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Type: Article
Published: 2021-06-30
Page range: 164–179
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Polyploidization within the Funariaceae—a key principle behind speciation, sporophyte reduction and the high variance of spore diameters?

State Museum of Natural History, Rosenstein 1, 70191 Stuttgart, Germany; Plant Biotechnology, Faculty of Biology, University of Freiburg, Schaenzlestrasse 1, 79104 Freiburg, Germany
Plant Biotechnology, Faculty of Biology, University of Freiburg, Schaenzlestrasse 1, 79104 Freiburg, Germany
State Museum of Natural History, Rosenstein 1, 70191 Stuttgart, Germany; Nees Institute for Biodiversity of Plants, University of Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany
Institute of Botany and Botanical Garden, Faculty of Biology, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia
Plant Cell Biology, Faculty of Biology, University of Marburg, Karl-von-Frisch-Str. 8, 35043 Marburg, Germany; SYNMIKRO Center for Synthetic Microbiology, University of Marburg, Karl-von-Frisch-Straße 16, 35043 Marburg, Germany; Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Schaenzlestrasse 18, 79104 Freiburg, Germany
State Museum of Natural History, Rosenstein 1, 70191 Stuttgart, Germany
Plant Biotechnology, Faculty of Biology, University of Freiburg, Schaenzlestrasse 1, 79104 Freiburg, Germany; Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Schaenzlestrasse 18, 79104 Freiburg, Germany; Cluster of Excellence livMATs @ FIT-Freiburg Center for Interactive Materials and Bioinspired Technologies, University of Freiburg, Georges-Köhler-Allee 105, 79110 Freiburg, Germany
Bryophyte convergent evolution genome duplication hybridization mosses post-duplication diversification Entosthodon hungaricus Physcomitrella patens


Although being recognized as a major force behind speciation in flowering plants, the evolutionary relevance of genome duplication (polyploidization) remains largely unexplored in mosses. Phylogenetic and-genomic insights from the model organism Physcomitrella patens and closely related species revealed that polyploidization, likely via hybridization (allopolyploidization), gives rise to new species within the Funariaceae. Based on the phylogenetic analysis of the nuclear single copy gene BRK1 combined with the measurement of DNA content by flow cytometry, we identified Entosthodon hungaricus as such an allopolyploid species. Together with Physcomitrium pyriforme, Physcomitrium eurystomum and Physcomitrium collenchymatum, which were identified previously as species that likely arose by hybridization, E. hungaricus represents an additional allopolyploid lineage of a species complex that is characterized by convergent sporophyte reduction and a considerable variance in spore sizes. Based on morphological and cytological data from 18 species, we highlight the potential impact of polyploidization on the size of the spores and on sporophyte architecture.


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  1. Ahrens, M. (1996) Entosthodon hungaricus in Südwestdeutschland. Herzogia 12: 199–206.
    Ahrens, M. (2000) Funariaceae. In: Nebel, M.P. & Philippi, G. (Wds.) Die Moose Baden-Württembergs, Band 1. Verlag Eugen Ulmer, Stuttgart.
    Allen, B. (2002) Moss Flora of Central America Part 2. Missouri Botanical Garden Press, St. Louis, Missouri.
    Bartram, E.B. (1972) Mosses of the Philippines. Otto Koeltz Publishers, Koenigstein-Taunus.
    Beever, J., Allison, K.W. & Child, J. (1992) The mosses of New Zealand. University of Otago Press, Dunedin.
    Beike, A.K., von Stackelberg, M., Schallenberg-Rüdinger M., Hanke, S.T., Follo, M., Quandt, D., McDaniel, S.F., Reski, R., Tan, B.C. & Rensing, S.A. (2014) Molecular evidence for convergent evolution and allopolyploid speciation within the Physcomitrium-Physcomitrella species complex. BMC Evolutionary Biology 14: 158.
    Boros, Á. (1924) Funaria hungarica, nov. spec. Magyar Botanikai Lapok 23: 73–75.
    Boros, A., Járai-Komlódi, M., Tóth, Z. & Nilsson, S. (1993) An atlas of recent European bryophyte spores. Academic Press (Akadémiai Nyomda), Budapest.
    Bridel, S.E. (1827) Bryologia universa seu systematica ad novam methodum dispositio, historia et descriptio omnium muscorum frondosorum huscusque cognitorum cum synonymia ex auctoribus probatissimis. J.A. Barth, Leipzig, 848 pp.
