Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations

Article


Frew, Adam, Powell, Jeff R., Glauser, Gaetan, Bennett, Alison E. and Johnson, Scott N.. 2018. "Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations." Soil Biology and Biochemistry. 126, pp. 123-132. https://doi.org/10.1016/j.soilbio.2018.08.019
Article Title

Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations

ERA Journal ID5272
Article CategoryArticle
AuthorsFrew, Adam (Author), Powell, Jeff R. (Author), Glauser, Gaetan (Author), Bennett, Alison E. (Author) and Johnson, Scott N. (Author)
Journal TitleSoil Biology and Biochemistry
Journal Citation126, pp. 123-132
Number of Pages10
Year2018
PublisherElsevier
Place of PublicationUnited Kingdom
ISSN0038-0717
1879-3428
Digital Object Identifier (DOI)https://doi.org/10.1016/j.soilbio.2018.08.019
Abstract

Arbuscular mycorrhizal (AM) fungi are ubiquitous components of the soil biota which live symbiotically with terrestrial plants. Plant-parasitic nematodes are an important group of soil-dwelling invertebrates that inflict considerable damage to crops, representing a serious threat to food security. The effects of the AM symbiosis on plant-parasitic nematodes can be variable, and the mechanisms driving such variability remain ambiguous.

We tested the impacts of inoculation with AM fungi on the root metabolic profile and nutritional chemistry of two varieties of wheat (Triticwn aestivum), and how this affected populations of the plant-parasitic nematode Pratylenchus neglectus.

AM fungi reduced plant biomass by almost 24%, yet increased root concentrations of phosphorus, potassium and zinc by 50%, 15% and 16%, respectively. Contrary to our predictions, nematode populations were 47 similar to 117% higher on AM inoculated plants, depending on variety. Untargeted metabolomic profiling revealed significant effects of mycorrhizal colonisation on certain markers of biological interest, these compounds were the benzoxazinoid glucoside defence compounds DIBOA-Glc, HMBOA-Glc and HDMBOA-Glc. Overall, mycorrhizae reduced abundances of these defence metabolites, which were potentially driving AM fungi nematode interactions; although for DIBOA-Glc this was dependent on wheat variety. Moreover, there was a negative correlation between total AM colonisation and DIBOA-Glc concentrations.

Our results demonstrate AM fungi can reduce plant biomass and supress root defence compounds associated with plant resistance to invertebrate pests, while still providing nutritional benefit to the host plant. This highlights that mycorrhizal colonisation of wheat varieties can have simultaneous positive and negative effects on different plant traits which drive plant-herbivore interactions. In working towards effective exploitation of the AM symbiosis in sustainable plant production, the context dependent outcomes of mycorrhizal-plant-nematode interactions is a key challenge. Untargeted metabolomic profiling offers the ability to reveal some of the driving mechanisms underpinning such complex tripartite interactions in the soil.

Keywordsbelow-ground, Benzoxazinoids, growth, defence, metabolomics Mycorrhiza, plant defence
ANZSRC Field of Research 2020310302. Community ecology (excl. invasive species ecology)
410603. Soil biology
310899. Plant biology not elsewhere classified
310703. Microbial ecology
Public Notes

Files associated with this item cannot be displayed due to copyright restrictions.

Byline AffiliationsUniversity of Western Sydney
Western Sydney University
University of Neuchatel, Switzerland
Ohio State University, United States
Institution of OriginUniversity of Southern Queensland
Permalink -

https://research.usq.edu.au/item/q56xz/mycorrhizal-fungi-enhance-nutrient-uptake-but-disarm-defences-in-plant-roots-promoting-plant-parasitic-nematode-populations

  • 153
    total views
  • 8
    total downloads
  • 0
    views this month
  • 0
    downloads this month

