Circumscription of the East Asia clade (Apiaceae subfamily Apioideae) and the taxonomic placements of several problematic genera

doi:10.1016/j.pld.2023.11.002

Abstract

Abstract: The East Asia (or Physospermopsis) clade was recognized in previous molecular phylogenetic investigations into the higher-level relationships of Apiaceae subfamily Apioideae. The composition of this clade, the phylogenetic relationships among its constituent taxa, and the placement of species previously determined to be problematic have yet to be resolved. Herein, nrDNA ITS sequences were obtained for 150 accessions of Apioideae, representing species whose distributions are in East Asia or genera having one or more species included within the East Asia clade. These data, along with published ITS sequences from other Apioideae (for 3678 accessions altogether), were subjected to maximum likelihood and Bayesian inference analyses. The results show that the East Asia clade contains representatives of 11 currently recognized genera: Hansenia, Hymenolaena, Keraymonia, Sinolimprichtia, Acronema, Hymenidium, Physospermopsis, Pimpinella, Sinocarum, Tongoloa, and Trachydium. However, the latter seven genera have members falling outside of the East Asia clade, including the generic types of all except Tongoloa. Within the clade, the species comprising these seven genera are widely intermingled, greatly increasing confusion among relationships than previously realized. The problematic species Physospermopsis cuneata is confirmed as falling within the East Asia clade, whereas P. rubrinervis allies with the generic type in tribe Pleurospermeae. Physospermopsis kingdon-wardii is confirmed as a member of the genus Physospermopsis, whereas the generic attributions of P. cuneata and Tongoloa stewardii remain unclear. Two species of Sinocarum (S. filicinum and S. wolffianum) are transferred into the genus Meeboldia. This is the most comprehensive molecular phylogenetic investigation of the East Asia clade to date, and while the results increase systematic understanding of the clade, they also highlight the need for further studies of one of the most taxonomically intractable groups in Apioideae.

Key words: Physospermopsis, Pimpinella, Sinocarum, Tongoloa, Trachydium

Jing Zhou, Xinyue Wang, Shilin Zhou, Junmei Niu, Jiarui Yue, Zhenwen Liu, Stephen R. Downie. Circumscription of the East Asia clade (Apiaceae subfamily Apioideae) and the taxonomic placements of several problematic genera[J]. Plant Diversity, 2024, 46(02): 206-218.

