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AbstractAsparagales, the largest monocot order, is renowned for its ecological, economic, and medicinal significance. Here, we leverage transcriptome data from 455 Asparagales species to explore the phylogeny of Asparagales. Moreover, we investigate the evolutionary patterns of the genes involved in allium flavor formation.
摘要天冬酰胺是最大的单子叶植物目,以其生态,经济和药用意义而闻名。在这里,我们利用来自455种天冬酰胺物种的转录组数据来探索天冬酰胺的系统发育。此外,我们研究了参与葱风味形成的基因的进化模式。
We not only establish a robust bifurcating phylogeny of Asparagales but also explore their reticulate relationships. Notably, we find that eight genes involved in the biosynthesis of allium flavor compounds underwent expansion in Allium species. Furthermore, we observe Allium-specific mutations in one amino acid within alliinase and three within lachrymatory factor synthase.
我们不仅建立了天冬酰胺的强大分叉系统发育,而且还探索了它们的网状关系。值得注意的是,我们发现参与葱风味化合物生物合成的八个基因在葱属物种中经历了扩增。此外,我们观察到蒜氨酸酶中一个氨基酸和泪腺因子合酶中三个氨基酸的蒜特异性突变。
Overall, our findings highlight the role of gene expansion, increased expression, and amino acid mutations in driving the evolution of Allium-specific compounds. These insights not only deepen our understanding of the phylogeny of Asparagales but also illuminate the genetic mechanisms underpinning specialized compounds..
总体而言,我们的发现突出了基因扩增,表达增加和氨基酸突变在驱动葱特异性化合物进化中的作用。这些见解不仅加深了我们对天冬酰胺系统发育的理解,而且阐明了支持特殊化合物的遗传机制。。
IntroductionAsparagales consists of approximately 1030 genera and 39,000 species distributed across 14 families, including Orchidaceae, which is one of the largest families of angiosperms according to the Angiosperm Phylogeny Group [APG] IV1 and the Plants of World Online (POWO; https://powo.science.kew.org/).
简介天冬酰胺由大约1030属39000种组成,分布在14个科中,包括兰科,根据被子植物系统发育组(APG)IV1和世界植物在线(POWO);https://powo.science.kew.org/)。
Known for their diverse applications, Asparagales species serve as vegetables (onions, chives, garlic, asparagus), spices (vanilla), and ornamentals (orchids) and possess medicinal properties (Gastrodiae Rhizoma [Tianma] and Dendrobii Caulis [Shihu] in China and Cypripedium species in North America).
芦笋因其多种应用而闻名,可作为蔬菜(洋葱,韭菜,大蒜,芦笋),香料(香草)和观赏植物(兰花),并具有药用特性(中国的天麻,石斛,北美的鲤属)。
Despite several studies having investigated the phylogeny of Asparagales2,3, there is still uncertainty regarding its evolutionary relationships. One area of debate involves the families Ixioliriaceae, Tecophilaeaceae, and Doryanthaceae. Analyses based only on plastid rbcL supported a relationship (Ixioliriaceae, (Tecophilaeaceae, (Doryanthaceae, others)))4.
尽管有几项研究调查了天冬酰胺2,3的系统发育,但其进化关系仍存在不确定性。争论的一个领域涉及Ixioliriaceae,Tecophilaeae和Doryanthaceae家族。仅基于质体rbcL的分析支持一种关系(Ixioliriaceae,(Tecophilaeae,(Doryanthaceae,其他)))4。
In contrast, analyses using plastid genomes5 and nuclear genes6,7,8 suggested alternative topologies. Transcriptome-based phylogenetics are robust approaches9,10 that can be used to explore the phylogeny of Asparagales better.Asparagales has a global distribution spanning all continents, with North America and Asia exhibiting the highest species diversity, according to POWO.
