Articles

Plastome phylogenomics of the East Asian endemic genus Dobinea

  • 包新康 ,
  • 杨增武 ,
  • 赵伟 ,
  • 石存海 ,
  • 杨永伟 ,
  • 王亮 ,
  • Changkun Liu ,
  • Jin Yang ,
  • Lei Jin ,
  • Shuying Wang ,
  • Zhenyan Yang ,
  • Yunheng Ji
展开
  • a CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China;
    b School of Life Science, Yunnan University, Kunming, 650091, China;
    c School of Traditional Chinese Medicine, Guangdong Pharmaceutical University, Guangzhou, 510006, China

收稿日期: 2020-02-14

  修回日期: 2020-05-14

  网络出版日期: 2021-03-25

基金资助

This study was financially supported by the Major program of National Natural Science Foundation of China (31590823). We are grateful to Drs. Zhiling Dao and Ting Zhang for providing photos of Dobinea species.

Plastome phylogenomics of the East Asian endemic genus Dobinea

  • Bao Xinkang ,
  • Yang Zengwu ,
  • Zhao Wei ,
  • Shi Cunhai ,
  • Yang Yongwei ,
  • Wang Liang ,
  • Changkun Liu ,
  • Jin Yang ,
  • Lei Jin ,
  • Shuying Wang ,
  • Zhenyan Yang ,
  • Yunheng Ji
Expand
  • a CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China;
    b School of Life Science, Yunnan University, Kunming, 650091, China;
    c School of Traditional Chinese Medicine, Guangdong Pharmaceutical University, Guangzhou, 510006, China

Received date: 2020-02-14

  Revised date: 2020-05-14

  Online published: 2021-03-25

Supported by

This study was financially supported by the Major program of National Natural Science Foundation of China (31590823). We are grateful to Drs. Zhiling Dao and Ting Zhang for providing photos of Dobinea species.

摘要

Dobinea is a dioecious genus endemic to East Asia that consists of two extant species: Dobinea delavayi and Dobinea vulgaris. Although the genus is morphologically distinct, its phylogenetic position remains controversial. In this study, we investigated the phylogenetic relationships between Dobinea and related taxa by sequencing the whole plastome DNA sequences for both extant species of Dobinea and comparing them to published plastomes within Sapindales. The complete plastomes of D. vulgaris and D. delavayi were 160,683 and 160, 154 base pairs (bp) in length, including a pair of inverted repeat regions (IRs, 26,889 and 26,759 bp) divided by the large single-copy region (LSC, 87,962 and 87,555 bp) and small single-copy region (SSC, 18,943 and 19,081 bp), and identically encoded 113 unique genes (79 protein-coding genes, 30 tRNAs, and 4 rRNA genes). Plastid phylogenomic analyses showed that Dobinea was a well-supported monophyletic unit and sister to the clade including tribes Anacardieae and Rhoideae, which suggests that Dobinea is a member of Anacardiaceae. In addition, molecular dating inferred D. delavayi and D. vulgaris diverged approximately 10.76 Ma, suggesting the divergence between these two species may have been driven by the intensification of the Asian summer monsoon and the establishment of distinct monsoon regimes in East Asia.

本文引用格式

包新康 , 杨增武 , 赵伟 , 石存海 , 杨永伟 , 王亮 , Changkun Liu , Jin Yang , Lei Jin , Shuying Wang , Zhenyan Yang , Yunheng Ji . Plastome phylogenomics of the East Asian endemic genus Dobinea[J]. Plant Diversity, 2021 , 43(01) : 35 -42 . DOI: 10.1016/j.pld.2020.05.002