Export as

Related outputs

Community assembly of root-colonizing arbuscular mycorrhizal fungi: beyond carbon and into defence?
Frew, Adam, Weinberger, Natascha, Powell, Jeff R., Watts-Williams, Stephanie J. and Aguilar-Trigueros, Carlos A.. 2024. "Community assembly of root-colonizing arbuscular mycorrhizal fungi: beyond carbon and into defence?" The ISME Journal: multidisciplinary journal of microbial ecology. 18 (1). https://doi.org/10.1093/ismejo/wrae007
Integrating soil microbial communities into fundamental ecology, conservation, and restoration: examples from Australia
Birnbaum, Christina, Dearnaley, John, Egidi, Eleonora, Frew, Adam, Hopkins, Anna, Powell, Jeff, Aguilar-Trigueros, Carlos, Liddicoat, Craig, Albornoz, Felipe, Heuck, Meike K., Dadzie, Frederick A., Florence, Luke, Singh, Pankaj, Mansfield, Tomas, Rajapaksha, Kumari, Stewart, Jana, Rallo, Paola, Peddle, Shawn D. and Chiarenza, Giancarlo. 2024. "Integrating soil microbial communities into fundamental ecology, conservation, and restoration: examples from Australia." New Phytologist. 241 (3), pp. 974-981. https://doi.org/10.1111/nph.19440
Herbivory-driven shifts in arbuscular mycorrhizal fungal community assembly: increased fungal competition and plant phosphorus benefits
Frew, Adam, Opik, Maarja, Oja, Jane, Vahter, Tanel, Hiiesalu, Inga and Aguilar-Trigueros, Carlos A.. 2024. "Herbivory-driven shifts in arbuscular mycorrhizal fungal community assembly: increased fungal competition and plant phosphorus benefits." New Phytologist. 241 (5), pp. 1891-1899. https://doi.org/10.1111/nph.19474
Soil abounds with life – and supports all life above it. But Australian soils need urgent repair
Frew, Adam, Birnbaum, Christina, Egidi, Eleonora and Heuck, Meike Katharina. 2023. "Soil abounds with life – and supports all life above it. But Australian soils need urgent repair." The Conversation.
Belowground crop responses to root herbivory are associated with the community structure of native arbuscular mycorrhizal fungi
Ng, Anna, Wilson, Bree A.L. and Frew, Adam. 2023. "Belowground crop responses to root herbivory are associated with the community structure of native arbuscular mycorrhizal fungi." Applied Soil Ecology. 185. https://doi.org/10.1016/j.apsoil.2022.104797
Friends to the rescue: using arbuscular mycorrhizal fungi to future-proof Australian agriculture
Heuck, Meike Katharina, Birnbaum, Christina and Frew, Adam. 2023. "Friends to the rescue: using arbuscular mycorrhizal fungi to future-proof Australian agriculture." Microbiology Australia. 44 (1), pp. 5-8. https://doi.org/10.1071/MA23002
Host filtering, not competitive exclusion, may be the main driver of arbuscular mycorrhizal fungal community assembly under high phosphorus
Frew, Adam, Heuck, Meike and Aguilar-Trigueros, Carlos A.. 2023. "Host filtering, not competitive exclusion, may be the main driver of arbuscular mycorrhizal fungal community assembly under high phosphorus." Functional Ecology. 37 (7), pp. 1856-1869. https://doi.org/10.1111/1365-2435.14349
Australia offers unique insight into the ecology of arbuscular mycorrhizal fungi: An opportunity not to be lost
Frew, Adam and Aguilar-Trigueros, Carlos A.. 2023. "Australia offers unique insight into the ecology of arbuscular mycorrhizal fungi: An opportunity not to be lost." Austral Ecology: a journal of ecology in the Southern Hemisphere. 48 (8), pp. 1713-1720. https://doi.org/10.1111/aec.13451
Water availability alters the community structure of arbuscular mycorrhizal fungi and determines plant mycorrhizal benefit
Frew, Adam. 2023. "Water availability alters the community structure of arbuscular mycorrhizal fungi and determines plant mycorrhizal benefit." Plants, People, Planet. 5 (5), pp. 683-689. https://doi.org/10.1002/ppp3.10372
