Targeted plant defense: silicon conserves hormonal defense signaling impacting chewing but not fluid‐feeding herbivores

Article


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
Article Title

Targeted plant defense: silicon conserves hormonal defense signaling impacting chewing but not fluid‐feeding herbivores

ERA Journal ID3236
Article CategoryArticle
AuthorsJohnson, Scott N. (Author), Hartley, Susan E. (Author), Ryalls, James M. W. (Author), Frew, Adam (Author) and Hall, Casey R. (Author)
Journal TitleEcology
Journal Citation102 (3), pp. 1-7
Article Numbere03250
Number of Pages7
Year2021
Place of PublicationUnited States
ISSN0012-9658
1939-9170
Digital Object Identifier (DOI)https://doi.org/10.1002/ecy.3250
Web Address (URL)https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.3250
Abstract

Plants deploy an arsenal of chemical and physical defenses against arthropod herbivores, but it may be most cost efficient to produce these only when attacked. Herbivory activates complex signaling pathways involving several phytohormones, including jasmonic acid (JA), which regulate production of defensive compounds. The Poaceae also have the capacity to take up large amounts of silicon (Si) which accumulates in plant tissues. Si accumulation has anti‐herbivore properties, but it is poorly understood how Si defenses relate to defense hormone signaling. Here we show that Si enrichment causes the model grass Brachypodium distachyon to show lower levels of JA induction when attacked by chewing herbivores. Triggering this hormone even at lower concentrations, however, prompts Si uptake and physical defenses (e.g. leaf hairs) which negatively impact chewing herbivores. Removal of leaf hairs restored performance. Crucially, activation of such Si‐based defense is herbivore‐specific and occurred only in response to chewing and not fluid‐feeding (aphid) herbivores. This aligned with our meta‐analysis of 88 studies that showed Si defenses were more effective against chewing herbivores than fluid‐feeders. Our results suggest integration between herbivore defenses in a model Si‐accumulating plant, which potentially allows it to avoid unnecessary activation of other costly defenses.

Keywordsherbivory, insects, jasmonic acid, plant defense, physical defense, silica, silicon
ANZSRC Field of Research 2020410299. Ecological applications not elsewhere classified
310302. Community ecology (excl. invasive species ecology)
310899. Plant biology not elsewhere classified
Byline AffiliationsWestern Sydney University
University of Sheffield, United Kingdom
University of Western Sydney
Institution of OriginUniversity of Southern Queensland
Permalink -

https://research.usq.edu.au/item/q5zx5/targeted-plant-defense-silicon-conserves-hormonal-defense-signaling-impacting-chewing-but-not-fluid-feeding-herbivores

  • 120
    total views
  • 108
    total downloads
  • 1
    views this month
  • 0
    downloads this month