Abstract

Dobinea is a dioecious genus endemic to East Asia that consists of two extant species: Dobinea delavayi and Dobinea vulgaris. Although the genus is morphologically distinct, its phylogenetic position remains controversial. In this study, we investigated the phylogenetic relationships between Dobinea and related taxa by sequencing the whole plastome DNA sequences for both extant species of Dobinea and comparing them to published plastomes within Sapindales. The complete plastomes of D. vulgaris and D. delavayi were 160,683 and 160, 154 base pairs (bp) in length, including a pair of inverted repeat regions (IRs, 26,889 and 26,759 bp) divided by the large single-copy region (LSC, 87,962 and 87,555 bp) and small single-copy region (SSC, 18,943 and 19,081 bp), and identically encoded 113 unique genes (79 protein-coding genes, 30 tRNAs, and 4 rRNA genes). Plastid phylogenomic analyses showed that Dobinea was a well-supported monophyletic unit and sister to the clade including tribes Anacardieae and Rhoideae, which suggests that Dobinea is a member of Anacardiaceae. In addition, molecular dating inferred D. delavayi and D. vulgaris diverged approximately 10.76 Ma, suggesting the divergence between these two species may have been driven by the intensification of the Asian summer monsoon and the establishment of distinct monsoon regimes in East Asia.

