New insights into the phylogeny and infrageneric taxonomy of Saussurea based on hybrid capture phylogenomics (Hyb-Seq)

doi:10.1016/j.pld.2024.10.003

Abstract

Abstract: Saussurea is one of the largest and most rapidly evolving genera within the Asteraceae, comprising approximately 520 species from the Northern Hemisphere. A comprehensive infrageneric classification, supported by robust phylogenetic trees and corroborated by morphological and other data, has not yet been published. For the first time, we recovered a well-resolved nuclear phylogeny of Saussurea consisting of four main clades, which was also supported by morphological data. Our analyses show that ancient hybridization is the most likely source of deep cytoplasmic-nuclear conflict in Saussurea, and a phylogeny based on nuclear data is more suitable than one based on chloroplast data for exploring the infrageneric classification of Saussurea. Based on the nuclear phylogeny obtained and morphological characters, we proposed a revised infrageneric taxonomy of Saussurea, which includes four subgenera and 13 sections. Specifically, 1) S. sect. Cincta, S. sect. Gymnocline, S. sect. Lagurostemon, and S. sect. Strictae were moved from S. subg. Saussurea to S. subg. Amphilaena, 2) S. sect. Pseudoeriocoryne was moved from S. subg. Eriocoryne to S. subg. Amphilaena, and 3) S. sect. Laguranthera was moved from S. subg. Saussurea to S. subg. Theodorea.

Key words: Asteraceae, Morphology, Next-generation sequencing, Phylogenomics, Subgenus

Liansheng Xu, Zhuqiu Song, Tian Li, Zichao Jin, Buyun Zhang, Siyi Du, Shuyuan Liao, Xingjie Zhong, Yousheng Chen. New insights into the phylogeny and infrageneric taxonomy of Saussurea based on hybrid capture phylogenomics (Hyb-Seq)[J]. Plant Diversity, 2025, 47(01): 21-33.

