Supplementary Table 5). Using single-copy orthologues, we generation genome data for two species of Epidendroideae, covering ­performed a BUSCO8 assessment that indicated that the completeness all five orchid subfamilies. A. shenzhenica shows clear evidence of of the genome was 93.62%, suggesting that the A. shenzhenica genome a whole-genome duplication, which is shared by all orchids and ­assembly is of high quality (Supplementary Table 6). For comparative occurred shortly before their divergence. Comparisons between analyses, we also improved the quality of the previously published­ A. shenzhenica and other orchids and angiosperms also permitted genome assemblies of the orchids Phalaenopsis equestris9 and the reconstruction of an ancestral orchid gene toolkit. We identify Dendrobium catenatum10 (see Methods and Supplementary Tables 6 new gene families, gene family expansions and contractions, and and 7). changes within MADS-box gene classes, which control a diverse We constructed a high-confidence phylogenetic tree and estimated suite of developmental processes, during orchid evolution. This the divergence times of 15 plant species using genes extracted from a study sheds new light on the genetic mechanisms underpinning total of 439 single-copy families (Fig. 1 and Extended Data Fig. 2). We key orchid innovations, including the development of the labellum undertook a computational analysis of gene family sizes (CAFÉ 2.211) and gynostemium, pollinia, and seeds without endosperm, as well to study gene family expansion and contraction during the evolution as the evolution of epiphytism; reveals relationships between the of orchids and related species (Fig. 1 and Supplementary Note 1.1). Orchidaceae subfamilies; and helps clarify the evolutionary history By comparing 12 plant species, we found 474 gene families (Extended of orchids within the angiosperms. Data Fig. 3) that appeared unique to orchids (Supplementary Note 1.2). The Apostasioideae are a small subfamily of orchids that includes Gene Ontology and Kyoto Encyclopedia of Genes and Genomes only two genera (Apostasia and Neuwiedia2,5), consisting of terres- (KEGG) enrichment analysis found these gene families to be specifi- trial species confined to the humid areas of southeast Asia, Japan, cally enriched in the terms ‘O-methyltransferase activity’, ‘cysteine-type and ­northern Australia6. Although Apostasioideae share some peptidase activity’, ‘flavone and flavonol biosynthesis’ and ‘stilbenoid, ­synapomorphies with other orchids (for example, small seeds with diarylheptanoid and gingerol biosynthesis’ (Supplementary Note 1.2). a reduced embryo and a myco-heterotrophic protocorm stage), they Distributions of synonymous substitutions per synonymous site possess ­several unique traits, the most conspicuous of which is their (KS) (see Supplementary Note 2.1) for paralogous A. shenzhenica genes 7 floral morphology . Apostasia has a non-resupinate, solanum-type showed a clear peak at KS ≈​ 1 (Extended Data Fig. 4). Similar peaks at flower with anthers closely encircling the stigma (including post- KS values of 0.7 to 1.1 were identified in 11 other orchids, covering all genital fusion), a long ovary, and an actinomorphic perianth with an 5 orchid subfamilies (Supplementary Fig. 2). These peaks might reflect undifferentiated labellum. Three stamens (two of which are fertile) multiple independent whole-genome duplication (WGD) events across are basally fused to the style, forming a relatively simple gynoste- orchid sublineages or, more parsimoniously, a single WGD event shared mium, and the anthers contain powdery pollen (grains not unified by all (extant) orchids. Comparisons of orchid paralogue KS distribu- into ­pollinia). These characteristics (Extended Data Fig. 1a) differ from tions with KS distributions of orthologues between orchid species, and 1Shenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Center of China and The Orchid Conservation and Research Center of Shenzhen, Shenzhen 518114, China. 2Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium. 3VIB Center for Plant Systems Biology, 9052 Gent, Belgium. 4Orchid Research and Development Center, National Cheng Kung University, Tainan 701, Taiwan. 5Department of Life Sciences, National Cheng Kung University, Tainan 701, Taiwan. 6State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. 7College of Forestry, South China Agricultural University, Guangzhou 510640, China. 8Technology Center, Taisei Corporation, Nase-cho 344-1, Totsuka-ku, Yokohama, Kanagawa 245-0051, Japan. 9Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Central 6, Higashi 1-1-1, Tsukuba, Ibaraki 305-8562, Japan. 10PubBio-Tech Services Corporation, Wuhan 430070, China. 11Graduate School of Science and Engineering, Saitama University, 255 Shimo-Okubo, Sakura-ku, Saitama 338-8570, Japan. 12NARO Institute of Floricultural Science (NIFS), 2-1 Fujimoto, Tsukuba, Ibaraki 305-8519, Japan. 13Institute of Tropical Plant Sciences, National Cheng Kung University, Tainan 701, Taiwan. 14Department of Genetics, Genomics Research Institute, Pretoria 0028, South Africa. 15College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou 350002, China. 16The Center for Biotechnology and BioMedicine, Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China. †Present address: Biotechnology Center in Southern Taiwan, Agricultural Biotechnology Research Center, Academia Sinica, 741 Tainan, Taiwan. *These authors contributed equally to this work. 21 SEPTEMBER 2017 | VOL 549 | NATURE | 379 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. RESEARCH LETTER +575/–1,591 Amborella trichopoda Supplementary Note 2.2). Co-linearity and synteny analyses between A. shenzhenica and Amborella trichopoda, and between A. shenzhenica +473/–4,118 Spirodela polyrhiza and Vitis vinifera, also support at least two WGDs in A. shenzhenica +557/–1,384 Phalaenopsis (Supplementary Figs 4 and 5); for example, four paralogous segments in equestris +207/–550 A. shenzhenica corresponded to one orthologous region in A. trichopoda +872/–703 +113/–1,047 Dendrobium (Fig. 2c). Detailed genome comparisons of A. shenzhenica with Ananas catenatum +4/–435 comosus (pineapple) and A. officinalis revealed a specific 4:4 co-linearity +522/–1,661 Apostasia shenzhenica pattern (Extended Data Fig. 6 and Supplementary Figs 6–8) that is MRCA +2/–473 (11,156) consistent with the two monocot WGDs proposed for A. comosus, indi- +1,204/–2,248 Asparagus officinalis cating that all three species possess a similar evolutionary history with +807/–650 Sorghum regard to WGDs (Supplementary Note 2.2). Together, these patterns bicolor of co-linearity suggest that the older of the two WGDs evident in +906/–689 +44/–123 +629/–652 Brachypodium A. shenzhenica is likely to be shared with A. comosus and A. officinalis distachyon (representing the τ WGD13,14 shared by most monocots), and +178/–578 +16/–131 +607/–858 Oryza sativa corroborate the idea that the younger WGD represents an independent +2/–6 event, specific to the Orchidaceae lineage. Analyses of gene trees that +1,145/–1,247 Ananas comosus contained at least one paralogue pair from co-linear regions from one +213/–206 +3,913/–1,013 Musa of the three
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