Molecular phylogeny of Chinese Stephania (Menispermaceae) and reassessment of the subgeneric and sectional classifications
Daotao Xie A , Jiayong He A , Jianming Huang A , Hui Xie A , Yaqin Wang A , Yun Kang A C , Florian Jabbour B and Jixian Guo A
+ Author Affiliations
- Author Affiliations
A Department of Pharmacognosy, School of Pharmacy, Fudan University, Shanghai, 201203, P.R. China.
B Institut de Systématique, Evolution, Biodiversité, ISYEB UMR 7205 CNRS–MNHN–UPMC–EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 57 Rue Cuvier CP39, F-75005 Paris, France.
C Corresponding author. Email: ykang123@fudan.edu.cn
Australian Systematic Botany 28(4) 246-255 https://doi.org/10.1071/SB14023
Submitted: 11 August 2014 Accepted: 5 November 2015 Published: 23 December 2015
Abstract
Many species of Stephania Lour. are used traditionally in South-east Asia as medicinal plants. Understanding and predicting their therapeutic properties could be improved, provided that the evolutionary relationships among lineages are clarified. We present the first molecular phylogeny of the genus Stephania, focusing on the species occurring in China on the basis of nuclear (internal transcribed spacer, ITS) and chloroplast (trnL–F) markers sequenced from 29 species of Stephania. Our results showed that S. subgenus Stephania and S. subgenus Tuberiphania are not monophyletic, owing to the phylogenetic placement of a single species (S. mashanica). The relationships with the third subgenus, S. subgenus Botryodiscia, are not resolved. None of the sections in our analyses is monophyletic. Our study calls for further phylogenetic investigations including more accessions from the whole distribution area of the genus. A taxonomic revision of the genus Stephania, which would reassess the appropriateness of the macromorphological characters used so far to distinguish among subgenera (e.g. flower merism, size and aspect of the rootstock and main root), and sections (e.g. inflorescence morphology, sessiliflorous or not), is much needed.
Additional keywords: ITS, evolutionary relationship, taxonomy, trnL–F.
References
Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Molecular Phylogenetics and Evolution 1, 3–16.| Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1eksLo%3D&md5=d44c7d82e68f83fa18e31daa164aca1fCAS | 1342921PubMed |
Baldwin BG (1993) Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined. American Journal of Botany 80, 222–238.
| Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVGgt7o%3D&md5=e326fe87a162b2744d3b29e27dc678d6CAS |
Bay-Smidt MGK, Jäger AK, Krydsfeldt K, Meerow AW, Stafford GI, Van Staden J, Rønsted N (2011) Phylogenetic selection of target species in Amaryllidaceae tribe Haemantheae for acetylcholinesterase inhibition and affinity to the serotonin reuptake transport protein. South African Journal of Botany 77, 175–183.
| Phylogenetic selection of target species in Amaryllidaceae tribe Haemantheae for acetylcholinesterase inhibition and affinity to the serotonin reuptake transport protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKltr0%3D&md5=9ed5686d8d5cc62657a535d6aff9ae3dCAS |
Chi Y, Tian T, Li X (2008) Pharmaceutical value and advances in tissue culture of Shan–Wu–Gui. Chinese Journal of Ethnomedicine and Ethnopharmacy 12, 13–15.
Chinese Pharmacopoeia Commission (2010) ‘Pharmacopoeia of the People’s Republic of China. Vol. 1.’ (China Medical Science Press: Beijing)
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=d825e650a54338bd3c5abca29f87da4bCAS | 22847109PubMed |
DeWet H, Struwig M, Wyk BEV (2014) Taxonomic notes on the genus Stephania (Menispermaceae) in southern Africa. South African Journal of Botany 95, 146–151.