参考文献

An, Z.S., Kutzbach, J.E., Prell, W.L., Porter, S.C., 2001. Evolution of Asian monsoons and phased uplift of the HimalayaeTibetan plateau since Late Miocene times.Nature 411, 62-66.
Angiosperm phylogeny group, 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG IV. Bot. J. Linn.Soc. 181, 1-20.
Appelhans, M.S., Krohm, S., Manafzadeh, S., Wen, J., 2016. Phylogenetic placement of Psilopeganum, a rare monotypic genus of Rutaceae (the citrus family) endemic to China. J. Syst. Evol. 54 (5), 535-544.
Attigala, L., Wysocki, W.P., Duvall, M.R., Clark, L.G., 2016. Phylogetic estimation and morphorlogical evolution of Arundinarieae (Bambusoideae:poaceae) based on plastome phylogenomic analysis. Mol. Phylogenet. Evol. 101, 111-121.
Axelrod, D.I., Al-Shehbaz, I., Raven, P.H., 1998. History of the modern flora of China.In:Zhang, A.L., Wu, S.G. (Eds.), Floristic Characteristics and Diversity of East Asian Plants. China Higher Education Press, Beijing, pp. 43-55.
Bell, C.D., Soltis, D.E., Soltis, P.S., 2010. The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296-1303.
Chen, Y.S., Deng, T., Zhou, Z., Sun, H., 2018. Is the East Asian flora ancient or not? Natl. Sci. Rev. 5, 920-932.
Clayton, J.W., Fernando, E.S., Soltis, P.S., Soltis, D.E., 2007. Molecular phylogeny of the tree-of-heaven family (Simaroubaceae) based on chloroplast and nuclear markers. Int. J. Plant Sci. 168 (9), 1325-1339.
Deng, Y., Gao, C., Xia, N., Peng, H., 2016. Wuacanthus (Acanthaceae), a new Chinese endemic genus segregated from Justicia (Acanthaceae). Plant Divers. 38 (6), 312-321.
Dierckxsens, N., Mardulyn, P., Smits, G., 2017. NOVOPlasty:de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45, e18.
Don, D., 1825. Prodromus florae Nepalensis etc. J. Gale. Londini. 249.
Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
Drummond, A.J., Rambaut, A., 2007. BEAST:Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.
Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
Engler, A., 1892. Anacardiaceae. In:Engler, A., Prantl, K. (Eds.), Die Naturlichen Pflanzenfamilien, vol. 3. Engelmann, Leipzig, pp. 137-178, 5.
Estrada-Ruiz, E., Martinez-Cabrera, H.I., Cevallos-Ferriz, S.R.S., 2010. Upper cretaceous woods from the olmos formation (late campanian-early maastrichtian), coahuila, Mexico. Am. J. Bot. 97, 1179-1194.
Forman, L.L., 1973. Podoaceae. In:Airy Shaw, H.K. (Ed.), A Dictionary of the Flowering Plants and Ferns, eighth ed. Cambridge University Press, Cambridge, p. 923.
Frazer, K.A., Pachter, L., Poliakov, A., et al., 2004. VISTA:computational tools for comparative genomics. Nucleic Acids Res. 32, W273-W279.
Gadek, P.A., Fernando, E.S., Quinn, C.J., et al., 1996. Sapindales:molecular delimitation and infraordinal groups. Am. J. Bot. 83 (6), 802-811.
Hu, Y., Yan, J., Feng, X., et al., 2017. Characterization of the complete chloroplast genome of wheel wingnut (Cyclocarya paliurus), an endemic in China. Conserv.Genet. Resour. 9 (2), 273-275.
Huang, Y., Li, X., Yang, Z., et al., 2016. Analysis of complete chloroplast genome sequences improves phylogenetic resolution in Paris (Melanthiaceae). Front.Plant Sci. 7, 1797.
Hutchinson, J., 1973. The Families of Flowering Plants. Clarendon Press, Oxford.
Jacques, F.M.B., Guo, S.X., Su, T., et al., 2011. Quantitative reconstruction of the Late Miocene monsoon climates of southwest China:a case study of the Lincang flora from Yunnan Province. Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 318-327.
Jansen, R.K., Cai, Z., Raubeson, L.A., et al., 2007. Analysis of 81 genes from 64 chloroplast genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc. Natl. Acad. Sci. U.S.A. 104, 19369-19374.
Ji, Y., Yang, L., Chase, M.W., et al., 2019. Plastome phylogenomics, biogeography, and clade diversification of Paris (Melanthiaceae). BMC Plant Biol. 19 (1), 1-14.
Jin, J.J., Yu, W.B., Yang, J.B., et al., 2018. GetOrganelle:a simple and fast pipeline for de novo assembly of a complete circular chloroplast genome using genome skimming data bioRxiv 256479.
Kane, N., Sveinsson, S., Dempewolf, H., et al., 2012. Ultra-barcoding in cacao (Theobroma spp.; Malvaceae) using whole chloroplast genomes and nuclear ribosomal DNA. Am. J. Bot. 99, 320-329.