References

[1] Bentham G, Hooker JD. 1867. Umbelliferae. Genera plantarum 1:859-931.
[2] Boissier E. 1875. Flora Orientalis. Vol. 3:Calyciflorae, Gamopetalae. Geneve & Basileae:apud H. Georg, et Lugduni:apud eumdem.
[3] Boissieu HD. 1902. Note sur quelques Ombelliferes de Chine d'apres les collections du Museum d'Histoire naturelle de Paris. Bulletin de l'Herbier Boissier 2(2):801-810.
[4] Clarkson JJ, Zuntini AR, Maurin O, Downie SR, Plunkett G, Nicolas AN, Smith JF, Feist MAE, Gutierrez K, Malakasi P, Bailey P, Brewer GE, Epitawalage N, Zmarzty S, Forest F, Baker WJ. 2021. A higher-level nuclear phylogenomic study of the carrot family (Apiaceae). American Journal of Botany 108(7):1252-1269.
[5] Calvino CI, Tilney PM, Van Wyk BE, Downie SR. 2006. A molecular phylogenetic study of southern African Apiaceae. American Journal of Botany 93:1828-1847.
[6] Cheng T, Xu C, Lei L, Li CH, Zhang Y, Zhou SL. 2016. Barcoding the kingdom plantae:new PCR primers for ITS regions of plants with improved universality and specificity. Molecular Ecology Resources 16:138-149.
[7] Christenhusz M, Byng JW. 2016. The number of known plant species in the world and its annual increase. Phytotaxa 261:201-217.
[8] Constance L. 1971. History of the classification of Umbelliferae (Apiaceae). In Heywood VH eds. The biology and chemistry of the Umbelliferae. London:Academic Press, UK. 1-8.
[9] Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2:More models, new heuristics and parallel computing. Nature Methods 9(8):772.
[10] De Candole AP. 1827. Dictionnaire classique d'histoire naturelle 11. Rey et Gravier, Libraries-Editeurs ed. 406.
[11] Downie SR, Plunkett GM, Watson MF, Spalik K, Katz-Downie DS, Valiejo-Roman CM, Terentieva EI, Troitsky AV, Lee BY, Lahham J, El-Oqlah A. 2001. Tribes and clades within Apiaceae subfamily Apioideae:the contribution of molecular data. Edinburgh Journal of Botany 58:301-330.
[12] Downie SR, Spalik K, Katz-Downie DS, Reduron JP. 2010. Major clades within Apiaceae subfamily Apioideae as inferred by phylogenetic analysis of nrDNA ITS sequences. Plant Diversity and Evolution 128:111-136.
[13] Fereidounfar S, Ghahremaninejad F, Khajehpiri M. 2016. Phylogeny of the Southwest Asian Pimpinella and related genera based on nuclear and plastid sequences. Genetics and Molecular Research 15:gmr15048767.
[14] Franchet A. 1894. Notes sur quelques Ombelliferes du Yunnan. Bulletin de la Societe Philomathique de Paris 86:106-146.
[15] Gou W, Guo XL, Zhou SD, He XJ. 2021. Phylogeny and taxonomy of Meeboldia, Sinodielsia and their relatives (Apiaceae:Apioideae) inferred from nrDNA ITS, plastid DNA intron (rpl16 and rps16) sequences and morphological characters. Phytotaxa 482(2):121-142.
[16] Gui LJ, Jia SB, Guo XL, Price M, Zhou SD, He XJ. 2020a. Tongoloa tagongensis (Apiaceae), a new species from the Hengduan Mountains, China. Phytotaxa 461(1):17-25.
[17] Gui LJ, Wen J, Xiao YP, Ren T, Zheng HY, He XJ. 2020b. Tongoloa arguta (Apiaceae), a new species from southwest China. PhytoKeys 164:11-19.
[18] Hall T. 1999. BioEdit:biological sequence alignment editor for Win95/98/NT/2K/XP version 6.0.7. http://www.mbio.ncsu.edu/BioEdit/bioedit.html.
[19] Hardway TM, Spalik K, Watson MF, Katz-Downie DS, Downie SR. 2004 Circumscription of Apiaceae tribe Oenantheae. South African Journal of Botany 70:393-406.
[20] Hiroe M. 1958:Umbelliferae of Asia (excluding Japan). Kyoto:Eicodo (Akira Imagawa), Maruzen Ltd. 1-219.
[21] Hiroe M. 1979. Umbelliferae of World. Tokyo:Ariake Book Company. 741-747.
[22] Jia SB, Guo XL, Zhou SD, He XJ. 2019. Hansenia pinnatiinvolucellata is conspecific with H. weberbaueriana (Apiaceae) based on morphology and molecular data. Phytotaxa 418(2):203-210.
[23] Jiang QP, Price M, Zhang XY, He XJ. 2022. Hansenia trifoliolata, a new species (Apiaceae) from Shaanxi, China. PhytoKeys 213:79-93.
