Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T05:30:03.605Z Has data issue: false hasContentIssue false
  • English
  • Français

Silicon is an inducible and effective herbivore defence against Helicoverpa punctigera (Lepidoptera: Noctuidae) in soybean

Published online by Cambridge University Press:  09 December 2019

Scott N. Johnson Open the ORCID record for Scott N. Johnson [Opens in a new window] ,
Rhiannon C. Rowe  and
Casey R. Hall
Scott N. Johnson*
Affiliation:
Hawkesbury Institute for the Environment, Western Sydney University, NSW, Australia
Rhiannon C. Rowe
Affiliation:
Hawkesbury Institute for the Environment, Western Sydney University, NSW, Australia
Casey R. Hall
Affiliation:
Hawkesbury Institute for the Environment, Western Sydney University, NSW, Australia
*
Author for correspondence: Scott N. Johnson, E-mail: Scott.Johnson@westernsydney.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The role of silicon (Si) in alleviating the effects of biotic and abiotic stresses, including defence against insect herbivores, in plants is widely reported. Si defence against insect herbivores is overwhelmingly studied in grasses (especially the cereals), many of which are hyper-accumulators of Si. Despite being neglected, legumes such as soybean (Glycine max) have the capacity to control Si accumulation and benefit from increased Si supply. We tested how Si supplementation via potassium, sodium or calcium silicate affected a soybean pest, the native budworm Helicoverpa punctigera Wallengren (Lepidoptera: Noctuidae). Herbivory reduced leaf biomass similarly in Si-supplemented (+Si) and non-supplemented (–Si) plants (c. 29 and 23%, respectively) relative to herbivore-free plants. Both Si supplementation and herbivory increased leaf Si concentrations. In relative terms, herbivores induced Si uptake by c. 19% in both +Si and –Si plants. All Si treatments reduced H. punctigera relative growth rates (RGR) to a similar extent for potassium (−41%), sodium (−49%) and calcium (−48%) silicate. Moreover, there was a strong negative correlation between Si accumulation in leaves and herbivore RGR. To our knowledge, this is only the second report of Si-based herbivore defence in soybean; the rapid increase in leaf Si following herbivory being indicative of an induced defence. Taken together with the other benefits of Si supplementation of legumes, Si could prove an effective herbivore defence in legumes as well as grasses.

Keywords

Defenceherbivoreinduced defencelegumesresistancesilicasilicon
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 3 , June 2020 , pp. 417 - 422
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

