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Chinaxiv:202107.00062V1 中图分类号：Q949 文献标识码：A ChinaXiv合作期刊 利用叶绿体基因组数据解析锦葵科梧桐亚科的系统位置和 属间关系 黎若竹 1,2，蔡杰 3，杨俊波 3，张志荣 3，李德铢 3，郁文彬 1,4,5* （1. 中国科学院西双版纳热带植物园 综合保护中心，云南 勐腊 666303；2. 中国科学院大 学，北京 100049; 3. 中国科学院昆明植物研究所 中国西南野生生物种质资源库，昆明 650201； 4. 中国科学院核心植物园保护生物学协同中心，云南 勐腊 666303；5. 中国科学 院东南亚生物多样性研究中心，云南 勐腊 666303） 摘 要：分子系统学研究将传统梧桐科与锦葵科、木棉科和椴树科合并为广义锦葵科，并进 一步分为 9 个亚科。然而，9 个亚科之间的关系尚未完全明确，且梧桐亚科内的属间关系也 未得到解决。为了明确梧桐亚科在锦葵科中的系统发育位置，厘清梧桐亚科内部属间系统发 育关系，该研究对锦葵科 8 个亚科进行取样，共选取 55 个样本，基于叶绿体基因组数据， 采用最大似然法和贝叶斯分析构建系统发育树。结果表明：（1）广义锦葵科中，刺果藤亚科 和扁担杆亚科组成 Byttneriina 分支，Malvadendrina 分支中山芝麻亚科为其他亚科的姐妹群， 随后分出梧桐亚科（WCG、LSC 和 SSC 矩阵构成的数据集），以及 Malvatheca 分支（木棉 亚科和锦葵亚科）与非洲芙蓉亚科-椴树亚科的姐妹关系；（2）在梧桐亚科中，可乐果属分 支（ Cola clade）是独立一支，随后是酒瓶树属分支（Brachychiton clade）与 苹 婆 属（ Sterculia clade）+ 银叶树属分支（Heritiera clade）形成姐妹关系（WCG、LSC 和 CDS 矩阵）；（3） 在可乐果属分支（Cola clade）中，可乐果属等为梧桐属（含闭果桐属）和胖大海属+舟翅桐 属的姐妹群。该研究基于叶绿基因组数据基本澄清了广义锦葵科的亚科系统关系以及梧桐亚 科内各属关系，系统发育树框架基本明晰，但梧桐亚科在 Malvadendrina 分支的位置和酒瓶 树属在梧桐亚科的位置，以 及 梧桐属的概念及范围仍需进一步研究，尤其是结合核基因组数 据进行分析。 关键词：梧桐亚科，梧桐属，锦葵科，系统发育基因组，叶绿体基因组 chinaXiv:202107.00062v1 中图分类号：Q949 文献标识码：A 收稿日期：2021-03-24 基金项目：中国科学院重大科技基础设施开放研究项目（2017-LSF-GBOWS-02）；云南省万人计划“青年 拔尖人才”[Supported by the Large-scale Scientific Facilities of the Chinese Academy of Sciences (No. 2017-LSF-GBOWS-02); Ten Thousand Talents Program of Yunnan for Top‐notch Young Talents.]。 作者简介：黎若竹（1996- ），硕士研究生，主要研究方向为保护生物学，（E-mail）[email protected]。 *通讯作者：郁文彬，博士，研究员，研究方向为植物系统演化，（E-mail）[email protected]。 1 ChinaXiv合作期刊 Plastid phylogenomics resolving phylogenetic placement and genera phylogeny of Sterculioideae (Malvaceae s. l.) LI Ruozhu1,2, CAI Jie3, YANG Junbo3, ZHANG Zhirong3, LI Dezhu3, YU Wenbin1,4,5* (1. Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China; 3. The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; 4. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Mengla 666303, Yunnan China; 5. Southeast Asia Biodiversity Research Institute, Chinese Academy of Science, Mengla 666303, Yunnan, China) Abstract: Phylogenetic analyses supported that four traditionally defined families Sterculiaceae, Tiliaceae, Bombacaece and Malvaceae were subsumed into Malvaceae s.l. and nine subfamilies have been recognized within Malvaceae s.l. However, phylogenetic relationships among the nine subfamilies were not well resolved. Moreover, phylogenetic relationships among