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Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea

All perennial plants harbor diverse endophytic fungal communities, but why they tolerate these complex asymptomatic symbioses is unknown. Using a multi-pronged approach, we conclusively found that a dryland grass supports endophyte communities comprised predominantly of latent saprophytes that can e...

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Autores principales: Wenndt, Anthony J., Evans, Sarah E., van Diepeningen, Anne D., Logan, J. Robert, Jacobson, Peter J., Seely, Mary K., Jacobson, Kathryn M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8217645/
https://www.ncbi.nlm.nih.gov/pubmed/34168636
http://dx.doi.org/10.3389/fmicb.2021.691584
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author Wenndt, Anthony J.
Evans, Sarah E.
van Diepeningen, Anne D.
Logan, J. Robert
Jacobson, Peter J.
Seely, Mary K.
Jacobson, Kathryn M.
author_facet Wenndt, Anthony J.
Evans, Sarah E.
van Diepeningen, Anne D.
Logan, J. Robert
Jacobson, Peter J.
Seely, Mary K.
Jacobson, Kathryn M.
author_sort Wenndt, Anthony J.
collection PubMed
description All perennial plants harbor diverse endophytic fungal communities, but why they tolerate these complex asymptomatic symbioses is unknown. Using a multi-pronged approach, we conclusively found that a dryland grass supports endophyte communities comprised predominantly of latent saprophytes that can enhance localized nutrient recycling after senescence. A perennial bunchgrass, Stipagrostis sabulicola, which persists along a gradient of extreme abiotic stress in the hyper-arid Namib Sand Sea, was the focal point of our study. Living tillers yielded 20 fungal endophyte taxa, 80% of which decomposed host litter during a 28-day laboratory decomposition assay. During a 6-month field experiment, tillers with endophytes decomposed twice as fast as sterilized tillers, consistent with the laboratory assay. Furthermore, profiling the community active during decomposition using next-generation sequencing revealed that 59–70% of the S. sabulicola endophyte community is comprised of latent saprophytes, and these dual-niche fungi still constitute a large proportion (58–62%) of the litter community more than a year after senescence. This study provides multiple lines of evidence that the fungal communities that initiate decomposition of standing litter develop in living plants, thus providing a plausible explanation for why plants harbor complex endophyte communities. Using frequent overnight non-rainfall moisture events (fog, dew, high humidity), these latent saprophytes can initiate decomposition of standing litter immediately after tiller senescence, thus maximizing the likelihood that plant-bound nutrients are recycled in situ and contribute to the nutrient island effect that is prevalent in drylands.
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spelling pubmed-82176452021-06-23 Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea Wenndt, Anthony J. Evans, Sarah E. van Diepeningen, Anne D. Logan, J. Robert Jacobson, Peter J. Seely, Mary K. Jacobson, Kathryn M. Front Microbiol Microbiology All perennial plants harbor diverse endophytic fungal communities, but why they tolerate these complex asymptomatic symbioses is unknown. Using a multi-pronged approach, we conclusively found that a dryland grass supports endophyte communities comprised predominantly of latent saprophytes that can enhance localized nutrient recycling after senescence. A perennial bunchgrass, Stipagrostis sabulicola, which persists along a gradient of extreme abiotic stress in the hyper-arid Namib Sand Sea, was the focal point of our study. Living tillers yielded 20 fungal endophyte taxa, 80% of which decomposed host litter during a 28-day laboratory decomposition assay. During a 6-month field experiment, tillers with endophytes decomposed twice as fast as sterilized tillers, consistent with the laboratory assay. Furthermore, profiling the community active during decomposition using next-generation sequencing revealed that 59–70% of the S. sabulicola endophyte community is comprised of latent saprophytes, and these dual-niche fungi still constitute a large proportion (58–62%) of the litter community more than a year after senescence. This study provides multiple lines of evidence that the fungal communities that initiate decomposition of standing litter develop in living plants, thus providing a plausible explanation for why plants harbor complex endophyte communities. Using frequent overnight non-rainfall moisture events (fog, dew, high humidity), these latent saprophytes can initiate decomposition of standing litter immediately after tiller senescence, thus maximizing the likelihood that plant-bound nutrients are recycled in situ and contribute to the nutrient island effect that is prevalent in drylands. Frontiers Media S.A. 2021-06-08 /pmc/articles/PMC8217645/ /pubmed/34168636 http://dx.doi.org/10.3389/fmicb.2021.691584 Text en Copyright © 2021 Wenndt, Evans, van Diepeningen, Logan, Jacobson, Seely and Jacobson. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wenndt, Anthony J.
Evans, Sarah E.
van Diepeningen, Anne D.
Logan, J. Robert
Jacobson, Peter J.
Seely, Mary K.
Jacobson, Kathryn M.
Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title_full Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title_fullStr Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title_full_unstemmed Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title_short Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea
title_sort why plants harbor complex endophytic fungal communities: insights from perennial bunchgrass stipagrostis sabulicola in the namib sand sea
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8217645/
https://www.ncbi.nlm.nih.gov/pubmed/34168636
http://dx.doi.org/10.3389/fmicb.2021.691584
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