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Issue: Vol. 625 No. 3: 14 Nov. 2023
Type: Article
Published: 2023-11-14
DOI: 10.11646/phytotaxa.625.3.1
Page range: 227-247
Abstract views: 241
PDF downloaded: 144

The third opinion on fern phylogenetics with novel insights into their mitogenome evolution

Biodiversity Unit; FI-20014 University of Turku; Turku; Finland
Biodiversity Unit; FI-20014 University of Turku; Turku; Finland
mitochondrial marker plastid marker plastome purifying selection RNA editing Pteridophytes

Abstract

The current understanding of fern phylogeny is primarily based on plastid and nuclear sequences, but the third genome—the mitogenome—has remained practically unstudied. We inferred the first broad scale fern phylogeny based on mitogenomic data, obtained from the One Thousand Plant Transcriptomes Initiative project, and compared it with the plastid phylogeny. The trees were mostly congruent and corresponded to the current understanding of the fern phylogeny, but we observed different evolutionary patterns between the two genomes. Protein-coding markers located in the plastome had, on average, over two times higher substitution rate than the markers from the mitogenome. The similar rate variation pattern between the genomes in different fern lineages supports the idea that a common mechanism, like life history traits, drives the rates of molecular evolution. The few conflicting nodes we observed have also been difficult to resolve in other studies, suggesting that even genomic data may not suffice to resolve them.

 

References

  1. Adanson, M. (1763) Familles des plantes. Chez Vincent, Imprimeur-Libraire de Mgr le Comte de Provence, Paris, 640 pp. https://doi.org/10.5962/bhl.title.271
  2. Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., dePamphilis, C., Albert, V.A., Aono, N., Aoyama, T., Ambrose, B.A., Ashton, N.W., Axtell, M.J., Barker, E., Barker, M.S., Bennetzen, J.L., Bonawitz, N.D., Chapple, C., Cheng, C., Correa, L.G., Dacre, M., DeBarry, J., Dreyer, I., Elias, M., Engstrom, E.M., Estelle, M., Feng, L., Finet, C., Floyd, S.K., Frommer, W.B., Fujita, T., Gramzow, L., Gutensohn, M., Harholt, J., Hattori, M., Heyl, A., Hirai, T., Hiwatashi, Y., Ishikawa, M., Iwata, M., Karol, K.G., Koehler, B., Kolukisaoglu, U., Kubo, M., Kurata, T., Lalonde, S., Li, K., Li, Y., Litt, A., Lyons, E., Manning, G., Maruyama, T., Michael, T.P., Mikami, K., Miyazaki, S., Morinaga, S., Murata, T., Mueller-Roeber, B., Nelson, D.R., Obara, M., Oguri, Y., Olmstead, R.G., Onodera, N., Petersen, B.L., Pils, B., Prigge, M., Rensing, S.A., Riaño-Pachón, D.M., Roberts, A.W., Sato, Y., Scheller, H.V., Schulz, B., Schulz, C., Shakirov, E.V., Shibagaki, N., Shinohara, N., Shippen, D.E., Sørensen, I., Sotooka, R., Sugimoto, N., Sugita, M., Sumikawa, N., Tanurdzic, M., Theissen, G., Ulvskov, P., Wakazuki, S., Weng, J.K., Willats, W.W., Wipf, D., Wolf, P.G., Yang, L., Zimmer, A.D., Zhu, Q., Mitros, T., Hellsten, U., Loqué, D., Otillar, R., Salamov, A., Schmutz, J., Shapiro, H., Lindquist, E., Lucas, S., Rokhsar, D. & Grigoriev, I.V. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960–963. https://doi.org/10.1126/science.1203810
  3. Bell, D., Lin, Q., Gerelle, W.K., Joya, S., Chang, Y., Taylor, Z.N., Rothfels, C.J., Larsson, A., Villarreal, J.C., Li, F.W., Pokorny, L., Szövényi, P., Crandall-Stotler, B., DeGironimo, L., Floyd, S.K., Beerling, D.J., Deyholos, M.K., von Konrat, M., Ellis, S., Shaw, A.J., Chen, T., Wong, G.K.S., Stevenson, D.W., Palmer, J.D. & Graham, S.W. (2020) Organellomic data sets confirm a cryptic consensus on (unrooted) land-plant relationships and provide new insights into bryophyte molecular evolution. American Journal of Botany 107: 91–115. https://doi.org/10.1002/ajb2.1397
  4. Bernhardi, D.I.I. (1800) Tentamen alterum filices in genera redigendi. Journal für die Botanik 2: 121–136.
  5. Bernhardi, J.J. (1805) Dritter Versuch einer Anordnung der Farrnkräuter. Neues Journal für die Botanik 3: 1–50.
  6. Blume, C.L. (1828) Enumeratio plantarum Javae et insularum adjacentium: minus cognitarum vel novarum ex herbariis Reinwardtii, Kuhlii, Hasseltii et Blumii. Apud J. W. van Leeuwen, Lugduni Batavorum, 276 pp. https://doi.org/10.5962/bhl.title.44901
  7. Bonavita, S. & Rosaria, T.M.R. (2016) The evolutionary conservation of rps3 introns and rps19-rps3-rpl16 gene cluster in Adiantum capillus-veneris mitochondria. Current Genetics 62: 173–184. https://doi.org/10.1007/s00294-015-0512-z
  8. Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F.K., Müller, N.F., Ogilvie, H.A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, Ch.-H., Xie, D., Zhang, Ch., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS computational biology 15: e1006650. https://doi.org/10.1371/journal.pcbi.1006650
  9. Brongniart, M.Ad. (1821) Description d’ un nouveau de Fougére, nommé Ceratopteris. Bulletin des Sciences, par la Société Philomatique de Paris 1821: 184–187.