| Taxonomic notes on the genus Stephania (Menispermaceae) in southern Africa.Crossref | GoogleScholarGoogle Scholar |
Diels L (1910) Menispermaceae. In ‘Das Pflanzenreich IV 94’. (Ed. A Engler) pp. 259–283. (Verlag Von Wilhelm Engelmann: Leipzig, Germany)
Haston EM, Lewis GP, Hawkins JA (2005) A phylogenetic reappraisal of the Peltophorum group (Caesalpinieae: Leguminosae) based on the chloroplast trnL–F, rbcL and rps16 sequence data. American Journal of Botany 92, 1359–1371.
| A phylogenetic reappraisal of the Peltophorum group (Caesalpinieae: Leguminosae) based on the chloroplast trnL–F, rbcL and rps16 sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahur%2FK&md5=67fa71b6c0bb9c21ab0c9727ba486f7dCAS | 21646156PubMed |
Fabricant DS, Farnsworth NR (2001) The value of plants used in traditional medicine for drug discovery. Environmental Health Perspectives 109, 69–75.
| The value of plants used in traditional medicine for drug discovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitlKhtLs%3D&md5=a165ce4fd6f01696e4ed246c5651bfdcCAS | 11250806PubMed |
Fairbrothers DE, Mabry TJ, Scogin RL, Turner BL (1975) Bases of angiosperm phylogeny–chemotaxonomy. Annals of the Missouri Botanical Garden 62, 765–800.
| Bases of angiosperm phylogeny–chemotaxonomy.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Forest F, Grenyer R, Rouget M, Davies TJ, Cowling RM, Faith DP, Balmford A, Manning JC, Proches S, van der Bank M, Reeves G, Hedderson TA, Savolainen V (2007) Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760.
| Preserving the evolutionary potential of floras in biodiversity hotspots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhslSqs7s%3D&md5=e7f682a608b1c1b4762049ce884615b3CAS | 17301791PubMed |
Forman LL (1956) The Menispermaceae of Malaysia: I. Kew Bulletin 11, 41–69.
| The Menispermaceae of Malaysia: I.Crossref | GoogleScholarGoogle Scholar |
Forman LL (1988) A synopsis of Thai Menispermaceae. Kew Bulletin 43, 369–407.
| A synopsis of Thai Menispermaceae.Crossref | GoogleScholarGoogle Scholar |
Gielly L, Taberlet P (1994) The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. Molecular Biology and Evolution 11, 769–777.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=2e3e202e8279618465b24e4d9cc74b41CAS | 20525638PubMed |
Havill NP, Campbell CS, Vining TF, LePage B, Bayer RJ, Donoghue MJ (2008) Phylogeny and biogeography of Tsuga (Pinaceae) inferred from nuclear ribosomal ITS and chloroplast DNA sequence data. Systematic Botany 33, 478–489.
| Phylogeny and biogeography of Tsuga (Pinaceae) inferred from nuclear ribosomal ITS and chloroplast DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
Hong YP, Chen ZD, Lu AM (2001a) Phylogeny of the tribe Menispermeae (Menispermaceae) reconstructed by ITS sequence data. Acta Phytotaxonomica Sinica 39, 97–104.
Hong YP, Pan KY, Chen ZD, Lu AM (2001b) Characters of leaf epidermis and their systematic significance in Menispermaceae. Acta Botanica Sinica 43, 615–623.
Hoot SB, Zautke H, Harris DJ, Crane PR, Neves SS (2009) Phylogenetic patterns in Menispermaceae based on multiple chloroplast sequence data. Systematic Botany 34, 44–56.
| Phylogenetic patterns in Menispermaceae based on multiple chloroplast sequence data.Crossref | GoogleScholarGoogle Scholar |
Huang JM, Guo JX (1998) Research progress on the alkaloids from the genus Stephania in China. West China Journal of Pharmaceutical Sciences 13, 97–99.
Huang JM, Guo JX, Pan SL (1999) A preliminary study on chemotaxonomy of the genus Stephania. West China Journal of Pharmaceutical Sciences 14, 108–110.