    Bruch, P., Schimper, W.P. & Gümbel, W.T. (1849) Bryologia Europaea seu genera muscorum Europaeorum monographice illustrata. E. Schweizerbart, Stuttgart, 108 pp.
    Bryan, V.S. (1957) Cytotaxonomic studies in the Ephemeraceae and Funariaceae. The Bryologist 60: 103–126.
    Bryhn, N. (1908) Ad cognitionem bryophytorum archipelagi Canariensis. Det Kongelige Norske Videnskabers Selskabs Skrifter 8: 1–36.
    Cano, M.J., Ros, R.M., Guerra, J. & Gonzalez, J. (1999) The identity of Entosthodon hungaricus (Boros) Loeske and E. maroccanus (Meyl.) Hebr. & Lo Giudice (=Physcomitrium maroccanum Meyl.). Journal of Bryology 21: 67–70.
    Crawford, M., Jesson, L.K. & Garnock-Jones, P.J. (2009) Correlated evolution of sexual system and life-history traits in mosses. Evolution 63: 1129–1142.
    Crow, K.D. & Wagner, G.P. (2006) Proceedings of the SMBE Tri-National Young Investigators’ Workshop 2005. What is the role of genome duplication in the evolution of complexity and diversity? Molecular Biology and Evolution 23: 887–892.
    Crum, H.A. & Anderson, L.E. (1955) Taxonomic studies in the Funariaceae. The Bryologist 58: 1–15.
    Crum, H.A. & Anderson, L.E. (1981) Mosses of Eastern North America, Vol. 1. Columbia University Press, New York, 1328 pp.
    Danilkiv, I.S. (1981) Chromosome numbers of the leafy mosses from the Kaliningrad region of RSFSR. Ukrainian Botanical Journal 38: 49–53.
    De Sloover, J.L. (1975) Note de bryologie africaine III. Physcomitrella magdalenae sp. nov. Bulletin du Jardin botanique national de Belgique / Bulletin van de National Plantentuin van België 45: 131–135.
    Dickson, J.J. (1801) Fasciculus Plantarum Cryptogamicarum Britanniae, 4. G. Nicol, London, pp. 1–28.
    Dirkse, G.M. & Losada-Lima, A. (2011) Additions and amendments to the Moss Flora of the Canary Islands. Cryptogamie, Bryologie 32: 37–41.
    Doyle, J.J. & Doyle, J.L. (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13–15.
    Drummond, T. (1841) Musci Americani: Specimens of Mosses and Junger-manniae collected by the late Thomas Drummond in the Southern States of North America, arranged and named by W. Wilson and WJ Hooker, No. 20, Warrington, 180 pp.
    During, H. (1979) Life strategies of bryophytes: A preliminary review. Lindbergia 5: 2–18.
    Fedosov, V.E., Ignatova, E.A., Ignatov, M.S. & Doroshina, G.Y. (2010) On the genus Entosthodon (Funariaceae: Musci) in the Caucasus. Arctoa 19: 75–86.
    Felsenstein, J. (1985) Phylogenies and the comparative method. The American Naturalist 125: 1–15.
    Flowers, S. (1973) Mosses: Utah and the West. Brigham Young University Press, Utah.
    Frahm, J.P. & Frey, W. (2004) Moosflora. Verlag Eugen Ulmer, Stuttgart.
    Fritsch, R. (1991) Bryophytorum Bibliotheca 40: Index to bryophyte chromosome counts. Schweizerbart Science Publishers, Stuttgart.
    Garland, T.Jr. & Díaz-Uriarte, R. (1999) Polytomies and phylogenetically independent contrasts: examination of the bounded degrees of freedom approach. Systematic Biology 48: 547–558.
    Gier, L.G. (1955) Physcomitrium collenchymatum. Transactions of the Kansas Academy of Science 58: 330–333.
    Györffy, B. (1964) Chromosome studies on Hungarian mosses. Acta Biologica Academia Scientia Hungarica 15: 26–27.
    Hébrard, J.P. & Lo Giudice, R. (1997) Entosthodon maroccanus (Meylan) Hébrard et Lo Giudice, nouvelle combinaison pour Physcomitrium maroccanum Meylan (Musci, Funariaceae). Bulletin de la société linnéenne de Provence 48: 145–146.
    Heck, M.A., Lüth, V.M., van Gessel, N., Krebs, M., Kohl, M., Prager, A., Joosten, H., Decker, E.L. & Reski, R. (2021) Axenic in vitro cultivation of 19 peat moss (Sphagnum L.) species as a resource for basic biology, biotechnology, and paludiculture. New Phytologist 229: 861–876.