‘Dig Up Dirt’, using citizen science to understand the diversity of beneficial fungi in Australian agroecosystems
Heuck, M.K., Birnbaum, C., Kath, J., Powell, J. and Frew, A.. 2022. "‘Dig Up Dirt’, using citizen science to understand the diversity of beneficial fungi in Australian agroecosystems." 2022 Conference of the Ecological Society of Australia (ESA 2022). Wollongong, Australia 28 Nov - 02 Dec 2022 Australia.
From Little Things, Big Things Grow: Fungi, Security, and the Future of Food
Frew, Adam, Heuck, Meike and Birnbaum, Christina. 2022. "From Little Things, Big Things Grow: Fungi, Security, and the Future of Food." Australian Quarterly. 93 (4), pp. 26-31.
Silicon accumulation suppresses arbuscular mycorrhizal fungal colonisation in the model grass Brachypodium distachyon
Johnson, Scott N., Powell, Jef R., Frew, Adam and Cibils–Stewart, Ximena. 2022. "Silicon accumulation suppresses arbuscular mycorrhizal fungal colonisation in the model grass Brachypodium distachyon." Plant and Soil: international journal on plant-soil relationships. 477 (1-2), pp. 219-232. https://doi.org/10.1007/s11104-022-05463-9
Root herbivory reduces species richness and alters community structure of root-colonising arbuscular mycorrhizal fungi
Frew, Adam. 2022. "Root herbivory reduces species richness and alters community structure of root-colonising arbuscular mycorrhizal fungi." Soil Biology and Biochemistry. 171. https://doi.org/10.1016/j.soilbio.2022.108723
Plant herbivore protection by arbuscular mycorrhizas: a role for fungal diversity?
Frew, Adam, Antunes, Pedro M., Cameron, Duncan D., Hartley, Susan E., Johnson, Scott N., Rillig, Matthias C. and Bennett, Alison E.. 2022. "Plant herbivore protection by arbuscular mycorrhizas: a role for fungal diversity?" New Phytologist. 233 (3), pp. 1022-1031. https://doi.org/10.1111/nph.17781
Aboveground herbivory suppresses the arbuscular mycorrhizal symbiosis, reducing plant phosphorus uptake
Frew, Adam. 2021. "Aboveground herbivory suppresses the arbuscular mycorrhizal symbiosis, reducing plant phosphorus uptake." Applied Soil Ecology. 168. https://doi.org/10.1016/j.apsoil.2021.104133
Different mycorrhizal fungal communities differentially affect plant phenolic-based resistance to insect herbivory
Frew, Adam and Wilson, Bree A. L.. 2021. "Different mycorrhizal fungal communities differentially affect plant phenolic-based resistance to insect herbivory." Rhizosphere. 19, pp. 1-4. https://doi.org/10.1016/j.rhisph.2021.100365
Impacts of elevated atmospheric CO2 on arbuscular mycorrhizal fungi and their role in moderating plant allometric partitioning
Frew, Adam, Price, Jodi N., Oja, Jane, Vasar, Martti and Opik, Maarja. 2021. "Impacts of elevated atmospheric CO2 on arbuscular mycorrhizal fungi and their role in moderating plant allometric partitioning." Mycorrhiza. https://doi.org/10.1007/s00572-021-01025-6
Targeted plant defense: silicon conserves hormonal defense signaling impacting chewing but not fluid‐feeding herbivores
Johnson, Scott N., Hartley, Susan E., Ryalls, James M. W., Frew, Adam and Hall, Casey R.. 2021. "Targeted plant defense: silicon conserves hormonal defense signaling impacting chewing but not fluid‐feeding herbivores." Ecology. 102 (3), pp. 1-7. https://doi.org/10.1002/ecy.3250
Increasing species richness of arbuscular mycorrhizal fungi benefits some plants, but not others
Frew, Adam. 2019. "Increasing species richness of arbuscular mycorrhizal fungi benefits some plants, but not others." 2019 Conference of the Ecological Society of Australia (ESA 2019). Launceston, Australia 24 - 29 Nov 2019
