Abstract
Plants exhibit a remarkable capacity to discern between self-inflicted damage, herbivore attacks, and mechanical harm through pattern recognition, detecting specific signals associated with each type of damage. Mechanical damage significantly influences plant defence responses against herbivorous insects. This study aimed to artificially activate the plant defence system and observe the performance of aphid (Myzus persicae Sulzer) (Hemiptera: Aphididae) and their parasitoid (Diaeretiella rapae M’Intosh) (Hymenoptera: Braconidae) on brassica plants. Mechanically damaged and undamaged plants were subjected to aphid infestation, and various parameters related to aphid and parasitoid performance, including adult survival, fecundity, aphid settlement, and oviposition behavior, were measured. Results revealed that plants with artificial damage exhibited greater resistance to aphids than undamaged plants. In the cage bioassay, there was a notable 17% reduction in aphid larviposition on damaged plants, with no significant impact on adult mortality. The aphid settlement bioassay demonstrated a significant 33% reduction in aphid settlement on damaged plants compared to undamaged ones. Conversely, mechanical damage increased parasitism behavior, leading to a substantial 32% increase in parasitoids’ oviposition preference on damaged plants. These findings highlight the significance of considering mechanical damage as a crucial factor in altering plant–insect interactions. The study suggests that mechanical damage could be a potential tool for plant protection in agricultural settings by significantly suppressing aphid performance and enhancing parasitoid behaviour.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support our findings of this study are available from the first author upon reasonable request.
References
Aartsma Y (2018) Herbivore-induced plant volatiles and tritrophic interactions: from local to landscape scale. Wageningen University and Research
Abd El-Rahman SS, Mazen MM, Mohamed HI, Mahmoud NM (2012) Induction of defence related enzymes and phenolic compounds in lupin (Lupinus albus L.) and their effects on host resistance against Fusarium wilt. Europ J Plant Pathol 134:105–116. https://doi.org/10.1007/s10658-012-0028-z
Abdul Malik NA, Kumar IS, Nadarajah K (2020) Elicitor and receptor molecules: Orchestrators of plant defence and immunity. Inter J Mol Sci 21(3):963. https://doi.org/10.3390/ijms21030963
Aguirre-Becerra H, Vazquez-Hernandez MC, Saenz de la OD, Alvarado-Mariana A, Guevara-Gonzalez RG, Garcia-Trejo JF, Feregrino-Perez AA (2021) Role of stress and defense in plant secondary metabolites production. In: Pal D, Nayak AK (eds.) Bioactive natural products for pharmaceutical applications. Advanced Structured Materials 140: 151–195. Springer, Cham. https://doi.org/10.1007/978-3-030-54027-2_5
Ahmad P, Jamsheed S, Hameed A, Rasool S, Sharma I, Azooz MM, Hasanuzzaman M (2014) Drought stress induced oxidative damage and antioxidants in plants. In: Oxidative damage to plants (pp 345–367). Elsevier. https://doi.org/10.1016/B978-0-12-799963-0.00011-3
Ahuja I, Rohloff J, Bones AM (2011) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. Sustain Agric 2:623–670. https://doi.org/10.1051/agro/2009025
Ajeigb HA, Waliyar F, Echekwu CA, Kunihya A, Motagi BN, Eniaiyeju D, Inuwa A (2015) A farmer’s guide to profitable groundnut production in Nigeria. Patancheru 502324, Telangana, India: international crops research institute for the semi-arid tropics, p 36
Ali J (2023) The peach potato aphid (Myzus persicae): ecology and management. CRC Press. https://doi.org/10.1201/9781003400974
Ali J, Covaci AD, Roberts JM, Sobhy IS, Kirk WDJ, Bruce TJA (2021) Effects of cis-jasmone treatment of brassicas on interactions with myzus persicae aphids and their parasitoid diaeretiella rapae. Front Plant Sci 12:711896. https://doi.org/10.3389/fpls.2021.711896