相反,使用质体基因组5和核基因6,7,8的分析提出了替代拓扑。基于转录组的系统发育学是强有力的方法9,10,可用于更好地探索天冬酰胺的系统发育。据POWO称,天冬酰胺在全球各大洲均有分布,其中北美和亚洲的物种多样性最高。
Several studies investigated the biogeography of Asparagales11,12,13,14. For example, the ancestral area for Asteliaceae11, Blandfordiaceae11, Boryaceae11, Iridaceae13, and Orchidaceae14 was determined to be Australia. In total, biogeographic origins for 11 out of the 14 families within Asparagales are reported to be from Australia, South Africa, or Gondwana.
。例如,Asteliaceae11,Blandfordiaceae11,Boryaceae11,Iridaceae13和Orchidaceae14的祖先区域被确定为澳大利亚。据报道,Asparagales内14个家族中有11个家族的生物地理起源来自澳大利亚,南非或冈瓦纳大陆。
However, the biogeographic origins of the remaining three families, Amaryllidaceae, A.
然而,其余三个科,石蒜科,A的生物地理起源。
We employed ultra-high performance liquid chromatography (UPLC) with quadrupole time-of-flight (QTOF) mass spectrometry (MS) to detect eight compounds in the CSOs biosynthesis pathway across nine Allium species and seven other species within Asparagales. The results indicated that three compounds upstream of the CSOs biosynthesis pathway—serine, valine, and glutathione—were detected in both Allium and non-Allium species (Fig. 3a).
我们采用超高效液相色谱(UPLC)和四极杆飞行时间(QTOF)质谱(MS)检测了9种葱属物种和天冬酰胺中其他7种物种的CSO生物合成途径中的8种化合物。结果表明,在葱属和非葱属物种中均检测到CSO生物合成途径上游的三种化合物-丝氨酸,缬氨酸和谷胱甘肽(图3a)。
However, the remaining five compounds were exclusively detected in Allium species (Fig. 3a and Supplementary Figs. 9 and 10). Refer to Supplementary Data 6 for details about the compounds. Notably, γ-glutamyl-S-allylcysteine emerged as the most upstream metabolite, specific to Allium in the pathway.
然而,其余五种化合物仅在葱属物种中检测到(图3a和补充图9和10)。有关化合物的详细信息,请参阅补充数据6。值得注意的是,γ-谷氨酰-S-烯丙基半胱氨酸是该途径中葱属特有的最上游代谢物。
The gene responsible for synthesizing γ-glutamyl-S-allylcysteine could play a pivotal role in the pathway despite its unreported status.Fig. 3: Identification of S-Alk(en)ylcysteine sulfoxides (CSOs) using UPLC-QTOF-MS.a A summary of metabolites identified for 16 Asparagales species. b Extracted-ion chromatograms of isoalliin and alliin from nine Allium species.
尽管尚未报道,但负责合成γ-谷氨酰-S-烯丙基半胱氨酸的基因可能在该途径中起关键作用。图3:使用UPLC-QTOF-MS鉴定S-Alk(en)基半胱氨酸亚砜(CSO).a鉴定出16种天冬酰胺物种的代谢物的总结。b从9种葱属植物中提取异蒜氨酸和蒜氨酸的离子色谱图。
Plant photos were taken by Bing Liu, Xiao-Wei Xin, Xiao-Xiao Wang, and Ling-Yun Chen. c Secondary ion fragments for alliin and isoalliin are depicted as shaded areas on the chromatograms. Red numbers indicate the characteristic secondary fragment ion of alliin.Full size imageTwo upstream sub-pathways, designated as way 1 (glutathione biosynthesis) and way 2 (valine catabolism), as illustrated in Fig. 4a, along with a downstream sub-pathway, comprised a total of 13 genes (Supplementary Data 7), involved in CSOs biosynthesis.
植物照片由刘冰、辛晓伟、王晓晓和陈凌云拍摄。c蒜氨酸和异蒜氨酸的二次离子片段被描绘为色谱图上的阴影区域。红色数字表示蒜氨酸的特征性二级碎片离子。全尺寸图像如图4a所示,两个上游子途径,命名为途径1(谷胱甘肽生物合成)和途径2(缬氨酸分解代谢),以及下游子途径,共包含13个基因(补充数据7),参与CSO生物合成。
Gene trees were constructed, and gene copy numbers for each species were quantified (Supplementary Figs. 11–15). The Mann–Whitney U test indicated that three genes in wa.