  10. Brown, R. (1810) Prodromus floræ Novæ Hollandiæ et Insulæ Van-Diemen: exhibens characteres plantarum quas annis 1802–1805. Typis R. Taylor et socii, Londini, 592 pp. https://doi.org/10.5962/bhl.title.52309
  11. Brasdell, R.F. (1963) A monographic study of the fern genus Cystopteris. Memoirs of the Torrey Botanical Club 21 (4): 1–120.
  12. Breinholt, J.W., Carey, S.B., Tiley, G.P., Davis, E.C., Endara, L., McDaniel, S.F., Neves, L.G., Sessa, E.B., von Konrat, M., Chantanaorrapint, S., Fawcett, S., Ickert-Bond, S.M., Labiak, P.H., Larraín, J., Lehnert, M., Lewis, L.R., Nagalingum, N.S., Patel, N., Rensing, S.A., Testo, W., Vasco, A., Villarreal, J.C., Williams, E.W. & Burleigh, J.G. (2021) A target enrichment probe set for resolving the flagellate land plant tree of life. Applications in plant sciences 24: e11406. https://doi.org/10.1002/aps3.11406
  13. Brown, R. (1810) Prodromus floræ Novæ Hollandiæ et Insulæ Van-Diemen: exhibens characteres plantarum quas annis 1802–1805. Londini, typis R. Taylor et socii, London, 592 pp. https://doi.org/10.5962/bhl.title.52309
  14. Britton, N.L., Sterns, E.E. & Poggenburg, J.F. (1888) Preliminary catalogue of Anthophyta and Pteridophyta, reported as growing spontaneously within one hundred miles of New York City. Price, One Dollar, New York, 90 pp.
  15. Burman, N.L. (1768) Nicolai Laurentii Burmanni Flora Indica: cui accedit series zoophytorum Indicorum, nec non prodromus florae Capensis. Apud Cornelium Haek, Amstelaedami, 292 pp. https://doi.org/10.5962/bhl.title.60581
  16. Carpenter, E.J., Matasci, N., Ayyampalayam, S., Wu, S., Sun, J., Yu, J., Jimenez Vieira, F.R., Bowler, C., Dorrell, R.G., Gitzendanner, M.A., Li, L., Du, W., Ullrich, K.K., Wickett, N.J., Barkmann, T.J., Barker, M.S., Leebens-Mack, J.H. & Wong, G.K.S. (2019) Access to RNA-sequencing data from 1,173 plant species: The 1000 Plant transcriptomes initiative (1KP). GigaScience 8: giz126. https://doi.org/10.1093/gigascience/giz126
  17. Chaw, S.M., Shih, A.C., Wang, D., Wu, Y.W., Liu, S.M. & Chou, T.Y. (2008) The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Molecular Biology and Evolution 25: 603–615. https://doi.org/10.1093/molbev/msn009
  18. Cho, Y., Mower, J.P., Qiu, Y.L. & Palmer, J.D. (2004) Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. PNAS 101: 17741–17746. https://doi.org/10.1073/pnas.0408302101
  19. Diels, L. (1899) Polypodiaceae. In: Engler, A., Krause, K., Pilger, R. & Prantl, K. (Eds.) Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrten begründet. Verlag von Wilhelm Engelmann, Leipzig, pp. 139–380.
  20. Drouin, G., Daoud, H. & Xia, J. (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Molecular phylogenetics and evolution 49: 827–831. https://doi.org/10.1016/j.ympev.2008.09.009
  21. Du, X.Y., Kuo, L.Y., Zuo, Z.Y., Li, D.Z. & Lu, J.M. (2022) Structural variation of plastomes provides key insight into the deep phylogeny of ferns. Frontiers in Plant Science 13: 862772. https://doi.org/10.3389/fpls.2022.862772
  22. Du, X.Y., Lu, J.M., Zhang, L.B., Wen, J., Kuo, L.Y., Mynssen, C.M., Schneider, H. & Li, D.Z. (2021) Simultaneous diversification of Polypodiales and angiosperms in the Mesozoic. Cladistics 37: 518–539. https://doi.org/10.1111/cla.12457
  23. Eaton, D.C. (1865) On the genus Woodsia. The Canadian naturalist and geologist 2: 89–92.
  24. Engler, A. & Prantl, K. (1902) Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrten begründet. Teil 1, Abt. 4 Leipzig, 808 pp.
  25. Farrar, D.R. & Mickel, J.T. (1991) Vittaria appalachiana: A Name for the “Appalachian Gametophyte”. American Fern Journal 81 (3): 69–75. https://doi.org/10.2307/1547574
  26. Fawcett, S., Smith, A.R., Sundue, M., Burleigh, J.G., Sessa, E.B., Kuo, L-Y., Ch., Ch-W, Testo, W., Kessler, M., Consortium, GoFlag & Barrington, D.S. (2021) A Global Phylogenomic Study of the Thelypteridaceae. Systematic Botany 46 (4): 891–915. https://doi.org/10.1600/036364421X16370109698650
  27. Fée, A.L.A. (1857) Iconographie des espèces nouvelles décrites ou énumérées dans le genera filicum et révision des publications antérieures relatives à la famille des fougères. Sixième, septième et Huitième Mémoires. Veuve Berger-Levrault et Fils, Libraires, Paris, 193 pp.
