Goldenrod herbariomics: Hybrid-sequence capture reveals the phylogeny of Solidago.
Anchored Hybrid Enrichment
Asteraceae
Chrysoma
North America
Oligoneuron
herbarium specimens
polyploidy
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
26
03
2023
received:
03
04
2022
accepted:
27
03
2023
medline:
18
7
2023
pubmed:
5
4
2023
entrez:
4
4
2023
Statut:
ppublish
Résumé
The phylogenetic relationships among the ca. 138 species of goldenrods (Solidago; Asteraceae) have been difficult to infer due to species richness, and shallow interspecific genetic divergences. This study aims to overcome these obstacles by combining extensive sampling of goldenrod herbarium specimens with the use of a custom Solidago hybrid-sequence capture probe set. A set of tissues from herbarium samples comprising ca. 90% of Solidago species was assembled and DNA was extracted. A custom hybrid-sequence capture probe set was designed, and data from 854 nuclear regions were obtained and analyzed from 209 specimens. Maximum likelihood and coalescent approaches were used to estimate the genus phylogeny for 157 diploid samples. Although DNAs from older specimens were both more fragmented and produced fewer sequencing reads, there was no relationship between specimen age and our ability to obtain sufficient data at the target loci. The Solidago phylogeny was generally well-supported, with 88/155 (57%) nodes receiving ≥95% bootstrap support. Solidago was supported as monophyletic, with Chrysoma pauciflosculosa identified as sister. A clade comprising Solidago ericameriodes, Solidago odora, and Solidago chapmanii was identified as the earliest diverging Solidago lineage. The previously segregated genera Brintonia and Oligoneuron were identified as placed well within Solidago. These and other phylogenetic results were used to establish four subgenera and fifteen sections within the genus. The combination of expansive herbarium sampling and hybrid-sequence capture data allowed us to quickly and rigorously establish the evolutionary relationships within this difficult, species-rich group.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e16164Informations de copyright
© 2023 Botanical Society of America.
Références
Alexander, P. J., M. D. Windham, J. B. Beck, I. A. Al-Shehbaz, L. Allphin, and C. D. Bailey. 2013. Molecular phylogenetics and taxonomy of the genus Boechera and related genera (Brassicaceae: Boechereae). Systematic Botany 38: 192-209.
Banker S. E., A. R. Lemmon, A. B. Hassinger, M. Dye, S. D. Holland, M. L. Kortyna, O. E. Ospina, et al. 2020. Hierarchical hybrid enrichment: Multitiered genomic data collection across evolutionary scales, with application to chorus frogs (Pseudacris). Systematic Biology 69: 756-773.
Beck, J. B., P. J. Alexander, L. Allphin, I. A. Al-Shehbaz, C. Rushworth, C. D. Bailey, and M. D. Windham. 2012. Does hybridization drive the transition to asexuality in diploid Boechera? Evolution 66: 985-995.
Beck, J. B., M. L. Markley, M. G. Zielke, J. R. Thomas, H. J. Hale, L. D. Williams, and M. G. Johnson. 2022. Are Palmer's elm-leaf goldenrod and the smooth elm-leaf goldenrod real? The Angiosperms353 kit provides within-species signal in Solidago ulmifolia s.l. Systematic Botany 46: 1107-1113.
Beck, J. B., and J. C. Semple. 2015. Next-generation sampling: Pairing genomics with herbarium specimens provides species-level signal in Solidago (Asteraceae). Applications in Plant Sciences 3: 1500014.
Brammall, R. A., and J. C. Semple. 1990. The cytotaxonomy of Solidago nemoralis (Compositae: Astereae). Canadian Journal of Botany 68: 2065-2069.
Breinholt, J. W., S. B. Carey, G. P. Tiley, E. C. Davis, L. Endara, S. F. McDaniel, L. G. Neves, et al. 2021. A target enrichment probe set for resolving the flagellate land plant tree of life. Applications in Plant Sciences 9: e11406.
Brewer, G. E., J. J. Clarkson, O. Maurin, A. R. Zuntini, V. Barber, S. Bellot, N. Biggs, et al. 2019. Factors affecting targeted sequencing of 353 nuclear genes from herbarium specimens spanning the diversity of angiosperms. Frontiers in Plant Science 10: 1102.
Buddenhagen, C. E., A. R. Lemmon, E. M. Lemmon, J. Bruhl, J. Cappa, W. L. Clement, M. Donoghue, et al. 2016. Anchored phylogenomics of angiosperms I: Assessing the robustness of phylogenetic estimates. bioRxiv 086298. https://doi.org/10.1101/086298
Chen, J. 2010. Molecular phylogeny of Salix L. (Salicaceae) inferred from three chloroplast datasets and its systematic implications. Taxon 59: 29-37.