    Hedwig, J. (1801) Species Muscorum Frondosorum, descriptae et tabulis aeneis lxxvii coloratis illustratae. J.A. Barth, Leipzig, 325 pp.
    Herrnstadt, I., Heyn, C.C. & Crosby, M.R. (1991) A checklist of the mosses of Israel. Bryologist 94: 168–178.
    Hooker, W.J. (1816) Plantae cryptogamicae quas in plaga orbis novi aequinoctali collegerunt Alexander de Humboldt et Amat. Bonpland. J. Harding, London.
    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
    Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J. & dePamphilis, C.W. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100.
    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.
    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.
    Košnar, J., Herbstová, M., Kolář, F., Koutecký, P. & Kučera, J. (2012) A case study of intragenomic ITS variation in bryophytes: Assessment of gene flow and role of polyploidy in the origin of European taxa of the Tortula muralis (Musci: Pottiaceae) complex. Taxon 61: 709–720.
    Lang, D., Ullrich, K.K., Murat, F., Fuchs, J., Jenkins, J., Haas, F.B., Piednoel, M., Gundlach, H., Van Bel, M., Meyberg, R., Vives, C., Morata, J., Symeonidi, A., Hiss, M., Muchero, W., Kamisugi, Y., Saleh, O., Blanc, G., Decker, E.L., van Gessel, N., Grimwood, J., Hayes, R.D., Graham, S.W., Gunter, L.E., McDaniel, S., Hoernstein, S.N.W., Larsson, A., Li, F.-W., Phillips, J., Ranjan, P., Rokshar, D.S., Rothfels, C.J., Schneider, L., Shu, S., Stevenson, D.W., Thümmler, F., Tillich, M., Villarreal Aguilar, J.C., Widiez, T., Wong, G.K.-S., Wymore, A., Zhang, Y., Zimmer, A.D., Quatrano, R.S., Mayer, K.F.X., Goodstein, D., Casacuberta, J.M., Vandepoele, K., Reski, R., Cuming, A.C., Tuskan, J., Maumus, F., Salse, J., Schmutz, J. & Rensing, S.A. (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant Journal 93: 515–533.
    Lewis, L.R., Behling, E., Gousse, H., Qian, E., Elphick, C.S., Lamarre, J.F., Bêty, J., Liebezeit, J., Rozzi, R., & Goffinet, B. (2014) First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ 2: e424.
    Limpricht, G. (1895) Die Laubmoose Deutschlands, Oesterreichs und der Schweiz. In: Fischer, A., Hauck, F., Limpricht, G., Luerssen, C., Migula, W., Rehm, H., Richter, P. & Winter, G. (Eds.) Dr. L. Rabenhorst´s Kryptogamen-Flora von Deutschland, Oesterreich und der Schweiz. Verlag von Eduard Kummer, Leipzig, 853 pp.
    Liu, Y., Budke, J.M. & Goffinet, B. (2012) Phylogenetic inference rejects sporophyte-based classification of the Funariaceae (Bryophyta): rapid radiation suggests rampant homoplasy in sporophyte evolution. Molecular Phylogenetics and Evolution 62: 130–145.
    Loeske, L. (1929) Die Laubmoose Europas II. Funariaceae. Repertorium Specierum Novarum Regni Vegetabilis, Sonderbeiheft B 3 (2): 1–171.
    Ludwig, C. (1810) Deutschlands kryptogamische Gewächse oder die 24. Classe des Linné`schen Systems, 2. Band, C. Schkuhr, Wittenberg, 212 pp.
    Maddison, W.P. & Maddison, D.R. (2006) Mesquite: A modular system for evolutionary analysis. Version 1.1. []
    McDaniel, S.F., von Stackelberg, M., Richardt, S., Quatrano, R.S., Reski, R. & Rensing, S.A. (2010) The speciation history of the Physcomitrium-Physcomitrella species complex. Evolution 64: 217–231.
    McIntosh, T.T. (2007) Funariaceae Schwägrichen. In: Crosby, M.R., Delgadillo, M.C., Harris, H., Hill, M., Kiger, R.W., McIntosh, T., Murray, B.M., Reese, W.D., Stark, L.R., Thiers, B., Vitt, D.H., Yatskievych, K. , Zander, R.H. & Zarucchi, J.L. (Eds.) Flora of North America: Volume 27: Bryophytes: Mosses, Part 1. Oxford University Press, New York.