References

Andres-Sanchez, S., Galbany-Casals, M., Bergmeier, E., et al., 2014. Systematic significance and evolutionary dynamics of the achene twin hairs in Filago (Asteraceae, Gnaphalieae) and related genera: further evidence of morphological homoplasy. Plant Syst. Evol. 301, 1653-1668. https://doi.org/10.1007/s00606-014-1185-7.
Bankevich, A., Nurk, S., Antipov, D., et al., 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477. https://doi.org/10.1089/cmb.2012.0021.
Borowiec, M.L., 2016. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4, e1660. https://dx.doi.org/10.7287/peerj.preprints.1355v1.
Candolle, A. P. de., 1810. Observations sur les plantes Composees ou syngeneses. Premier memoire. Sur les Composees et les Cinarocephales en general. Ann. Mus. Hist. Nat. 16, 135-158.
Chen, Y.S., 2015. Asteraceae II: Saussurea. In: Hong, D.Y., (Ed.), Flora of Pan-Himalaya. Beijing, pp. 1-315.
Cheon, K.S., Kim, H.J., Han, J.S., et al., 2016. The complete chloroplast genome sequence of Saussurea chabyoungsanica (Asteraceae), an endemic to Korea. Conserv. Genet. Resour. 9, 51-53. https://doi.org/10.1007/s12686-016-0617-9.
Fer, T. & Schmickl, R.E., 2018. HybPhyloMaker: target enrichment data analysis from raw reads to species trees. Evol. Bioinformatics 14, 1176934317742613. https://doi.org/10.1177/1176934317742613.
Folk, R.A., Mandel, J.R., & Freudenstein, JV., 2017. Ancestral gene flow and parallel organellar genome capture result in extreme phylogenomic discord in a lineage of angiosperms. Syst. Biol. 66, 320-337. https://doi.org/10.1093/sysbio/syw083.
Guindon, S., Dufayard, J.F., Lefort, V., et al., 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59: 307-321. https://doi.org/10.1093/sysbio/syq010.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
Hatami, E., Jones, K.E., Kilian, N., 2022. New insights into the relationships within subtribe Scorzonerinae (Cichorieae, Asteraceae) using hybrid capture phylogenomics (Hyb-Seq). Front. Plant Sci. 13, 851716. https://doi.org/10.3389/fpls.2022.851716.
Herrando-Moraira, S., Calleja, J.A., Carnicero-Campmany, P., et al., 2018. Exploring data processing strategies in NGS target enrichment to disentangle radiations in the tribe Cardueae (Compositae). Mol. Phylogenet. Evol. 128, 69-87. https://doi.org/10.1016/j.ympev.2018.07.012.
Herrando-Moraira, S., Calleja, J.A., Galbany-Casals, M., et al., 2019. Nuclear and plastid DNA phylogeny of tribe Cardueae (Compositae) with Hyb-Seq data: A new subtribal classification and a temporal diversification framework. Mol. Phylogenet. Evol. 137, 313-332. https://doi.org/10.1016/j.ympev.2019.05.001.
Herrando-Moraira, S., Calleja, J.A., Chen, Y.S., et al., 2020. Generic boundaries in subtribe Saussureinae (Compositae: Cardueae): Insights from Hyb-Seq data. Taxon 69, 694-714. https://doi.org/10.1002/tax.12314.
Johnson, M.G., Gardner, E.M., Liu, Y., et al., 2016. HybPiper: extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment. Appl. Plant Sci. 4, 1600016. https://doi.org/10.3732/apps.1600016.
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. https://doi.org/10.1093/bioinformatics/bts199.
Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. https://doi.org/10.1093/molbev/mst010.
Kita, Y., Fujikawa, K., Ito, M., et al., 2004. Molecular phylogenetic analyses and systematics of the genus Saussurea and related genera (Asteraceae, Cardueae). Taxon 53, 679-690. https://doi.org/10.2307/4135443.
Li, H., Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324.
Lipschitz, S., 1979. Genus Saussurea DC. (Asteraceae), Leningrad: Nauka.
Mandel, J.R., Dikow, R.B., Funk, V.A., et al., 2014. A target enrichment method for gathering phylogenetic information from hundreds of loci: An example from the Compositae. Appl. Plant Sci. 2, 1300085. https://doi.org/10.3732/apps.1300085.
Mandel, J.R., Dikow, R.B., Siniscalchi, C.M., et al., 2019. A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae. Proc. Natl. Acad. Sci. USA 116, 14083-14088. https://doi.org/10.1016/j.ympev.2011.12.007.
Minh, B.Q., Nguyen, M.A., Haeseler, A.V., 2013. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol., 30, 1188-1195. https://doi.org/10.1093/molbev/mst024.
Minh, B.Q., Schmidt, H.A., Chernomor, O., et al., 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530-1534. https://doi.org/10.1093/molbev/msaa015.
Moore-Pollard, E.R., Jones, D.S., Mandel, J.R., 2024. Compositae-ParaLoss-1272: A complementary sunflower-specific probe set reduces paralogs in phylogenomic analyses of complex systems. Appl. Plant Sci. 12, e11568. https://doi.org/10.1002/aps3.11568.
Price, M.N., Dehal, P.S., Arkin, A.P., 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490. https://doi.org/10.1371/journal.pone.0009490.