Ali J, Sobhy IS, Bruce TJ (2022) Wild potato ancestors as potential sources of resistance to the aphid Myzus persicae. Pest Manag Sci 78(9):3931–3938. https://doi.org/10.1002/ps.6957
Ali J, Bayram A, Mukarram M, Zhou F, Karim MF, Hafez MMA, Mahamood M, Yusuf AA, King PJH, Adil MF (2023a) Peach-potato Aphid Myzus persicae: current management strategies, challenges, and proposed solutions. Sustainability 15(14):11150. https://doi.org/10.3390/su151411150
Ali J, Wei D, Mahamood M, Zhou F, King PJH, Zhou W, Shamsi IH (2023b) Exogenous application of methyl salicylate induces defence in brassica against peach potato aphid Myzus persicae. Plants 12(9):1770. https://doi.org/10.3390/plants12091770
Ali J (2022) The chemical ecology of a model aphid pest, Myzus persicae, and its natural enemies. Keele University
Aly AA, Mansour M, Mohamed HI, Abd-Elsalam KA (2012) Examination of correlations between several biochemical components and powdery mildew resistance of flax cultivars. Plant Patholo J 28(2):149–155
Aly AA, Mohamed HI, Mansour MT, Omar MR (2013) Suppression of powdery mildew on flax by foliar application of essential oils. J Phytopathol 161(6):376–381
Ashry NA, Ghonaim MM, Mohamed HI, Mogazy AM (2018) Physiological and molecular genetic studies on two elicitors for improving the tolerance of six Egyptian soybean cultivars to cotton leaf worm. Plant Physiol Biochem 130:224–234. https://doi.org/10.1016/j.plaphy.2018.07.010
Badenes-Perez FR, Gershenzon J, Heckel DG (2014) Insect attraction versus plant defence: young leaves high in glucosinolates stimulate oviposition by a specialist herbivore despite poor larval survival due to high saponin content. PLoS ONE 9(4):e95766. https://doi.org/10.1371/journal.pone.0095766
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. https://doi.org/10.1007/s11103-008-9435-0
Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM, Foster SP, Gutbrod O, Nauen R, Slater R, Williamson MS (2014) The evolution of insecticide resistance in the peach potato aphid Myzus Persicae. Insect Biochem Mol Biol 51(1):41–51. https://doi.org/10.1016/j.ibmb.2014.05.003
Bhaskara Reddy MV, Arul J, Angers P, Couture L (1999) Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. J Agric Food Chem 47(3):1208–1216. https://doi.org/10.1021/jf981225k
Birkett MA, Campbell CA, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams GH, Wadhams LJ, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defence. Proceed Nat Acad Sci USA 97(16):9329–9334. https://doi.org/10.1073/pnas.160241697
Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide. (Issue Ed. 2). Wiley
Branca F, Cartea E (2010) Brassica. In: Wild crop relatives: genomic and breeding resources: oilseeds (pp 17–36). Springer. https://doi.org/10.1007/978-3-642-14228-4
Bruce TJA, Smart LE, Birch ANE, Blok VC, MacKenzie K, Guerrieri E, Cascone P, Luna E, Ton J (2017) Prospects for plant defence activators and biocontrol in IPM—concepts and lessons learnt so far. Crop Protect 97:128–134. https://doi.org/10.1016/j.cropro.2016.10.003
Chen C, Zhao C, Wu Z, Liu G, Yu X, Zhang P (2021) Whitefly induced tomato volatiles mediate host habitat location of the parasitic wasp Encarsia formosa, and enhance its efficacy as a bio-control agent. Pest Manag Sci 77(2):749–757. https://doi.org/10.1002/ps.6071
Chowdhury P (2022) Glucosinolates and its role in mitigating abiotic and biotic stress in Brassicaceae. Plant Stress Physiol Perspect Agric. https://doi.org/10.5772/intechopen.102367
Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Ann Rev Ecol Evol Syst 36:169–189. https://doi.org/10.1146/annurev.ecolsys.36.102003.152617
DeerInWater K M (2015) Plant volatiles as information sources influencing herbivore preference and performance. University of California, Davis