genera were also not clear in Sterculioideae. In this study, we reconstructed phylogenetic trees of Malvaceae s.l. based on chloroplast genome sequences from 55 species that representing eight recognized subfamilies for clarifying phylogenetics relationships of subfamilies and Sterculioideae. The results were as follows: (1) Byttnerioideae and Grewioideae formed the Byttneriina clade in Malvaceae s.l. as sister to the Malvadendrina clade which by having Helicteroideae as the first divergent subfamily, followed by Sterculioideae (WCG, LSC and SSC datasets), and the Malvatheca clade (Bombacoideae + Malvoideae) and the clade Dombeyoideae + Tilioideae as sister. (2) The Cola clade was the first divergent clade in Sterculioideae, then the Brachychiton clade was sister to the clade Sterculia + Heritiera (WCG, LSC and CDS datasets); (3) In the Cola clade, Cola + Octolobus + Pterygota were the first divergent group, then Firmiana spp. (including Hildegardia) were sister to the clade Scaphium + Pterocymbium. In this study, plastid chinaXiv:202107.00062v1 phylogenomic analyses have well resolved the phylogenetic framework of subfamilies in Malvaceae s.l., and phylogenetic relationship among genera in Sterculioideae. However, phylogenetic positions of Sterculioideae in the Malvadendrina clade and Brachychiton in Sterculioideae, respectively, as well as the concept and circumscription of Firmiana, need to confirm and further investigate using nuclear genomic data in the future. Keywords: Sterculioideae, Firmiana, Malvaceae, phylogenomics, chloroplast 传统的梧 桐 科（ Sterculiaceae）由 Ventenat 于 1830 年建立，模式属是苹 婆 属（ Steculia L.）。 梧桐科隶属于锦葵目（Malvales），是一个多型的科，拥有多样的花部特征和果实类型（徐 颂军和徐祥浩, 2012）。由于缺乏关键的识别特征，不同学者在梧桐科的范围和划分上持有不 同观点，所包含属种变动很大（Cronquist & Takhtajan, 1992; Takhtajan, 2009; 徐颂军和徐祥 浩, 2012）。形态上，梧桐科与同属锦葵目的椴树科（Tiliaceae）、锦葵科（Malvaceae）及木 棉科（Bombacaceae）关系近缘，被认为是核心锦葵目（core Malvales）成员。从形态学来 2 ChinaXiv合作期刊 看，这 4 个科的形态特征十分相似，甚至有所重合，因而这几个科的界限也不甚明确（徐颂 军和徐祥浩, 2000）。 分子系统学研究结果表明，锦葵目核心四科中唯有锦葵科是单系，其他 3 个科为多系或 并系类群（Alverson et al., 1999; Bayer et al., 1999）。由于主要支系之间的形态分化水平不足 以支持科级分类，所以 Bayer et al.（1999）和 Alverson et al.（1999）建议将 4 个科合并为 1 个大科，采用 Malvaceae 作为科名，并综合考虑形态特征、生物地理学信息及系统发育结果， 将锦葵科内部主要的 9 个分支处理为亚科等级。锦葵科的 9 个亚科分别为木棉亚科 （Bombacoideae）、杯萼椴亚科（Brownlowioideae）、刺果藤亚科（Byttnerioideae）、非洲芙 蓉亚科（Dombeyoideae）、扁担杆亚科（Grewioideae）、山芝麻亚科（Helicteroideae）、锦葵 亚科（Malvoideae）、 梧桐亚科（Sterculioideae）以及椴树亚科（Tilioideae）。