Abstract
Silicon (Si) accumulation in plants is widely recognised as an effective physical defence against chewing herbivores. However, its effects on some feeding guilds such as cell-content feeders are understudied despite being severe economic pests (e.g. Tetranychus urticae). Moreover, most studies focus on direct impacts of Si, but there is growing evidence that Si also impacts indirect defence. We examined the effects of Si on French bean, Phaseolus vulgaris, defences against the two-spotted spider mite, T. urticae. We grew plants hydroponically with (+ Si) or without (–Si) silicon, assessed T. urticae performance and tested the preference of the predatory mite, Phytoseiulus persimilis, for volatiles from T. urticae-infested (+ M) or uninfested (–M) plants. The provision of Si to plants suppressed T. urticae egg-laying, population growth and leaflet damage, and partially ameliorated T. urticae-induced reductions in stomatal conductance and net photosynthesis. Furthermore, T. urticae infestation increased foliar Si accumulation. Predatory mites were more attracted (64%) to volatiles from + Si plants experiencing herbivory than to –Si plants. The relative emissions (%) of volatile compounds, viz. E-2-hexanyl benzoate, hexanal, E-trans-β-ocimene, D-limonene, β-caryophyllene and methyl salicylate were elevated from + Si + M plants, while the relative emissions of 3-hexanol, trans-calamenene, o-xylene and o-cymene were lowered compared to –Si + M plants. Our results show, for the first time, that Si defences are inducible and effective even in low Si-accumulating plants against T. urticae and suggest that Si could play a role in pest biocontrol.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data are posted on the figshare repository https://doi.org/10.6084/m9.figshare.14174351.v2
References
Agut B, Pastor V, Jaques JA, Flors V (2018) Can plant defence mechanisms provide new approaches for the sustainable control of the two-spotted spider mite Tetranychus urticae? Int J Mol Sci 19:614. https://doi.org/10.3390/ijms19020614
Alba JM, Schimmel BC, Glas JJ, Ataide LM, Pappas ML, Villarroel CA, Schuurink RC, Sabelis MW, Kant MR (2015) Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol 205:828–840. https://doi.org/10.1111/nph.13075
Barber A, Campbell C, Crane H, Lilley R, Tregidga E (2003) Biocontrol of two-spotted spider mite Tetranychus urticae on dwarf hops by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontrol Sci Technol 13:275–284. https://doi.org/10.1080/0958315031000110300
Bensoussan N, Santamaria ME, Zhurov V, Diaz I, Grbić M, Grbić V (2016) Plant-herbivore interaction: Dissection of the cellular pattern of Tetranychus urticae feeding on the host plant. Front Plant Sci 7:1105. https://doi.org/10.3389/fpls.2016.01105
Cazaux M, Navarro M, Bruinsma KA, Zhurov V, Negrave T, Van Leeuwen T, Grbic V, Grbic M (2014) Application of two-spotted spider mite Tetranychus urticae for plant-pest interaction studies. J Vis Exp 6:543–559. https://doi.org/10.3791/51738
Colazza S, McElfresh JS, Millar JG (2004) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964. https://doi.org/10.1023/B:JOEC.0000028460.70584.d1
Connick VJ (2011) The impact of silicon fertilisation on the chemical ecology of the grapevine, Vitis vinifera; constitutive and induced chemical defenses against arthropod pests and their natural enemies. In: Master’s thesis, Charles Sturt University, Bathurst NSW
Cooke J, Leishman MR (2011) Is plant ecology more siliceous than we realise? Trends Plant Sci 16:61–68. https://doi.org/10.1016/j.tplants.2010.10.003
Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The controversies of silicon’s role in plant biology. New Phytol 221:67–85. https://doi.org/10.1111/nph.15343
