Cargando…

Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands

BACKGROUND: Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop co...

Descripción completa

Detalles Bibliográficos
Autores principales: Li, Jiahuan, Guo, Lizhu, Wilson, Gail W. T., Cobb, Adam B., Wang, Kun, Liu, Li, Zhao, Huan, Huang, Ding
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636817/
https://www.ncbi.nlm.nih.gov/pubmed/36335298
http://dx.doi.org/10.1186/s12862-022-02082-x
_version_ 1784825037966016512
author Li, Jiahuan
Guo, Lizhu
Wilson, Gail W. T.
Cobb, Adam B.
Wang, Kun
Liu, Li
Zhao, Huan
Huang, Ding
author_facet Li, Jiahuan
Guo, Lizhu
Wilson, Gail W. T.
Cobb, Adam B.
Wang, Kun
Liu, Li
Zhao, Huan
Huang, Ding
author_sort Li, Jiahuan
collection PubMed
description BACKGROUND: Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop concentrically with each growing season. We evaluated fairy ring dynamics in a field study conducted in semiarid grasslands to elucidate above- and belowground interactions driving distinct vegetation patterns. We followed this initial field investigation with a complementary greenhouse experiment, using soils collected from specific fairy ring zones (inside, ring-edge, outside) to examine plant-soil-microbial interactions under controlled conditions. We selected Leymus chinensis (a dominant grass) as our model plant species to assess the role of diverse fairy ring microbial communities on plant growth and nutrition. RESULTS: In our field study, plants on the ring-edge produced greater shoot biomass with higher concentrations of N and P, compared to plants inside the ring or adjacent (outside) controls. Soil microbial community biomarkers indicate shifts in relative microbial biomass as fairy rings expand. Inside the ring, plant roots showed greater damage from pathogenic fungi, compared to outside or ring-edge. Our greenhouse experiment confirmed that inoculation with live ring-edge soil generally promoted plant growth but decreased shoot P concentration. Inoculation with soil collected from inside the ring increased root pathogen infection and reduced shoot biomass. CONCLUSION: We propose that soil microbial activity within ring-edges promotes plant growth via mobilization of plant-available P or directed stimulation. However, as the ring expands, L. chinensis at the leading edge may increase pathogen accumulation, resulting in reduced growth at the center of the ring in subsequent growing seasons. Our results provide new insights into the plant-soil-microbial dynamics of fairy rings in grasslands, helping to elucidate these mysterious vegetation patterns. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02082-x.
format Online
Article
Text
id pubmed-9636817
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-96368172022-11-06 Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands Li, Jiahuan Guo, Lizhu Wilson, Gail W. T. Cobb, Adam B. Wang, Kun Liu, Li Zhao, Huan Huang, Ding BMC Ecol Evol Research BACKGROUND: Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop concentrically with each growing season. We evaluated fairy ring dynamics in a field study conducted in semiarid grasslands to elucidate above- and belowground interactions driving distinct vegetation patterns. We followed this initial field investigation with a complementary greenhouse experiment, using soils collected from specific fairy ring zones (inside, ring-edge, outside) to examine plant-soil-microbial interactions under controlled conditions. We selected Leymus chinensis (a dominant grass) as our model plant species to assess the role of diverse fairy ring microbial communities on plant growth and nutrition. RESULTS: In our field study, plants on the ring-edge produced greater shoot biomass with higher concentrations of N and P, compared to plants inside the ring or adjacent (outside) controls. Soil microbial community biomarkers indicate shifts in relative microbial biomass as fairy rings expand. Inside the ring, plant roots showed greater damage from pathogenic fungi, compared to outside or ring-edge. Our greenhouse experiment confirmed that inoculation with live ring-edge soil generally promoted plant growth but decreased shoot P concentration. Inoculation with soil collected from inside the ring increased root pathogen infection and reduced shoot biomass. CONCLUSION: We propose that soil microbial activity within ring-edges promotes plant growth via mobilization of plant-available P or directed stimulation. However, as the ring expands, L. chinensis at the leading edge may increase pathogen accumulation, resulting in reduced growth at the center of the ring in subsequent growing seasons. Our results provide new insights into the plant-soil-microbial dynamics of fairy rings in grasslands, helping to elucidate these mysterious vegetation patterns. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02082-x. BioMed Central 2022-11-05 /pmc/articles/PMC9636817/ /pubmed/36335298 http://dx.doi.org/10.1186/s12862-022-02082-x 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
Li, Jiahuan
Guo, Lizhu
Wilson, Gail W. T.
Cobb, Adam B.
Wang, Kun
Liu, Li
Zhao, Huan
Huang, Ding
Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_full Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_fullStr Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_full_unstemmed Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_short Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_sort assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636817/
https://www.ncbi.nlm.nih.gov/pubmed/36335298
http://dx.doi.org/10.1186/s12862-022-02082-x
work_keys_str_mv AT lijiahuan assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT guolizhu assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT wilsongailwt assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT cobbadamb assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT wangkun assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT liuli assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT zhaohuan assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands
AT huangding assessingsoilmicrobesthatdrivefairyringpatternsintemperatesemiaridgrasslands