刺果藤亚科和 扁担杆亚科互为姐妹关系，组成 Byttneriina 分支，与余下 7 个亚科组成的 Malvadendrina 分 支互为姐妹关系（Baum et al., 1998; Alverson et al., 1999）。在 Malvadendrina 分支内部，锦葵 亚科与木棉亚科聚为一支，并得到良好地支持（BS=82%），这一分支被命名为 Malvatheca （Baum et al., 1998）。9 个亚科的单系性及 Byttneriina 和 Malvadendrina 两大分支在后续的研 究中都得到了支持（Nyffeler et al., 2005; Hernandez-Gutierrez & Magallon, 2019; Wang et al., 2021）。在 Malvadendrina 分支内部，最先得到确定的是锦葵亚科和木棉亚科的姐妹关系 （Alverson et al., 1999; Baum et al., 2004），其他亚科的系统位置则因取样的多少及使用的基 因片段不同而发生变动（Nyffeler et al., 2005; Conover et al., 2019; Hernandez-Gutierrez & Magallon, 2019）。叶绿体基因组较基因片段包含更为丰富的遗传变异信息，如今测序技术日 臻完善，测序成本随之降低，叶绿体基因组也被用于解决锦葵科系统发育关系（Wang et al., 2021）。通过对锦葵目的 39 个叶绿体基因组（包括锦葵科 8 个亚科，缺少杯萼椴亚科）划分 的不同数据集进行系统发育分析，Wang et al.（2021）确定了山芝麻亚科处在 Malvadendrina 分支基部，为其他亚科的姐妹群，椴树亚科和非洲芙蓉亚科为姐妹关系。然而，梧桐亚科与 Malvatheca 分支，及椴树亚科-非洲芙蓉亚科分支之间的关系尚未得到解决。 基于现有分子系统学证据，传统梧桐科的属主要分散在刺果藤亚科、非洲芙蓉亚科、山 芝麻亚科中，另有一属（Fremontodendron Coville）被归入木棉亚科，只有原苹婆族（Sterculieae） 及蝴蝶树族（Tarritieae）的部分属为梧桐亚科的主要成员（Bayer & Kubitzki, 2003）。新界定 的梧桐亚科包含 12～13 属，主要取决于是将 Argyrodendron F. Muell.并入银叶树属（Heritiera Aiton）还是作为一个独立的属（Bayer & Kubitzki, 2003; Wilkie et al., 2006）。梧桐亚科的单 系性得到了分子系统学和形态学证据的共同支持。在形态结构上，梧桐亚科各属以无花瓣的 chinaXiv:202107.00062v1 花，花瓣状的萼片，心皮离生，具雌雄蕊柄等共有特征和其他亚科区分开来（Bayer et al., 1999; Bayer & Kubitzki, 2003）。包含梧桐亚科各属的 ndhF 基因所构建的系统发育树表明，梧桐亚 科内部分为四个分支，即 可乐果属分支（Cola clade），酒瓶树属分支（Brachychiton clade）， 苹婆属分支（Sterculia clade）及银叶树属分支（Heritiera clade）（Wilkie et al., 2006）。然而 这四个分支之间的关系尚未得到解决，且分支内部属间关系尚不明确，有待进一步探究。 本研究通过对锦葵科各亚科尤其是梧桐亚科进行取样，尽可能多地获取浅层测序数据及 叶绿体基因组数据，利用叶绿体基因组数据重建锦葵科及梧桐亚科系统发育关系，试 图 明确 梧桐亚科在锦葵科中的系统发育位置，并厘清梧桐亚科内部属间系统发育关系。 1 材料与方法 1.1 材料采集与数据来源 （1）叶绿体基因组数据的获取：从活植株上采集无病虫害的幼嫩叶片，经硅胶干燥后， 用于 DNA 的提取及测序。本研究新测了锦葵科 19 属的 29 种植物的叶绿体基因组数据，并 从 NCBI 数据库（https://www.ncbi.nlm.nih.gov/）下载了 26 个锦葵科及 1 个红木科的叶绿体 3 ChinaXiv合作期刊 基因组数据，共计 56 个样本用于分析。其中，55 个锦葵科样本中代表了 8 个亚科 35 属 55 种 ，缺 少 杯萼椴亚科（Bayer & Kubitzki, 2003），涵盖原梧桐科的 26 个属（徐颂军和徐祥浩， 2012）。样本具体信息详见表 1。 （2）叶绿体片段数据的来源：为了进一步阐明梧桐属（Firmiana Marsili）与闭果桐属 （Hildegardia Schott & Endl.）之间的关系，在 Wilkie et al. (2006) 的取样基础上，增加了 matK 和 rbcL 基因片段进行联合分析。数据主要从 NCBI 数据库中下载，并从本研究选取的 叶绿体基因组数据样本中提取相应片段进行补充，详见表 1。 