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Identifying a mysterious aquatic fern gametophyte

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Abstract

Süßwassertang, a popular aquatic plant that is sold worldwide in aquarium markets, has been long considered a liverwort because of its ribbon-like thallus. However, its antheridia are remarkably fern-like in morphology. To corroborate the hypothesis that Süßwassertang is a fern gametophyte and to determine its closest relative, we have sequenced five chloroplast regions (rbcL, accD, rps4–trnS, trnL intron, and trnL-F intergenic spacer), applying a DNA-based identification approach. The BLAST results on all regions revealed that Süßwassertang is a polypod fern (order: Polypodiales) with strong affinities to the Lomariopsidaceae. Our phylogenetic analyses further showed that Süßwassertang is nested within the hemi-epiphytic fern genus Lomariopsis (Lomariopsidaceae) and aligned very close to L. lineata. Our study brings new insights on the unexpected biology of Lomariopsis gametophytes—the capacity of retaining a prolonged gametophytic stage under water. It is of great interest to discover that a fern usually known to grow on trees also has gametophytes that thrive in water.

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Acknowledgment

The authors thank Li-Yaung Kuo for laboratory help, Tien-Chuan Hsu for collecting Taiwanese Lomariopsis spectabilis, and Dr. Wen-Liang Chiou (Taiwan Forestry Research Institute) for valuable comments.

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Author notes

  1. Dietmar Quandt

    Present address: Nees Institute for Biodiversity of Plants, University of Bonn, Meckneheimer Allee 170, 53115, Bonn, Germany

Authors and Affiliations

  1. Department of Life Science, National Taiwan University, Taipei, 106, Taiwan

    Fay-Wei Li & Chun-Neng Wang

  2. The Herbarium, Singapore Botanic Gardens, Singapore, 295969, Singapore

    Benito C. Tan

  3. Plant Phylogenetics and Phylogenomics Group, Institute of Botany, Dresden University of Technology, 01062, Dresden, Germany

    Volker Buchbender & Dietmar Quandt

  4. The New York Botanical Garden, Bronx, New York, NY, 10458-5126, USA

    Robbin C. Moran

  5. Muséum National d’Histoire Naturelle, UMR 7205, Herbier National, CP39, 16 rue Buffon, 75005, Paris, France

    Germinal Rouhan

  6. Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, 106, Taiwan

    Chun-Neng Wang

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  1. Fay-Wei Li
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Correspondence to Fay-Wei Li, Chun-Neng Wang or Dietmar Quandt.

Appendix

Appendix

Voucher information and GenBank accession numbersa for rbcL, accD, trnL-F and rps4 (plus rps4-trnS IGS) sequences used in this study.

Part 1: rbcL and accD

Taxon—GenBank accessions: rbcL, accD; voucher (collection locality; herbarium) or reference.

Arachniodes aristata (G.Forst.) Tindale—AB232490, AB232418; Tsutsumi and Kato 2006. Araiostegia faberiana (C.Chr.) Ching—AB212688*; Tsutsumi and Kato 2005. Arthropteris backleri (Hook.) Mett.—AB212686*; Tsutsumi and Kato 2005. Athyrium niponicum (Mett.) Hance—AB232413, AB232441; Tsutsumi and Kato 2006. Bolbitis repanda (Blume) Schott—AB232399, AB232427; Tsutsumi and Kato 2006. Colysis wrightii (Hook.) Ching—AB232406, AB232434; Tsutsumi and Kato 2006. Crypsinus enervis (Cav.) Copel.—AB232407, AB232435; Tsutsumi and Kato 2006. Ctenitis eatonii (Baker) Ching—AB232391, AB232419; Tsutsumi and Kato 2006. Cyclopeltis crenata (Fée) C. Chr.—DQ054517+; Li and Lu 2006. Cyclopeltis crenata (Fée) C. Chr+, EU216746; F. W. Li 568 (private garden, originally from Thailand; TAIF). Davallia formosana Hayata—AB212704*; Tsutsumi and Kato 2005. Dryopteris erythrosora (D.C.Eaton) Kuntze—AB232392, AB232420; Tsutsumi and Kato 2006. Elaphoglossum callifolium (Blume) T.Moore—AB232400, AB232428; Tsutsumi and Kato 2006. Goniophlebium persicifolium (Desv.) Bedd.—AB232408, AB232436; Tsutsumi and Kato 2006. Grammitis reinwardtii Blume—AB232398, AB232426; Tsutsumi and Kato 2006. Gymnogrammitis dareiformis (Hook.) Ching ex Tardieu and C.Chr.—AB232409, AB232437; Tsutsumi and Kato 2006. Hypodematium crenatum (Forssk.) Kuhn ssp. fauriei (Kodama) K.Iwats.—AB232414, AB232442; Tsutsumi and Kato 2006. Leucostegia immersa (Wall. ex Hook.) C.Presl—AB232388, AB232416; Tsutsumi and Kato 2006. Leucostegia pallida (Mett.) Copel.—AB232389, AB232417; Tsutsumi and Kato 2006. Lomariopsis marginata (Schrad.) Kuhn.—AY818677, NA; Skog et al. 2004. Lomariopsis sp. (Süßwassertang)—EU216743, EU216744; F. W. Li 569 (unknown origin; TAIF). Lomariopsis sp. (Süßwassertang) —AM946394+; F042 (unknown origin; SING). Lomariopsis spectabilis (Kunze) Mett.—AB232401, AB232429; Tsutsumi and Kato 2006. Loxogramme avenia (Blume) C.Presl—AB232410, AB232438; Tsutsumi and Kato 2006. Matteuccia struthiopteris (L.) Tod.—AB232415, AB232443; Tsutsumi and Kato 2006. Microsorum zippelii (Blume) Ching—AB232411, AB232439; Tsutsumi and Kato 2006. Nephrolepis acuminata (Houtt.) Kuhn—AB232403, AB232431; Tsutsumi and Kato 2006. Nephrolepis cordifolia (L.) C.Presl—AB232404, AB232432; Tsutsumi and Kato 2006. Oleandra pistillaris (Sw.) C.Chr.—AB232405, AB232433; Tsutsumi and Kato 2006. Oleandra wallichii (Hook.) C.Presl—AB212687*; Tsutsumi and Kato 2005. Polybotrya caudata Kunze—AB232393, AB232421; Tsutsumi and Kato 2006. Polystichum fibrilloso-paleaceum (Kodama) Tagawa—AB232394, AB232422; Tsutsumi and Kato 2006. Pyrrosia rasamalae (Racib.) K·H.Shing—AB232412, AB232440; Tsutsumi and Kato 2006. Quercifilix zeylanica (Houtt.) Copel.—AB232395, AB232423; Tsutsumi and Kato 2006. Rumohra adiantiformis (G.Forst.) Ching—AB232396, AB232424; Tsutsumi and Kato 2006. Tectaria phaeocaulis (Rosenst.) C.Chr.—AB232397, AB232425; Tsutsumi and Kato 2006. Teratophyllum wilkesianum (Brack.) Holttum—AB232402, AB232430; Tsutsumi and Kato 2006.