  28. Feng, Y. & Wicke, S. (2022) New mitochondrial genomes of leptosporangiate ferns allow modeling the mitogenomic inflation syndrome across all land plant lineages. bioRxiv. https://doi.org/10.1101/2022.12.23.521604
  29. Fernald, M.L. (1915) Book Review. Flora of the vicinity of New York. Rhodora, Journal of the New England Botanical Club 17: 62–70.
  30. Franklin, J. (1823) Narrative of a journey to the shores of the polar sea, in the years 1819, 20, 21, and 22. John Murray, Albemarles-Street, London, 790 pp. https://doi.org/10.5479/sil.75582.39088002032894
  31. Gitzendanner, M.A., Soltis, P.S., Wong, G.K.-S., Ruhfel, B.R. & Soltis, D.E. (2018) Plastid phylogenomic analysis of green plants: a billion years of evolutionary history. American Journal of Botany 05: 291–301. https://doi.org/10.1002/ajb2.1048
  32. Grewe, F., Guo, W., Gubbels, E.A., Hansen, A.K. & Mower, J.P. (2013) Complete plastid genomes from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale reveal an ancestral land plant genome structure and resolve the position of Equisetales among monilophytes. BMC Evolutionary Biology 13: 8. https://doi.org/10.1186/1471-2148-13-8
  33. Grusz, A.L., Rothfels, C.J. & Schuettpelz, E. (2016) Transcriptome sequencing reveals genome-wide variation in molecular evolutionary rate among ferns. BMC Genomics 17: 692. https://doi.org/10.1186/s12864-016-3034-2
  34. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321. https://doi.org/10.1093/sysbio/syq010
  35. Guo, W., Grewe, F., Fan, W., Young, G.J., Knoop, V., Palmer, J.D. & Mower, J.P. (2016) Ginkgo and Welwitschia mitogenomes reveal extreme contrasts in gymnosperm mitochondrial evolution. Molecular Biology and Evolution 33: 1448–1460. https://doi.org/10.1093/molbev/msw024
  36. Guo, W., Zhu, A., Fan, W. & Mower, J.P. (2017) Complete mitochondrial genomes from the ferns Ophioglossum californicum and Psilotum nudum are highly repetitive with the largest organellar introns. The New Phytologist 213: 391–403. https://doi.org/10.1111/nph.14135
  37. Hasebe, M., Omori, T., Nakazawa, M., Sano, T., Kato, M. & Iwatsuki, K. (1994) rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proceedings of the National Academy of Sciences 91: 5730–5734. https://doi.org/10.1073/pnas.91.12.5730
  38. Haufler, C.H. & Windham, M.D. (1991) New species of North American Cystopteris and Polypodium, with comments on their reticulate relationships. American Fern Journal 81 (1): 7–23. https://doi.org/10.2307/1547129
  39. Hooker, W.J. & Greville, R.K. (1831 [1829]) Icones filicum ad eas potissimum species illustrandas destinatæ, quæ hactenus, vel in herbariis delituerunt prorsus incognitae, vel saltem nondum per icones botanicis innotuerunt. Figures and descriptions of ferns, principally of such as have been altogether unnoticed by botanists, or as have not yet been correctly figured. Prostant Venales Apud Treuttel et Würtz, Treuttel Fil. et Richter, 30, Soho-Square, Parisiis, 253 pp. https://doi.org/10.5962/bhl.title.3867
  40. Hornschuch, Ch.F. (1828) Sylloge plantarum novarum itemque minus cognitarum: a praestantissimis botanicis adhuc viventibus collecta et a Societate regia botanica Ratisbonensi edita. Ratisbonae, Typis viduae C.E. Brenck, Ratisbonae, 256 pp.
  41. Houttuyn, M. (1783) Natuurlyke Historie of Uitvoerige Beschrijving der Dieren, Planten en Mineraalen, Volgens het Samenstel van den Heer Linnaeus. Met Naauwkeurige Afbeeldingen Tweede DeelsVeertiende Stuk. De Varens, Mossen, enz. Eerste Stuk. Amsterdam, 698 pp.