Jacques FMB, Wang W, Ortiz RDC, Li HL, Zhou ZK, Chen ZD (2011) Integrating fossils in a molecular-based phylogeny and testing them as calibration points for divergence time estimates in Menispermaceae. Journal of Systematics and Evolution 49, 25–49.
| Integrating fossils in a molecular-based phylogeny and testing them as calibration points for divergence time estimates in Menispermaceae.Crossref | GoogleScholarGoogle Scholar |
Kazemi M, Kazempour OS, Maassoumi AA, Rastegar PE (2009) Molecular phylogeny of selected Old World Astragalus (Fabaceae): incongruence among chloroplast trnL, ndhF and nuclear ribosomal DNA ITS sequences. Nordic Journal of Botany 27, 425–436.
| Molecular phylogeny of selected Old World Astragalus (Fabaceae): incongruence among chloroplast trnL, ndhF and nuclear ribosomal DNA ITS sequences.Crossref | GoogleScholarGoogle Scholar |
Kessler PJA (1993) Menispermaceae. In ‘The Families and Genera of Vascular Plants II. Flowering Plants: Dicotyledons’. (Eds K Kubitzki, JG Rohwer, V Bittrich) pp. 402–418. (Springer-Verlag: Berlin)
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=21273bde9fb028226329c9dc861fb918CAS | 15260895PubMed |
Kundu BC, Guha S (1977) The genus Perichasma (Menispermaceae). Adansonia 17, 221–234.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
| Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=4b9552bbb92af4d110d503ec492f3c0bCAS | 17846036PubMed |
Larsen MM, Adsersen A, Davis AP, Lledó MD, Jäger AK, Rønsted N (2010) Using a phylogenetic approach to selection of target plants in drug discovery of acetylcholinesterase inhibiting alkaloids in Amaryllidaceae tribe Galantheae. Biochemical Systematics and Ecology 38, 1026–1034.
| Using a phylogenetic approach to selection of target plants in drug discovery of acetylcholinesterase inhibiting alkaloids in Amaryllidaceae tribe Galantheae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktVOksg%3D%3D&md5=33aaeb65e6dc3df6154dc5780e15f764CAS |
Liu JQ, Li HY (2000) Comparative study on the leaf venation of Menispermaceae in Fujian. Journal of Fujian Normal University 16, 80–84.
Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Molecular Biology 26, 775–778.
| A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitVeisLs%3D&md5=5a200585b82f8184ab7a2456132f9b01CAS | 7948932PubMed |
Loureiro J (1790) Genus VI: Stephania. In ‘Flora Cochinchinensis: sistens plantas in regno Cochinchina nascentes: quibus accedunt aliae observatae in Sinensi imperio, Africa orientali, Indiaeque locis variis: omnes dispositae secundum systema sexuale Linnaeanum’. pp. 608–609. (Typis, et Expensis Academicis: Ulyssipone, Portugal)
Lukhoba CW, Simmonds MSJ, Paton AJ (2006) Plectranthus: a review of ethnobotanical uses. Journal of Ethnopharmacology 103, 1–24.
| Plectranthus: a review of ethnobotanical uses.Crossref | GoogleScholarGoogle Scholar | 16289602PubMed |
Luo XR (1978) A preliminary study on the genus Stephania in China. Acta Phytotaxonomica Sinica 16, 10–40.
Luo XR (1982) A systematic notes on the genus Stephania of China. Bulletin of Botanical Research 2, 33–59.
Luo XR (1996) Menispermaceae. In ‘Flora Republicae Popularis Sinicae’. (Ed. YH Liu) pp. 1–81. (Science Press: Beijing)
Luo XR, Chen T, Gilbert MG (2008) Stephania. In ‘Flora of China. Vol. 7’. (Eds ZY Wu, PH Raven) pp. 15–27. (Science Press: Beijing, and Missouri Botanical Garden Press: St Louis, MO)
Ma YM (2004) Research progress on chemical constituents of Stephania plants. Journal of Northwest Forestry University 19, 125–130.
