Plastid phylogenomics and biogeography of the medicinal plant lineage Hyoscyameae (Solanaceae)

doi:10.1016/j.pld.2021.01.005

Abstract

Abstract: The cosmopolitan family Solanaceae, which originated and first diversified in South America, is economically important. The tribe Hyoscyameae is one of the three clades in Solanaceae that occurs outside of the New World; Hyoscyameae genera are distributed mainly in Europe and Asia, and have centers of species diversity in the Qinghai-Tibet Plateau and adjacent regions. Although many phylogenetic studies have focused on Solanaceae, the phylogenetic relationships within the tribe Hyoscyameae and its biogeographic history remain obscure. In this study, we reconstructed the phylogeny of Hyoscyameae based on whole chloroplast genome data, and estimated lineage divergence times according to the newly reported fruit fossil from the Eocene Patagonia, Physalis infinemundi, the earliest known fossil of Solanaceae. We reconstructed a robust phylogeny of Hyoscyameae that reveals the berry fruit-type Atropa is sister to the six capsule-bearing genera (Hyoscyameae sensu stricto), Atropanthe is sister to the clade (Scopolia, Physochlaina, Przewalskia), and together they are sister to the robustly supported Anisoduse-Hyoscyamus clade. The stem age of Hyoscyameae was inferred to be in the Eocene (47.11 Ma, 95% HPD:36.75-57.86 Ma), and the crown ages of Hyoscyameae sensu stricto were estimated as the early Miocene (22.52 Ma, 95% HPD:15.19-30.53 Ma), which shows a close correlation with the rapid uplift of the Qinghai-Tibet Plateau at the Paleogene/Neogene boundary. Our results provide insights into the phylogenetic relationships and the history of the biogeographic diversification of the tribe Hyoscyameae, as well as plant diversification on the Qinghai-Tibet Plateau.

Key words: Biogeography, Hyoscyameae, Plastid phylogenomics, Qinghai-Tibet Plateau, Rapid radiation, Solanaceae

Feng-Wei Lei, Ling Tong, Yi-Xuan Zhu, Xian-Yun Mu, Tie-Yao Tu, Jun Wen. Plastid phylogenomics and biogeography of the medicinal plant lineage Hyoscyameae (Solanaceae)[J]. Plant Diversity, 2021, 43(03): 192-197.