  42. Jackman, S.D., Coombe, L., Warren, R.L., Kirk, H., Trinh, E., MacLeod, T., Pleasance, S., Pandoh, P., Zhao, Y., Coope, R.J., Bousquet, J., Bohlmann, J., Jones, S.J.M. & Birol, I. (2020) Complete mitochondrial genome of a gymnosperm, Sitka Spruce (Picea sitchensis), indicates a complex physical structure. Genome Biology and Evolution 12: 1174–1179. https://doi.org/10.1093/gbe/evaa108
  43. Jones, W.G., Hill, K.D. & Allen, J.M. (1995) Wollemia nobilis, a new living Australian genus and species in the Araucariaceae. Telopea; Contributions from the National Herbarium of New South Wales 6 (2–3): 173–176. https://doi.org/10.7751/telopea19953014
  44. Kan, S.L., Shen, T.T., Gong, P., Ran, J.H. & Wang, X.Q. (2020) The complete mitochondrial genome of Taxus cuspidata (Taxaceae): eight protein-coding genes have transferred to the nuclear genome. BMC Evolutionary Biology 20: 10. https://doi.org/10.1186/s12862-020-1582-1
  45. Kato, M. (1977) Classification of Athyrium and allied genera of Japan. The Botanical Magazine. [Shokubutsu-gaku zasshi]. Tokyo 90 (1): 23–40. https://doi.org/10.1007/BF02489467
  46. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  47. Kinosian, S.P., Pearse, W.D. & Wolf, P.G. (2020) There and back again: Reticulate evolution in Ceratopteris. American Fern Journal 110: 193–210. https://doi.org/10.1640/0002-8444-110.4.193
  48. Klekowski, E.J. (1984) Mutational load in clonal plants: a study of two fern species. Evolution 38: 417–426. https://doi.org/10.2307/2408500
  49. Knie, N., Fischer, S., Grewe, F., Polsakiewicz, M. & Knoop, V. (2015) Horsetails are the sister group to all other monilophytes and Marattiales are sister to leptosporangiate ferns. Molecular Phylogenetics and Evolution 90: 140–149. https://doi.org/10.1016/j.ympev.2015.05.008
  50. Knie, N., Grewe, F., Fischer, S. & Knoop, V. (2016) Reverse U-to-C editing exceeds C-to-U RNA editing in some ferns—a monilophyte-wide comparison of chloroplast and mitochondrial RNA editing suggests independent evolution of the two processes in both organelles. BMC Evolutionary Biology 16: 134. https://doi.org/10.1186/s12862-016-0707-z
  51. Knoop, V. (2013) Plant mitochondrial genome peculiarities evolving in the earliest vascular plant lineages. Journal of Systematics and Evolution 5: 1–12. https://doi.org/10.1111/j.1759-6831.2012.00228.x
  52. Korall, P., Schuettpelz, E. & Pryer, K.M. (2010) Abrupt deceleration of molecular evolution linked to the origin of arborescence in ferns. Evolution 64: 2786–2792. https://doi.org/10.1111/j.1558-5646.2010.01000.x
  53. Kunth, C.S. (1815) Nova genera et species plantarum: quas in peregrinatione ad plagam aequinoctialem orbis novi collegerunt /descripserunt, partim adumbraverunt Amat. Bonpland et Alex. de Humboldt; ex schedis autographis Amati Bonplandi in ordinem digessit Carol. Sigismund. Kunth. Vol 1. Sumtibus Librariæ Graeco-Latino-Germanicæ, Lutettiæ Parisiorum, 302 pp.
  54. Kunze, G. (1835) Thyrsopteris, eine neue Farrngattung. Linnaea: Ein Journal für die Botanik in ihrem ganzen Umfange 9 (4): 503–508.
  55. Kuo, L.Y., Qi, X., Ma, H. & Li, F.W. (2018a) Order-level fern plastome phylogenomics: new insights from Hymenophyllales. American Journal of Botany 105: 1545–1555. https://doi.org/10.1002/ajb2.1152
  56. Kuo, L.Y., Tang, T.Y., Li, F.W., Su, H.J., Chiou, W.L., Huang, Y.M. & Wang, C.N. (2018b) Organelle genome inheritance in Deparia ferns (Athyriaceae, Aspleniineae, Polypodiales). Frontiers in Plant Science 9: 486. https://doi.org/10.3389/fpls.2018.00486
  57. Labiak, P.H. & Karol, K.G. (2017) Plastome sequences of an ancient fern lineage reveal remarkable changes in gene content and architecture. American Journal of Botany 104: 1008–1018. https://doi.org/10.3732/ajb.1700135
  58. LaBillardiere, J.-J. (1824) Sertum Austro-Caledonicum. Ex Typographia Dominæ Huzard, Parisiis, 262 pp.
  59. Lamarck, J.-B. (1797) Encyclopédie Méthodique. Botanique. Chez H. Agasse, Paris, 764 pp.
  60. Lanfear, R., Calcott, B., Ho, S.Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular biology and evolution 29: 1695–1701. https://doi.org/10.1093/molbev/mss020
  61. Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772–773. https://doi.org/10.1093/molbev/msw260
  62. Lehtonen, S. (2011) Towards resolving the complete fern tree of life. PLoS ONE 6: e24851. https://doi.org/10.1371/journal.pone.0024851
  63. Lehtonen, S. & Caìrdenas, G.G. (2019) Dynamism in plastome structure observed across the phylogenetic tree of ferns. Botanical Journal of the Linnean Society 190: 229–241. https://doi.org/10.1093/botlinnean/boz020
  64. Lehtonen, S., Poczai, P., Sablok, G., Hyvönen, J., Karger, D.N. & Flores, J. (2020) Exploring the phylogeny of the marattialean ferns. Cladistics 36: 569–593. https://doi.org/10.1111/cla.12419
  65. Lehtonen, S., Silvestro, D., Karger, D.N., Scotese, C., Tuomisto, H., Kessler, M., Peña, C., Wahlberg, N. & Antonelli, A. (2017) Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Scientific Reports 7: 4831. https://doi.org/10.1038/s41598-017-05263-7
  66. Lellinger, D.B. (1981) Notes on North American Ferns. American Fern Journal 71: 90–94. https://doi.org/10.2307/1546734
  67. Letunic, I. & Bork, P. (2021) Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49: 293–296. https://doi.org/10.1093/nar/gkab301
  68. Li, F.-W., Pryer, K.M. & Windham, M.D. (2012) Gaga, a new fern genus segregated from Cheilanthes (Pteridaceae). Systematic Botany; Quarterly Journal of the American Society of Plant Taxonomists 37 (4): 845–860. https://doi.org/10.1600/036364412X656626
  69. Lindley, J. (1843) Miscellaneous matter of the Botanical Register. Edwards’s Botanical Register; or, Flower Garden and Shrubbery 29: 1–85.