Katoh, K., Misawa, K., Kuma, K.I., Miyata, T., 2002. MAFFT:a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066.
Kearse, M., Moir, R., Wilson, A., et al., 2012. Geneious Basic:an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649.
Li, F.J., Rousseau, D.D., Wu, N.Q., et al., 2008. Late Neogene evolution of the East Asian monsoon revealed by terrestrial mollusk record in western Chinese loess plateau:from winter to summer dominated subregime. Earth Planet Sci. Lett. 274, 439-447.
Lin, H.Y., Hao, Y.J., Li, J.H., et al., 2019. Phylogenomic conflict resulting from ancient introgression following species diversification in Stewartia s.l. (Theaceae). Mol.Phylogenet. Evol. 135, 1-11.
Lin, N., Moore, M.J., Deng, T., et al., 2018. Complete plastome sequencing from Toona(Meliaceae) and phylogenomic analyses within Sapindales. Appl. Plant Sci. 6 (4), e1040.
Lohse, M., Drechsel, O., Bock, R., 2007. OrganellarGenomeDRAW (OGDRAW):a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr. Genet. 52, 267-274.
Lu, L.M., Mao, L.F., Yang, T., et al., 2018. Evolutionary history of the angiosperm flora of China. Nature 554 (7691), 234-238.
Ma, X., Wang, Z., Tian, B., Sun, H., 2019. Phylogeographic analyses of the East Asian endemic genus Prinsepia and the role of the East Asian monsoon system in shaping a north-south divergence pattern in China. Front. Genet. 10, 128.
Ma, X.G., Sun, W.G., Zhu, W.D., Sun, H., 2017. Resolving the phylogenetic relationships and evolutionary history of the East Asian endemic genus Rodgersia(Saxifragaceae) using multilocus data. Perspect. Plant Ecol. 25, 20-28.
Manchester, S.R., Chen, Z.D., Lu, A.M., Uemura, K., 2009. Eastern Asian endemic seed plant genera and their paleogeographic history throughout the northern hemisphere. J. Syst. Evol. 47 (1), 1-42.
Min, T.L., Barfod, A., 2008. Dobinea. In:Wu, Z.Y., Raven, P.H. (Eds.), Flora of China, vol. 11. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, p. 357.
Moore, M.J., Bell, C.D., Soltis, P.S., Soltis, D.E., 2007. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc. Natl. Acad. Sci. Unit. States Am. 104, 19363-19368.
Moore, M.J., Soltis, P.S., Bell, C.D., et al., 2010. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc. Natl. Acad. Sci.U.S.A. 107, 4623-4628.
Morot, L., 1889. Sur les affinités anatomique du genre Podoon. J. Bot. Paris 3, 388-390.
Muellner, A.N., Samuel, R., Johnson, S.A., et al., 2003. Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences. Am. J. Bot. 90 (3), 471-480.
Muellner, A.N., Vassiliades, D.D., Renner, S.S., 2007. Placing Biebersteiniaceae, a herbaceous clade of Sapindales, in a temporal and geographic context. Plant Systemat. Evol. 266 (3-4), 233-252.
Muellner-Riehl, A.N., Weeks, A., Clayton, J.W., et al., 2016. Molecular phylogenetics and molecular clock dating of Sapindales based on plastid rbcL, atpB and trnLtrnF DNA sequences. Taxon 65 (5), 1019-1036.
Nock, C.J., Waters, D.L.E., Edwards, M.A., et al., 2011. Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol. J. 9, 328-333.
Pan, Y.Z., Gong, X., Yang, Y., 2008. Phylogenetic position of the genus Dobinea:evidence from nucleotide sequences of the chloroplast gene rbcL and the nuclear ribosomal ITS region. J. Syst. Evol. 46 (4), 586-594.
Parks, M., Cronn, R., Liston, A., 2009. Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes.BMC Biol. 7, 1.
Posada, D., Buckley, T.R., 2004. Model selection and model averaging in phylogenetics:advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53, 793-808.
Radlkofer, L.A., 1888. Ueber die Versetzung der Gattung Dobinea von den Acerineen zu den Anacardiaceen. S. B. Bayer. Akad. Wiss. 18, 385-395.
Radlkofer, L.A., 1890. Ueber die Gliederung der Familie der Sapindaceen. Sitz. Ber.Akad. Muenchen 20, 105-319.
Rambaut, A., Drummond, A., 2015. FigTree, version 1.4.2. Available from:http://tree.bio.ed.ac.uk/software/figtree/. (Accessed 6 November 2019).
Rambaut, A., Drummond, A., Suchard, M., 2014. Tracer, version 1.6. Available from:http://tree.bio.ed.ac.uk/software/tracer/. (Accessed 6 November 2019).
Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3:Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