Dara SK, Peck D, Murray D (2018) Chemical and non-chemical options for managing twospotted spider mite, western tarnished plant bug and other arthropod pests in strawberries. Insects 9:156. https://doi.org/10.3390/insects9040156
De Angelis JD, Larson K, Berry RE, Krantz G (1982) Effects of spider mite injury on transpiration and leaf water status in peppermint. Environ Entomol 11:975–978. https://doi.org/10.1093/ee/11.4.975
De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271. https://doi.org/10.1023/B:JOEC.0000017976.60630.8c
de Freitas BA, de Freitas Bueno RCO, Nabity PD, Higley LG, Fernandes OA (2009) Photosynthetic response of soybean to twospotted spider mite (Acari: Tetranychydae) injury. Braz Arch Biol Technol 52:825–834. https://doi.org/10.1590/S1516-89132009000400005
de Oliveira RS, Peñaflor M, Gonçalves FG, Sampaio MV, Korndörfer AP, Silva WD, Bento JMS (2020) Silicon-induced changes in plant volatiles reduce attractiveness of wheat to the bird cherry-oat aphid Rhopalosiphum padi and attract the parasitoid Lysiphlebus testaceipes. PLoS ONE 15:e0231005. https://doi.org/10.1371/journal.pone.0231005
Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83:303–315. https://doi.org/10.1007/s11103-013-0087-3
Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant Cell Environ 32:654–665. https://doi.org/10.1111/j.1365-3040.2008.01913.x
Dicke M, Beek TAV, Posthumus MA, Dom NB, Bokhoven HV, Groot AD (1990) Isolation and identification of volatile kairomone that affects acarine predator-prey interactions: involvement of host plant in its production. J Chem Ecol 16:381–396. https://doi.org/10.1007/BF01021772
Döker İ, Kazak C (2019) Non-target effects of five acaricides on a native population of Amblyseius swirskii (Acari: Phytoseiidae). Int J Acarol 45:69–74. https://doi.org/10.1080/01647954.2018.1542457
Frew A, Powell JR, Hiltpold I, Allsopp PG, Sallam N, Johnson SN (2017) 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. https://doi.org/10.1016/j.soilbio.2017.05.008
Gatarayiha MC, Laing MD, Miller RM (2010) Combining applications of potassium silicate and Beauveria bassiana to four crops to control two spotted spider mite, Tetranychus urticae Koch. Int J Pest Manage 56:291–297. https://doi.org/10.1080/09670874.2010.495794
Grbić M, Van Leeuwen T, Clark RM et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492. https://doi.org/10.1038/nature10640
Hall CR, Mikhael M, Hartley SE, Johnson SN (2020) Elevated atmospheric CO2 suppresses jasmonate and silicon-based defences without affecting herbivores. Funct Ecol 34:993–1002. https://doi.org/10.1111/1365-2435.13549
Hall CR, Waterman JM, Vandegeer RK, Hartley SE, Johnson SN (2019) The role of silicon in antiherbivore phytohormonal signalling. Front Plant Sci 10:1132. https://doi.org/10.3389/fpls.2019.01132
Harizanova A, Koleva-Valkova L, Stoeva A, Sevov A (2019) Effect of silicon on the activity of antioxidant enzymes and the photosynthetic rate of cucumber under mite infestation. Sci Papers Series A Agron 62:519–528
Hoffland E, Dicke M, Van Tintelen W, Dijkman H, Van Beusichem ML (2000) Nitrogen availability and defense of tomato against two-spotted spider mite. J Chem Ecol 26:2697–2711. https://doi.org/10.1023/A:1026477423988
Hou M, Han Y (2010) Silicon-mediated rice plant resistance to the asiatic rice borer (Lepidoptera: Crambidae): effects of silicon amendment and rice varietal resistance. J Econ Entomol 103:1412–1419. https://doi.org/10.1603/ec09341
Islam T, Moore BD, Johnson SN (2020) Novel evidence for systemic induction of silicon defences in cucumber following attack by a global insect herbivore. Ecol Entomol 45:1373–1381. https://doi.org/10.1111/een.12922
Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, Berkeley
Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: The future of biocontrol or playing with fire? Biol Control 60:77–89. https://doi.org/10.1016/j.biocontrol.2011.10.017
