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Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation

BACKGROUND: The development of suppressive soils is a promising strategy to protect plants against soil-borne diseases in a sustainable and viable manner. The use of crop rotation and the incorporation of plant residues into the soil are known to alleviate the stress imposed by soil pathogens throug...

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Autores principales: Yuan, Xianfu, Hong, Shan, Xiong, Wu, Raza, Waseem, Shen, Zongzhuan, Wang, Beibei, Li, Rong, Ruan, Yunze, Shen, Qirong, Dini-Andreote, Francisco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8507339/
https://www.ncbi.nlm.nih.gov/pubmed/34635164
http://dx.doi.org/10.1186/s40168-021-01133-7
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author Yuan, Xianfu
Hong, Shan
Xiong, Wu
Raza, Waseem
Shen, Zongzhuan
Wang, Beibei
Li, Rong
Ruan, Yunze
Shen, Qirong
Dini-Andreote, Francisco
author_facet Yuan, Xianfu
Hong, Shan
Xiong, Wu
Raza, Waseem
Shen, Zongzhuan
Wang, Beibei
Li, Rong
Ruan, Yunze
Shen, Qirong
Dini-Andreote, Francisco
author_sort Yuan, Xianfu
collection PubMed
description BACKGROUND: The development of suppressive soils is a promising strategy to protect plants against soil-borne diseases in a sustainable and viable manner. The use of crop rotation and the incorporation of plant residues into the soil are known to alleviate the stress imposed by soil pathogens through dynamics changes in soil biological and physicochemical properties. However, relatively little is known about the extent to which specific soil amendments of plant residues trigger the development of plant-protective microbiomes. Here, we investigated how the incorporation of pineapple residues in soils highly infested with the banana Fusarium wilt disease alleviates the pathogen pressure via changes in soil microbiomes. RESULTS: The addition of above- and below-ground pineapple residues in highly infested soils significantly reduced the number of pathogens in the soil, thus resulting in a lower disease incidence. The development of suppressive soils was mostly related to trackable changes in specific fungal taxa affiliated with Aspergillus fumigatus and Fusarium solani, both of which displayed inhibitory effects against the pathogen. These antagonistic effects were further validated using an in vitro assay in which the pathogen control was related to growth inhibition via directly secreted antimicrobial substances and indirect interspecific competition for nutrients. The disease suppressive potential of these fungal strains was later validated using microbial inoculation in a well-controlled pot experiment. CONCLUSIONS: These results mechanistically demonstrated how the incorporation of specific plant residues into the soil induces trackable changes in the soil microbiome with direct implications for disease suppression. The incorporation of pineapple residues in the soil alleviated the pathogen pressure by increasing the relative abundance of antagonistic fungal taxa causing a negative effect on pathogen growth and disease incidence. Taken together, this study provides a successful example of how specific agricultural management strategies can be used to manipulate the soil microbiome towards the development of suppressive soils against economically important soil-borne diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01133-7.
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spelling pubmed-85073392021-10-20 Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation Yuan, Xianfu Hong, Shan Xiong, Wu Raza, Waseem Shen, Zongzhuan Wang, Beibei Li, Rong Ruan, Yunze Shen, Qirong Dini-Andreote, Francisco Microbiome Research BACKGROUND: The development of suppressive soils is a promising strategy to protect plants against soil-borne diseases in a sustainable and viable manner. The use of crop rotation and the incorporation of plant residues into the soil are known to alleviate the stress imposed by soil pathogens through dynamics changes in soil biological and physicochemical properties. However, relatively little is known about the extent to which specific soil amendments of plant residues trigger the development of plant-protective microbiomes. Here, we investigated how the incorporation of pineapple residues in soils highly infested with the banana Fusarium wilt disease alleviates the pathogen pressure via changes in soil microbiomes. RESULTS: The addition of above- and below-ground pineapple residues in highly infested soils significantly reduced the number of pathogens in the soil, thus resulting in a lower disease incidence. The development of suppressive soils was mostly related to trackable changes in specific fungal taxa affiliated with Aspergillus fumigatus and Fusarium solani, both of which displayed inhibitory effects against the pathogen. These antagonistic effects were further validated using an in vitro assay in which the pathogen control was related to growth inhibition via directly secreted antimicrobial substances and indirect interspecific competition for nutrients. The disease suppressive potential of these fungal strains was later validated using microbial inoculation in a well-controlled pot experiment. CONCLUSIONS: These results mechanistically demonstrated how the incorporation of specific plant residues into the soil induces trackable changes in the soil microbiome with direct implications for disease suppression. The incorporation of pineapple residues in the soil alleviated the pathogen pressure by increasing the relative abundance of antagonistic fungal taxa causing a negative effect on pathogen growth and disease incidence. Taken together, this study provides a successful example of how specific agricultural management strategies can be used to manipulate the soil microbiome towards the development of suppressive soils against economically important soil-borne diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01133-7. BioMed Central 2021-10-12 /pmc/articles/PMC8507339/ /pubmed/34635164 http://dx.doi.org/10.1186/s40168-021-01133-7 Text en © The Author(s) 2021 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
Yuan, Xianfu
Hong, Shan
Xiong, Wu
Raza, Waseem
Shen, Zongzhuan
Wang, Beibei
Li, Rong
Ruan, Yunze
Shen, Qirong
Dini-Andreote, Francisco
Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title_full Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title_fullStr Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title_full_unstemmed Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title_short Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation
title_sort development of fungal-mediated soil suppressiveness against fusarium wilt disease via plant residue manipulation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8507339/
https://www.ncbi.nlm.nih.gov/pubmed/34635164
http://dx.doi.org/10.1186/s40168-021-01133-7
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