Cook, R. E. 2002. A cytotaxonomic and multivariate morphometric analysis of members of Solidago subsection Glomeruliflorae (Torr. & Gray) Nesom. Ph.D. dissertation, University of Waterloo, Waterloo, Ontario, Canada.
Cook, R. E., and J. C. Semple. 2008. The cytogeography of Solidago subsect. Glomeruliflorae (Asteraceae: Astereae). Canadian Journal of Botany 86: 1488-1496.
Correll, D. S., and M. C. Johnston. 1970. Manual of the vascular plants of Texas. Texas Research Foundation, Renner, Texas, USA.
Croat, T. B. 1967. The genus Solidago of the north central Great Plains. Ph.D. dissertation, University of Kansas, Lawrence, Kansas, USA.
Cronquist, A. 1947. Notes on the Compositae of the northeastern United States IV. Solidago. Rhodora 49: 69-79.
Cronquist, A. 1980. Vascular flora of the southeastern United States. I. Asteraceae. University of North Carolina Press, Chapel Hill, North Carolina, USA.
Dobeš, C., and J. Paule. 2010. A comprehensive chloroplast DNA-based phylogeny of the genus Potentilla (Rosaceae): Implications for its geographic origin, phylogeography and generic circumscription. Molecular Phylogenetics and Evolution 56: 156-175.
Donoghue, M. J., and B. R. Moore. 2003. Toward an integrative historical biogeography. Integrative and Comparative Biology 43: 261-270.
Fazekas, A. J., K. S. Burgess, P. R. Kesanakurti, S. W. Graham, S. G. Newmaster, B. C. Husband, D. M. Percy, et al. 2008. Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PLoS One 3: e2802.
Fazekas, A. J., P. R. Kesanakurti, K. S. Burgess, D. M. Percy, S. W. Graham, S. C. H. Barrett, S. G. Newmaster, et al. 2009. Are plant species inherently harder to discriminate than animal species using DNA barcoding markers? Molecular Ecology Resources 9: 130-139.
Ferguson, C. J., and R. K. Jansen. 2002. A chloroplast DNA phylogeny of eastern Phlox (Polemoniaceae): Implications of congruence and incongruence with the ITS phylogeny. American Journal of Botany 89: 1324-1335.
Fernald, M. L. 1908. Notes on some plants of northeastern America. Rhodora 8: 46-55.
Fernald, M. L. 1950. Gray's manual of botany. Van Nostrand, New York, New York, USA.
Folk, R. A., H. R. Kates, R. LaFrance, D. E. Soltis, P. S. Soltis, and R. P. Guralnick. 2021. High-throughput methods for efficiently building massive phylogenies from natural history collections. Applications in Plant Sciences 9: e11410.
Forrest, L. L., M. L. Hart, M. Hughes, H. P. Wilson, K.-F. Chung, Y.-H. Tseng, and C. A. Kidner. 2019. The limits of hyb-seq for herbarium specimens: Impact of preservation techniques. Frontiers in Ecology and Evolution 7: 439.
Gray, A. 1884. Synoptical flora of North America. vol. 1, part. 2. Ivison, Blakemean, Taylor & Co., New York.
Hamilton, C. A., A. R. Lemmon, E. M. Lemmon, and J. E. Bond. 2016. Expanding anchored hybrid enrichment to resolve both deep and shallow relationships within the spider tree of life. BMC Evolutionary Biology 16: 1-20.
Johnson, M. G., L. Pokorny, S. Dodsworth, L. R. Botigue, R. S. Cowan, A. Devault, W. L. Eiserhardt, et al. 2019. A universal probe set for targeted sequencing of 353 nuclear genes from any flowering plant designed using k-medoids clustering. Systematic Biology 68: 594-606.
Jordon-Thaden, I. E., J. B. Beck, C. A. Rushworth, M. D. Windham, N. Diaz, J. T. Cantley, C. T. Martine, and C. J. Rothfels. 2020. A basic ddRADseq two-enzyme protocol performs well with herbarium and silica-dried tissues across four genera. Applications in Plant Sciences 8: e11344.
Kates, H. R., J. R. Doby, C. M. Siniscalchi, R. LaFrance, D. E. Soltis, P. S. Soltis, R. P. Guralnick, and R. A. Folk. 2021. The effects of herbarium specimen characteristics on short-read NGS sequencing success in nearly 8000 specimens: Old, degraded samples have lower DNA yields but consistent sequencing success. Frontiers in Plant Science 12: 1076.