  70. Linné, C.v. (1753) Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Vol 2. Impensis Laurentii Salvii, Holmiæ, 570 pp. https://doi.org/10.5962/bhl.title.59734
  71. Linné, C.v. (1759) Caroli Linnæi Equitis de Stella Polari, Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Vol 2. Impresis Direct, Laurentii Salvii, pp. 825–1384. https://doi.org/10.5962/bhl.title.542
  72. Linné, C.c. (1771) Car. A Linné Mantissa Plantarum: Generum editionis VI et specierum editionis II. Holmiæ, Impensis Direct. Laurentii Salvii, Stockholm, 588 pp.
  73. Liu, S., Wang, Z., Wang, H., Su, Y. & Wang, T. (2020) Patterns and rates of plastid rps12 gene evolution inferred in a phylogenetic context using plastomic data of ferns. Scientific Reports 10: 9394. https://doi.org/10.1038/s41598-020-66219-y
  74. Liu, Y., Johnson, M.G., Cox, C.J., Medina, R., Devos, N., Vanderpoorten, A., Hedenäs, L., Bell, N.E., Shevock, J.R., Aguero, B., Quandt, D., Wickett, N.J., Shaw, A.J. & Goffinet, B. (2019) Resolution of the ordinal phylogeny of mosses using targeted exons from organellar and nuclear genomes. Nature Communications 10: 1485. https://doi.org/10.1038/s41467-019-09454-w
  75. Maddison, W.P. & Maddison, D.R. (2021) Mesquite: a modular system for evolutionary analysis. Version 3.70. [http://www.mesquiteproject.org]
  76. Matasci, N., Hung, L.H., Yan, Z., Carpenter, E.J., Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Ayyampalayam, S., Barker, M., Burleigh, J.G., Gitzendanner, M.A., Wafula, E., Der, J.P., dePamphilis, C.W., Roure, B., Philippe, H., Ruhfel, B.R., Miles, N.W., Graham, S.W., Mathews, S., Surek, B., Melkonian, M., Soltis, D.E., Soltis, P.S., Rothfels, C., Pokorny, L., Shaw, J.A., DeGironimo, L., Stevenson, D.W., Villarreal, J.C., Chen, T., Kutchan, T.M., Rolf, M., Baucom, R.S., Deyholos, M.K., Samudrala, R., Tian, Z., Wu, X., Sun, X., Zhang, Y., Wang, J., Leebens-Mack, J. & Wong, G.K.S. (2014) Data access for the 1,000 Plants (1KP) project. GigaScience 3: 17. https://doi.org/10.1186/2047-217X-3-17
  77. Maxon, W.R. (1918) Notes on American ferns–XII. American Fern Journal 8: 114–121. https://doi.org/10.2307/1544342
  78. Mettenius, G. (1866) Filices, praesertim indicae et Laponicae. Annales Musei Botanici Lugduno-Batavi 2: 219–240.
  79. Michaux, A. (1803) Flora boreali-americana, sistens caracteres plantarum quas in America septentrionali collegit et detexit Andreas Michaux. Parisiis et Argentorati, apud fratres Levrault, Paris, 340 pp. https://doi.org/10.5962/bhl.title.330
  80. Moore, T. (1861) Index filicum: a synopsis, with characters, of the genera, and an enumeration of the species of ferns, with synonymes, references, &c., &c. W. Pamplin, 1857–62, London, 396 pp. https://doi.org/10.5962/bhl.title.19640
  81. Morton, C.V. (1959) The Californian species of Thelypteris. American Fern Journal; a quarterly devoted to ferns 48 (4): 136–145. https://doi.org/10.2307/1545449
  82. Mu, Y., Yan, Y., Liu, B. & Shang, H. (2020) The complete chloroplast genome sequence of Hypolepis sparsisora (Dennstaedtiaceae). Mitochondrial DNA Part B 5: 298–299. https://doi.org/10.1080/23802359.2019.1693915
  83. Murray, J.A. (1784) Systema Vegetabilium: secundum classes ordines genera species cum characteribus et differentiis. Editio decima quarta. Typis et Impensis Jo. Christ. Dieterich, Gottingae, 1004 pp.
  84. Nakai, T. (1928) Notes on Japanese Ferns VII. (Plagiogyriaceæ, Cheiropleuriaceæ, Dipteridaceæ & Polypodiaceæ I). Botanical Magazine, Tokyo 42: 203–218. https://doi.org/10.15281/jplantres1887.42.203
  85. Nascimento, F.F., Reis dos, M. & Yang, Z. (2017) A biologist’s guide to Bayesian phylogenetic analysis. Nature Ecology & Evolution 1: 1446–1454. https://doi.org/10.1038/s41559-017-0280-x