[24] Mousavi S, Mozaffarian V, Mummenhoff K, Downie SR, Zarre S. 2021. An updated lineage-based tribal classification of Apiaceae subfamily Apioideae with special focus on Iranian genera. Systematics and Biodiversity 19(1):89-109.
[25] Neves SS, Watson MF. 2004. Phylogenetic relationships in Bupleurum (Apiaceae) based on nuclear ribosomal DNA ITS sequence data. Annals of Botany 93:379-398.
[26] Pan ZH, Watson MF. 2005a. Tongoloa H. Wolff. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:34-37.
[27] Pan ZH, Watson MF. 2005b. Sinolimprichtia H.Wolff. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:55-56.
[28] Pan ZH, Watson MF. 2005c. Pleurospermum Hoffm. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:158-169.
[29] Pan ZH, Watson MF. 2005d. Physospermopsis H.Wolff. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:31-33.
[30] Pimenov MG. 2017. Updated checklist of Chinese Umbelliferae:Nomenclature, synonymy, typification, distribution. Turczaninowia 20(2):106-239.
[31] Pimenov MG, Kljuykov EV. 1999. New nomenclatural combinations for Chinese Umbelliferae. Feddes Repertorium 110:481-491.
[32] Pimenov MG, Kljuykov EV. 2000. Taxonomic revision of Pleurospermum Hoffm. and related genera of Umbelliferae. II:The genera Pleurospermum, Pterocyclus, Trachydium, Keraymonia, Pseudotrachydium, Aulacospermum, and Hymenolaena. Feddes Repertorium 111:517-534.
[33] Pimenov MG, Kljuykov EV. 2004. Hymenidium (Umbelliferae) in China and India:The new species, a new combination and some corrections. Botanicheskii Zhurnal 89:1652-1665.
[34] Pimenov MG, Kljuykov EV. 2006. Generic disposition of Vicatia bipinnata in Melanosciadium and a new species (Umbelliferae). Feddes Repertorium 117(7-8):471-472.
[35] Pimenov MG, Kljuykov EV, Ostroumova TA. 2008 Reduction of Notopterygium to Hansenia (Umbelliferae). Willdenowia 38:155-172.
[36] Pimenov MG, Leonov MV. 1993. The Genera of the Umbelliferae:A Nomenclator. London:Royal Botanic Gardens.
[37] Posada D. 2008. jModelTest:Phylogenetic model averaging. Molecular Biology and Evolution 25:1253-1256.
[38] Pu GZ, Liu QX. 2005. Comparative anatomical study on the genus Physospermopsis fruit from China and its systematic significance. Journal of Plant Resources and Environment 14:l-6.
[39] Pu FD, Watson MF. 2005. Pimpinella L. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:93-104.
[40] Pu FD, Watson MF, Holmes-Smith I. 2005. Sinocarum H. Wolff ex R.H.Shan & F.T.Pu. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:82-85.
[41] Ronquist F, Huelsenbeck JP. 2003. MrBayes 3:Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
[42] Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2:Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61:539-542.
[43] Saslis-Lagoudakis CH, Savolainen V, Williamson EM, Forest F, Wagstaff SJ, Baral SR, Watson MF, Pendry CA, Hawkins JA. 2012. Phylogenies reveal predictive power of traditional medicine in bioprospecting. Proceedings of the National Academy of Sciences of the United States of America 109(39):15835-15840.
[44] Shan RH, Pu FD. 1989. New Taxa of the Chinese Umbelliferae (3). Acta Phytotaxonomica Sinica 27(1):62-67.
[45] Shan RH., Sheh ML. 1979. Pleurospermum Hoffm. In:Flora Reipublicae Popularis Sinicae Editorial Committee eds. Flora Reipublicae Popularis Sinicae. Beijing:Science Press. 55(1):133-184.
[46] Shan RH, Sheh ML. 1985a. Pimpinella L. In:Flora Reipublicae Popularis Sinicae Editorial Committee eds. Flora Reipublicae Popularis Sinicae. Beijing:Science Press. 55(2):67-113.
[47] Shan RH, Sheh ML. 1985b. Sinocarum Wolff ex R.H.Shan & F.T.Pu. In:Flora Reipublicae Popularis Sinicae Editorial Committee eds. Flora Reipublicae Popularis Sinicae. Beijing:Science Press. 55(2):30-38.