Part 2: trnL-F

Taxon—GenBank accessions: trnL-F; voucher (collection locality; herbarium) or reference.

Lomariopsis: L. amydrophlebia (Sloss. ex Maxon) Holttum—DQ396555; Rouhan et al. 2007. L. boivinii Holttum—DQ396557; Rouhan et al. 2007. L. cordata (Bonap.) Alston—DQ396558; Rouhan et al. 2007. L. crassifolia Holttum—DQ396559; Rouhan et al. 2007. L. guineensis (Underw.) Alston—DQ396560; Rouhan et al. 2007. L. hederacea Alston—DQ396561; Rouhan et al. 2007. L. jamaicensis (Underw.) Holttum—DQ396562; Rouhan et al. 2007. L. japurensis (Mart.) J. Sm.—DQ396567; Rouhan et al. 2007. L. kunzeana (Underw.) Holttum—DQ396570; Rouhan et al. 2007. L. latipinna Stolze—DQ396571; Rouhan et al. 2007. L. lineata (C. Presl) Holttum—DQ396572; Rouhan et al., 2007. L. longicaudata (Bonap.) Holttum—DQ396573; Rouhan et al. 2007. L. madagascarica (Bonap.) Alston—DQ396576; Rouhan et al. 2007. L. mannii (Underw.) Alston—DQ396577; Rouhan et al. 2007. L. marginata (Schrad.) Kuhn—DQ396579; Rouhan et al. 2007. L. maxonii (Underw.) Holttum—DQ396580; Rouhan et al. 2007. L. muriculata Holttum—DQ396582; Rouhan et al. 2007. L. nigropaleata Holttum—DQ396584; Rouhan et al. 2007. L. palustris (Hook.) Mett. ex Kuhn—DQ396585; Rouhan et al. 2007. L. pervillei (Mett.) Kuhn—DQ396587; Rouhan et al. 2007. L. pollicina Willem. ex Kuhn—DQ396588; Rouhan et al. 2007. L. prieuriana Fée—DQ396590; Rouhan et al. 2007. L. recurvata Fée—DQ396592; Rouhan et al., 2007. L. rossii Holttum—DQ396594; Rouhan et al. 2007. L. salicifolia (Kunze) Lellinger—DQ396595; Rouhan et al. 2007. L. sp.—DQ396602; Rouhan et al. 2007. L. sp.—DQ396601; Rouhan et al. 2007. L. sp.—DQ396603; Rouhan et al. 2007. L. sp. (Süßwassertang)—EU216745; F. W. Li 569 (unknown origin; TAIF). Lomariopsis sp. (Süßwassertang) —AM946393; F042 (unknown origin; SING). L. spectabilis—EU216748; F.W. Li 567 (Wulai, Taiwan; TAIF). L. vestita E. Fourn.—DQ396598; Rouhan et al. 2007. L. wrightii Mett. ex D. C. Eaton—DQ396600; Rouhan et al. 2007.

Cyclopeltis crenata (Fée) C. Chr.—EU216746; F. W. Li 568 (private garden, originally from Thailand; TAIF). Hypodematium crenatum (Forssk.) Kuhn—AF425122; Smith and Cranfill 2002.

Part 3: rps4 (plus rps4-trnS IGS)

Lomariopsis sp. (Süßwassertang) — AM947063; F042 (unknown origin; SING).

aAsterisk, The same accession as previously noted; cross, this sequence is available in a different voucher but the same taxon; NA, data are not available for this taxon.

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Li, FW., Tan, B.C., Buchbender, V. et al. Identifying a mysterious aquatic fern gametophyte. Plant Syst Evol 281, 77–86 (2009). https://doi.org/10.1007/s00606-009-0188-2

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