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Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids

BACKGROUND: Mycorrhiza is a ubiquitous form of symbiosis based on the mutual, beneficial exchange of resources between roots of autotrophic (AT) plants and heterotrophic soil fungi throughout a complex network of fungal mycelium. Mycoheterotrophic (MH) and mixotrophic (MX) plants can parasitise this...

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Autores principales: Minasiewicz, Julita, Zwolicki, Adrian, Figura, Tomáš, Novotná, Alžběta, Bocayuva, Melissa F., Jersáková, Jana, Selosse, Marc-André
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10496321/
https://www.ncbi.nlm.nih.gov/pubmed/37700257
http://dx.doi.org/10.1186/s12870-023-04436-z
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author Minasiewicz, Julita
Zwolicki, Adrian
Figura, Tomáš
Novotná, Alžběta
Bocayuva, Melissa F.
Jersáková, Jana
Selosse, Marc-André
author_facet Minasiewicz, Julita
Zwolicki, Adrian
Figura, Tomáš
Novotná, Alžběta
Bocayuva, Melissa F.
Jersáková, Jana
Selosse, Marc-André
author_sort Minasiewicz, Julita
collection PubMed
description BACKGROUND: Mycorrhiza is a ubiquitous form of symbiosis based on the mutual, beneficial exchange of resources between roots of autotrophic (AT) plants and heterotrophic soil fungi throughout a complex network of fungal mycelium. Mycoheterotrophic (MH) and mixotrophic (MX) plants can parasitise this system, gaining all or some (respectively) required nutrients without known reciprocity to the fungus. We applied, for the first time, an ecological stoichiometry framework to test whether trophic mode of plants influences their elemental carbon (C), nitrogen (N), and phosphorus (P) composition and may provide clues about their biology and evolution within the framework of mycorrhizal network functioning. RESULTS: We analysed C:N:P stoichiometry of 24 temperate orchid species and P concentration of 135 species from 45 plant families sampled throughout temperate and intertropical zones representing the three trophic modes (AT, MX and MH). Welch’s one-way ANOVA and PERMANOVA were used to compare mean nutrient values and their proportions among trophic modes, phylogeny, and climate zones. Nutrient concentration and stoichiometry significantly differentiate trophic modes in orchids. Mean foliar C:N:P stoichiometry showed a gradual increase of N and P concentration and a decrease of C: nutrients ratio along the trophic gradient AT < MX < MH, with surprisingly high P requirements of MH orchids. Although P concentration in orchids showed the trophy-dependent pattern regardless of climatic zone, P concentration was not a universal indicator of trophic modes, as shown by ericaceous MH and MX plants. CONCLUSION: The results imply that there are different evolutionary pathways of adaptation to mycoheterotrophic nutrient acquisition, and that the high nutrient requirements of MH orchids compared to MH plants from other families may represent a higher cost to the fungal partner and consequently lead to the high fungal specificity observed in MH orchids. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04436-z.
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spelling pubmed-104963212023-09-13 Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids Minasiewicz, Julita Zwolicki, Adrian Figura, Tomáš Novotná, Alžběta Bocayuva, Melissa F. Jersáková, Jana Selosse, Marc-André BMC Plant Biol Research BACKGROUND: Mycorrhiza is a ubiquitous form of symbiosis based on the mutual, beneficial exchange of resources between roots of autotrophic (AT) plants and heterotrophic soil fungi throughout a complex network of fungal mycelium. Mycoheterotrophic (MH) and mixotrophic (MX) plants can parasitise this system, gaining all or some (respectively) required nutrients without known reciprocity to the fungus. We applied, for the first time, an ecological stoichiometry framework to test whether trophic mode of plants influences their elemental carbon (C), nitrogen (N), and phosphorus (P) composition and may provide clues about their biology and evolution within the framework of mycorrhizal network functioning. RESULTS: We analysed C:N:P stoichiometry of 24 temperate orchid species and P concentration of 135 species from 45 plant families sampled throughout temperate and intertropical zones representing the three trophic modes (AT, MX and MH). Welch’s one-way ANOVA and PERMANOVA were used to compare mean nutrient values and their proportions among trophic modes, phylogeny, and climate zones. Nutrient concentration and stoichiometry significantly differentiate trophic modes in orchids. Mean foliar C:N:P stoichiometry showed a gradual increase of N and P concentration and a decrease of C: nutrients ratio along the trophic gradient AT < MX < MH, with surprisingly high P requirements of MH orchids. Although P concentration in orchids showed the trophy-dependent pattern regardless of climatic zone, P concentration was not a universal indicator of trophic modes, as shown by ericaceous MH and MX plants. CONCLUSION: The results imply that there are different evolutionary pathways of adaptation to mycoheterotrophic nutrient acquisition, and that the high nutrient requirements of MH orchids compared to MH plants from other families may represent a higher cost to the fungal partner and consequently lead to the high fungal specificity observed in MH orchids. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04436-z. BioMed Central 2023-09-12 /pmc/articles/PMC10496321/ /pubmed/37700257 http://dx.doi.org/10.1186/s12870-023-04436-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Minasiewicz, Julita
Zwolicki, Adrian
Figura, Tomáš
Novotná, Alžběta
Bocayuva, Melissa F.
Jersáková, Jana
Selosse, Marc-André
Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title_full Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title_fullStr Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title_full_unstemmed Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title_short Stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
title_sort stoichiometry of carbon, nitrogen and phosphorus is closely linked to trophic modes in orchids
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10496321/
https://www.ncbi.nlm.nih.gov/pubmed/37700257
http://dx.doi.org/10.1186/s12870-023-04436-z
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