Dark septate endophytes and arbuscular mycorrhizal fungi (Paris‐morphotype) affect the stable isotope composition of ‘classically’ non‐mycorrhizal plants

The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as non‐mycorrhizal, however, are not necessarily free of any fungi, but are frequently colonized by elusive fungal endophytes, such as dark septate e...

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Published inFunctional ecology Vol. 34; no. 12; pp. 2453 - 2466
Main Authors Giesemann, Philipp, Eichenberg, David, Stöckel, Marcus, Seifert, Lukas F., Gomes, Sofia I. F., Merckx, Vincent S. F. T., Gebauer, Gerhard, Bennett, Alison
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LanguageEnglish
Published London Wiley Subscription Services, Inc 01.12.2020
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Abstract The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as non‐mycorrhizal, however, are not necessarily free of any fungi, but are frequently colonized by elusive fungal endophytes, such as dark septate endophytes (DSE) or fine root endophytes (FRE). While a functional role of FRE in the improvement of nutrient gain was recently elucidated, the function of DSE is still in discussion and was here addressed for 36 plant species belonging to the families Equisetaceae, Cypereaceae and Caryophyllaceae. Molecular and microscopic staining approaches were conducted to verify the presence of DSE in the investigated species. Stable isotope natural abundances of the elements carbon, nitrogen, hydrogen and oxygen and total nitrogen concentrations were analysed for the respective species of the target plant families and accompanying mycorrhizal and non‐mycorrhizal (Brassicaceae) plant species. Staining approaches confirmed the presence of DSE in all investigated species within the families Equisetaceae, Cyperaceae and Caryophyllaceae. A co‐colonization with Paris‐type arbuscular mycorrhiza (AM) was occasionally found by staining and molecular approaches in species of the Equisetaceae. Species of the Equisetaceae, Cyperaceae and Caryophyllaceae were significantly 15N‐enriched in comparison to accompanying plants. In addition, a significant 13C and 2H enrichment and increased total nitrogen concentrations were found for representatives of the Equisetaceae. The 15N enrichment found here for representatives of Equisetaceae, Cyperaceae and Caryophyllaceae provides evidence for a functional role of the ubiquitous DSE fungi. DSE fungi obviously provide access to 15N‐enriched soil organic compounds probably in exchange for organic carbon compounds from plant photosynthesis. As indicated by additional 13C and 2H enrichments, representatives of the Equisetaceae apparently gain simultaneously organic carbon compounds from their AM fungi of the Paris‐morphotype. Thus, species of the Equisetaceae have to be considered as partially, or in case of the achlorophyllous fertile Equisetum arvense, as fully mycoheterotrophic at least in some stages of their life cycle. So far, mostly underappreciated fungi classified as DSE are suggested to occupy an ecologically relevant role similar to mycorrhizae and the occurrence of simultaneous functions of DSE and AM fungi in Equisetaceae is proposed. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
AbstractList Abstract The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as non‐mycorrhizal, however, are not necessarily free of any fungi, but are frequently colonized by elusive fungal endophytes, such as dark septate endophytes ( DSE ) or fine root endophytes ( FRE ). While a functional role of FRE in the improvement of nutrient gain was recently elucidated, the function of DSE is still in discussion and was here addressed for 36 plant species belonging to the families Equisetaceae, Cypereaceae and Caryophyllaceae. Molecular and microscopic staining approaches were conducted to verify the presence of DSE in the investigated species. Stable isotope natural abundances of the elements carbon, nitrogen, hydrogen and oxygen and total nitrogen concentrations were analysed for the respective species of the target plant families and accompanying mycorrhizal and non‐mycorrhizal (Brassicaceae) plant species. Staining approaches confirmed the presence of DSE in all investigated species within the families Equisetaceae, Cyperaceae and Caryophyllaceae. A co‐colonization with Paris ‐type arbuscular mycorrhiza (AM) was occasionally found by staining and molecular approaches in species of the Equisetaceae. Species of the Equisetaceae, Cyperaceae and Caryophyllaceae were significantly 15 N‐enriched in comparison to accompanying plants. In addition, a significant 13 C and 2 H enrichment and increased total nitrogen concentrations were found for representatives of the Equisetaceae. The 15 N enrichment found here for representatives of Equisetaceae, Cyperaceae and Caryophyllaceae provides evidence for a functional role of the ubiquitous DSE fungi. DSE fungi obviously provide access to 15 N‐enriched soil organic compounds probably in exchange for organic carbon compounds from plant photosynthesis. As indicated by additional 13 C and 2 H enrichments, representatives of the Equisetaceae apparently gain simultaneously organic carbon compounds from their AM fungi of the Paris ‐morphotype. Thus, species of the Equisetaceae have to be considered as partially, or in case of the achlorophyllous fertile Equisetum arvense , as fully mycoheterotrophic at least in some stages of their life cycle. So far, mostly underappreciated fungi classified as DSE are suggested to occupy an ecologically relevant role similar to mycorrhizae and the occurrence of simultaneous functions of DSE and AM fungi in Equisetaceae is proposed. A free Plain Language Summary can be found within the Supporting Information of this article.
