Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density

Societal Impact Statement Plant‐parasitic nematodes are a major concern for global food security, and many existing control options are being phased out due to adverse impacts on the environment. Here, we show that although application of arbuscular mycorrhizal fungi (AMF) increases host tolerance t...

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Main Authors: Christopher A. Bell, Emily Magkourilou, Helen Barker, Anthony Barker, Peter E. Urwin, Katie J. Field
Format: Article
Language:English
Published: Wiley 2023-03-01
Series:Plants, People, Planet
Subjects:
Online Access:https://doi.org/10.1002/ppp3.10338
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author Christopher A. Bell
Emily Magkourilou
Helen Barker
Anthony Barker
Peter E. Urwin
Katie J. Field
author_facet Christopher A. Bell
Emily Magkourilou
Helen Barker
Anthony Barker
Peter E. Urwin
Katie J. Field
author_sort Christopher A. Bell
collection DOAJ
description Societal Impact Statement Plant‐parasitic nematodes are a major concern for global food security, and many existing control options are being phased out due to adverse impacts on the environment. Here, we show that although application of arbuscular mycorrhizal fungi (AMF) increases host tolerance to these parasites, these benefits decrease as the parasite burden increases, limiting long‐term benefits. This effect was consistent between experiments in the glasshouse and in the field environment, demonstrating the relevance of research into usable technologies. Our findings have potential to aid decision making regarding application of AMF inocula for optimum results in agricultural systems. Summary Plant‐parasitic nematodes are a leading global threat to crop production and food security aims. Control strategies based on nematicides and fertilisers are increasingly undesirable due to economic and environmental impacts. Arbuscular mycorrhizal fungi (AMF) may induce host tolerance against pests such as the potato cyst nematode (PCN). Here, we determined the impact of PCN density on the tolerance induced by AMF‐host interactions. Additionally, we evaluated the effects of five AMF inocula on PCN fitness though glasshouse and field trials. Greater PCN densities reduce the increased tolerance that AMF may confer on their hosts. This may be due to reduced mycorrhizal colonisation of hosts under higher PCN infection and potentially a threshold at which the presence of PCN severely impacts fungal growth. When tested in the field, the outcomes of AMF inoculation on crop yields were still positive. Inoculation of soil in the field also increased PCN multiplication, suggesting that AMF‐induced tolerance may become reduced in the near future when the threshold PCN density is reached. Addition of AMF to agricultural soils may provide a short‐term benefit yet lead to a long‐term detriment by increasing PCN populations. The effects observed were driven by only one out of the five introduced AMF species, indicating that the remaining species were redundant for this application. This raises important considerations for future application of AMF inocula in agricultural systems and aids our understanding of how widely used ‘beneficial’ soil amendments impact the agricultural ecosystem.
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spelling doaj.art-1a0e102ad3c947daa9a34022f1fa8b032023-02-22T08:10:49ZengWileyPlants, People, Planet2572-26112023-03-015224125310.1002/ppp3.10338Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen densityChristopher A. Bell0Emily Magkourilou1Helen Barker2Anthony Barker3Peter E. Urwin4Katie J. Field5School of Biology University of Leeds Leeds UKSchool of Biology University of Leeds Leeds UKBarworth Agriculture Sleaford UKBarworth Agriculture Sleaford UKSchool of Biology University of Leeds Leeds UKPlants, Photosynthesis and Soil, School of Biosciences University of Sheffield Sheffield UKSocietal Impact Statement Plant‐parasitic nematodes are a major concern for global food security, and many existing control options are being phased out due to adverse impacts on the environment. Here, we show that although application of arbuscular mycorrhizal fungi (AMF) increases host tolerance to these parasites, these benefits decrease as the parasite burden increases, limiting long‐term benefits. This effect was consistent between experiments in the glasshouse and in the field environment, demonstrating the relevance of research into usable technologies. Our findings have potential to aid decision making regarding application of AMF inocula for optimum results in agricultural systems. Summary Plant‐parasitic nematodes are a leading global threat to crop production and food security aims. Control strategies based on nematicides and fertilisers are increasingly undesirable due to economic and environmental impacts. Arbuscular mycorrhizal fungi (AMF) may induce host tolerance against pests such as the potato cyst nematode (PCN). Here, we determined the impact of PCN density on the tolerance induced by AMF‐host interactions. Additionally, we evaluated the effects of five AMF inocula on PCN fitness though glasshouse and field trials. Greater PCN densities reduce the increased tolerance that AMF may confer on their hosts. This may be due to reduced mycorrhizal colonisation of hosts under higher PCN infection and potentially a threshold at which the presence of PCN severely impacts fungal growth. When tested in the field, the outcomes of AMF inoculation on crop yields were still positive. Inoculation of soil in the field also increased PCN multiplication, suggesting that AMF‐induced tolerance may become reduced in the near future when the threshold PCN density is reached. Addition of AMF to agricultural soils may provide a short‐term benefit yet lead to a long‐term detriment by increasing PCN populations. The effects observed were driven by only one out of the five introduced AMF species, indicating that the remaining species were redundant for this application. This raises important considerations for future application of AMF inocula in agricultural systems and aids our understanding of how widely used ‘beneficial’ soil amendments impact the agricultural ecosystem.https://doi.org/10.1002/ppp3.10338arbuscular mycorrhizal fungifood securityplant‐parasitic nematodepotatopotato cyst nematodesoil community
spellingShingle Christopher A. Bell
Emily Magkourilou
Helen Barker
Anthony Barker
Peter E. Urwin
Katie J. Field
Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
Plants, People, Planet
arbuscular mycorrhizal fungi
food security
plant‐parasitic nematode
potato
potato cyst nematode
soil community
title Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
title_full Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
title_fullStr Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
title_full_unstemmed Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
title_short Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density
title_sort arbuscular mycorrhizal fungal induced tolerance is determined by fungal identity and pathogen density
topic arbuscular mycorrhizal fungi
food security
plant‐parasitic nematode
potato
potato cyst nematode
soil community
url https://doi.org/10.1002/ppp3.10338
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