Kim YH, Khan AL, Waqas M, Jeong HJ, Kim DH, Shin JS, Kim JG, Yeon MH, Lee IJ (2014) Regulation of jasmonic acid biosynthesis by silicon application during physical injury to Oryza sativa L. J Plant Res 127:525–532. https://doi.org/10.1007/s10265-014-0641-3
Krugner R, Wallis CM, Walse SS (2014) Attraction of the egg parasitoid, Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae) to synthetic formulation of a (E)-β-ocimene and (E, E)-α-farnesene mixture. Biol Control 77:23–28. https://doi.org/10.1016/j.biocontrol.2014.06.005
Kvedaras OL, An M, Choi YS, Gurr GM (2010) Silicon enhances natural enemy attraction and biological control through induced plant defences. Bull Entomol Res 100:367–371. https://doi.org/10.1017/S0007485309990265
Leroy N, Tombeur F, Walgraffe Y, Cornélis JT, Verheggen FJ (2019) Silicon and plant natural defenses against insect pests: impact on plant volatile organic compounds and cascade effects on multitrophic interactions. Plants (Basel) 8:444. https://doi.org/10.3390/plants8110444
Liu J, Zhu J, Zhang P et al (2017) Silicon supplementation alters the composition of herbivore induced plant volatiles and enhances attraction of parasitoids to infested rice plants. Front Plant Sci 8:1265. https://doi.org/10.3389/fpls.2017.01265
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397. https://doi.org/10.1016/j.tplants.2006.06.007
Massey FP, Ennos AR, Hartley SE (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. J Anim Ecol 75:595–603. https://doi.org/10.1111/j.1365-2656.2006.01082.x
Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291. https://doi.org/10.1111/j.1365-2656.2008.01472.x
Miresmailli S, Isman MB (2006) Efficacy and persistence of rosemary oil as an acaricide against twospotted spider mite (Acari: Tetranychidae) on greenhouse tomato. J Econ Entomol 99:2015–2023. https://doi.org/10.1603/0022-0493-99.6.2015
Nachappa P, Margolies DC, Nechols JR, Loughin T (2006) Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days. Exp Appl Acarol 40:231–239. https://doi.org/10.1007/s10493-006-9043-0
Opit G, Nechols J, Margolies D (2004) Biological control of twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), using Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on ivy geranium: assessment of predator release ratios. Biol Control 29:445–452. https://doi.org/10.1016/j.biocontrol.2003.08.007
Park Y-L, Lee J-H (2002) Leaf cell and tissue damage of cucumber caused by twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 95:952–957. https://doi.org/10.1093/jee/95.5.952
Patil C, Udikeri S, Karabhantanal S (2018) A note on pesticide induced resurgence of two spotted spider mite, Tetranychus urticae (Acari: Tetranychidae) on grape. Persian J Acarol 7:75–84. https://doi.org/10.22073/pja.v7i1.27987
Ponzio C, Gols R, Pieterse CM, Dicke M (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct Ecol 27:587–598. https://doi.org/10.1111/1365-2435.12035
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. https://doi.org/10.1038/nature03451
Reddall A, Sadras V, Wilson L, Gregg P (2004) Physiological responses of cotton to two-spotted spider mite damage. Crop Sci 44:835–846. https://doi.org/10.2135/cropsci2004.8350
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. https://doi.org/10.1111/j.1469-8137.2012.04179.x
Reynolds OL, Keeping MG, Meyer JH (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. Ann Appl Biol 155:171–186. https://doi.org/10.1111/j.1744-7348.2009.00348.x
Reynolds OL, Padula MP, Zeng R, Gurr GM (2016) Silicon: potential to promote direct and indirect effects on plant defense against arthropod pests in agriculture. Front Plant Sci 7:744. https://doi.org/10.3389/fpls.2016.00744
