Skip to main content
SpringerLink
Log in

Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Arbuscular mycorrhizal (AM) fungi associate with the majority of terrestrial plants, influencing their growth, nutrient uptake and defence chemistry. Consequently, AM fungi can significantly impact plant-herbivore interactions, yet surprisingly few studies have investigated how AM fungi affect plant responses to root herbivores. This study aimed to investigate how AM fungi affect plant tolerance mechanisms to belowground herbivory.

Methods

We examined how AM fungi affect plant (Saccharum spp. hybrid) growth, nutrient dynamics and secondary chemistry (phenolics) in response to attack from a root-feeding insect (Dermolepida albohirtum).

Results

Root herbivory reduced root mass by almost 27%. In response, plants augmented investment in aboveground biomass by 25%, as well as increasing carbon concentrations. The AM fungi increased aboveground biomass, phosphorus and carbon. Meanwhile, root herbivory increased foliar phenolics by 31% in mycorrhizal plants, and increased arbuscular colonisation of roots by 75% overall. AM fungi also decreased herbivore performance, potentially via increasing root silicon concentrations.

Conclusions

Our results suggest that AM fungi may be able to augment plant tolerance to root herbivory via resource allocation aboveground and, at the same time, enhance plant root resistance by increasing root silicon. The ability of AM fungi to facilitate resource allocation aboveground in this way may be a more widespread strategy for plants to cope with belowground herbivory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Data available from the Figshare Repository: https://doi.org/10.6084/m9.figshare.9831053

References

  • Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991

    Article  PubMed  Google Scholar 

  • Barber NA, Kiers ET, Theis N et al (2013) Linking agricultural practices, mycorrhizal fungi, and traits mediating plant–insect interactions. Ecol Appl 23:1519–1530

    Article  PubMed  Google Scholar 

  • Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. ArXiv E-Prints arXiv:1406.5823v1

  • Bell MJ, Stirling GR, Pankhurst CE (2007) Management impacts on health of soils supporting Australian grain and sugarcane industries. Soil Tillage Res 97:256–271

    Article  Google Scholar 

  • Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am Nat 167:141–152

    Article  PubMed  Google Scholar 

  • Bennett AE, Macrae AM, Moore BD et al (2013) Early root herbivory impairs arbuscular mycorrhizal fungal colonization and shifts defence allocation in establishing Plantago lanceolata. PLoS One 8:e66053

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blackshaw R, Kerry B (2008) Root herbivory in agricultural ecosystems. In: Johnson SN, Murray PJ (eds) Root feeders - an ecosystem perspective. CABI, Wallingford, pp 35–53

    Chapter  Google Scholar 

  • Briske DD, Boutton TW, Wang Z (1996) Contribution of flexible allocation priorities to herbivory tolerance in C4 perennial grasses: an evaluation with C13 labeling. Oecologia 105:151–159

    Article  CAS  PubMed  Google Scholar 

  • Ceccarelli N, Curadi M, Martelloni L et al (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335:311–323

    Article  CAS  Google Scholar 

  • Currie AF, Murray PJ, Gange AC (2006) Root herbivory by Tipula paludosa larvae increases colonization of Agrostis capillaris by arbuscular mycorrhizal fungi. Soil Biol Biochem 38:1994–1997

    Article  CAS  Google Scholar 

  • Currie AF, Murray PJ, Gange AC (2011) Is a specialist root-feeding insect affected by arbuscular mycorrhizal fungi? Appl Soil Ecol 47:77–83

    Article  Google Scholar 

  • Daniels BA, Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Methods and principles of Mycorrhizal research. American Phytopathological Society, St Paul, MN, pp 133–151

    Google Scholar 

  • de Azevedo LCB, Stürmer SL, Lambais MR (2014) Early changes in arbuscular mycorrhiza development in sugarcane under two harvest management systems. Braz J Microbiol 45:995–1005

    Article  PubMed Central  PubMed  Google Scholar 

  • De Mendiburu F (2014) Agricolae: statistical procedures for agricultural research. R Package Version 1.3: https://CRAN.R-project.org/package=agricolae

  • Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407

    Article  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, Second edn. Sage Publications, Thousand Oaks

    Google Scholar 

  • Frew A, Powell JR, Sallam N et al (2016) Trade-offs between silicon and phenolic defenses may explain enhanced performance of root herbivores on phenolic-rich plants. J Chem Ecol 42:768–771

    Article  CAS  PubMed  Google Scholar 

  • Frew A, Powell JR, Allsopp PG et al (2017a) Arbuscular mycorrhizal fungi promote silicon accumulation in plant roots, reducing the impacts of root herbivory. Plant Soil 419:423–433

    Article  CAS  Google Scholar 

  • Frew A, Powell JR, Hiltpold I et al (2017b) Host plant colonisation by arbuscular mycorrhizal fungi stimulates immune function whereas high root silicon concentrations diminish growth in a soil-dwelling herbivore. Soil Biol Biochem 112:117–126

    Article  CAS  Google Scholar 

  • Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environ Entomol 38:93–102

    Article  PubMed  Google Scholar 

  • Hill EM, Robinson LA, Abdul-Sada A et al (2018) Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes. J Chem Ecol 44:198–208

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hiltpold I, Demarta L, Johnson SN et al (2016) Silicon and other essential element composition in roots using X-ray fluorescence spectroscopy: a high throughput approach. In: Johnson SN (ed) Invertebrate ecology in Australasian grasslands. Proceedings of the Ninth ACGIE. Western Sydney University, Hawkesbury, NSW, Australia

    Google Scholar 

  • Hunter MD (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agric For Entomol 3:3–9