Raab-Straube, E. von, 2003. Phylogenetic relationships in Saussurea (Compositae, Cardueae) sensu lato, inferred from morphological, ITS and trnL-trnF sequence data, with a synopsis of Himalaiella gen. nov., Lipschitziella and Frolovia. Willdenowia 33, 379-402. https://doi.org/10.1093/botlinnean/boy081.
Raab-Straube, E. von, 2017. Taxonomic Revision of Saussurea Subgenus Amphilaena (Compositae, Cardueae). Botanic Garden and Botanical Museum, Berlin.
Sayyari, E, Mirarab, S., 2016. Fast coalescent-based computation of local branch support from quartet frequencies. Mol. Biol. Evol. 33, 1654-1668. https://doi.org/10.1093/molbev/msw079.
Shi, Z., Raab-Straube, E. von, 2011. Saussurea group. In: Wu, Z.Y., Raven, P.H., Hong, D.Y. (Eds.), Flora of China. Science Press, Beijing, pp. 54-149.
Siniscalchi, C.M., Loeuille, B., Funk, V.A,. et al., 2019. Phylogenomics yields new insight into relationships within Vernonieae (Asteraceae). Front. in Plant Sci. 10, 1224. https://doi.org/10.3389/fpls.2019.01224.
Smith, S. A., Moore, M. J., Brown, J. W. & Yang, Y., 2015. Analysis of phylogenomic datasets reveals conflict, concordance, and gene duplications with examples from animals and plants. BMC Evol. Biol. 15, 150. https://doi.org/10.1186/s12862-015-0423-0.
Solis-Lemus, C., Ane, C., 2016. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. Plos Genet. 12, e1005896. https://doi.org/10.1371/journal.pgen.1005896.
Solis-Lemus, C., Bastide, P., & Ane, C., 2017. PhyloNetworks: a package for phylogenetic networks. Mol. Biol. Evol. 34, 3292-3298. https://doi.org/10.1093/molbev/msx235.
Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312.-1213. https://doi.org/10.1093/bioinformatics/btu033.
Sukumaran, J., Holder, M.T., 2010. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569-1571. https://doi.org/10.1093/bioinformatics/btq228.
Wang, Y.J., Milnes, R., Susanna, A., et al., 2009. Island-like radiation of Saussurea (Asteraceae: Cardueae) triggered by uplifts of the Qinghai-Tibetan Plateau. Bot. J. Linn. Soc. 97, 893-903. https://doi.org/10.1111/j.1095-8312.2009.01225.x.
Wang, Y.J., Raab-Straube, E. von, Susanna, A., et al., 2013. Shangwua, (Compositae), a new genus from the Qinghai-Tibetan Plateau and Himalayas. Taxon 62, 984-996. https://doi.org/10.12705/625.19.
Xu, L.S., Chen, Y.S., 2021. Phylogeny, origin, and dispersal of Dubyaea (Asteraceae) based on Hyb-Seq data. Mol. Phylogenet. Evol. 164, 107289. https://doi.org/10.1016/j.ympev.2021.107289.
Xu, L.S., Herrando-Moraira, S., Susanna, A., et al., 2019. Phylogeny, origin and dispersal of Saussurea (Asteraceae) based on chloroplast genome data. Mol. Phylogenet. Evol. 141, 106613. https://doi.org/10.1016/j.ympev.2019.106613.
Xu, L.S., Song, Z.Q., Liao, S.Y., et al., 2024. Qineryangia, a new genus from the Hengduan Mountains and new insights into the phylogeny of the subtribe Crepidinae (Cichorieae, Asteraceae). J. Syst. Evol. 13066. https://doi.org/10.1111/jse.13066.
Yu, Y., Blair, C., He, X.J., 2020. RASP 4: Ancestral state reconstruction tool for multiple genes and characters. Mol. Biol. Evol. 37, 604-606. https://doi.org/10.1093/molbev/msz257.
Yuan, Q., Bi, Y.C., Chen, Y.S., 2015. Diplazoptilon (Asteraceae) is merged with Saussurea based on evidence from morphology and molecular systematics. Phytotaxa 236, 53-61. https://doi.org/10.11646/phytotaxa.236.1.4.
Zhang, C., Rabiee, M., Sayyari, E., et al., 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 153. https://doi.org/10.1186/s12859-018-2129-y.
Zhang, C.F., Huang, C.H., Liu, M., et al., 2021a. Phylotranscriptomic insights into Asteraceae diversity, polyploidy, and morphological innovation. J. Integr. Plant Biol. 63, 1273-1293. https://doi.org/10.1111/jipb.13078.
Zhang, X., Landis, J.B., Sun, Y.X., et al., 2021b. Macroevolutionary pattern of Saussurea (Asteraceae) provides insights into the drivers of radiating diversification. Proc. R. Soc. London, Ser. B 288, 20211575. https://doi.org/10.1098/rspb.2021.1575.
Zhang, X., Sun, Y.X., Landis, J.B., et al., 2021c. Transcriptomes of Saussurea (Asteraceae) provide insights into high-altitude adaptation. Plants 10, 1715. https://doi.org/10.3390/plants10081715.
Zhang, Y.Z., Chen, J.G., Sun, H., 2021d. Alpine speciation and morphological innovations: revelations from a species-rich genus in the Northern Hemisphere. AoB PLANTS 13, plab018. https://doi.org/10.1093/aobpla/plab018.
Zhou, B.F., Yuan, S, Crowl A.A., et al., 2022. Phylogenomic analyses highlight innovation and introgression in the continental radiations of Fagaceae across the Northern Hemisphere. Nat. Commun. 13, 1320. https://doi.org/10.1038/s41467-022-28917-1.

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