APHA (2017) 3125 Metals by inductively coupled plasma-mass spectrometry. Standard methods for the examination of water and wastewater. doi: 10.2105/smww.2882.048. Available at https://www.standardmethods.org/doi/abs/10.2105/SMWW.2882.048 (Accessed 20 May 2019).Google Scholar
Arsenault-Labrecque, G, Menzies, JG and Bélanger, RR (2012) Effect of silicon absorption on soybean resistance to Phakopsora pachyrhizi in different cultivars. Plant Disease 96, 37–42.CrossRefGoogle ScholarPubMed
Chou, YM, Polansky, AM and Mason, RL (1998) Transforming non-normal data to normality in statistical process control. Journal of Quality Technology 30, 133–141.CrossRefGoogle Scholar
Clissold, FJ (2008) The biomechanics of chewing and plant fracture: mechanisms and implications. Advances in Insect Physiology 34, 317–372.CrossRefGoogle Scholar
Cohen, AC (2004) Insect Diets: Science and Technology. Boca Ratin, FL, USA: CRC Press.Google Scholar
Cooke, J and Leishman, MR (2012) Tradeoffs between foliar silicon and carbon-based defences: evidence from vegetation communities of contrasting soil types. Oikos 121, 2052–2060.CrossRefGoogle Scholar
Cooke, J and Leishman, MR (2016) Consistent alleviation of abiotic stress with silicon addition: a meta-analysis. Functional Ecology 30, 1340–1357.CrossRefGoogle Scholar
Coskun, D, Deshmukh, R, Sonah, H, Menzies, JG, Reynolds, OL, Ma, JF, Kronzucker, HJ and Bélanger, RR (2019) The controversies of silicon's role in plant biology. New Phytologist 221, 67–85.CrossRefGoogle ScholarPubMed
Cruz, MFA, Rodrigues, FA, Diniz, APC, Moreira, MA and Barros, EG (2014) Soybean resistance to Phakopsora pachyrhizi as affected by acibenzolar-S-methyl, jasmonic acid and silicon. Journal of Phytopathology 162, 133–136.CrossRefGoogle Scholar
Dakora, FD and Nelwamondo, A (2003) Silicon nutrition promotes root growth and tissue mechanical strength in symbiotic cowpea. Functional Plant Biology 30, 947–953.CrossRefGoogle Scholar
Debona, D, Rodrigues, FA and Datnoff, LE (2017) Silicon's role in abiotic and biotic plant stresses. Annual Review of Phytopathology 55, 85–107.CrossRefGoogle ScholarPubMed
Deshmukh, R and Bélanger, RR (2016) Molecular evolution of aquaporins and silicon influx in plants. Functional Ecology 30, 1277–1285.CrossRefGoogle Scholar
Deshmukh, RK, Vivancos, J, Guérin, V, Sonah, H, Labbé, C, Belzile, F and Bélanger, RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Molecular Biology 83, 303–315.CrossRefGoogle ScholarPubMed
Ferreira, RS, Moraes, JC and Antunes, CS (2011) Silicon influence on resistance induction against Bemisia tabaci Biotype B (Genn.) (Hemiptera: Aleyrodidae) and on vegetative development in two soybean cultivars. Neotropical Entomology 40, 495–500.CrossRefGoogle Scholar
Frew, A, Powell, JR, Sallam, N, Allsopp, PG and Johnson, SN (2016) Trade-offs between silicon and phenolic defences may explain enhanced performance of root herbivores on phenolic-rich plants. Journal of Chemical Ecology 42, 768–771.CrossRefGoogle Scholar
Frew, A, Weston, LA, Reynolds, OL and Gurr, GM (2018) The role of silicon in plant biology: a paradigm shift in research approach. Annals of Botany 121, 1265–1273.CrossRefGoogle ScholarPubMed
Frew, A, Weston, LA and Gurr, GM (2019) Silicon reduces herbivore performance via different mechanisms, depending on host-plant species. Austral Ecology 44, 1092–1097.CrossRefGoogle Scholar
Garbuzov, M, Reidinger, S and Hartley, SE (2011) Interactive effects of plant-available soil silicon and herbivory on competition between two grass species. Annals of Botany 108, 1355–1363.CrossRefGoogle ScholarPubMed
Guntzer, F, Keller, C and Meunier, JD (2012) Benefits of plant silicon for crops: a review. Agronomy for Sustainable Development 32, 201–213.CrossRefGoogle Scholar
Hall, CR, Waterman, JM, Vandegeer, RK, Hartley, SE and Johnson, SN (2019) The role of silicon in phytohormonal signalling. Frontiers in Plant Science 10, 1132.CrossRefGoogle ScholarPubMed
Hartley, SE, Fitt, RN, McLarnon, EL and Wade, RN (2015) Defending the leaf surface: intra- and inter-specific differences in silicon deposition in grasses in response to damage and silicon supply. Frontiers in Plant Science 6, 35.CrossRefGoogle ScholarPubMed
Haynes, RJ, Belyaeva, ON and Kingston, G (2013) Evaluation of industrial wastes as sources of fertilizer silicon using chemical extractions and plant uptake. Journal of Plant Nutrition and Soil Science 176, 238–248.CrossRefGoogle Scholar
Hiltpold, I, Demarta, L, Johnson, SN, Moore, BD, Power, SA and Mitchell, C (2017) Silicon and other essential element composition in roots using X-ray fluorescence spectroscopy: a high throughput approach. In Johnson, SN (ed.), Invertebrate Ecology of Australasian Grasslands. Proceedings of the Ninth Australasian Conference in Grassland Invertebrate Ecology ACGIE, 4–7 April 2016, Hawkesbury, NSW, Australia: Western Sydney University, pp. 191–196.Google Scholar
Hodson, MJ, White, PJ, Mead, A and Broadley, MR (2005) Phylogenetic variation in the silicon composition of plants. Annals of Botany 96, 1027–1046.CrossRefGoogle Scholar
Hunt, JW, Dean, AP, Webster, RE, Johnson, GN and Ennos, AR (2008) A novel mechanism by which silica defends grasses against herbivory. Annals of Botany 102, 653–656.CrossRefGoogle ScholarPubMed
Johnson, NL (1949) Systems of frequency curves generated by methods of translation. Biometrika 36, 149–176.CrossRefGoogle Scholar