    Medina, R., Johnson, M., Liu, Y., Wilding, N., Hedderson, T.A., Wickett, N. & Goffinet, B. (2018) Evolutionary dynamism in bryophytes: Phylogenomic inferences confirm rapid radiation in the moss family Funariaceae. Molecular Phylogenetics and Evolution 120: 240–247.
    Medina, R., Johnson, M.G., Liu, Y., Wickett, N.J., Shaw, A.J. & Goffinet, B. (2019) Phylogenomic delineation of Physcomitrium (Bryophyta: Funariaceae) based on targeted sequencing of nuclear exons and their flanking regions rejects the retention of Physcomitrella, Physcomitridium and Aphanorrhegma. Journal of Systematics and Evolution 57: 404–417.
    Meylan, C. (1937) Note sur une nouvelle espèce de Physcomitrium. Bulletin de la Société d’Histoire Naturelle de l’Afrique du Nord 28: 426–427.
    Michaux, A. (1803) Flora Boreali-Americana, sistens caracteres plantarum quas in America septentrionali collegit et detexit Andreas Michaux, Tomus Secundus. Fratres Levrault, Paris/ Strasbourg, 340 pp.
    Midford, P.E., Garland, T.Jr. & Maddison, W.P. (2005) PDAP Package of Mesquite. Version 1.07.
    Mitten, W. (1851) A list of all the Mosses and Hepaticae hitherto observed in Sussex. Annals and Magazine of Natural History, series 2, 8: 362–370.
    Mitten, W. (1869) Musci Austro-Americani. Journal of the Linnean Society, Botany 12: 1–632.
    Mitten, W. (1891) An Enumeration of all the Species of Musci and Hepaticae recorded from Japan. Transactions of the Linnean Society of London, 2nd series, Botany 3: 153–206.
    Perroud, P.F. & Quatrano, R.S. (2008) BRICK1 is required for apical cell growth in filaments of the moss Physcomitrella patens but not for gametophore morphology. Plant Cell 20: 411–422.
    Perroud, P.F., Cove, D.J., Quatrano, R.S., McDaniel, S.F. (2011) An experimental method to facilitate the identification of hybrid sporophytes in the moss Physcomitrella patens using fluorescent tagged lines. New Phytologist 191: 301–306.
    Pisarenko, O.Y., Ignatova, E.A. & Ignatov, M.S. (2001) Entosthodon hungaricus (Boros) Loeske (Funariaceae, Musci) in Altaisky Territory, South Siberia. Arctoa 10: 97–102.
    Rensing, S.A., Ick, J., Fawcett, J.A., Lang, D., Zimmer, A.D., Van de Peer, Y. & Reski, R. (2007) An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evolutionary Biology 7: 130.
    Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P.F., Lindquist, E.A., Kamisugi, Y., Tanahashi, T., Sakakibara, K., Fujita, T., Oishi, K., Shin-I, T., Kuroki, Y., Toyoda, A., Suzuki, Y., Hashimoto, S., Yamaguchi, K., Sugano, S., Kohara, Y., Fujiyama, A., Anterola, A., Aoki, S., Ashton, N., Barbazuk, W.B., Barker, E., Bennetzen, J.L., Blankenship, R., Cho, S.H., Dutcher, S.K., Estelle, M., Fawcett, J.A., Gundlach, H., Hanada, K., Heyl, A., Hicks, K.A., Hughes, J., Lohr, M., Mayer, K., Melkozernov, A., Murata, T., Nelson, D.R., Pils, B., Prigge, M., Reiss, B., Renner, T., Rombauts, S., Rushton, P.J., Sanderfoot, A., Schween, G., Shiu, S.H., Stueber, K., Theodoulou, F.L., Tu, H., Van de Peer, Y., Verrier, P.J., Waters, E., Wood, A., Yang, L., Cove, D., Cuming, A.C., Hasebe, M., Lucas, S., Mishler, B.D., Reski, R., Grigoriev, I.V., Quatrano, R.S. & Boore, J.L. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64–69.
    Rensing, S.A., Beike, A.K. & Lang, D. (2013) Evolutionary importance of generative polyploidy for genome evolution of haploid-dominant land plants. In: Leitch, I.J., Greilhuber, J., Dolezel, J. & Wendel, J. (Eds.) Plant Genome Diversity Volume 2, Springer, Vienna, 356 pp.
    Rensing, S.A. (2014) Gene duplication as a driver of plant morphogenetic evolution. Current Opinion in Plant Biology 17: 43–48.
    Reski, R. & Abel, W.O. (1985) Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165: 354–358.