Diaz I (2018) Plant defence genes against biotic stresses. Inter J Mol Sci 19(8):2446. https://doi.org/10.3390/ijms19082446
Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol Plant-Microbe Interact 20(6):707–716. https://doi.org/10.1094/MPMI-20-6-0707
Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defence priming against herbivores: getting ready for a different battle. Plant Physiol 146(3):818–824. https://doi.org/10.1104/pp.107.113027
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defence against insect herbivores. Inter J Mol Sci 14(5):10242–10297. https://doi.org/10.3390/ijms140510242
Graham JS, Hall G, Pearce G, Ryan CA (1986) Regulation of synthesis of proteinase inhibitors I and II mRNAs in leaves of wounded tomato plants. Planta 169:399–405. https://doi.org/10.1007/BF00392137
Heckel DG (2014) Insect detoxification and sequestration strategies. Ann Plant Rev Insect Plant Interact 47:77–114. https://doi.org/10.1002/9781118829783.ch3
Heidel-Fischer HM, Vogel H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci 8:8–14. https://doi.org/10.1016/j.cois.2015.02.004
Hjältén J (1999) Willow response to pruning: the effect on plant growth, survival and susceptibility to leaf gallers. Ecoscience 6(1):62–67. https://doi.org/10.1080/11956860.1999.11952198
Hjältén J, Price PW (1996) The effect of pruning on willow growth and sawfly population densities. Oikos 77:549–555. https://doi.org/10.2307/3545944
Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Ann Rev Entomolo 54:57–83. https://doi.org/10.1146/annurev.ento.54.110807.090623
Howard RJ, Valent B (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Ann Rev Microbiol 50(1):491–512. https://doi.org/10.1146/annurev.micro.50.1.491
Jha Y, Mohamed HI (2022) Plant secondary metabolites as a tool to investigate biotic stress tolerance in plants: a review. Gesunde Pflanz 74:71–790. https://doi.org/10.1007/s10343-022-00669-4
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291(5511):2141–2144. https://doi.org/10.1126/science.291.5511.2141
Kumari M, Naidu S, Kumari B, Singh IK, Singh A (2023) Comparative transcriptome analysis of Zea mays upon mechanical wounding. Mol Biol Rep 6:5319–5343. https://doi.org/10.1007/s11033-023-08429-x
León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signalling in plants. J Expe Bot 52(354):1–9. https://doi.org/10.1093/jexbot/52.354.1
Maffei ME, Mithöfer A, Boland W (2007) Before gene expression: early events in plant–insect interaction. Trends Plant Sci 12(7):310–316. https://doi.org/10.1016/j.tplants.2007.06.001
Mattiacci L, Dicke M, Posthumus MA (1994a) Induction of parasitoid attracting synomone in brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. J Chem Ecol 20(9):2229–2247. https://doi.org/10.1007/BF02033199
Mattiacci L, Dicke M, Posthumus MA (1994b) Induction of parasitoid attracting synomone in brussels sprouts plants by feeding ofPieris brassicae larvae: role of mechanical damage and herbivore elicitor. J Chem Ecol 20(9):2229–2247. https://doi.org/10.1007/BF02033199
Mukarram M, Ali J, Dadkhah-Aghdash H, Kurjak D, Kacˇık F, Dˇurkovicˇ J (2023) Chitosan-induced biotic stress tolerance and crosstalk with phytohormones, antioxidants, and other signalling molecules. Front Plant Sci 14:1217822. https://doi.org/10.3389/fpls.2023.1217822
Peñaflor M, Bento JMS (2013) Herbivore-induced plant volatiles to enhance biological control in agriculture. Neotrop Entomol 42(4):331–343. https://doi.org/10.1007/s13744-013-0147-z
Piesik D, Łyszczarz A, Tabaka P, Lamparski R, Bocianowski J, Delaney KJ (2010) Volatile induction of three cereals: influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Ann Appl Biol 157(3):425–434. https://doi.org/10.1111/j.1744-7348.2010.00432.x
Raghava T, Ravikumar P, Hegde R, Kush A (2010) Spatial and temporal volatile organic compound response of select tomato cultivars to herbivory and mechanical injury. Plant Sci 179(5):520–526. https://doi.org/10.1016/j.plantsci.2010.07.020