构建了基因树,并量化了每个物种的基因拷贝数(补充图11-15)。。
Data availability
数据可用性
Raw sequence reads of the 244 samples generated in this study have been deposited in the NCBI Sequence Read Archive under BioProject nos. PRJNA1107703 and PRJNA1107706. Raw reads or annotations for other samples were accessed from the internet with accession nos. provided in Supplementary Data 1. The assembled transcriptomes for the samples sequenced in this study, CDSs and PEPs for all the 501 samples used in phylogenetic analyses, as well as those for the 16 samples used in gene expression level analyses, are available at Figshare: [https://doi.org/10.6084/m9.figshare.25516204].
本研究中产生的244个样品的原始序列读数已保存在生物项目PRJNA1107703和PRJNA1107706下的NCBI序列读取档案中。其他样品的原始读数或注释可从互联网上访问,登录号见补充数据1。本研究中测序的样品的组装转录组,用于系统发育分析的所有501个样品的CDSs和PEPs,以及用于基因表达水平分析的16个样品的转录组,可在Figshare获得:[https://doi.org/10.6084/m9.figshare.25516204]。
Additionally, the sequences of orthologs, data matrices for phylogenetic analyses, divergence times, ancestral area reconstructions, and Source Data are also available at Figshare: [https://doi.org/10.6084/m9.figshare.25516204]. Specimens have been deposited at the Herbarium of Guangxi Botanical Garden of Medicinal Plants..
此外,Figshare还提供了直系同源序列,用于系统发育分析的数据矩阵,发散时间,祖先区域重建和源数据:[https://doi.org/10.6084/m9.figshare.25516204]。标本保存于广西药用植物植物园植物标本室。。
Code availability
代码可用性
Codes used in this study have been deposited at Figshare: [https://doi.org/10.6084/m9.figshare.25516204].
[https://doi.org/10.6084/m9.figshare.25516204]。
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Download referencesAcknowledgementsWe thank the Kunming Institute of Botany, Chinese Academy of Sciences (CAS), Xishuangbanna Tropical Botanical Garden (CAS), Guiyang Medicinal Botanical Garden, and Shenyang Botanical Garden for assistance in plant collection; Can Dai (Hubei University) for discussion on this study; Michael L.
下载参考文献致谢我们感谢中国科学院昆明植物研究所(CAS),西双版纳热带植物园(CAS),贵阳药用植物园和沈阳植物园在植物采集方面的帮助;Can Dai(湖北大学)就这项研究进行了讨论;迈克尔L。
Moody (University of Texas at El Paso) for discussion and providing plant photo; Xu Lu, Hui-Ying Wang (China Pharmaceutical University) and Xiang-Yang Leng (SCIEX, China) for technical assistance; Xiao-Wei Xin (Shandong Drug and Food Vocational College) for providing plant materials; Bing Liu (Institute of Botany, CAS), Zhong Zhang (Jinggangshan National Nature Reserve) and Ye-Chun Xu (Guangdong Academy of Agricultural Sciences) for providing plant photos; Ya-Dong Zhou (Nanchang University) for assisting in data analyses and providing plant photos; Guo-Yong Xie (China Pharmaceutical University) for assisting in plant cultivation; Li Feng, Xing-Ze Li, Wen-Da Zhang, Wen-Fang Zheng, and Wen-Yu Du (China Pharmaceutical University) for assisting in data analyses; John A.