Rowe RC, Trębicki P, Gherlenda AN, Johnson SN (2020) Cereal aphid performance and feeding behaviour largely unaffected by silicon enrichment of host plants. J Pest Sci 93:41–48. https://doi.org/10.1007/s10340-019-01144-2
Sabelis MW, Van de Baan HE (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol Exp Appl 33:303–314. https://doi.org/10.1111/j.1570-7458.1983.tb03273.x
Schausberger P, Peneder S, Jürschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449. https://doi.org/10.1111/j.1365-2435.2011.01947.x
Takahashi E, Ma J, Miyake Y (1990) The possibility of silicon as an essential element for higher plants. Comments Agric Food Chem 2:99–102
Tholl D, Boland W, Hansel A, Loreto F, Röse USR, Schnitzler J-P (2006) Practical approaches to plant volatile analysis. Plant J 45:540–560. https://doi.org/10.1111/j.1365-313X.2005.02612.x
Ueno O, Agarie S (2015) Silica deposition in cell walls of the stomatal apparatus of rice leaves. Plant Prod Sci 8:71–73. https://doi.org/10.1626/pps.8.71
Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572. https://doi.org/10.1016/j.ibmb.2010.05.008
Van Poecke RM, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911–1928. https://doi.org/10.1023/A:1012213116515
van Wijk M, De Bruijn PJ, Sabelis MW (2008) Predatory mite attraction to herbivore-induced plant odors is not a consequence of attraction to individual herbivore-induced plant volatiles. J Chem Ecol 34:791–803. https://doi.org/10.1007/s10886-008-9492-5
van Wijk M, de Bruijn PJ, Sabelis MW (2010) The predatory mite Phytoseiulus persimilis does not perceive odor mixtures as strictly elemental objects. J Chem Ecol 36:1211–1225. https://doi.org/10.1007/s10886-010-9858-3
Villarroel CA, Jonckheere W, Alba JM, Glas JJ, Dermauw W, Haring MA, Van Leeuwen T, Schuurink RC, Kant MR (2016) Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. Plant J 86:119–131. https://doi.org/10.1111/tpj.13152
Wei J-N, Zhu J, Kang L (2006) Volatiles released from bean plants in response to agromyzid flies. Planta 224:279–287. https://doi.org/10.1007/s00425-005-0212-x
Ximénez-Embún MG, Glas JJ, Ortego F, Alba JM, Castañera P, Kant MR (2017) Drought stress promotes the colonization success of a herbivorous mite that manipulates plant defenses. Exp Appl Acarol 73:297–315. https://doi.org/10.1007/s10493-017-0200-4
Yano S, Wakabayashi M, Takabayashi J, Takafuji A (1998) Factors determining the host plant range of the phytophagous mite, Tetranychus urticae (Acari: Tetranychidae): a method for quantifying host plant acceptance. Exp Appl Acarol 22:595–601. https://doi.org/10.1023/A:1006138527904
Ye M, Song Y, Long J et al (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 110:E3631–E3639. https://doi.org/10.1073/pnas.1305848110
Acknowledgements
TI is the holder of a scholarship as part of an Australian Research Council Future Fellowship (FT170100342) awarded to SNJ. We would like to thank Dr Laura Castaneda Gomez for her illustration in Fig. 1. We sincerely thank Associate Professor Robert Spooner-Hart for providing the spider mite colony and Biological Services (Loxton, SA, Australia) for supplying P. persimilis without a cost. We thank Dr Craig Barton, Dr Dominika Wojtalewicz and Burhan Amiji for their technical supports to the work. We also thank Dr Rebecca K. Vandegeer, Dr Casey R. Hall, Jamie M. Waterman, Rocky Putra, Ximena Cibils-Stewart, Fikadu N. Biru and Rhiannon C. Rowe for their helpful suggestions and edits to the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there is no conflict of interest.
Additional information
Communicated by Ivan Hiltpold.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Islam, T., Moore, B.D. & Johnson, S.N. Silicon suppresses a ubiquitous mite herbivore and promotes natural enemy attraction by altering plant volatile blends. J Pest Sci 95, 423–434 (2022). https://doi.org/10.1007/s10340-021-01384-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01384-1