Ruhsam, M., Rai, H.S., Mathews, S., et al., 2015. Does complete plastid genome sequencing improve species discrimination and phylogenetic resolution in Araucaria? Mol. Ecol. Resour. 15 (5), 1067-1078.
Santosh, M., 2011. History of supercontinents and its relation to the origin of Japanese islands. J. Geodyn. 120, 100-114.
Schattner, P., Brooks, A.N., Lowe, T.M., 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686-W689.
Singh, V.N., Sinha, B.K., Phukan, S., Singh, B., 2011. Dobinea Buchanon-Hamilton ex D. Don-a new generic record for Meghalaya and Nagaland, India. Pleione 5 (1), 198-200.
Stamatakis, A., 2006. RAxML-VI-HPC:maximum likelihood-based phylogenetic analysis with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
Sun, X.J., Wang, P.X., 2005. How old is the Asian monsoon system? Palaeobotanical records from China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 222, 181-222.
Sun, Y., Wang, A., Wan, D., et al., 2012. Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Mol. Phylogenet. Evol. 63 (1), 150-158.
Tonti-Filippini, J., Nevill, P.G., Dixon, K., Small, I., 2017. What can we do with 1000 plastid genomes? Plant J. 90, 808-818.
Wan, S.M., Li, A.C., Clift, P.D., Stut, J.B.W., 2007. Development of the East asian monsoon:mineralogical and sedimentologic records in the northern south China sea since 20 Ma. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 561-582.
Wang, L., Schneider, H., Zhang, X.C., Xiang, Q.P., 2012. The rise of the Himalaya enforced the diversification of SE Asian ferns by altering the monsoon regimes.BMC Plant Biol. 12 (1), 210.
Wang, Y.J., Susanna, A., Von Raab-Straube, E., et al., 2009. Island-like radiation of Saussurea (asteraceae:cardueae) triggered by uplifts of the qinghaieTibetan plateau. Biol. J. Linn. Soc. 97 (4), 893-903.
Wannan, B.S., Quinn, C., 1990. Pericarp structure and generic affinities in the Anacardiaceae. Bot. J. Linn. Soc. 102, 225-252.
Wannan, B.S., Quinn, C., 1991. Floral structure and evolution in the Anacardiaceae.Bot. J. Linn. Soc. 107, 349-385.
Wen, J., Zhang, J.Q., Nie, Z.L., et al., 2014. Evolutionary diversifications of plants on the qinghai-Tibetan plateau. Front. Genet. 5, 4.
Wu, Z.Y., Sun, H., Zhou, Z.K., Peng, H., Li, D.Z., 2005. Origin and differentiation of endemism in the flora of China. Acta Bot. Yunnanica 27 (6), 577-604.
Wyman, S.K., Jansen, R.K., Boore, J.L., 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20, 3252-3255.
Xie, D.F., Yu, Y., Deng, Y.Q., et al., 2018. Comparative analysis of the chloroplast genomes of the Chinese endemic genus Urophysa and their contribution to chloroplast phylogeny and adaptive evolution. Int. J. Mol. Sci. 19 (7), 1847.
Xie, L., Yang, Z.Y., Wen, J., et al., 2014. Biogeographic history of Pistacia (Anacardiaceae), emphasizing the evolution of the Madrean-Tethyan and the eastern Asian-Tethyan disjunctions. Mol. Phylogenet. Evol. 77, 136-146.
Yang, J.B., Tang, M., Li, H.T., et al., 2013. Complete chloroplast genome of the genus Cymbidium:lights into the species identification, phylogenetic implications and population genetic analyses. BMC Evol. Biol. 13, 1.
Yang, L., Yang, Z., Liu, C., et al., 2019. Chloroplast phylogenomic analysis provides insights into the evolution of the largest eukaryotic genome holder, Paris japonica (Melanthiaceae). BMC Plant Biol. 19 (1), 293.
Yang, Y.Y., Meng, Y., Wen, J., et al., 2016. Phylogenetic analyses of Searsia (Anacardiaceae) from eastern Asia and its biogeographic disjunction with its African relatives. South Afr. J. Bot. 106, 129-136.
Yao, Y.F., Bruch, A.A., Mosbrugger, V., Li, C.S., 2011. Quantitative reconstruction of Miocene climate patterns and evolution in southern China based on plant fossils. Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 291-307.
Yi, T., Miller, A.J., Wen, J., 2004. Phylogenetic and biogeographic diversification of Rhus (Anacardiaceae) in the northern hemisphere. Mol. Phylogenet. Evol. 33 (3), 861-879.
Zhang, Q.Q., Ferguson, D.K., Mosbrugger, V., et al., 2012. Vegetation and climatic changes of SW China in response to the uplift of Tibetan Plateau. Palaeogeogr.Palaeoclimatol. Palaeoecol. 363, 23-36.
文章导航

/