  86. Newman, E. (1851) Synoptical Table of the British Ferns. Phytologist: a Popular Botanical Miscellany 4: I–XXXII.
  87. Nitta, J.H., Schuettpelz, E., Ramírez-Barahona, S. & Iwasaki, W. (2022) An open and continuously updated fern tree of life. Frontiers in Plant Science 13: 909768. https://doi.org/10.3389/fpls.2022.909768
  88. Ogihara, Y., Yamazaki, Y., Murai, K., Kanno, A., Terachi, T., Shiina, T., Miyashita, N., Nasuda, S., Nakamura, C., Mori, N., Takumi, S., Murata, M., Futo, S. & Tsunewaki, K. (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Research 33: 6235–6250. https://doi.org/10.1093/nar/gki925
  89. One Thousand Plant Transcriptomes Initiative. (2019) One thousand plant transcriptomes and phylogenomics of green plants. Nature 574: 679–685. https://doi.org/10.1038/s41586-019-1693-2
  90. Palmer, J.D. & Herbon, L.A. (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. Journal of Molecular Evolution 28: 87–97. https://doi.org/10.1007/BF02143500
  91. Paradis, E. & Schliep, K. (2019) Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528. https://doi.org/10.1093/bioinformatics/bty633
  92. Paris, C.A. (1991) Adiantum viridimontanum, a new maidenhair fern in Eastern North America. Rhodora. Journal of the New England Botanical Club 93: 105–121.
  93. Parkinson, C.L., Mower, J.P., Qiu, Y.L., Shirk, A.J., Song, K., Young, N.D., dePamphilis, C.W. & Palmer, J.D. (2005) Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evolutionary Biology 5: 73. https://doi.org/10.1186/1471-2148-5-73
  94. Pelosi, J.A., Kim, E.H., Barbazuk, W.B. & Sessa, E.B. (2022) Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns. Frontiers in Plant Science 13: 882441. https://doi.org/10.3389/fpls.2022.882441
  95. Pichi Sermolli, R.E.G. (1977) Fragmenta Pteridologiae—VI. Webbia; Raccolta de Scritti Botanici 31 (1): 237–259. https://doi.org/10.1080/00837792.1977.10670073
  96. PPG I. (2016) A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563–603. https://doi.org/10.1111/jse.12229
  97. Prantl, K. (1883) Systematische Uebersicht der Ophioglosseen. Berichte der Deutschen Botanischen Gesellschaft 1: 348–353.
  98. Presl, C.B. (1836) Tentamen Pteridographiae, seu Genera Filicacearum. Praesertim juxta venarum decursum et distributionem exposita. Typis Filiorum Theophili Haase, Pragae, 314 pp. https://doi.org/10.5962/bhl.title.630
  99. Presl, K.B. (1847) Die Gefässbündel im Stipes der Farrn. Abhandlungen der mathematisch-naturwissenschaftlichen Classe der königl.- böhmischen Gesellschaft der Wissenschaften 5: 307–356.
  100. Pryer, K.M., Schuettpelz, E., Wolf, P.G., Schneider, H., Smith, A.R. & Cranfill, R. (2004) Phylogeny and evolution of ferns (Monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91: 1582–1598. https://doi.org/10.3732/ajb.91.10.1582
  101. Qi, X., Kuo, L.Y., Guo, C., Li, H., Li, Z., Qi, J., Wang, L., Hu, Y., Xiang, J., Zhang, C., Guo, J., Huang, C.H. & Ma, H. (2018) A well-resolved fern nuclear phylogeny reveals the evolution history of numerous transcription factor families. Molecular Phylogenetics and Evolution 127: 961–977. https://doi.org/10.1016/j.ympev.2018.06.043
  102. Rai, H.S. & Graham, S.W. (2010) Utility of a large, multigene plastid data set in inferring higher-order relationships in ferns and relatives (monilophytes). American Journal if Botany 97: 1444–1456. https://doi.org/10.3732/ajb.0900305
  103. Rambaut, A. (2018) FigTree v1.4.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. [http://tree.bio.ed.ac.uk/software/tree/]
  104. Rambaut, A. & Drummond, A.J. (2002–2021a) LogCombiner v2.6.6. (Part of the BEAST 2 package: http://beast2.cs.auckland.ac.nz/)
  105. Rambaut, A. & Drummond, A.J. (2002–2021b) TreeAnnotator v2.6.6. [https://www.beast2.org]
  106. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032
  107. Reinwardt, C.G.C. (1828) Sylloge Plantarum Novarum Itemque Minus Cognitarum a Praestantissimis Botanicis adhuc Viventibus Collecta et a Societate Regia Botanica Ratisbonensi Edita. Typis Viduae C. E. Brenck, Ratisbonae, 256 pp.
  108. Richardson, A.O., Rice, D.W., Young, G.J., Alverson, A.J. & Palmer, J.D. (2013) The “fossilized” mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biology 11: 29. https://doi.org/10.1186/1741-7007-11-29
  109. Rota, J., Malm, T., Chazot, N., Peña, C. & Wahlberg, N. (2018) A simple method for data partitioning based on relative evolutionary rates. Peer Journal of Life & Environmental Sciences 6: e5498. https://doi.org/10.7717/peerj.5498
  110. Roth, A.G. (1794) Obfervationes botanical. Neue Annalen der Botanick. Herausgegeben von Dr. Paulus Usteri. Viertes Stück 10: 34–57.
  111. Roth, A.W. (1799) Tentamen florae Germanicae; continens enumerationem plantarum in Germania sponte nascentium. Vol 3. In Bibliopolio Gleditschiano, Lipsiae, 581 pp.
