Skip to main content
SpringerLink
Log in

Plant Defense and Insect Adaptation with Reference to Secondary Metabolites

  • Reference work entry
  • First Online:
Co-Evolution of Secondary Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

Abstract

Insects pose a great threat to plants, and plants, in turn, withstand to insect attack through various morphological and biochemical traits. Among the plant defensive traits, secondary metabolites play a major role against insect herbivory as they are highly dynamic. They either occur constitutively in plants or are induced in response to insect herbivory. These metabolites include sulfur- (terpenes and flavonoids) and nitrogen-containing metabolites (alkaloids, cyanogenic glucosides, and nonprotein amino acids), which are being implicated by plants against insect pests. Plant secondary metabolites either are directly toxic to insect pests or mediate signaling pathways that produce plant toxins. Further, some of the plant secondary metabolites act through antixenosis mode by developing non-preference in host plant to the insect pests. However, some plant secondary metabolites recruit natural enemies of the insect pests, thus indirectly defending plants against insect pests. However, insects have developed adaptations to these plant secondary metabolites. In this chapter, important plant secondary metabolites, their mechanism of action against insect pests, counter-adaptation by insects, and promising advances and challenges are discussed.

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

Access this chapter

Log in via an institution

Institutional subscriptions

References

  1. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A 103:8894–8899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Wu JQ, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Ann Rev Plant Biol 59:41–66

    Article  CAS  Google Scholar 

  4. War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  PubMed  PubMed Central  Google Scholar 

  5. War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Plant defence against herbivory and insect adaptations. AoB PLANTS 10:ply037. https://doi.org/10.1093/aobpla/ply037

    Article  CAS  Google Scholar 

  6. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J: Cell Mol Biol 32:701–712

    Article  CAS  Google Scholar 

  7. Wink M, Schimmer O (2010) Molecular modes of action of defensive secondary metabolites. In: Wink M (ed) Functions and biotechnology of plant secondary metabolites. Wiley-Blackwell, Oxford, pp 21–161

    Chapter  Google Scholar 

  8. Wink M (2018) Plant secondary metabolites modulate insect behavior-steps toward addiction? Front Physiol 9:364. https://doi.org/10.3389/fphys.2018.00364

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19

    Article  CAS  PubMed  Google Scholar 

  10. Mason PA, Singer MS (2015) Defensive mixology: combining acquired chemicals towards defence. Funct Ecol 29:441–450

    Article  Google Scholar 

  11. Detzel A, Wink M (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18

    Article  CAS  Google Scholar 

  12. Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL et al (2008) Beta-glucosidases as detonators of plant chemical defense. Phytochemistry 69:1795–1813

    Article  CAS  PubMed  Google Scholar 

  13. Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PEA (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci U S A 104:12976–12981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397

    Article  CAS  PubMed  Google Scholar 

  15. Alborn T, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  16. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore- specific plant responses. Plant Physiol 125:711–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. von Dahl CC, Winz RA, Halitschke R, Kühnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J 51:293–307

    Article  CAS  Google Scholar 

  18. Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, Bruessow F, Sobhy I, Reymond P (2012) Insect oral secretions suppress wound-induced responses in Arabidopsis. J Exp Bot 63:727–737

    Article  CAS  PubMed  Google Scholar 

  19. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416:599–600

    Article  CAS  PubMed  Google Scholar 

  20. Tian D, Peiffer M, Shoemaker E, Tooker J, Haubruge E, Francis F, Luthe DS, Felton GW (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Louis J, Peiffer M, Ray S, Luthe DS, Felton GW (2013) Host-specific salivary elicitor(s) of European corn borer induce defenses in tomato and maize. New Phytol 199:66–73

    Article  CAS  PubMed  Google Scholar 

  22. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602

    Article  CAS  PubMed  Google Scholar 

  23. Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society for Plant Physiologists, Rockville, Maryland, USA, pp 1250–1318

    Google Scholar 

  24. War AR, Sharma HC, Paulraj MG, War MY, Ignacimuthu S (2011) Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav 6:1973–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Puttick GM, Bowers MD (1988) Effect of qualitative and quantitative variation in allelochemicals on a generalist insect: iridoid glycosides and the southern armyworm. J Chem Ecol 14:335–351