References

Brochmann, C., Brysting, A.K., Alsos, I.G., et al., 2004. Polyploidy in arctic plants. Biol. J. Linn. Soc. 82, 521-536. https://doi.org/10.1111/j.1095-8312.2004.00337.x.
Castresana, J., 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. https://doi.org/10.1093/oxfordjournals.molbev.a026334.
D'Arcy, W.G., 1991. The Solanaceae since 1976, with a review of its biogeography. In:Hawkes, J.G., Lester, R.N., Nee, M., Estrada-Ramos, N. (Eds.), Solanaceae III:Taxonomy, Chemistry, Evolution. Royal Botanic Garden, Kew, London.
D'Arcy, W.G., Zhang, Z.Y., 1992. Notes on the Solanaceae of China and neighboring areas. Novon 2, 124-128. https://doi.org/10.2307/3391672.
Darriba, D., Taboada, G.L., Doallo, R., et al., 2012. JModelTest 2:more models, new heuristics and parallel computing. Nat. Methods 9, 772. https://doi.org/10.1038/nmeth.2109.
Deanna, R., Larter, M.D., Barboza, G.E., et al., 2019. Repeated evolution of a morphological novelty:a phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae). Am. J. Bot. 106, 270-279. https://doi.org/10.1002/ajb2.1242.
Deng, T., Wang, X.M., Wu, F.X., et al., 2019. Review:implications of vertebrate fossils for paleo-elevations of the Tibetan Plateau. Global Planet. Change 174, 58-69.https://doi.org/10.1016/j.gloplacha.2019.01.005.
Dillon, M.O., Tu, T.Y., Xie, L., et al., 2009. Biogeographic diversification in Nolana(Solanaceae), a ubiquitous member of the atacama and Peruvian deserts along the western coast of South America. J. Syst. Evol. 47, 457-476. https://doi.org/10.1111/j.1759-6831.2009.00040.x.
Dupin, J., Matzke, N.J., Särkinen, T., et al., 2017. Bayesian estimation of the global biogeographical history of the Solanaceae. J. Biogeogr. 44, 887-899. https://doi.org/10.1111/jbi.12898.
Ebersbach, J., Muellner-Riehl, A.N., Michalak, I., et al., 2017. In and out of the Qinghai-Tibet Plateau:divergence time estimation and historical biogeography of the large arctic-alpine genus Saxifraga L. J. Biogeogr. 44, 900-910. https://doi.org/10.1111/jbi.12899.
Favre, A., Paeckert, M., Pauls, S.U., et al., 2015. The role of the uplift of the QinghaiTibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. 90, 236-253.https://doi.org/10.1111/brv.12107.
Favre, A., Michalak, I., Chen, C., et al., 2016. Out-of-Tibet:the spatio-temporal evolution of Gentiana (Gentianaceae). J. Biogeogr. 43, 1967-1978. https://doi.org/10.1111/jbi.12840.
Gandini, C.L., Garcia, L.E., Abbona, C.C., et al., 2019. The complete organelle genomes of Physochlaina orientalis:insights into short sequence repeats across seed plant mitochondrial genomes. Mol. Phylogenet. Evol. 137, 274-284. https://doi.org/10.1016/j.ympev.2019.05.012.
Gemeinholzer, B., Wink, M., 2001. Solanaceae:occurrence of secondary compounds versus molecular phylogeny. In:van den Berg, R.G., Barendse, G.W.M., van der Weerden, G.M., Mariani, C. (Eds.), Solanaceae V:Advances in Taxonomy and Utilization. Nijmegen University Press, Nijmegen, pp. 165-177.
Guo, C., Guo, Z.H., Li, D.Z., 2019. Phylogenomic analyses reveal intractable evolutionary history of a temperate bamboo genus (Poaceae:bambusoideae). Plant Divers. 41, 213-219. https://doi.org/10.1016/j.pld.2019.05.003.
Hoang, D.T., Chernomor, O., von Haeseler, A., et al., 2018. UFBoot2:improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518-522. https://doi.org/10.1093/molbev/msx281.
Huang, J., Yang, L.Q., Yu, Y., et al., 2018. Molecular phylogenetics and historical biogeography of the tribe Lilieae (Liliaceae):bi-directional dispersal between biodiversity hotspots in Eurasia. Ann. Bot. 122, 1245-1262. https://doi.org/10.1093/aob/mcy138.
Hunziker, A., 2001. Genera Solanacearum:the Genera of Solanaceae Illustrated, Arranged According to a New System. ARG Gantner Verlag KG, Ruggell.
Jia, D.R., Abbott, R.J., Liu, T.L., et al., 2012. Out of the Qinghai-Tibet Plateau:evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophae rhamnoides (Elaeagnaceae). New Phytol. 194, 1123-1133. https://doi.org/10.1111/j.1469-8137.2012.04115.x.
Katoh, K., Rozewicki, J., Yamada, K.D., 2019. MAFFT online service:multiple sequence alignment, interactive sequence choice and visualization. Briefings Bioinf. 20, 1160-1166. https://doi.org/10.1093/bib/bbx108.
Lu, A.M., Zhang, Z.Y., 1986. Studies of the subtribe hyoscyaminae in China. In:D'Arcy, W.G. (Ed.), Solanaceae:Biology and Systematics. Columbia University Press, New York, pp. 56-78. Madlung, A., 2013. Polyploidy and its effect on evolutionary success:old questions revisited with new tools. Heredity 110, 99-104. https://doi.org/10.1038/hdy.2012.79.
Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In:Gateway Computing Environments Workshop (GCE) (New Orleans, LA).
Mu, X.Y., Tong, L., Sun, M., et al., 2020. Phylogeny and divergence time estimation of the walnut family (Juglandaceae) based on nuclear RAD-Seq and chloroplast genome data. Mol. Phylogenet. Evol. 147, 106802. https://doi.org/10.1016/j.ympev.2020.106802.
Nguyen, L., Schmidt, H.A., von Haeseler, A., et al., 2015. IQ-TREE:a fast and effective stochastic algorithm for estimating Maximum-Likelihood phylogenies. Mol. Biol. Evol. 32, 268-274. https://doi.org/10.1093/molbev/msu300.