chinaXiv:202107.00062v1 4 ChinaXiv合作期刊 表 1 用于系统发育分析的叶绿体基因组及基因片段凭证信息 Table 1 Accession of chloroplast genome and gene sequences used for studying phylogeny 亚科 Subfamily 物种名 Species 凭证标本或 GenBank 号 Voucher or GenBank accession number 木棉亚科 Bombacoideae 木棉 Bombax ceiba MG569974.1 木棉亚科 Bombacoideae 美丽异木棉 Ceiba speciosa 黎若竹 : LRZ1204001 (HITBC) 刺果藤亚科 Bytterioideae 昂天莲 Ambroma augustum 王立彦、左常盛、桂魏: SCSB-TBG-055 (KUN) 刺果藤亚科 Bytterioideae Byttneria sp. SRR7122070 刺果藤亚科 Bytterioideae 山麻树 Commersonia bartramia 杨秀森、龙文兴: LWX10145 (KUN) 刺果藤亚科 Bytterioideae Herrania umbratica SRR5580908 刺果藤亚科 Bytterioideae 鹧鸪麻 Kleinhovia hospita 杨秀森、龙文兴: LWX10025 (KUN) 刺果藤亚科 Bytterioideae Melochia villosa N. Zamora: NZ7083 (KUN) 刺果藤亚科 Bytterioideae Seringia elliptica SRR8666286 刺果藤亚科 Bytterioideae 可可 Theobroma cacao HQ336404.2 刺果藤亚科 Bytterioideae Waltheria virgata SRR8666755 刺果藤亚科 Bytterioideae 瓜楚麻 Guazuma ulmifolia N. Zamora: NZ6921 (KUN) 非洲芙蓉亚科 Dombeyoideae 田麻 Corchoropsis crenata 易思荣: YiSR312 (KUN) 非洲芙蓉亚科 Dombeyoideae Dombeya sp. CPG考察队: 30554 (PE) 非洲芙蓉亚科 Dombeyoideae 火绳树 Eriolaena spectabilis 张挺、蔡杰、刘成、郭永杰: 08CS161 (KUN) 非洲芙蓉亚科 Dombeyoideae Melhania oblongifolia SRR866295 非洲芙蓉亚科 Dombeyoideae Nesogordonia sp. CPG考察队: 31468 (PE) 非洲芙蓉亚科 平当树 张挺、蔡杰 Dombeyoideae Paradombeya sinensis : 14CS9043 (KUN) chinaXiv:202107.00062v1 非洲芙蓉亚科 Dombeyoideae 景东翅子树 Pterospermum kingtungense MK962315.1 扁担杆亚科 Grewioideae 海南破布叶 Grewia chungii MN533967.1 扁担杆亚科 Grewioideae Sparrmannia sp. CPG考察队: 30755 (PE) 山芝麻亚科 Helicteroideae 榴梿 Durio zibethinus MG138151.1 山芝麻亚科 Helicteroideae 火索麻 Helicteres isora 杨秀森、龙文兴: LWX10021 (KUN) 5 ChinaXiv合作期刊 山芝麻亚科 Helicteroideae 两广梭罗 Reevesia thyrsoidea NC_041441.1 锦葵亚科 Malvoideae 木槿 Hibiscus syriacus NC_026909.1 锦葵亚科 Malvoideae 野葵 Malva parviflora MK860036.1 梧桐亚科 Sterculioideae Brachychiton gregorii SRR8666699 梧桐亚科 Sterculioideae 杨叶酒瓶树 B. populneus 黎若竹: LRZ20200703001 (HITBC) 黎若竹: LRZ20191125001 (HITBC); Parmentier Ingrid & Mambo Peter: 梧桐亚科 Sterculioideae 可乐果 Cola acuminata * KC628256 (rbcL); Kubitzki 93-12 (HBG): AF111759 (ndhF) 梧桐亚科 Sterculioideae 光亮可乐果 C. nitida * 黎若竹: LRZ20200523002 (HITBC) 梧桐亚科 Sterculioideae 火桐 Firmiana colorata SRR7121997 梧桐亚科 Sterculioideae 丹霞梧桐 F. danxiaensis * 郁文彬: YWB2013144 (KUN) 梧桐亚科 Sterculioideae 云南梧桐 F. major * NC_037242.1 梧桐亚科 Sterculioideae 马来火桐 F. malayana * P. Wilkie PW164(E): AY795587 (ndhF) 梧桐亚科 Sterculioideae 美丽梧桐 F. pulcherrima * MF621982.1 梧桐亚科 Sterculioideae 梧桐 F. simplex * MH671308.1; P. Wilkie PW469 (E): AY795589 (ndhF) 梧桐亚科 Sterculioideae Heritiera angustata MG897126.1 梧桐亚科 Sterculioideae H. fomes NC_043924.1
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