How fungi’s knack for networking boosts ecological recovery after bushfires
Frew, Adam, Le Brocque, Andy, Nimmo, Dale, Egidi, Eleonora, Price, Jodi and Greenwood, Leanne. 2020. "How fungi’s knack for networking boosts ecological recovery after bushfires." The Conversation. 20 March 2020, pp. 1-8.
Contrasting effects of commercial and native arbuscular mycorrhizal fungal inoculants on plant biomass allocation, nutrients, and phenolics
Frew, Adam. 2021. "Contrasting effects of commercial and native arbuscular mycorrhizal fungal inoculants on plant biomass allocation, nutrients, and phenolics." Plants, People, Planet. 3 (5), pp. 536-540. https://doi.org/10.1002/ppp3.10128
Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis
Frew, Adam, Powell, Jeff R. and Johnson, Scott N.. 2020. "Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis." Plant and Soil: international journal on plant-soil relationships. 447 (1-2), pp. 463-473. https://doi.org/10.1007/s11104-019-04399-x
Fire Effects on Soil Properties by P Pereira, J Mataix-Solera, X Ubeda, G Reain & A Cerda
Frew, Adam. 2020. "Fire Effects on Soil Properties by P Pereira, J Mataix-Solera, X Ubeda, G Reain & A Cerda." Austral Ecology: a journal of ecology in the Southern Hemisphere. 45, pp. 659-659. https://doi.org/10.1111/aec.12843
‘Soil probiotics’ promise bigger, healthier crops, but there’s a downside
Frew, Adam. 2018. "‘Soil probiotics’ promise bigger, healthier crops, but there’s a downside." The Conversation. 23 October 2018, pp. 1-9.
Arbuscular mycorrhizal fungi promote silicon accumulation in plant roots, reducing the impacts of root herbivory
Frew, Adam, Powell, Jeff R., Allsopp, Peter G., Sallam, Nader and Johnson, Scott N.. 2017. "Arbuscular mycorrhizal fungi promote silicon accumulation in plant roots, reducing the impacts of root herbivory." Plant and Soil: international journal on plant-soil relationships. 419 (1-2), pp. 423-433. https://doi.org/10.1007/s11104-017-3357-z
Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants
Frew, Adam. 2019. "Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants." Soil Biology and Biochemistry. 135, pp. 248-250. https://doi.org/10.1016/j.soilbio.2019.05.015
Mycorrhizal‐mediated plant–herbivore interactions in a high CO2 world
Frew, Adam and Price, Jodi N.. 2019. "Mycorrhizal‐mediated plant–herbivore interactions in a high CO2 world." Functional Ecology. 33 (8), pp. 1376-1385. https://doi.org/10.1111/1365-2435.13347
Silicon reduces herbivore performance via different mechanisms, depending on host–plant species
Frew, Adam, Weston, Leslie A. and Gurr, Geoff M.. 2019. "Silicon reduces herbivore performance via different mechanisms, depending on host–plant species." Austral Ecology: a journal of ecology in the Southern Hemisphere. 44 (6), pp. 1092-1097. https://doi.org/10.1111/aec.12767
Dryland management regimes alter forest habitats and understory arthropod communities
Johnson, S. N., Lopaticki, G., Aslam, T. J., Barnett, K., Frew, A., Hartley, S. E., Hiltpold, I., Nielsen, U. N. and Ryalls, J. M. W.. 2018. "Dryland management regimes alter forest habitats and understory arthropod communities." Annals of Applied Biology. 172 (3), pp. 282-294. https://doi.org/10.1111/aab.12419
Benefits from below: silicon supplementation maintains legume productivity under predicted climate change scenarios
Johnson, Scott N., Ryalls, James M. W., Gherlenda, Andrew N., Frew, Adam and Hartley, Susan E.. 2018. "Benefits from below: silicon supplementation maintains legume productivity under predicted climate change scenarios." Frontiers in Plant Science. 9, pp. 1-9. https://doi.org/10.3389/fpls.2018.00202
The role of silicon in plant biology: a paradigm shift in research approach
