Aphid-induction of defence-related metabolites in Arabidopsis thaliana is dependent upon density, aphid species and duration of infestation

  • Simon HodgeEmail author
  • Mark Bennett
  • John W. Mansfield
  • Glen Powell
Original Paper


Plants display a wide range of chemical defence responses when challenged by sap feeding insects. In this study, we examined changes in leaf chemistry in Arabidopis thaliana when challenged by three species of aphid which were all able to grow and reproduce on Arabidopsis: a generalist with wide host range, Myzus persicae, and two brassica specialists Brevicoryne brassicae and Lipaphis pseudobrassicae. Most glucosinolates were reduced in concentration by aphid feeding, but Myzus persicae consistently increased the levels of 4-methoxy-indolyl-glucosinolate, which is a known feeding deterrent for M. persicae, whilst decreasing other indolyls, suggesting the plant is converting these compounds to the former. The foliar concentrations of jasmonic acid and salicyclic acid were increased by M. persicae but not by B. brasssicae and L. pseudobrassicae, whereas the phytoalexin camalexin and its precursor, the amino acid tryptophan, was induced after feeding by all three aphids. Many of the compounds induced by M. persicae (e.g., jasmonic acid; salicylic acid; camalexin; tryptophan; 4-methoxy-indolyl-glucosinolate) exhibited positive relationships with aphid density and the duration of feeding prior to harvest, indicating that they are responding to the overall level of herbivore challenge that has taken place. The study reinforces the need to consider components of the experimental system (e.g., insect density, insect species, duration of feeding prior to harvest) when making inter-study comparisons of the chemical responses of plants to aphid feeding.


Brevicoryne brassicae Camalexin Glucosinolates Jasmonic acid Lipaphis pseudobrassicae Myzus persicae Salicylic acid 



This work was funded by a research Grant from the Biotechnology and Biological Sciences Research Council, UK. Our thanks go to Martin Selby for technical support, and Colin Turnbull, John Rossiter and Murray Grant for advice throughout this study. We thank three anonymous referees for their helpful comments on an earlier draft of this manuscript.