Rakow G (2004) Species origin and economic importance of Brassica. Brassica 54:3–11. https://doi.org/10.1007/978-3-662-06164-0_1
Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defence gene expression. Curr Opin Plant Biol 1(5):404–411. https://doi.org/10.1016/S1369-5266(98)80264-1
Ryan CA (1990) Protease inhibitors in plants: genes for improving defences against insects and pathogens. Ann Rev Phytopathol 28(1):425–449
Savatin DV, Gramegna G, Modesti V, Cervone F (2014) Wounding in the plant tissue: the defence of a dangerous passage. Front Plant Sci 5:470. https://doi.org/10.3389/fpls.2014.00470
Shroff R, Vergara F, Muck A, Svatoš A, Gershenzon J (2008) Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defence. Proceed Nat Acad Sci 105(16):6196–6201. https://doi.org/10.1073/pnas.0711730105
Singh A, Tyagi C, Nath O, Singh IK (2018) Helicoverpa-inducible thioredoxin h from cicer arietinum: structural modeling and potential targets. Inter J Biol Macromol 109:231–243. https://doi.org/10.1016/j.ijbiomac.2017.12.079
Singh RS (2018) Plant diseases. Oxford and IBH Publishing
Smith L, Beck JJ (2013) Effect of mechanical damage on emission of volatile organic compounds from plant leaves and implications for evaluation of host plant specificity of prospective biological control agents of weeds. Biocontrol Scie Technol 23(8):880–907. https://doi.org/10.1080/09583157.2013.807908
Sobhy IS, Bruce TJA, Turlings TCJ (2018) Priming of cowpea volatile emissions with defence inducers enhances the plant’s attractiveness to parasitoids when attacked by caterpillars. Pest Manag Sci 74(4):966–977. https://doi.org/10.1002/ps.4796
Sudisha J, Sharathchandra RG, Amruthesh KN, Kumar A, Shetty HS (2012) Pathogenesis related proteins in plant defense response. In: Mérillon J, Ramawat K (eds.) Plant defence: biological control. Progress in Biological Control, Springer, Dordrecht. vol 12. pp 379–403. https://doi.org/10.1007/978-94-007-1933-0_17
Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. Adv Insect Chem Ecol 2:21–75. https://doi.org/10.1017/CBO9780511542664.003
Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250(4985):1251–1253. https://doi.org/10.1126/science.250.4985.1251
Van Emden HF, Eastop VF, Hughes RD, Way MJ (1969) The ecology of Myzus persicae. Ann Rev Entomol 14(1):197–270. https://doi.org/10.1146/annurev.en.14.010169.001213
Verma S, Nizam S, Verma PK (2013) Biotic and abiotic stress signaling in plants. Stress Signal Plants Genom Proteom Perspective 1:25–49. https://doi.org/10.1007/978-1-4614-6372-6_2
War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defence system in chickpea (Cicer arietinum L.). Plant Signal Behav 6(11):1787–1792. https://doi.org/10.4161/psb.6.11.17685
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defence against insect herbivores. Plant Signal Behav 7(10):1306–1320. https://doi.org/10.4161/psb.21663
War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Plant defence against herbivory and insect adaptations. AoB Plants 10(4):ply037. https://doi.org/10.1093/aobpla/ply037
Acknowledgements
Figure 1 was created with Biorender.com.
Funding
No funding was received for this work.
Author information
Authors and Affiliations
Contributions
JA conceived the idea and designed the experiments. JA performed the experiments and collected the data. JA, MM, HIM AA and MU analysed the data and wrote the manuscript. MM and PFJ carried data visualization and representation. All authors have contributed significantly to the manuscript and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ali, J., Mukarram, M., Abbas, A. et al. Wound to survive: mechanical damage suppresses aphid performance on brassica. J Plant Dis Prot 131, 781–792 (2024). https://doi.org/10.1007/s41348-024-00871-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-024-00871-8