Frew, Adam, Weston, Leslie A., Reynolds, Olivia L. and Gurr, Geoff M.. 2018. "The role of silicon in plant biology: a paradigm shift in research approach." Annals of Botany. 121 (7), pp. 1265-1273. https://doi.org/10.1093/aob/mcy009
Silicon‐induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance
Johnson, Scott N., Hartley, Susan E., Ryalls, James M. W., Frew, Adam, DeGabriel, Jane L., Duncan, Michael and Gherlenda, Andrew G.. 2017. "Silicon‐induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance." Functional Ecology. 31 (10), pp. 1903-1909. https://doi.org/10.1111/1365-2435.12893
Do eucalypt plantation management practices create understory reservoirs of scarab beetle pests in the soil?
Frew, Adam, Nielsen, Uffe N., Riegler, Markus and Johnson, Scott N.. 2013. "Do eucalypt plantation management practices create understory reservoirs of scarab beetle pests in the soil?" Forest Ecology and Management. 306, pp. 275-280. https://doi.org/10.1016/j.foreco.2013.06.051
Host plant colonisation by arbuscular mycorrhizal fungi stimulates immune function whereas high root silicon concentrations diminish growth in a soil-dwelling herbivore
Frew, Adam, Powell, Jeff R., Hiltpold, Ivan, Allsopp, Peter G., Sallam, Nader and Johnson, Scott N.. 2017. "Host plant colonisation by arbuscular mycorrhizal fungi stimulates immune function whereas high root silicon concentrations diminish growth in a soil-dwelling herbivore." Soil Biology and Biochemistry. 112, pp. 117-126. https://doi.org/10.1016/j.soilbio.2017.05.008
Increased root herbivory under elevated atmospheric carbon dioxide concentrations is reversed by silicon‐based plant defences
Frew, Adam, Allsopp, Peter G., Gherlenda, Andrew G. and Johnson, Scott N.. 2017. "Increased root herbivory under elevated atmospheric carbon dioxide concentrations is reversed by silicon‐based plant defences." Journal of Applied Ecology. 54 (5), pp. 1310-1319. https://doi.org/10.1111/1365-2664.12822
New frontiers in belowground ecology for plant protection from root-feeding insects
Johnson, Scott N., Benefer, Carly M., Frew, Adam, Griffiths, Bryan S., Hartley, Susan E., Karley, Alison J., Rasmann, Sergio, Schumann, Mario, Sonnemann, Illja and Robert, Christelle A. M.. 2016. "New frontiers in belowground ecology for plant protection from root-feeding insects." Applied Soil Ecology. 108, pp. 96-107. https://doi.org/10.1016/j.apsoil.2016.07.017
Trade-offs between silicon and phenolic defenses may explain enhanced performance of root herbivores on phenolic-rich plants
Frew, Adam, Powell, Jeff R., Sallam, Nader, Allsopp, Peter G. and Johnson, Scott N.. 2016. "Trade-offs between silicon and phenolic defenses may explain enhanced performance of root herbivores on phenolic-rich plants." Journal of Chemical Ecology. 42 (8), pp. 768-771. https://doi.org/10.1007/s10886-016-0734-7
The importance of testing multiple environmental factors in legume–insect research: replication, reviewers, and rebuttal
Johnson, Scott N., Gherlenda, Andrew N., Frew, Adam and Ryalls, James M. W.. 2016. "The importance of testing multiple environmental factors in legume–insect research: replication, reviewers, and rebuttal." Frontiers in Plant Science. 7 (489), pp. 1-4. https://doi.org/10.3389/fpls.2016.00489
Belowground ecology of scarabs feeding on grass roots: current knowledge and future directions for management in Australasia
Frew, Adam, Barnett, Kirk, Nielsen, Uffe N., Riegler, Markus and Johnson, Scott N.. 2016. "Belowground ecology of scarabs feeding on grass roots: current knowledge and future directions for management in Australasia." Frontiers in Plant Science. 7 (321), pp. 1-15. https://doi.org/10.3389/fpls.2016.00321