  112. Rothfels, C.J., Larsson, A., Kuo, L.Y., Korall, P., Chiou, W.L. & Pryer, K.M. (2012) Overcoming deep roots, fast rates, and short internodes to resolve the ancient rapid radiation of eupolypod II ferns. Systematic Biology 61: 490–509. https://doi.org/10.1093/sysbio/sys001
  113. Rothfels, C.J., Li, F.W., Sigel, E.M., Huiet, L., Larsson, A., Burge, D.O., Ruhsam, M., Deyholos, M., Soltis, D.E., Stewart, Jr.C.N., Shaw, S.W., Pokorny, L., Chen, T., dePamphilis, C., DeGironimo, L., Chen, L., Wei, X., Sun, X., Korall, P., Stevenson, D.W., Graham, S.W., Wong, G.K.S. & Pryer, K.M. (2015) The evolutionary history of ferns inferred from 25 low-copy nuclear genes. American Journal of Botany 102: 1089–1107. https://doi.org/10.3732/ajb.1500089
  114. Rothfels, C.J. & Schuettpelz, E. (2014) Accelerated rate of molecular evolution for vittarioid ferns is strong and not driven by selection. Systematic Biology 63: 31–54. https://doi.org/10.1093/sysbio/syt058
  115. Rubinstein, C.V., Gerrienne, P., de la Puente, G.S., Astini, R.A. & Steemans, P. (2010) Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytologist 188: 365–369. https://doi.org/10.1111/j.1469-8137.2010.03433.x
  116. Ruprecht, F.J. (1845) Distributio Cryptogamarum vascularium in Imperio Rossico. Beiträge zur Pflanzenkunde des Russischen Reiches 3: 1–56.
  117. Schneider, H., Liu, H., Clark, J., Hidalgo, O., Pellicer, J., Zhang, S., Kelly, L.J., Fay, M.F. & Leitch, I.J. (2015) Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns. The New Phytologist 207: 10–13. https://doi.org/10.1111/nph.13330
  118. Schott, H. (1834) Genera Filicum. Wallishausser, Vindobonae, 10 pp.
  119. Schott, H. (1835) Genera Filicum. Wallishausser, Vindobonae, 10 pp.
  120. Schuettpelz, E. & Pryer, K.M. (2006) Reconciling extreme branch length differences: decoupling time and rate through the evolutionary history of filmy ferns. Systematic Biology 55: 485–502. https://doi.org/10.1080/10635150600755438
  121. Schuettpelz, E. & Pryer, K.M. (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56: 1037–1050. https://doi.org/10.2307/25065903
  122. Shen, Ch.-F., Hill, K.D., Tsou, Ch.-H. & Chen, Ch.-J. (1994) Cycas taitungensis C.F. Shen, K.D. Hill, C.H. Tsou & C.J. Chen, sp. nov. (Cycadaceae), a new name for the widely known cycad species endemic in Taiwan. Botanical bulletin of Academia Sinica 35: 133–140.
  123. Shen, H., Jin, D., Shu, J.P., Zhou, X.L., Lei, M., Wei, R., Shang, H., Wei, H.J., Zhang, R., Liu, L., Gu, Y.F., Zhang, X.C. & Yan, Y.H. (2018) Large-scale phylogenomic analysis resolves a backbone phylogeny in ferns. GigaScience 7: 1–11. https://doi.org/10.1093/gigascience/gix116
  124. Siebold, Fr.de & Zuccarini, J.G. (1846) Flora Japonica, Familiae Naturales. Adjectis Generum et Specierum Exemplis Selectis. Abhandlungen der Mathematisch-Physikalischen Klasse der Königlich Bayerischen Akademie der Wissenschaften XX: 123–246. https://doi.org/10.5962/bhl.title.10718
  125. Small, I.D., Schallenberg-Rüdinger, M., Takenaka, M., Mireau, H. & Ostersetzer-Biran, O. (2020) Plant organellar RNA editing: what 30 years of research has revealed. The Plant Journal 101: 1040–1056. https://doi.org/10.1111/tpj.14578
  126. Smith, A.L.S (1842) An arrangement and definition of the Genera of Ferns, with observations on the affinities of each Genus. The Journal of botany; containing Figures and Descriptions of such plants as recommended themselves by their novelty, rarity, history, or uses; together with Botanical notices and information, and occasional portraits and memoirs of eminent botanists 4: 147–198.
  127. Smith, J. (1841) Enumeratio Filicum Philippinarum; or a Systematic Arrangement of the Ferns collected by H. Cuming, Esq., F.L.S., in the Philippine Islands and the Peninsula of Malacca, between the years 1836 and 1840. The Journal of Botany; containing figures and descriptions of such plants as recommend themselves by their novelty, rarity, history or uses; together with botanical notices and information, and occasional portraits and memoirs of eminent botanists 3: 392–422.
  128. Smith, J.E. (1793) Tentamen Botanicum de Filicum Generibus Dorsiferarum. Memoires de l’Academie Royale des Sciences (Turin) 5: 401–423.