    Article  Google Scholar 

  • Johnson SN, Hartley SE (2018) Elevated carbon dioxide and warming impact silicon and phenolic-based defences differently in native and exotic grasses. Glob Chang Biol 24:3886–3896

    Article  PubMed  Google Scholar 

  • Johnson SN, Rasmann S (2015) Root-feeding insects and their interactions with organisms in the rhizosphere. Annu Rev Entomol 60:517–535

    Article  CAS  PubMed  Google Scholar 

  • Johnson SN, Benefer CM, Frew A et al (2016a) New frontiers in belowground ecology for plant protection from root-feeding insects. Appl Soil Ecol 108:96–107

    Article  Google Scholar 

  • Johnson SN, Erb M, Hartley SE (2016b) Roots under attack: contrasting plant responses to below-and aboveground insect herbivory. New Phytol 210:413–418

    Article  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A et al (2008a) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406

    Article  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A et al (2008b) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    Article  PubMed  Google Scholar 

  • Kaschuk G, Kuyper TW, Leffelaar PA et al (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244

    Article  CAS  Google Scholar 

  • Kempel A, Schädler M, Chrobock T et al (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci 108:5685–5689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keymer A, Gutjahr C (2018) Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr Opin Plant Biol 44:137–144

    Article  CAS  PubMed  Google Scholar 

  • Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097

    Article  PubMed  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  PubMed  CAS  Google Scholar 

  • McKenzie SW, Johnson SN, Jones TH et al (2016) Root herbivores drive changes to plant primary chemistry, but root loss is mitigated under elevated atmospheric CO2. Front Plant Sci 7:837

    Article  PubMed Central  PubMed  Google Scholar 

  • Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    Article  PubMed  CAS  Google Scholar 

  • Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566

    Article  Google Scholar 

  • Oehl F, Sieverding E, Mäder P et al (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583

    Article  PubMed  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1

    Article  PubMed  Google Scholar 

  • Poveda K, Jiménez MIG, Kessler A (2010) The enemy as ally: herbivore-induced increase in crop yield. Ecol Appl 20:1787–1793

    Article  PubMed  Google Scholar 

  • Rasmann S, Agrawal AA (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr Opin Plant Biol 12:473–478

    Article  CAS  PubMed  Google Scholar 

  • Reidinger S, Ramsey MH, Hartley SE (2012) Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer. New Phytol 195:699–706

    Article  CAS  PubMed  Google Scholar 

  • Riley RC, Cavagnaro TR, Brien C et al (2019) Resource allocation to growth or luxury consumption drives mycorrhizal responses. Ecol Lett 22:1757–1766

    Article  PubMed  Google Scholar 

  • Robert CAM, Ferrieri RA, Schirmer S et al (2014) Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms. Plant Cell Environ 37:2613–2622

    Article  CAS  PubMed  Google Scholar 

  • Rokni N, Goltapeh EM (2011) Diversity of arbuscular mycorrhizal fungi associated with common sugarcane varieties in Iran. J Agric Technol 7:1017–1022

    Google Scholar 

  • Sallam N (2011) Review of current knowledge on the population dynamics of Dermolepida albohirtum (Waterhouse)(Coleoptera: Scarabaeidae). Aust J Entomol 50:300–308

    Google Scholar 

  • Salminen J-P, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338

    Article  Google Scholar 

  • Schädler M, Ballhorn DJ (2017) Beneficial soil microbiota as mediators of the plant defensive phenotype and aboveground plant-herbivore interactions. In: Cánovas FM, Lüttge U, Matyssek R (eds) Progress in botany Vol. 78. Springer international publishing, Cham, pp 305–343

    Google Scholar 

  • Schultz JC, Appel HM, Ferrieri AP, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4:324

  • Slansky FJ (1985) Food utilization by insects: interpretation of observed differences between dry weight and energy efficiencies. Entomol Exp Appl 39:47–60

    Article  Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • Sonnemann I, Baumhaker H, Wurst S (2012) Species specific responses of common grassland plants to a generalist root herbivore (Agriotes spp. larvae). Basic Appl Ecol 13:579–586

    Article  Google Scholar 

  • Stork NE (2018) How many species of insects and other terrestrial arthropods are there on earth? Annu Rev Entomol 63:31–45

    Article  CAS  PubMed  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  CAS  PubMed  Google Scholar 

  • Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Article  Google Scholar 

  • Vannette RL, Hunter MD (2009) Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agric For Entomol 11:351–358

    Article  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zvereva EL, Kozlov MV (2012) Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. Oecologia 169:441–452

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the teams at Sugar Research Australia Ltd. and the Hawkesbury Institute for the Environment. Funding was provided by Sugar Research Australia Ltd. (Project no. 2014/104).

Author information

Authors and Affiliations

  1. School of Sciences, Centre for Crop Health, University of Southern Queensland, Toowoomba, Queensland, Australia

    Adam Frew

  2. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia

    Adam Frew, Jeff R. Powell & Scott N. Johnson

  3. Institute for Land, Water and Society, Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, New South Wales, Australia

    Adam Frew

Authors
  1. Adam Frew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeff R. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Scott N. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AF, JRP and SNJ planned and designed the research. AF conducted the experimental work and collected the data. AF analysed the data with input from JRP and SNJ. AF led the writing of the manuscript with significant input from JRP and SNJ.

Corresponding author

Correspondence to Adam Frew.

Additional information

Responsible Editor: Katharina Pawlowski.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 271 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frew, A., Powell, J.R. & Johnson, S.N. Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis. Plant Soil 447, 463–473 (2020). https://doi.org/10.1007/s11104-019-04399-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04399-x

Keywords

Search

Navigation