穆迪(德克萨斯大学埃尔帕索分校)进行讨论并提供植物照片;Xu Lu,Hui Ying Wang(中国药科大学)和Xiang Yang Leng(中国SCIEX)提供技术援助;肖伟新(山东医药食品职业学院)提供植物材料;刘冰(中国科学院植物研究所),张忠(井冈山国家级自然保护区)和徐叶春(广东省农业科学院)提供了植物照片;周亚东(南昌大学)协助数据分析并提供植物照片;谢国勇(中国药科大学)协助植物栽培;;约翰·A。
Rhodes (University of Alaska Fairbanks) for explaining the results of MSCquartets; Ji Yang (Fudan University) and Tao Wan (Wuhan Botanical Garden) for suggestions on this manuscript. This work was supported by the Guangxi Innovation-Driven Development Project (no. GuiKe AA18242040 to K.-H.W.), the Construction of Southern Medicine Germplasm Resource Base for Guangdong Northern (20231206 to K.-H.
Rhodes(阿拉斯加州大学费尔班克斯分校)解释了MSCquartets的结果;济阳(复旦大学)和陶湾(武汉植物园)对这份手稿的建议。这项工作得到了广西创新驱动发展项目(桂科AA18242040至K.-H.W.),广东北部南方医学种质资源基地建设(20231206至K.-H.)的支持。
W.), the National Natural Science Foundation of China (32370242 to L.-Y.C.), the Fundamental Research Funds for the Central Universities (2632024TD04 to L.-Y.C.), and the Sino-Africa Joint Research Center (SAJC202101 to Q.-F.W.).Author informationAuthor notesThese authors contri.
W、 ),国家自然科学基金(32370242至洛杉矶),中央大学基础研究基金(2632024TD04至洛杉矶),以及中非联合研究中心(SAJC202101至Q.-F.W.)。作者信息作者注意到这些作者贡献了。
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PubMed Google ScholarContributionsQ.-F.W., L.-Y.C., K.-H.W., and N.-H.T. designed the research. Q.-F.W., K.-H.W., Y.H., X.-M.W., G.-W.H., X.-X.W., and L.-Y.C. contributed to the taxon sampling and sequencing. X.-X.W., C.-H.H., D.F.M.-B., N.Z., P.-G.Z., X.-Y.H., and L.-Y.C. performed data analyses.
PubMed谷歌学术贡献-F、 W.,L.-Y.C.,K.-H.W。和N.-H.T.设计了这项研究。Q、 -F.W.,K.-H.W.,Y.H.,X.-M.W.,G.-W.H.,X.-X.W。和L.-Y.C.对分类群的采样和测序做出了贡献。十、 -X.W.,C.-H.H.,D.F.M.-B.,N.Z.,P.-G.Z.,X.-Y.H.和L.-Y.C.进行了数据分析。
X.-X.W. performed wet lab experiments. X.-X.W., X.-Y.W., D.F.M.-B., and L.-Y.C. prepared the figures and tables. L.-Y.C. drafted the manuscript. Q.-F.W., C.-H.H., D.F.M.-B., X.-X.W., and L.-Y.C. revised this manuscript. All the authors read this manuscript.Corresponding authorsCorrespondence to.
十、 -X.W.进行了湿实验室实验。十、 -X.W.,X.Y.W.,D.F.M.B。和L.Y.C.准备了数字和表格。五十、 -Y.C.起草了手稿。Q、 -F.W.,C.-H.H.,D.F.M.-B.,X.-X.W。和L.-Y.C.修订了这份手稿。所有作者都阅读了这份手稿。通讯作者通讯。
Kun-Hua Wei, Ning-Hua Tan, Qing-Feng Wang or Ling-Yun Chen.Ethics declarations
魏坤华、谭宁华、王庆峰或陈凌云。道德宣言
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Reprints and permissionsAbout this articleCite this articleWang, XX., Huang, CH., Morales-Briones, D.F. et al. Phylotranscriptomics reveals the phylogeny of Asparagales and the evolution of allium flavor biosynthesis.
转载和许可本文引用本文Wang,XX。,Huang,CH.,Morales-Briones,D.F.等人。系统转录组学揭示了天冬酰胺的系统发育和葱味生物合成的进化。
Nat Commun 15, 9663 (2024). https://doi.org/10.1038/s41467-024-53943-6Download citationReceived: 23 April 2024Accepted: 29 October 2024Published: 08 November 2024DOI: https://doi.org/10.1038/s41467-024-53943-6Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.
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