Katoh K., and D. M. Standley. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
Kearse M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, et al. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
Koontz, J. A., P. S. Soltis, and D. E. Soltis. 2004. Using phylogeny reconstruction to test hypotheses of hybrid origin in Delphinium section Diedropetala (Ranunculaceae). Systematic Botany 29: 345-357.
Kress, W. J., K. J. Wurdack, E. A. Zimmer, L. A. Weigt, and D. H. Janzen. 2005. Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences, USA 102: 8369-8374.
Kyan, R., T. Kimura, T. Yamashiro, S. Fujii, S. Sakaguchi, M. Ito, A. J. Nagano, et al. 2021. Phylogeographic and demographic modeling analyses of the multiple origins of the rheophytic goldenrod Solidago yokusaiana Makino. Heredity 126: 831-845.
Laureto, P., and T. J. Barkman. 2011. Nuclear and chloroplast DNA suggest a complex single origin for the threatened allopolyploid Solidago houghtonii (Asteraceae) involving reticulate evolution and introgression. Systematic Botany 36: 209-226.
Laureto, P., and J. S. Pringle. 2010. Solidago vossii (Asteraceae), a new species of goldenrod from northern Michigan. Michigan Botanist 49: 105-117.
LeBlond, R. J. 2000. Solidago villosicarpa (Asteraceae: Astereae), a rare new southeastern coastal plain endemic. Sida 19: 291-300.
Lemmon, A. R., S. Emme, and E. M. Lemmon. 2012. Anchored hybrid enrichment for massively high-throughput phylogenetics. Systematic Biology 61: 721-744.
Lopez Laphitz, R. M., and J. C. Semple. 2015. A multivariate morphometric analysis of the Solidago chilensis group in South America and related taxa in North America (Asteraceae, Astereae). Annals of the Missouri Botanical Garden 100: 423-441.
Mandel, J. R., R. B. Dikow, V. A. Funk, R. R. Masalia, S. E. Staton, A. Kozik, R. W. Michelmore, et al. 2014. A target enrichment method for gathering phylogenetic information from hundreds of loci: An example from the Compositae. Applications in Plant Sciences 2: 1300085.
Martino, M., J. C. Semple, and J. B. Beck. 2020. Two cytotype niche shifts are of different magnitude in Solidago gigantea. American Journal of Botany 107: 1567-1576.
Meyer, M., and M. Kircher 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols 2010: prot5448.
Mitchell, N., P. O. Lewis, E. M. Lemmon, A. R. Lemmon, and K. E. Holsinger. 2017. Anchored phylogenomics resolves the evolutionary relationships in the rapid radiation of Protea L. (Proteaceae). American Journal of Botany 104: 102-115.
Morton, G. H. 1973. The taxonomy of the Solidago ar-uta - boottii complex. Ph.D. dissertation, University of Tennessee, Knoxville, Tennessee, USA.
Nesom, G. L. 1989. New species of Mexican Solidago (Compositae: Astereae). Phytologia 67: 142-147.
Nesom, G. L. 1993. Taxonomic infrastructure of Solidago and Oligoneuron (Asteraceae: Astereae) and observations on the phylogenetic position. Phytologia 75: 1-44.
Peirson, J. A., C. W. Dick, and A. A. Reznicek. 2013. Phylogeography and polyploid evolution of North American goldenrods (Solidago subsect. Humiles, Asteraceae). Journal of Biogeography 40: 1887-1898.
Peirson, J. A., A. A. Reznicek, and J. C. Semple. 2012. Polyploidy, infraspecific cytotype variation, and speciation in goldenrods: The cytogeography of Solidago subsect. Humiles (Asteraceae) in North America. Taxon 61: 197-210.
Prum, R. O., J. S. Berv, A. Dornburg, D. J. Field, J. P. Townsend, E. M. Lemmon, and A. R. Lemmon. 2015. A comprehensive phylogeny of birds (Aves) using targeted next generation DNA sequencing. Nature 526: 569-573.
Pyron, R. A., C. R. Hendry, F. Hsieh, A. R. Lemmon, and E. M. Lemmon. 2016. Integrating phylogenomic and morphological data to assess candidate species-delimitation models in brown and red-bellied snakes (Storeria). Zoological Journal of the Linnean Society, Linnean Society of London 177: 937-949.
Radford, A. E., H. E. Ahles, and C. R. Bell. 1968. Manual of the vascular flora of the Carolinas. University of North Carolina Press, Chapel Hill, North Carolina, USA.