Johnson, SN and Hartley, SE (2018) Elevated carbon dioxide and warming impact silicon and phenolic-based defences differently in native and exotic grasses. Global Change Biology 24, 3886–3896.CrossRefGoogle ScholarPubMed
Johnson, WA, Cloyd, RA, Nechols, JR, Williams, KA, Nelson, NO, Rotenberg, D and Kennelly, MM (2012) Effect of nitrogen source on Pac Choi (Brassica rapa L.) chemistry and interactions with the diamondback moth (Plutella xylostella L.). Hortscience 47, 1457–1465.CrossRefGoogle Scholar
Johnson, SN, Hartley, SE, Ryalls, JMW, Frew, A, DeGabriel, JL, Duncan, M and Gherlenda, A (2017) Silicon-induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance. Functional Ecology 31, 1903–1909.CrossRefGoogle Scholar
Johnson, SN, Reynolds, OL, Gurr, GM, Esveld, JL, Moore, BD, Tory, GJ and Gherlenda, AN (2019) When resistance is futile, tolerate instead: silicon promotes plant compensatory growth when attacked by above- and belowground herbivores. Biology Letters 15, 20190361.CrossRefGoogle ScholarPubMed
Katz, O (2014) Beyond grasses: the potential benefits of studying silicon accumulation in non-grass species. Frontiers in Plant Science 5, 376.CrossRefGoogle ScholarPubMed
Kvedaras, OL, Byrne, MJ, Coombes, NE and Keeping, MG (2009) Influence of plant silicon and sugarcane cultivar on mandibular wear in the stalk borer Eldana saccharina. Agricultural and Forest Entomology 11, 301–306.CrossRefGoogle Scholar
Lev-Yadun, S and Halpern, M (2019) Extended phenotype in action. Two possible roles for silica needles in plants: not just injuring herbivores but also inserting pathogens into their tissues. Plant Signaling & Behavior 14, e1609858.CrossRefGoogle ScholarPubMed
Ma, JF and Yamaji, N (2006) Silicon uptake and accumulation in higher plants. Trends in Plant Science 11, 392–397.CrossRefGoogle ScholarPubMed
Ma, JF and Yamaji, N (2015) A cooperative system of silicon transport in plants. Trends in Plant Science 20, 435–442.CrossRefGoogle ScholarPubMed
Massey, FP and Hartley, SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. Journal of Animal Ecology 78, 281–291.CrossRefGoogle ScholarPubMed
Massey, FP, Ennos, AR and Hartley, SE (2007) Herbivore specific induction of silica-based plant defences. Oecologia 152, 677–683.CrossRefGoogle ScholarPubMed
Moise, ERD, McNeil, JN, Hartley, SE and Henry, HAL (2019) Plant silicon effects on insect feeding dynamics are influenced by plant nitrogen availability. Entomologia Experimentalis et Applicata 167, 91–97.Google Scholar
Nascimento, KJT, Debona, D, França, SKS, Gonçalves, MGM, DaMatta, FM and Rodrigues, FA (2014) Soybean resistance to Cercopora sojina infection is reduced by silicon. Phytopathology 104, 1183–1191.CrossRefGoogle ScholarPubMed
Nelwamondo, A and Dakora, FD (1999) Silicon promotes nodule formation and nodule function in symbiotic cowpea (Vigna unguiculata). New Phytologist 142, 463–467.CrossRefGoogle Scholar
Nelwamondo, A, Jaffer, MA and Dakora, FD (2001) Subcellular organization of N2-fixing nodules of cowpea (Vigna unguiculata) supplied with silicon. Protoplasma 216, 94–100.CrossRefGoogle ScholarPubMed
Nolla, A, Korndörfer, GH and Coelho, L (2006) Efficiency of calcium silicate and carbonate in soybean disease control. Journal of Plant Nutrition 29, 2049–2061.CrossRefGoogle Scholar
Rasoolizadeh, A, Labbé, C, Sonah, H, Deshmukh, RK, Belzile, F, Menzies, JG and Bélanger, RR (2018) Silicon protects soybean plants against Phytophthora sojae by interfering with effector-receptor expression. BMC Plant Biology 18, 97.CrossRefGoogle ScholarPubMed
Raven, JA (1983) The transport and function of silicon in plants. Biological Reviews 58, 179–207.CrossRefGoogle Scholar
Reidinger, S, Ramsey, MH and Hartley, SE (2012) Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer. New Phytologist 195, 699–706.CrossRefGoogle ScholarPubMed
Reynolds, OL, Keeping, MG and Meyer, JH (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. Annals of Applied Biology 155, 171–186.CrossRefGoogle Scholar
Rowe, RC, Trębicki, P, Gherlenda, A and Johnson, SN (2019) Cereal aphid performance and feeding behaviour largely unaffected by silicon enrichment of host plants. Journal of Pest Science Online early. https://doi.org/10.1007/s10340-019-01144-2.Google Scholar
Sarfraz, RM, Dosdall, LM and Keddie, AB (2009) Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. European Journal of Entomology 106, 583–594.CrossRefGoogle Scholar
Teakle, RE and Jensen, JM (1985) Heliothis punctiger. In Singh, R and Moore, RF (eds), Handbook of Insect Rearing, vol. 2. Amsterdam, The Netherlands: Elsevier, pp. 312–322.Google Scholar
Thangavelu, K and Bania, HR (1990) Preliminary investigation on the effects of minerals in the rain water on the growth and reproduction of silkworm, Bombyx mori L. Indian Journal of Sericulture 29, 37–43.Google Scholar
Yamaji, N, Mitatni, N and Ma, JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20, 1381–1389.CrossRefGoogle ScholarPubMed
Zhang, W, Xie, Z, Lang, D, Cui, J and Zhang, X (2017) Beneficial effects of silicon on abiotic stress tolerance in legumes. Journal of Plant Nutrition 40, 2224–2236.CrossRefGoogle Scholar
Supplementary material: File

Johnson et al. supplementary material

Johnson et al. supplementary material

Download Johnson et al. supplementary material(File)
File 156.4 KB