    Article  CAS  PubMed  Google Scholar 

  26. Biere A, Marak HB, van Damme JM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441

    Article  PubMed  Google Scholar 

  27. Park KS, Kim BH, Chang IM (2010) Inhibitory potencies of several iridoids on cyclooxygenase-1, cyclooxygnase-2 enzymes activities, tumor necrosis factor-α and nitric oxide production in vitro. Evid Based Comp Alt Med 7:41–45

    Article  Google Scholar 

  28. Kim DH, Kim BR, Kim JY, Jeong YC (2000) Mechanism of covalent adduct formation of aucubin to proteins. Toxicol Lett 114:181–188

    Article  CAS  PubMed  Google Scholar 

  29. Konno K, Hirayama C, Yasui H, Nakamura M (1999) Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc Natl Acad Sci U S A 96:9159–9164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bowers MD, Puttick GM (1988) Response of generalist and specialist insects to qualitative allelochemical variation. J Chem Ecol 14:319–334

    Article  CAS  Google Scholar 

  31. Niemeyer HM (2009) Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J Agric Food Chem 57:1677–1696

    Article  CAS  PubMed  Google Scholar 

  32. Wouters FC, Blanchette B, Gershenzon J, Vassao DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev 15:1127–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Maag D, Erb M, Köllner T, Gershenzon J (2015) Defensive weapons and defense signals in plants: some metabolites serve both roles. BioEssays 37:167–174

    Article  PubMed  Google Scholar 

  34. Campos F, Atkinson J, Arnason JT, Philogéne BJR, Morand P, Werstiuk NH, Timmins G (1988) Toxicity and toxicokinetics of 6-methoxybenzoxazolinone (MBOA) in the European corn borer, Ostrinia nubilalis (Hubner). J Chem Ecol 14:989–1002

    Article  CAS  PubMed  Google Scholar 

  35. Atkinson J, Arnason J, Campos F, Niemeyer HM, Bravo HR (1992) Synthesis and reactivity of cyclic hydroxamic acids. In: Baker DR, Fenyes JG, Steffens JJ (eds) Synthesis and chemistry of agrochemicals III. American Chemical Society, Washington, DC

    Google Scholar 

  36. Houseman JG, Campos F, Thie NMR, Philogene BJR, Atkinson J, Morand P, Arnason JT (1992) Effect of the maize derived compounds DIMBOA and MBOA on growth and digestive processes of European corn borer (Lepidoptera, Pyralidae). J Econ Entomol 85:669–674

    Article  CAS  Google Scholar 

  37. Maag D, Dalvit C, Thevenet D, Köhler A, Wouters FC, Vassao DG, Gershenzon J, Wolfender JL, Turlings TC, Erb M, Glauser G (2014) 3-β-D-glucopyranosyl-6-methoxy-2- benzoxazolinone (MBOA-N-Glc) is an insect detoxification product of maize 1,4-benzoxazin-3-ones. Phytochemistry 102:97–105

    Article  CAS  PubMed  Google Scholar 

  38. Argandoǹa VH, Luza JG, Niemeyer HM, Corcuera LJ (1980) Role of hydroxamic acids in the resistance of cereals to aphids. Phytochemistry 19:1665–1668

    Article  Google Scholar 

  39. Corcuera LJ, Queirolo CB, Argandoǹa VH (1985) Effects of 2-b-D-glucosyl-4-hydroxy-7-methoxy-1,4-benzoxazin-3- one on Schizaphis graminum (Rondani) (Insecta, Aphididae) feeding on artificial diets. Experientia 41:514–516

    Article  CAS  Google Scholar 

  40. Bohidar K, Wratten SD, Niemeyer HM (1986) Effects of hydroxamic acids on the resistance of wheat to the aphid Sitobion avenae. Ann Appl Biol 109:193–198

    Article  CAS  Google Scholar 

  41. Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Glauser G, Erb M, Flors V, Frey M, Ton J (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol 157:317–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Cherrett JM (1972) Some factors involved in the selection of vegetable substrate by Atta cephalotes (L.) (hymenoptera: Formicidae) in tropical rain forest. J Anim Ecol 41:647–660