Rafinesque, C. S. 1836 [1837]. Flora Telluriana. Printed for the author by H. Probasco, Philadelphia, Pennsylvania, USA.
Rokyta, D. R., A. R. Lemmon, M. J. Margres, and K. Arnow. 2012. The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics 13: 312.
Rothfels, C. J. 2021. Polyploid phylogenetics. New Phytologist 230: 66-72.
Sakaguchi, S., T. Kimura, R. Kyan, M. Maki, T. Nishino, N. Ishikawa, A. J. Nagano, et al. 2018. Phylogeographic analysis of the East Asian goldenrod (Solidago virgaurea complex, Asteraceae) reveals hidden ecological diversification with recurrent formation of ecotypes. Annals of Botany 121: 489-500.
Schaefer, H. 2015. On the origin and systematic position of the Azorean goldenrod, Solidago azorica (Asteraceae). Phytotaxa 210: 47-59.
Schilling, E. E., J. B. Beck, P. J. Calie, and R. L. Small. 2008. Molecular analysis of Solidaster cv. Lemore, a hybrid goldenrod (Asteraceae). Journal of the Botanical Research Institute of Texas 2: 7-18.
Semple, J. C. 2006. Brintonia E.L. Greene. In Flora North America Editorial Committee [eds.], Flora of North America, vol. 20, Asteraceae, Part 2. Astereae and Senecioneae, 106. Oxford University Press, Oxford, UK.
Semple, J. C. 2016. An intuitive phylogeny and summary of chromosome number variation in the goldenrod genus Solidago (Asteraceae: Astereae). Phytoneuron 2016−32. 1-9.
Semple, J. C., and J. B. Beck. 2021. A revised infrageneric classification of Solidago (Asteraceae: Astereae). Phytoneuron 2021−10. 1-6.
Semple, J. C., J. G. Chmieleski, and R. A. Brammall. 1990. A multivariate morphometric study of Solidago nemoralis (Compositae: Astereae) and comparison with S. californica and S. sparsiflora. Canadian Journal of Botany 68: 2070-2082.
Semple, J. C., and R. E. Cook. 2006. Solidago Linnaeus. In Flora North America Editorial Committee [eds.], Flora of North America, vol. 20, Asteraceae, Part 2. Astereae and Senecioneae, 107-166. Oxford University Press, Oxford, UK.
Semple, J. C., H. Faheemuddin, Y. A. Chong, M. K. Sorour, J. A. Hood, I. Khamis, Y. Ma, and K. Kornobis. 2013. A multivariate morphometric study of the Solidago canadensis/S. lepida complex of Solidago subsect. Triplinerviae. I. Northeastern taxa (Asteraceae: Astereae). Phytoneuron 2013−58: 1-20.
Semple, J. C., H. Faheemuddin, M. Sorour, and Y. A. Chong. 2017a. A multivariate study of Solidago subsect. Triplinerviae in western North America: The Solidago lepida complex (Asteraceae: Astereae). Phytoneuron 2017−47: 1-43.
Semple, J. C., K. Kornobis, and S. Bzovsky. 2018. A multivariate morphometric analysis of Solidago subsect. Nemorales (Asteraceae: Astereae). Phytoneuron 2018−42: 1-40.
Semple, J. C., Y. Ma, U. Naik, N. Steenhof, and L. Tong. 2017b. A multivariate morphometric analysis of Solidago subsect. Thyrsiflorae (Asteraceae: Astereae). Phytoneuron 2017-77: 1-37.
Semple, J. C., Y. Ma, L. Tong, and M. Sorour. 2020. A multivariate morphometric analysis of Solidago sect. Solidago and sect. Multiradiatae (Asteraceae: Astereae). Phytoneuron 2020−38: 1-59.
Semple, J. C., K. Nizamani, K. Kornobis, G. Samra, L. Tong, and T. Stavroullakis. 2021. A multivariate study of Solidago sect. Argutae (Asteraceae: Astereae). Phytoneuron 2021−20: 1-56.
Semple, J. C., G. S. Ringius, and J. J. Zhang. 1999. The goldenrods of Ontario: Solidago L. and Euthamia Nutt. University of Waterloo Biology Series 36: 1-90.
Semple, J. C., T. Shea, M. El-Swesi, H. Rahman, and Y. Ma. 2016a. A multivariate study of the Solidago stricta complex (Asteraceae: Astereae: S. subsect. Maritimae). Phytoneuron 2016−86: 1-34.
