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 in | Functional ecology Vol. 34; no. 12; pp. 2453 - 2466 |
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Main Authors | , , , , , , , |
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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. |
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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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CitedBy_id | crossref_primary_10_1016_j_funeco_2022_101209 crossref_primary_10_1111_nph_18991 crossref_primary_10_1093_aob_mcab003 crossref_primary_10_1111_nph_18049 crossref_primary_10_1111_nph_18061 crossref_primary_10_1016_j_biocontrol_2023_105223 crossref_primary_10_1016_j_scitotenv_2021_148808 crossref_primary_10_1021_acsomega_1c00274 crossref_primary_10_1080_10256016_2021_1946532 crossref_primary_10_5209_bocm_72399 crossref_primary_10_1093_aob_mcab153 crossref_primary_10_1038_s42003_024_06042_7 crossref_primary_10_1016_j_pedsph_2024_01_004 crossref_primary_10_1186_s40793_022_00431_3 |
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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 |
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