  1. Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90CrossRefPubMedGoogle Scholar
  2. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbiores and plant defence. Trends Plant Sci 17:293–302CrossRefPubMedGoogle Scholar
  3. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633CrossRefGoogle Scholar
  5. Bones AM, Rossiter JT (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208CrossRefGoogle Scholar
  6. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  7. Clay NK, Adio AM, Denoux C, Jander GJ, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101CrossRefPubMedGoogle Scholar
  8. Cole RA (1997) The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated Brassica species. Entomol Exp Appl 85:121–133CrossRefGoogle Scholar
  9. Cumming G (2012) Understanding the new statistics. Routledge, LondonGoogle Scholar
  10. de Ilarduya OM, Xie QG, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microbe Interact 16:699–708CrossRefGoogle Scholar
  11. de Vos M, van Oosted VR, van Poecke RMP, van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux J-P, van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937CrossRefPubMedGoogle Scholar
  12. de Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis-aphid interactions. Bioessays 29:871–883CrossRefPubMedGoogle Scholar
  13. Donovan MP, Nabity PD, DeLucia EH (2013) Salicylic acid-mediated reductions in yield in Nicotiana attenuate challenged by aphid herbivory. Arthropod Plant Interact 7:45–52CrossRefGoogle Scholar
  14. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259CrossRefPubMedPubMedCentralGoogle Scholar
  15. Forcat S, Bennett MH, Mansfield JW, Grant MR (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4:16CrossRefPubMedPubMedCentralGoogle Scholar
  16. Glawischnig E (2007) Camalexin. Phytochemistry 68:401–406CrossRefPubMedGoogle Scholar
  17. Glawischnig E, Hansen BG, Olsen CE, Halkier BA (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc Natl Acad Sci USA 101:8245–8250CrossRefPubMedGoogle Scholar
  18. Goggin FL (2007) Plant–aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408CrossRefPubMedGoogle Scholar
  19. Henderson P, Seaby R (2008) A practical handbook for multivariate methods. Pisces Conservation Ltd., LymingtonGoogle Scholar
  20. Hillwig MS, Chiozza M, Casteel CL, Lau ST, Hohenstein J, Hernández E, Jander G, MacIntosh GC (2016) Abscisic acid deficiency increases defence responses against Myzus persicae in Arabidopsis. Mol Plant Pathol 17:225–235CrossRefPubMedGoogle Scholar
  21. Hodge S, Ward JL, Beale MH, Bennett M, Mansfield JW, Powell G (2013) Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237:1057–1064CrossRefPubMedGoogle Scholar
  22. Jaouannet M, Rodriguez PA, Thorpe P, Lenoir CJG, MacLeod R, Escudero-Martinez C, Bos JIB (2014) Plant immunity in plant–aphid interactions. Front Plant Sci 5:663CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jaouannet M, Morris JA, Hedley PE, Bos JIB (2015) Characterization of Arabidopsis transcriptional responses to different aphid species reveals genes that contribute to host susceptibility and non-host resistance. PLoS Pathog 11:e1004918. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kamphuis LG, Zulak K, Gao LL, Anderson J, Singh KB (2013) Plant–aphid interactions with a focus on legumes. Funct Plant Biol 40:1271–1284CrossRefGoogle Scholar
  25. Kettles GJ, Drurey C, Schoonbeek H, Maule AJ, Hogenhaut S (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198:1178–1190CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019CrossRefPubMedGoogle Scholar
  27. Kim JH, Lee BW, Schroeder FC, Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54:1015–1026CrossRefPubMedGoogle Scholar
  28. Kroes A, van Loon JJ, Dicke M (2015) Density-dependent interference of aphids with caterpillar-induced defenses in Arabidopsis: involvement of phytohormones and transcription factors. Plant Cell Physiol 56:98–106CrossRefPubMedGoogle Scholar
  29. Kroes A, Broekgaarden C, Castellanos Uribe M, May S, van Loon JJA, Dicke M (2017) Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner. Oecologia 183:107–120CrossRefPubMedGoogle Scholar
  30. Kuśnierczyk A, Winge PER, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defence against aphids: timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31:1097–1115CrossRefPubMedGoogle Scholar
  31. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  32. Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defense responses to the soybean aphid. New Phytol 179:185–195CrossRefPubMedGoogle Scholar
  33. Louis J, Shah J (2013) Arabidopsis thaliana—Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mai VC, Drzewiecka K, Jelen H, Narozna D, Rucinska-Sobkowiak R, Kesy J, Floryszak-Wieczorek J, Gabrys B, Morkunas I (2014) Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci 221/222:1–12CrossRefGoogle Scholar
  35. Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signalling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67:2450–2462CrossRefPubMedGoogle Scholar
  37. Mewis I, Khan MAM, Glawischnig E, Schreiner M, Ulrichs C (2012) Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PLoS ONE 7(11):e48661. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mohase L, van der Westhuizen AJ (2002) Salicylic acid is involved in resistance responses in the Russian wheat aphid-wheat interaction. J Plant Physiol 159:585–590CrossRefGoogle Scholar
  39. Moran P, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085CrossRefPubMedPubMedCentralGoogle Scholar
  40. Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch Insect Biochem Physiol 51:182–203CrossRefPubMedGoogle Scholar
  41. Nault LR, Styer WE (1972) Effects of sinigrin on host selection by aphids. Entomol Exp Appl 15:423–437CrossRefGoogle Scholar
  42. Pegadaraju V, Knepper C, Reese J, Shah J (2005) Premature leaf senescence modulated by the PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol 139:1927–1934CrossRefPubMedPubMedCentralGoogle Scholar
  43. Pfalz M, Vogel H, Kroymann J (2009) The gene controlling the Indole Glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21:985–999CrossRefPubMedPubMedCentralGoogle Scholar
  44. Ponzio C, Papazian S, Albrectsen BR, Dicke M, Rieta G (2017) Dual herbivore attack and herbivore density affect metabolic profiles of Brassica nigra leaves. Plant Cell Environ 40:1356–1367CrossRefPubMedGoogle Scholar
  45. Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioural, evolutionary, and applied perspectives. Annu Rev Entomol 51:309–330CrossRefPubMedGoogle Scholar
  46. Pratt C, Pope TW, Powell G, Rossiter JT (2008) Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two coccinellid species. J Chem Ecol 34:323–329CrossRefPubMedGoogle Scholar
  47. Rashid MH, Khan A, Hossain MT, Chung YR1 (2017) Induction of systemic resistance against aphids by endophytic Bacillus velezensis YC7010 via xpressing PHYTOALEXIN DEFICIENT4 in Arabidopsis. Front Plant Sci 8:211PubMedPubMedCentralGoogle Scholar
  48. Rohr F, Ulrichs C, Mewis I (2009) Variability of aliphatic glucosinolates in Arabidopsis thaliana (L.)—impact on glucosinolate profile and insect resistance. J Appl Bot Food Qual 82:131–135Google Scholar
  49. Rosa-Gomes MF, Salvadori JR, Schons J (2008) Damage of Rhopalosiphum padi (L.) (Hemiptera: Aphididae) on wheat plants related to duration time and density of infestation. Neotrop Entomol 37:577–581CrossRefGoogle Scholar
  50. Smith JL, De Moraes CM, Mescher MC (2009) Jasmonate- and salicylate mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503CrossRefPubMedGoogle Scholar
  51. Stewart SA, Hodge S, Ismail N, Mansfield JM, Feys BJ, Prosperi J-M, Huguet T, Ben C, Gentzbittel L, Powell G (2009) The RAP1 gene confers extreme, race-specific resistance to the pea aphid in Medicago truncatula independent of the hypersensitive reaction. Mol Plant Microbe Interact 12:1645–1655CrossRefGoogle Scholar
  52. Stewart SA, Hodge S, Bennett M, Mansfield JW, Powell G (2016) Aphid induction of phytohormones in Medicago truncatula is dependent upon time post-infestation, aphid density and the genotypes of both plant and insect. Arthropod Plant Interact 10:41–53CrossRefGoogle Scholar
  53. Studham ME, MacIntosh GC (2013) Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants. Mol Plant Microbe Interact 26:116–129CrossRefPubMedGoogle Scholar
  54. Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem feeding insects. J Exp Bot 57:755–766CrossRefPubMedGoogle Scholar
  55. Truong D-H, Delory BM, Vanderplanck M, Brostaux Y, Vandereycken A, Heuskin S, Delaplace P, Francis F, Lognay G (2014) Temperature regimes and aphid density interactions differentially influence VOC emissions in Arabidopsis. Arthropod Plant Interact 8:317–327Google Scholar
  56. Wentzell AM, Kliebenstein DJ (2008) Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiol 147:415–428CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zhang P-J, Huang F, Zhang J-M, Wei J-N, Lu Y-B (2015) The mealybug Phenacoccus solenopsis suppresses plant defense responses by manipulating JA-SA crosstalk. Sci Rep 5:9354. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zhu-Salzman K, Bi J-l, Liu T-X (2005) Molecular strategies of plant defense and insect counter defense. Insect Sci 12:3–15CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Division of BiologyImperial College LondonLondonUK
  2. 2.Future Farming CentreLincoln UniversityCanterburyNew Zealand
  3. 3.NIAB EMREast MallingUK

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