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A pantropically introduced tree is followed by specific ectomycorrhizal symbionts due to pseudo-vertical transmission

The ISME Journalvolume 12pages18061816 (2018) | Download Citation

Abstract

Global trade increases plant introductions, but joint introduction of associated microbes is overlooked. We analyzed the ectomycorrhizal fungi of a Caribbean beach tree, seagrape (Coccoloba uvifera, Polygonacaeae), introduced pantropically to stabilize coastal soils and produce edible fruits. Seagrape displays a limited symbiont diversity in the Caribbean. In five regions of introduction (Brazil, Japan, Malaysia, Réunion and Senegal), molecular barcoding showed that seagrape mostly or exclusively associates with Scleroderma species (Basidiomycota) that were hitherto only known from Caribbean seagrape stands. An unknown Scleroderma species dominates in Brazil, Japan and Malaysia, while Scleroderma bermudense exclusively occurs in Réunion and Senegal. Population genetics analysis of S. bermudense did not detect any demographic bottleneck associated with a possible founder effect, but fungal populations from regions where seagrape is introduced are little differentiated from the Caribbean ones, separated by thousands of kilometers, consistently with relatively recent introduction. Moreover, dry seagrape fruits carry Scleroderma spores, probably because, when drying on beach sand, they aggregate spores from the spore bank accumulated by semi-hypogeous Scleroderma sporocarps. Aggregated spores inoculate seedlings, and their abundance may limit the founder effect after seagrape introduction. This rare pseudo-vertical transmission of mycorrhizal fungi likely contributed to efficient and repeated seagrape/Scleroderma co-introductions.

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Acknowledgements

We thank three referees for revisions, David Marsh for English corrections, and the Service de Systématique Moléculaire (UMS2700 MNHN/CNRS) for its facilities. Seynabou Séne received grants from the Guadeloupe Region, Institut de Recherche pour le Développement, Ministry of Education and Research of Senegal, World Federation of Scientists, and the Laboratoire Mixte International-Adaptation des Plantes et microorganismes associés aux Stress Environnementaux (Dakar).

Author information

Author notes

  1. These authors contributed equally: Seynabou Séne, Marc-André Selosse, Amadou Bâ.

Affiliations

  1. LMI-LAPSE/Laboratoire Commun de Microbiologie, IRD/UCAD/ISRA, BP 1386, Dakar, Senegal

    • Seynabou Séne
    • , Khoudia Cissé
    • , Abdala Gamby Diédhiou
    •  & Samba Ndao Sylla
  2. Institut de Systématique, Évolution, Biodiversité (UMR 7205 – CNRS, MNHN, UPMC, EPHE), Muséum National d’Histoire Naturelle, Sorbonne Universités, 57 rue Cuvier, 75005, Paris, France

    • Seynabou Séne
    • , Marc-André Selosse
    • , Mathieu Forget
    •  & Josie Lambourdière
  3. Faculty of Biology, Department of Plant Taxonomy and Nature Conservation, University of Gdańsk, Wita Stwosza 59, 80-308, Gdansk, Poland

    • Marc-André Selosse
  4. Departamento de Biología, Universidad de Puerto Rico, Parque Industrial Minillas Carr 174, Bayamón, PR, 00959-1911, USA

    • Elsie Rivera-Ocasio
  5. Université de La Réunion, 15 Av. R. Cassin CS 92003, 97744, Saint-Denis, Réunion, France

    • Hippolyte Kodja
  6. Faculty of Agriculture, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    • Norikazu Kameyama
  7. Graduate School of Frontier Science, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8563, Japan

    • Kazuhide Nara
  8. Normandie Univ, UNIROUEN, IRSTEA, ECODIV, 76000, Rouen, France

    • Lucie Vincenot
  9. Laboratoire C3MAG, Université des Antilles, BP 592, 97159, Pointe-à-Pitre, Guadeloupe, France

    • Jean-Louis Mansot
  10. Pusat Asasi Sains Pertanian, Universiti Putra Malaysia, 43400 UPM, Serdang, Malaysia

    • Jean Weber
  11. Laboratoire Evolution et Diversité Biologique, Université Paul Sabatier – CNRS, 118 route de Narbonne, 31062, Toulouse Cedex, France

    • Mélanie Roy
  12. Laboratoire de Biologie et Physiologie Végétales, Université des Antilles, BP 592, 97159, Pointe-à-Pitre, France

    • Amadou Bâ
  13. Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR113 INRA/AGRO-M/CIRAD/IRD/UM2-TA10/J, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France

    • Amadou Bâ

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The authors declare that they have no conflict of interest.

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Correspondence to Marc-André Selosse.

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https://doi.org/10.1038/s41396-018-0088-y