    Reski, R., Faust, M., Wang, X.H., Wehe, M. & Abel, W.O. (1994) Genome analysis of the moss Physcomitrella patens (Hedw.) B.S.G.. Molecular & General Genetics 244: 352–359.
    Ricca, M., Shaw, A.J. (2010) Allopolyploidy and homoploid hybridization in the Sphagnum subsecundum complex (Sphagnaceae: Bryophyta). Biological Journal of the Linnean Society 99: 135–151.
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
    Ros, R.M. & Cano, M.J. (2008) Identity of North African endemic bryophytes, 2. Cryptogamie, Bryologie 29: 135–141.
    Roth, G. (1904) Die europäischen Laubmoose. Leipzig, Germany.
    Sabovljevic, M.S., Papp, B., Sabovljević, A., Vujičić, M., Szurdoki, E. & Segarra-Moragues, J.G. (2012) In vitro micropropagation of rare and endangered moss Entosthodon hungaricus (Funariaceae). Bioscience Journal 28: 632–640.
    Schwägrichen, C.F. (1816) Species Muscorum Frondosorum, descriptae et tabulis aeneis lxxvii coloratis illustratae, Supplementum Primum. J.A. Barth, Leipzig, pp. 1–373.
    Schwägrichen, C.F. (1823) Species Muscorum Frondosorum, descriptae et tabulis aeneis lxxvii coloratis illustratae, Supplementum Secundum. J.A. Barth, Leipzig, pp. 1–86.
    Sérgio, C. (1988) Morphological, karyological and phytogeographic observations on Entosthodon curvisetus (Schwager.) C. Müll. as a basis for a new genus, Funariella Sérgio (Funariaceae: Musci). Orsis: organismes i sistemes 3: 5–13.
    Schulte, J. & Reski, R. (2004) High throughput cryopreservation of 140,000 Physcomitrella patens mutants. Plant Biology 6: 119–127.
    Schween, G., Gorr, G., Hohe, A. & Reski, R. (2003) Unique tissue-specific cell cycle in Physcomitrella. Plant Biology 5: 50–58.
    Sharp, A.J., Crum, H. & Eckel, P.M. (1994) The moss flora of Mexico. Part One. The New York Botanical Garden, Bronx, New York, 580 pp.
    Sendtner, O. (1841) Musci quidam frondosi recentius detecti. Denkschriften der Bayerischen Botanischen Gesellschaft in Regensburg 3: 138–151.
    Soltis, D.E. & Soltis, P.S. (1999). Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348–352.
    Soltis, P.S. & Soltis, D.E. (2009) The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561–588.
    Stenøien, H.K., Shaw, A.J., Stengrundet, K. & Flatberg, K.I. (2011) The narrow endemic Norwegian peat moss Sphagnum troendelagicum originated before the last glacial maximum. Heredity 106: 370–382.
    Sullivant, W. (1848) Musci and hepaticae. In: Gray, A. (Ed.) A Manual of the Botany of the Northern United States. J. Monroe & Co., Boston, 647 pp.
    Toren, D. (2008) Funaria convexa Spruce (Musci: Funariaceae) new to North America. Evansia 25: 94–96.
    Trabut, L.C. (1922) Deux Funariacées nouvelles. Revue Bryologique 49: 64–65.
    Van de Peer, Y., Mizrachi, E. & Marchal, K. (2017) The evolutionary significance of polyploidy. Nature Review Genetics 18: 411–424.
    Von Wettstein, F. (1924) Morphologie und Physiologie des Formwechsels der Moose auf genetischer Grundlage I. Zeitschrift für induktive Abstammungs-und Vererbungslehre 33: 1–236.
    Williams, R. (1901) Funaria flavicans Michx. The Bryologist 4: 9–10.
    Wyatt, R., Odrzykoski, I.J., Stoneburner, A., Bass, H.W. & Galau, G.A. (1988) Allopolyploidy in bryophytes: Multiple origins of Plagiomnium medium. Proceedings of the National Academy of Sciences of the United States of America 85: 5601–5604.
    Wyatt, R., Odrzykoski, I.J. & Stoneburner, A. (1992) Isozyme evidence of reticulate evolution in mosses: Plagiomnium medium is an allopolyploid of P. ellipticum × P. insigne. Systematic Botany 17: 532–550.
    Wyatt, R. & Odrzykoski, I.J. (1998) On the origins of the allopolyploid moss Plagiomnium cuspidatum. Bryologist 101: 263–271.
    Zechmeister, H.G. (2005) Bryophytes of continental salt meadows in Austria. Journal of Bryology 27: 297–302.