Olmstead, R.G., Bohs, L., 2007. A summary of molecular systematic research in Solanaceae:1982-2006. In:Spooner, D.M., Bohs, L., Govannoni, J., Olmstead, R.G., Shibata, D. (Eds.), VI International Solanaceae Conference:Genomics Meets Biodiversity, vol. 745. ISHS Acta Horticulturae, Leuven, pp. 255-268. https://doi.org/10.17660/ActaHortic.2007.745.11.
Olmstead, R.G., Bohs, L., Migid, H.A., et al., 2008. A molecular phylogeny of the Solanaceae. Taxon 57, 1159-1181. https://doi.org/10.1002/tax.574010.
Olmstead, R.G., 2013. Phylogeny and biogeography in Solanaceae, Verbenaceae and Bignoniaceae:a comparison of continental and intercontinental diversification patterns. Bot. J. Linn. Soc. 171, 80-102. https://doi.org/10.1111/j.1095-8339.2012.01306.x.
Rambaut, A., Drummond, A.J., Xie, D., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Sys. Biol. 67, 901-904. https://doi.org/10.1093/sysbio/syy032.
Ramsey, J., 2011. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl. Acad. Sci. U.S.A. 108, 7096-7101. https://doi.org/10.1073/pnas.101 6631108.
Rana, S.K., Luo, D., Rana, H.K., et al., 2021. Geoclimatic factors influence the population genetic connectivity of Incarvillea arguta (Bignoniaceae) in the Himalaya Hengduan Mountains biodiversity hotspot. J. Syst. Evol. 59, 151-168. https://doi.org/10.1111/jse.12521.
Ronquist, F., Teslenko, M., van der Mark, P., et al., 2012. MrBayes 3.2:efficient Bayesian phylogenetic inference and model choice across a large model space.Syst. Biol. 61, 539-542. https://doi.org/10.1093/sysbio/sys029.
Sanchez-Puerta, M.V., Abbona, C.C., 2014. The chloroplast genome of Hyoscyamus niger and a phylogenetic study of the tribe Hyoscyameae (Solanaceae). PLoS One 9, e98353. https://doi.org/10.1371/journal.pone.0098353.
Särkinen, T., Bohs, L., Olmstead, R.G., et al., 2013. A phylogenetic framework for evolutionary study of the nightshades (Solanaceae):a dated 1000-tip tree. BMC Evol. Biol. 13, 214. https://doi.org/10.1186/1471-2148-13-214.
Särkinen, T., Kottner, S., Stuppy, W., et al., 2018. A new commelinid monocot seed fossil from the early Eocene previously identified as Solanaceae. Am. J. Bot. 105, 95-107. https://doi.org/10.1002/ajb2.1009.
Stebbins, G.L., 1971. Chromosome Evolution in Higher Plants. Edward Arnold Ltd, London.
Su, T., Farnsworth, A., Spicer, R.A., et al., 2019. No high Tibetan plateau until the neogene. Sci. Adv. 5, v2189. https://doi.org/10.1126/sciadv.aav2189.
Tang, H., Liu, J., Wu, F.X., et al., 2019. Extinct genus Lagokarpos reveals a biogeographic connection between Tibet and other regions in the Northern Hemisphere during the Paleogene. J. Systemat. Evol. 57, 670-677. https://doi.org/10.1111/jse.12505.
Tetenyi, P., 1987. A chemotaxonomic classification of the Solanaceae. Ann. Mo. Bot. Gard. 74, 600-608. https://doi.org/10.2307/2399328.
Tong, L., Zhu, Y.X., Lei, F.W., et al., 2019. The complete chloroplast genome of Physochlaina physaloides (Solanaceae), an important medicinal plant. Mitochond. DNA B. Res. 4, 3427-3428. https://doi.org/10.1080/23802359.2019.1674730.
Tu, T.Y., Sun, H., Gu, Z.J., et al., 2005. Cytological studies on the Sino-Himalayan endemic Anisodus and four related genera from the tribe Hyoscyameae (Solanaceae) and their systematic and evolutionary implications. Bot. J. Linn. Soc. 147, 457-468. https://doi.org/10.1111/j.1095-8339.2005.00384.x.
Tu, T.Y., Volis, S., Dillon, M.O., et al., 2010. Dispersals of Hyoscyameae and mandragoreae (Solanaceae) from the new world to Eurasia in the early Miocene and their biogeographic diversification within Eurasia. Mol. Phylogenet. Evol. 57, 1226-1237. https://doi.org/10.1016/j.ympev.2010.09.007.
Van de Peer, Y., Mizrachi, E., Marchal, K., 2017. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424. https://doi.org/10.1038/nrg.2017.26.
Wen, J., Zhang, J.Q., Nie, Z.L., et al., 2014. Evolutionary diversifications of plants on the Qinghai-Tibetan plateau. Front. Genet. 5, 4. https://doi.org/10.3389/fgene.2014.00004.
Wilf, P., Carvalho, M., Gandolfo, M., et al., 2017. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355, 71-75.https://doi.org/10.1126/science.aag2737.
Xia, X.H., 2018. DAMBE7:new and improved tools for data analysis in molecular biology and evolution. Mol. Biol. Evol. 35, 1550-1552. https://doi.org/10.1093/molbev/msy073.
Yang, D.Z., 2002. Tribe Hyoscyameae of the Solanaceae. Structure, Differentiation and Phylogenetic Relationship. Institute of Botany, the Chinese Academy of Sciences, Beijing. PhD thesis.
Yuan,Y.W.,Zhang, Z.Y.,Chen, Z.D., etal.,2006. Tracking ancient polyploids:a retroposon insertion reveals an extinct diploid ancestor in the polyploid origin of belladonna.Mol. Biol. Evol. 23, 2263-2267. https://doi.org/10.1093/molbev/msl099.
Zhang, J.Q., Meng, S.Y., Allen, G.A., et al., 2014. Rapid radiation and dispersal out of the Qinghai-Tibetan Plateau of an alpine plant lineage Rhodiola (Crassulaceae). Mol.Phylogenet. Evol. 77, 147-158. https://doi.org/10.1016/j.ympev.2014.04.013.

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