Mabberley DJ (1997) ‘The Plant Book.’ (Cambridge University Press: Cambridge, UK)
Meng AP, Zhang ZG, Li JQ, De Craene LR, Wang HC (2012) Floral development of Stephania (Menispermaceae): impact of organ reduction on symmetry. International Journal of Plant Sciences 173, 861–874.
| Floral development of Stephania (Menispermaceae): impact of organ reduction on symmetry.Crossref | GoogleScholarGoogle Scholar |
Ortiz RDC, Kellogg EA, Van der Werff H (2007) Molecular phylogeny of the moonseed family (Menispermaceae): implications for morphological diversification. American Journal of Botany 94, 1425–1438.
| Molecular phylogeny of the moonseed family (Menispermaceae): implications for morphological diversification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVajsr%2FK&md5=6e768d1d5a146d7e3cd2c94dba09d1feCAS |
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=41bced8ea81c55798727300505ccc162CAS | 12912839PubMed |
Rønsted N, Savolainen V, Mølgaard P, Jager AK (2008) Phylogenetic selection of Narcissus species for drug discovery. Biochemical Systematics and Ecology 36, 417–422.
| Phylogenetic selection of Narcissus species for drug discovery.Crossref | GoogleScholarGoogle Scholar |
Ruan DC, Zhang XM, Zhao CJ, Wang FC, Tian LX, Yang CR (1991) High performance liquid chromatographic analysis of alkaloids in Stephania plants. Acta Botanica Yunnanica 13, 225–230.
Salinas J, Matassi G, Montero LM, Bernardi G (1988) Compositional compartmentalization and compositional patterns in the nuclear genomes of plants. Nucleic Acids Research 16, 4269–4285.
| Compositional compartmentalization and compositional patterns in the nuclear genomes of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktleisr4%3D&md5=b6a73139d18d018c5f130355b6157766CAS | 3380684PubMed |
Saslis-Lagoudakis CH, Klitgaard BB, Forest F, Francis L, Savolainen V, Williamson EM, Hawkins JA (2011) The use of phylogeny to interpret cross-cultural patterns in plant use and guide medicinal plant discovery: an example from Pterocarpus (Leguminosae). PLoS One 6, e22275
| The use of phylogeny to interpret cross-cultural patterns in plant use and guide medicinal plant discovery: an example from Pterocarpus (Leguminosae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeht7vO&md5=12dce8500749313f4fcfcdb7271fffaaCAS | 21789247PubMed |
Semwal DK, Badoni R, Semwal R, Kothiyal SK, Singh GJP, Rawat U (2010) The genus Stephania (Menispermaceae): chemical and pharmacological perspectives. Journal of Ethnopharmacology 132, 369–383.
| The genus Stephania (Menispermaceae): chemical and pharmacological perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlOhtrvO&md5=ce0f5afb86d223a4401d8fa5c04bd1daCAS | 20801207PubMed |
Shaw J, Lickey E, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92, 142–166.
| The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Klsbc%3D&md5=dfc169995750f7ba18776e81f7a678b3CAS | 21652394PubMed |
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhslel&md5=7da114d7dcd800cbbe3423fa69803643CAS | 1932684PubMed |
Troupin G (1962) Monographie des Menispermaceae africaines. Memoirs de Académie Royale des Sciences D’Outre-Mer. Classe des Sciences Naturelles et Médicales Tome 13, 1–313.
Wang HC (2005) ‘Floral Organogenesis and Molecular Phylogeny of Menispermeae (Menispermaceae).’ (Wuhan Botanical Garden, the Chinese Academy of Sciences: Wuhan, China)
Wang HC, Meng AP, Li JQ, He ZC (2004) Chromosome numbers for eight species in five genera of Menispermaceae. The Journal of Japanese Botany 79, 241–246.