Semple, J. C., T. Shea, H. Rahman, Y. Ma, and K. Kornobis. 2016b. A multivariate study of the Solidago sempervirens complex (Asteraceae: Astereae: S. subsect. Maritimae). Phytoneuron 2016−73: 1-31.
Semple, J. C., T. Shea, H. Rahman, Y. Ma, and L. Tong. 2019. A multivariate morphometric analysis of the Solidago uliginosa complex (Asteraceae: Astereae; S. subsect. Maritimae) in eastern North America. Phytoneuron 2019−48: 1-44.
Semple, J. C., L. Tong, and Y. A. Chong. 2017c. Multivariate studies of Solidago subsect. Squarrosae. I. The Solidago speciosa complex (Asteraceae: Astereae). Phytoneuron 2017-18: 1-23.
Semple, J. C., L. Tong, and Y. A. Chong. 2017e. Multivariate studies of Solidago subsect. Squarrosae. III. S. georgiana, S. porteri, S. roanensis, S. squarrosa, and S. villosicarpa (Asteraceae: Astereae). Phytoneuron 2017−55: 1-17.
Semple, J. C., L. Tong, Y. A. Chong, and M. Kaddoura. 2017d. Multivariate studies of Solidago subsect. Squarrosae. II. The Solidago bicolor-hispida complex (Asteraceae: Astereae). Phytoneuron 2017−33: 1-44.
Shee, Z. Q., D. G. Frodin, R. Cámara-Leret, and L. Pokorny. 2020. Reconstructing the complex evolutionary history of the Papuasian Schefflera radiation through herbariomics. Frontiers in Plant Science 11: 258.
Slimp, M., L. D. Williams, H. Hale, and M. G. Johnson. 2021. On the potential of Angiosperms353 for population genomic studies. Applications in Plant Sciences 9: e11419.
Small, J. K. 1903. Flora of the southeastern United States. Published by the author, New York, New York, USA.
Small, J. K. 1933. Manual of the southeastern flora. University of North Carolina Press. Chapel Hill, North Carolina, USA.
Soltis, P. S., R. A. Folk, and D. E. Soltis. 2019. Darwin review: Angiosperm phylogeny and evolutionary radiations. Proceedings of the Royal Society, B, Biological Sciences 286: 20190099.
Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
Stebbins, G. L. 1993. Concepts of species and genera. In Flora of North America Editorial Commitee [eds.], Flora of North America, 1, 229-246. Oxford University Press, Oxford, UK.
Tank, D. C., and R. G. Olmstead. 2008. From annuals to perennials: Phylogeny of subtribe Castillejinae (Orobanchaceae). American Journal of Botany 95: 608-625.
Torrey, J., and A. Gray. 1842. Solidago. In Flora of North America, vol. 2. Part 2. 195-231. Wiley & Putnam, New York.
Thiers, B. 2022 [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. (website: https://sciweb.nybg.org/science2/IndexHerbariorum.asp) Virtual Herbarium, New York Botanical Garden, Bronx, New York, USA.
Vachaspati, P., and T. Warnow. 2015. ASTRID: Accurate Species Trees from Internode Distances. BMC Genomics 16: S3.
Voss, E. G. 1996. Michigan Flora. Part III. Dicots (Pyrolaceae-Compositae). Cranbrook Institute of Science Bulletin, vol. 61. Cranbrook Institute of Science, Ann Arbor, Michigan, USA.
Viruel, J., M. Conejero, O. Hidalgo, L. Pokorny, R. F. Powell, F. Forest, M. B. Kantar, et al. 2019. A target capture-based method to estimate ploidy from herbarium specimens. Frontiers in Plant Science 10: 937.
Weakley, A. 2020. Flora of the southeastern United States, 20 October 2020 edition. University of North Carolina, Chapel Hill, North Carolina, USA. Website: https://ncbg.unc.edu/research/unc-herbarium/flora-request/
Wieboldt, T. F., and J. C. Semple. 2003. Solidago faucibus (Asteraceae: Astereae), a new mesic forest goldenrod from the Appalachian Mountains. SIDA, Contributions to Botany 20: 1595-1603.
Wolfe, A. D., C. P. Randle, S. L. Datwyler, J. J. Morawetz, N. Arguedas, and J. Diaz. 2006. Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. American Journal of Botany 93: 1699-1713.
Zhang, J. 1996. A molecular biosystematic study on North American Solidago and related genera (Asteraceae: Astereae) based on chloroplast DNA RFLP analysis. Ph.D. dissertation, University of Waterloo, Waterloo, Ontario, Canada.