[48] Shan RH, Sheh ML, Yuan CQ, Wang TZ, Pu FD, Zhang HZ. 1980. New taxa of the Umbelliferae from Xizang (Tibet). Acta Phytotaxonomica Sinica 18(3):374-379.
[49] Sheh, M.L., Pu, F.D., Pan, Z.H., et al., 2005. Apiaceae. In:Flora of China Editorial Committee Eds. Flora of China. Beijing:Science Press, 14. Missouri Botanical Garden Press, St.Louis, pp. 1-205.
[50] Sheh ML, Watson MF. 2005. Haplosphaera Hand.-Mazz. In:Flora of China Editorial Committee eds. Flora of China. Beijing:Science Press; St.Louis:Missouri Botanical Garden Press. 14:37-38.
[51] Stamatakis A. 2014. RAxML version 8:A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.
[52] Tan JB, Jia SB, He XJ, Ma XG. 2020. Accommodating Haplosphaera in Hansenia (Apiaceae) based on morphological and molecular evidence. Phytotaxa 464(3):207-216.
[53] Tan JB, Wang ZX, Xie DF, He XJ. 2015. Pimpinella rhomboidea var. tenuiloba is a synonym of Melanosciadium bipinnatum (Apiaceae). Nordic Journal of Botany 33(6):659-661.
[54] Wang HC, Zhou XM, Sun H, Wang YH. 2013. Acronema crassifolium sp. nov. (Apiaceae), a distinct new species from Yunnan, southwest China. Phytotaxa 87(3):39-44.
[55] Wang ZX, Downie SR, Tan JB, Liao CY, Yu Y, He XJ. 2014. Molecular phylogenetics of Pimpinella and allied genera (Apiaceae), with emphasis on Chinese native species, inferred from nrDNA ITS and cpDNA intron sequence data. Nordic Journal of Botany 32:642-657.
[56] Wen J, Xie DF, Price M, Ren T, Deng YQ, Gui LJ, Guo XL, He XJ. 2021. Backbone phylogeny and evolution of Apioideae (Apiaceae):New insights from phylogenomic analyses of plastome data. Molecular Phylogenetics and Evolution 161:107183.
[57] Wen J, Zimmer EA. 1996. Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae):inferences from ITS sequences of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 6:167-177.
[58] White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In:Innis MA, Gelfand DH, Sninsky JJ, White TJ eds. PCR Protocols:A Guide to Methods and Applications. San Diego:Academic Press. 315-322.
[59] Wolff H. 1910. Umbelliferae-Apioideae-Bupleurum, Trinia et reliquae Ammineae heteroclitae. In:Engler A ed. Das Pflanzenreich IV. Berlin:Wilhelm Engelmann. 43:1-214.
[60] Wolff H. 1927. Umbelliferae-Apioideae-Ammineae-Carinae, Ammineae-novemjugatae et genuinae. In:Engler A ed. Das Pflanzenreich IV. Berlin:Wilhelm Engelmann. 90:1-398.
[61] Wolff H. 1929. Umbelliferae Asiatiae novae relictae. II. Repertorium specierum novarum regni vegetabilis 27:179-192.
[62] Wolff H. 1930. Umbelliferae asiaticae novae relictae. III. Repertorium specierum novarum regni vegetabilis 27:301-335.
[63] Xiao YP, Guo XL, Price M, Gou W, Zhou SD, He XJ. 2021. New insights into the phylogeny of Sinocarum (Apiaceae, Apioideae) based on morphological and molecular data. PhytoKeys 175:13-32.
[64] Xu XR, Guo XL, Price M, He XJ, Zhou SD. 2021. New insights into the phylogeny and taxonomy of Chinese Physospermopsis (Apiaceae). PhytoKeys 175:67-78.
[65] Zhou J, Gao YZ, Wei J, Liu ZW, Downie SR. 2020. Molecular phylogenetics of Ligusticum (Apiaceae) based on nrDNA ITS sequences:Rampant polyphyly, placement of the Chinese endemic species, and a much-reduced circumscription of the genus. International Journal of Plant Science 181(3):306-323.
[66] Zhou J, Gong X, Downie SR, Peng H. 2009. Towards a more robust molecular phylogeny of Chinese Apiaceae subfamily Apioideae:additional evidence from nrDNA ITS and cpDNA intron (rpl16 and rps16) sequences. Molecular Phylogenetics and Evolution 53:56-68.
[67] Zhou J, Guo MJ, Liu ZW. 2021. Advances in the study of systematics of "East-Asia Clade" in Apiaceae. Guihaia 41(1):21-30.
[68] Zhou J, Peng H, Downie SR, Liu ZW, Gong X. 2008. A molecular phylogeny of Chinese Apiaceae subfamily Apioideae inferred from nuclear ribosomal DNA internal transcribed spacer sequences. Taxon 57:402-416.