The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as non‐mycorrhizal, however, are not necessarily free of any fungi, but are frequently colonized by elusive fungal endophytes, such as dark septate endophytes (DSE) or fine root endophytes (FRE). While a functional role of FRE in the improvement of nutrient gain was recently elucidated, the function of DSE is still in discussion and was here addressed for 36 plant species belonging to the families Equisetaceae, Cypereaceae and Caryophyllaceae.Molecular and microscopic staining approaches were conducted to verify the presence of DSE in the investigated species. Stable isotope natural abundances of the elements carbon, nitrogen, hydrogen and oxygen and total nitrogen concentrations were analysed for the respective species of the target plant families and accompanying mycorrhizal and non‐mycorrhizal (Brassicaceae) plant species.Staining approaches confirmed the presence of DSE in all investigated species within the families Equisetaceae, Cyperaceae and Caryophyllaceae. A co‐colonization with Paris‐type arbuscular mycorrhiza (AM) was occasionally found by staining and molecular approaches in species of the Equisetaceae. Species of the Equisetaceae, Cyperaceae and Caryophyllaceae were significantly 15N‐enriched in comparison to accompanying plants. In addition, a significant 13C and 2H enrichment and increased total nitrogen concentrations were found for representatives of the Equisetaceae.The 15N enrichment found here for representatives of Equisetaceae, Cyperaceae and Caryophyllaceae provides evidence for a functional role of the ubiquitous DSE fungi. DSE fungi obviously provide access to 15N‐enriched soil organic compounds probably in exchange for organic carbon compounds from plant photosynthesis. As indicated by additional 13C and 2H enrichments, representatives of the Equisetaceae apparently gain simultaneously organic carbon compounds from their AM fungi of the Paris‐morphotype. Thus, species of the Equisetaceae have to be considered as partially, or in case of the achlorophyllous fertile Equisetum arvense, as fully mycoheterotrophic at least in some stages of their life cycle.So far, mostly underappreciated fungi classified as DSE are suggested to occupy an ecologically relevant role similar to mycorrhizae and the occurrence of simultaneous functions of DSE and AM fungi in Equisetaceae is proposed.A free Plain Language Summary can be found within the Supporting Information of this article.
The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as non‐mycorrhizal, however, are not necessarily free of any fungi, but are frequently colonized by elusive fungal endophytes, such as dark septate endophytes (DSE) or fine root endophytes (FRE). While a functional role of FRE in the improvement of nutrient gain was recently elucidated, the function of DSE is still in discussion and was here addressed for 36 plant species belonging to the families Equisetaceae, Cypereaceae and Caryophyllaceae. Molecular and microscopic staining approaches were conducted to verify the presence of DSE in the investigated species. Stable isotope natural abundances of the elements carbon, nitrogen, hydrogen and oxygen and total nitrogen concentrations were analysed for the respective species of the target plant families and accompanying mycorrhizal and non‐mycorrhizal (Brassicaceae) plant species. Staining approaches confirmed the presence of DSE in all investigated species within the families Equisetaceae, Cyperaceae and Caryophyllaceae. A co‐colonization with Paris‐type arbuscular mycorrhiza (AM) was occasionally found by staining and molecular approaches in species of the Equisetaceae. Species of the Equisetaceae, Cyperaceae and Caryophyllaceae were significantly 15N‐enriched in comparison to accompanying plants. In addition, a significant 13C and 2H enrichment and increased total nitrogen concentrations were found for representatives of the Equisetaceae. The 15N enrichment found here for representatives of Equisetaceae, Cyperaceae and Caryophyllaceae provides evidence for a functional role of the ubiquitous DSE fungi. DSE fungi obviously provide access to 15N‐enriched soil organic compounds probably in exchange for organic carbon compounds from plant photosynthesis. As indicated by additional 13C and 2H enrichments, representatives of the Equisetaceae apparently gain simultaneously organic carbon compounds from their AM fungi of the Paris‐morphotype. Thus, species of the Equisetaceae have to be considered as partially, or in case of the achlorophyllous fertile Equisetum arvense, as fully mycoheterotrophic at least in some stages of their life cycle. So far, mostly underappreciated fungi classified as DSE are suggested to occupy an ecologically relevant role similar to mycorrhizae and the occurrence of simultaneous functions of DSE and AM fungi in Equisetaceae is proposed. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
Author Stöckel, Marcus
Gebauer, Gerhard
Merckx, Vincent S. F. T.
Giesemann, Philipp
Gomes, Sofia I. F.
Bennett, Alison
Seifert, Lukas F.
Eichenberg, David
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Niu S. (e_1_2_8_51_1) 2003; 27
e_1_2_8_79_1
Abarenkov K. (e_1_2_8_2_1) 2020
Lenhard W. (e_1_2_8_43_1) 2017
e_1_2_8_10_1
e_1_2_8_31_1
e_1_2_8_56_1
e_1_2_8_77_1
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e_1_2_8_33_1
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e_1_2_8_73_1
e_1_2_8_50_1
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Snippet The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered as...
Abstract The vast majority of terrestrial plants exchange nutrients with fungal partners forming different mycorrhizal types. The minority of plants considered...
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SubjectTerms Arbuscular mycorrhizas
Carbon
Carbon 13
Carbon compounds
Caryophyllaceae
Colonization
Cyperaceae
dark septate endophytes
Endophytes
Enrichment
Equisetaceae
Exchanging
Flowers & plants
Fungi
Isotope composition
Life cycles
mycoheterotrophy
mycorrhiza
Nitrogen
Nitrogen isotopes
Nutrients
Organic carbon
Organic compounds
Organic soils
Photosynthesis
Plant species
Species
stable isotope natural abundance
Stable isotopes
Staining
Terrestrial environments
Title Dark septate endophytes and arbuscular mycorrhizal fungi (Paris‐morphotype) affect the stable isotope composition of ‘classically’ non‐mycorrhizal plants
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1365-2435.13673
https://www.proquest.com/docview/2467515371
Volume 34
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