Wang HC, Meng AP, Li JQ, Li XW (2005a) Cytological study of three Menispermaceous species from China. Journal of Wuhan Botanical Research 23, 96–98.
Wang A, Yang M, Liu J (2005b) Molecular phylogeny, recent radiation and evolution of gross morphology of the rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL–F sequences. Annals of Botany 96, 489–498.
| Molecular phylogeny, recent radiation and evolution of gross morphology of the rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL–F sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGltrrP&md5=6826a1047e2dbfff6b2be7ebd471be43CAS | 15994840PubMed |
Wang W, Wang HC, Chen ZD (2007) Phylogeny and morphological evolution of tribe Menispermeae (Menispermaceae) inferred from chloroplast and nuclear sequences. Perspectives in Plant Ecology, Evolution and Systematics 8, 141–154.
| Phylogeny and morphological evolution of tribe Menispermeae (Menispermaceae) inferred from chloroplast and nuclear sequences.Crossref | GoogleScholarGoogle Scholar |
Wang W, Ortiz RDC, Jacques FMB, Xiang XG, Li HL, Lin L, Li RQ, Liu Y, Soltis PS, Soltis DE, Chen ZD (2012) Menispermaceae and the diversification of tropical rainforests near the Cretaceous–Paleogene boundary. New Phytologist 195, 470–478.
| Menispermaceae and the diversification of tropical rainforests near the Cretaceous–Paleogene boundary.Crossref | GoogleScholarGoogle Scholar | 22548458PubMed |
White TJ, Bruns Y, Lee S, Taylor JW (1990) ‘Amplifications and direct sequencing of fungal ribosomal RNA genes for phylogenetics.’ (Academic Press: New York)
Wielgorskaya T (1995) ‘Dictionary of Generic Names of Seed Plants.’ (Columbia University Press: New York)
Willis JC (1973) ‘A Dictionary of Flowering Plants and Ferns.’ (Cambridge University Press: Cambridge, UK)
Wright CI, Van-Buren L, Kroner CI, Koning MMG (2007) Herbal medicines as diuretics: a review of the scientific evidence. Journal of Ethnopharmacology 114, 1–31.
| Herbal medicines as diuretics: a review of the scientific evidence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSksbnK&md5=4718a119f4a56f290bc6110e57baf4e4CAS | 17804183PubMed |
Yamaji H, Fukuda T, Yokoyama J, Pak JH, Zhou CZ, Yang CS, Kondo K, Morota T, Takeda S, Sasaki H, Maki M (2007) Reticulate evolution and phylogeography in Asarum sect. Asiasarum (Aristolochiaceae) documented in internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 44, 863–884.
| Reticulate evolution and phylogeography in Asarum sect. Asiasarum (Aristolochiaceae) documented in internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslGgsb4%3D&md5=610506222f0eba8dad5b28947634b321CAS | 17383903PubMed |
Yang HM, Chen Y (1994) Chemosystematic notes of genus Stephania (Menispermaceae) in China. Acta Botanica Sinica 36, 14–22.
Yang HM, Lo HS (1980) Botanical and pharmacognostical studies of the Chinese drug ‘Shan–Wu–Gui’. Acta Pharmacologica Sinica 15, 674–683.
Zhang ZG, Meng AP, Wang HC, Li JQ (2013) A new species of Stephania (Menispermaceae) from South Guangxi, China. Novon 22, 379–382.
| A new species of Stephania (Menispermaceae) from South Guangxi, China.Crossref | GoogleScholarGoogle Scholar |
Zheng XZ (1986) ‘Pharmacognosy.’ (People’s Medical Pubilshing House: Beijing)
Zhu ZY, Feng YX, Ho LY, Wang YC (1983) Utilization of medicinal plant resources of the genus Stephania of the family Menispermaceae in China. Acta Pharmacologica Sinica 18, 460–467.
Zhu CL, Zhao YH, Ma WG (2007) ‘Dai Medicine.’ (China Press of Traditional Chinese Medicine: Beijing)