Export as

Related outputs

A Novel Free-Air Diesel and Ozone Enrichment (FADOE) Research Platform
Mofikoya, Adedayo O., James, Laura, Mullinger, Neil J., Ryalls, James M.W. and Girling, Robbie D.. 2024. "A Novel Free-Air Diesel and Ozone Enrichment (FADOE) Research Platform." MethodsX. 12. https://doi.org/10.1016/j.mex.2024.102635
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
Mapping the effects of ozone pollution and mixing on floral odour plumes and their impact on plant-pollinator interactions
Langford, Ben, Ryalls, James M.W., Mullinger, Neil J., Hayden, Paul, Nemitz, Eiko, Pfrang, Christian, Robins, Alan, Touhami, Dalila, Bromfield, Lisa M. and Girling, Robbie D.. 2023. "Mapping the effects of ozone pollution and mixing on floral odour plumes and their impact on plant-pollinator interactions." Environmental Pollution. 336. https://doi.org/10.1016/j.envpol.2023.122336
Field-scale effects of elevated ozone and diesel exhaust emissions on insect pollination and natural enemy recruitment.
Ryalls, J., Mullinger, N.J., Langford, B., Nemitz, E., Pfrang, C. and Girling, R.. 2022. "Field-scale effects of elevated ozone and diesel exhaust emissions on insect pollination and natural enemy recruitment. " 26th International Congress of Entomology (ICE 2022). Helsinki, Finland 17 - 22 Jul 2022 Finland.
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
Ozone Mitigates the Adverse Effects of Diesel Exhaust Pollutants on Ground-Active Invertebrates in Wheat
Ryalls, James M. W., Staton, Tom, Mullinger, Neil J., Bromfield, Lisa M., Langford, Ben, Pfrang, Christian, Nemitz, Eiko, Blande, James D. and Girling, Robbie D.. 2022. "Ozone Mitigates the Adverse Effects of Diesel Exhaust Pollutants on Ground-Active Invertebrates in Wheat." Frontiers in Ecology and Evolution. 10. https://doi.org/10.3389/fevo.2022.833088
Anthropogenic air pollutants reduce insect-mediated pollination services
Ryalls, James M.W., Langford, Ben, Mullinger, Neil J., Bromfield, Lisa M., Nemitz, Eiko, Pfrang, Christian and Girling, Robbie D.. 2022. "Anthropogenic air pollutants reduce insect-mediated pollination services." Environmental Pollution. 297, p. 118847. https://doi.org/10.1016/j.envpol.2022.118847
Concurrent anthropogenic air pollutants enhance recruitment of a specialist parasitoid
Ryalls,James M. W., Bromfield, Lisa M., Bell, Luke, Jasper, Jake, Mullinger, Neil J., Blande, James D. and Girling, Robbie D.. 2022. "Concurrent anthropogenic air pollutants enhance recruitment of a specialist parasitoid." Proceedings of the Royal Society B: Biological Sciences. 289 (1986). https://doi.org/10.1098/rspb.2022.1692
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
Field-scale effects of air pollution on invertebrate community composition in wheat
Ryalls, JMW, Staton, T., Bromfield, LM, Mullinger, N, Langford, B and Girling, RD. 2021. "Field-scale effects of air pollution on invertebrate community composition in wheat." 36th Annual Meeing of the International Socity of Chemical Ecology. South Africa 05 - 10 Sep 2021 South Africa.
Diesel exhaust and ozone pollution reduce insect-mediated pollination services
Ryalls, James M W, Langford, Ben, Mullinger, Neil, Bromfield, Lisa M, Nemitz, Eiko, Pfrang, Christian and Girling, Robbie D. 2021. "Diesel exhaust and ozone pollution reduce insect-mediated pollination services." 36th Annual Meeing of the International Socity of Chemical Ecology. South Africa 05 - 10 Sep 2021 South Africa.
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.
Field-scale effects of elevated ozone and diesel exhaust emissions on insect pollination and natural enemy recruitment
Ryalls, J.M.W., Langford, B., Mullinger, N.J., Bromfield, L.M., Nemitz, E., Pfrang, C. and Girling, R.D.. 2020. "Field-scale effects of elevated ozone and diesel exhaust emissions on insect pollination and natural enemy recruitment." British Ecological Society Annual Meeting 2019. Belfast, Northern Ireland 10 - 13 Dec 2019
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
Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations
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
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
Acute exposure to diesel exhaust induces central nervous system stress and altered learning and memory in honey bees
Reitmayer, Christine M., Ryalls, James M. W., Farthing, Emily, Jackson, Christopher W., Girling, Robbie D. and Newman, Tracey A.. 2019. "Acute exposure to diesel exhaust induces central nervous system stress and altered learning and memory in honey bees." Scientific Reports. 9 (1), p. 5793. https://doi.org/10.1038/s41598-019-41876-w
Field assessments of the effects of elevated ozone and diesel exhaust emissions on insect pollination services
Girling, R., Ryalls, J., Mullinger, N., Langford, B., Nemitz, E. and Pfrang, C.. 2019. "Field assessments of the effects of elevated ozone and diesel exhaust emissions on insect pollination services." International Society of Chemical Ecology Annual Meeting 2019. Atlanta, Georgia, USA 02 - 06 Jun 2019