  129. Soltis, P.S., Soltis, D.E., Savolainen, V., Crane, P.R. & Barraclough, T.G. (2002) Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils. Proceedings of the National Academy of Sciences 99: 4430–4435. https://doi.org/10.1073/pnas.032087199
  130. Song, Y.-Y., Cui, X.-S., Xu, L., Xing, Y.-P., Bian, C., Qiao, Y., Yang, Y.-Y. & Kang, T.-G. (2021) The complete mitochondrial genome of Dryopteris crassirhizoma Nakai (Dryopteridaceae, Dryopteris Adanson). Mitochondrial DNA Part B Resources 6: 2704–2705. https://doi.org/10.1080/23802359.2021.1966344
  131. Sprengel, K. (1804) Anleitung zur Kenntniß der Gewächse, in Briefen. 3. Karl August Rümmel, Halle, 418 pp.
  132. Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  133. Steenwyk, J.L., Buida, T.J., Labella, A.L., Li, Y., Shen, X.X. & Rokas, A. (2021) PhyKIT: a broadly applicable UNIX shell toolkit for processing and analyzing phylogenomic data. Bioinformatics 37: 2325–2331. https://doi.org/10.1093/bioinformatics/btab096
  134. Sullivan, A.R., Eldfjell, Y., Schiffthaler, B., Delhomme, N., Asp, T., Hebelstrup, K.H., Keech, O., Öberg, L., Møller, I.M., Arvestad, L., Street, N.R. & Wang, R.X. (2020) The mitogenome of Norway spruce and a reappraisal of mitochondrial recombination in plants. Genome Biology and Evolution 12: 3586–3598. https://doi.org/10.1093/gbe/evz263
  135. Swartz, O.P. (1788) Nova Genera & Species Plantarum seu Prodromus descriptionum Vegetabilium, maximam partem incognitorum quae sub itinere in Indiam Occidentalem annis. Holmiae Stockholm Upsaliae/Aboae, Sweden, 158 pp. https://doi.org/10.5962/bhl.title.4400
  136. Swartz, O. (1800) Genera et Species Filicum ordine systematico redactarum adiectis synonymis et iconibus selectis, nec non speciebus recenter detectis, et demum plurimis dubiosis, vlterius inuestigandis. Journal für die Botanik 2: 3–120.
  137. Swartz, O. (1801) Genera et species filicum ordine systematico redactarum adiectis synonymis et iconibus selectis, nec non speciebus recenter detectis, et demum plurimis dubiosis, vlterius inuestigandis. Journal für die Botanik 1800 (2): 1–120.
  138. Swartz, O. (1806) Olai Swartz Acad. Imp. nat. cur. rel. sodalis Synopsis filicum: earum genera et species systematice complectens: adjectis lycopodineis, et descriptionibus novarum et rariorum specierum: cum tabulis aeneis quinque. Impenfis bibliopolii novi academici, Kiliae, 465 pp. https://doi.org/10.5962/bhl.title.81948
  139. Testo, W. & Sundue, M. (2016) A 4000-species dataset provides new insight into the evolution of ferns. Molecular Phylogenetics and Evolution 105: 200–211. https://doi.org/10.1016/j.ympev.2016.09.003
  140. Tryon, R.M. (1962) Taxonomic fern notes II. Pityrogramma (including Trismeria) and Anogramma. Contributions from the Gray Herbarium of Harvard University 189: 52–76. https://doi.org/10.5962/p.336400
  141. Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics 27: 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
  142. Varigerow, S., Teerkorn, T. & Knoop, V. (1999) Phylogenetic information in the mitochondrial nad5 gene of pteridophytes: RNA editing and intron sequences. Plant Biology 1: 235–243. https://doi.org/10.1111/j.1438-8677.1999.tb00249.x
  143. Wakefield, N.A. (1944) Two new species of Tmesipteris. The Victorian Naturalist 60: 142–143.
  144. Weatherby, C.A. (1935) A new variety of Cystopteris fragilis and some old ones. Rhodora 37: 373–378.
  145. Wei, R., Yang, J., He, L.J., Liu, H.M., Hu, J.Y., Liang, S.Q., Wei, X.P., Zhao, C.F. & Zhang, X.C. (2021) Plastid phylogenomics provides novel insights into the infrafamilial relationship of Polypodiaceae. Cladistics 37: 717–727. https://doi.org/10.1111/cla.12461
  146. White, C.T. (1993) Ligneous plants collected for the Arnold Arboretum in North Queensland by S. F. Kajewski in 1929. Vol.4. The Arnold Arboretum of Harvard University. Jamaica Plain, Mass, 124 pp.
  147. Wikström, N. & Pryer, K.M. (2005) Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Molecular Phylogenetics and Evolution 36: 484–493. https://doi.org/10.1016/j.ympev.2005.04.008
  148. Windham, M.D. (1993) New taxa and nomenclatural changes in the North American fern flora. Contributions from the University of Michigan Herbarium 19: 31–61.
  149. Wolf, P.G., Robison, T.A., Johnson, M.G., Sundue, M.A., Testo, W.L. & Rothfels, C.J. (2018) Target sequence capture of nuclear-encoded genes for phylogenetic analysis in ferns. Application in Plant Science 6: e01148. https://doi.org/10.1002/aps3.1148
  150. Wolf, P.G., Sessa, E.B., Marchant, D.B., Li, F.W., Rothfels, C.J., Sigel, E.M., Gitzendanner, M.A., Visger, C.J., Banks, J.A., Soltis, D.E., Soltis, P.S., Pryer, K.M. & Der, J.P. (2015) An exploration into fern genome space. Genome Biology and Evolution 7: 2533–2544. https://doi.org/10.1093/gbe/evv163
  151. Wolfe, K.H., Li, W.H. & Sharp, P.M. (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America 84: 9054–9058. https://doi.org/10.1073/pnas.84.24.9054
  152. Zardoya, R. (2020) Recent advances in understanding mitochondrial genome diversity. F1000Research 9: 270. https://doi.org/10.12688/f1000research.21490.1
  153. Zumkeller, S., Polsakiewicz, M. & Knoop, V. (2023) Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis. Communications Biology 6: 296 (2023). https://doi.org/10.1038/s42003-023-04659-8