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Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities

BACKGROUND: The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex pla...

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Autores principales: Perez-Lamarque, Benoît, Petrolli, Rémi, Strullu-Derrien, Christine, Strasberg, Dominique, Morlon, Hélène, Selosse, Marc-André, Martos, Florent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9297633/
https://www.ncbi.nlm.nih.gov/pubmed/35859141
http://dx.doi.org/10.1186/s40793-022-00434-0
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author Perez-Lamarque, Benoît
Petrolli, Rémi
Strullu-Derrien, Christine
Strasberg, Dominique
Morlon, Hélène
Selosse, Marc-André
Martos, Florent
author_facet Perez-Lamarque, Benoît
Petrolli, Rémi
Strullu-Derrien, Christine
Strasberg, Dominique
Morlon, Hélène
Selosse, Marc-André
Martos, Florent
author_sort Perez-Lamarque, Benoît
collection PubMed
description BACKGROUND: The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Réunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks. RESULTS: The 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina (Endogonales) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae, namely Helotiales, Sebacinales, and Cantharellales, also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks. CONCLUSIONS: This study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00434-0.
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spelling pubmed-92976332022-07-21 Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities Perez-Lamarque, Benoît Petrolli, Rémi Strullu-Derrien, Christine Strasberg, Dominique Morlon, Hélène Selosse, Marc-André Martos, Florent Environ Microbiome Research BACKGROUND: The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Réunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks. RESULTS: The 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina (Endogonales) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae, namely Helotiales, Sebacinales, and Cantharellales, also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks. CONCLUSIONS: This study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00434-0. BioMed Central 2022-07-20 /pmc/articles/PMC9297633/ /pubmed/35859141 http://dx.doi.org/10.1186/s40793-022-00434-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Perez-Lamarque, Benoît
Petrolli, Rémi
Strullu-Derrien, Christine
Strasberg, Dominique
Morlon, Hélène
Selosse, Marc-André
Martos, Florent
Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title_full Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title_fullStr Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title_full_unstemmed Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title_short Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
title_sort structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9297633/
https://www.ncbi.nlm.nih.gov/pubmed/35859141
http://dx.doi.org/10.1186/s40793-022-00434-0
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