    Article  Google Scholar 

  43. Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Annu Rev Plant Physiol Plant Mol Biol 52:689–724

    Article  CAS  PubMed  Google Scholar 

  44. Canals D, Irurre-Santilari J, Casas J (2005) The first cytochrome P450 in ferns. FEBS J 272:4817–4825

    Article  CAS  PubMed  Google Scholar 

  45. Cruickshank PA (1971) Insect juvenile hormone analogues: effects of some terpenoid amide derivatives. Bull World Health Org 44:395–396

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J Chem Ecol 35:28–38

    Article  CAS  PubMed  Google Scholar 

  47. Thipyapong P, Steffens JC (1997) Tomato polyphenol oxidase: differential response of the polyphenol oxidase F promoter to injuries and wound signals. Plant Physiol 115:409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci U S A 92:407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Leszczynski B (1995) The influence of phenolic compounds on the preference of winter wheat cultivars by cereal aphids. Insect Sci Appl 6:157–158

    Article  Google Scholar 

  50. War AR, Paulraj MG, Ignacimuthu S, Sharma HC (2015) Induced resistance to Helicoverpa armigera through exogenous application of jasmonic acid and salicylic acid in groundnut, Arachis hypogaea. Pest Manag Sci 71:72–82

    Article  PubMed  CAS  Google Scholar 

  51. Ruuhola T, Tikkanen O, Tahvanainen O (2001) Differences in host use efficiency of larvae of a generalist moth, Operophtera brumata on three chemically divergent Salix species. J Chem Ecol 27:1595–1615

    Article  CAS  PubMed  Google Scholar 

  52. Luczynski A, Isman MB, Rawirth DA (1999) Strawberry foliar phenolics and their relationship to development of the two-spotted spider mite. J Econ Entomol 83:557–563

    Article  Google Scholar 

  53. Maxwell FG, Lafever HN, Jenkins JN (1965) Blister beetles on glandless cotton. J Econ Entomol 58:792–798

    Article  Google Scholar 

  54. Abou-Donia MB (1989) Gossypol. In: Cheeke PR (ed) Toxicants of plant origin, Phenolics, vol 5. CRC Press, Boca Raton, pp 2–22

    Google Scholar 

  55. Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565

    Article  CAS  PubMed  Google Scholar 

  56. Barbehenn RV, Martin MM, Hagerman AE (1996) Reassessment of the roles of the peritrophic envelope and hydrolysis in protecting polyphagous grasshoppers from ingested hydrolyzable tannins. J Chem Ecol 22:1901–1919

    Article  CAS  PubMed  Google Scholar 

  57. Roitto M, Rautio P, Markkola A, Julkunen-Tiitto R, Varama M, Saravesi K, Tuomi J (2009) Induced accumulation of phenolics and sawfly performance in scots pine in response to previous defoliation. Tree Physiol 29:207–216

    Article  CAS  PubMed  Google Scholar 

  58. Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306

    Article  PubMed  Google Scholar 

  59. Rossi AM, Stiling P, Moon DC, Cattell MV, Drake BG (2004) Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO2. J Chem Ecol 30:1143–1152

    Article  CAS  PubMed  Google Scholar 

  60. Grayer RJ, Kimmins FM, Padgham DE, Harborne JB, Ranga Rao DV (1992) Condensed tannin levels and resistance in groundnuts (Arachis hypogaea (L.)) against Aphis craccivora (Koch). Phytochemistry 31:3795–3800

    Article  CAS  Google Scholar 

  61. Bernays EA (1981) Plant tannins and insect herbivores: an appraisal. Ecol Entomol 6:353–360

    Article  Google Scholar 

  62. Feeny PP (1968) Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. J Insect Physiol 14:805–817

    Article  CAS  Google Scholar 

  63. Simmonds MSJ (2003) Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30

    Article  CAS  PubMed  Google Scholar 

  64. War AR, Paulraj MG, Hussain B, Buhroo AA, Ignacimuthu S, Sharma HC (2013) Effect of plant secondary metabolites on Helicoverpa armigera. J Pest Sci 86:399–408

    Article  Google Scholar 

  65. Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157

    Article  CAS  Google Scholar 

  66. Simmonds MSJ, Blaney WM, Fellows LE (1990) Behavioural and electrophysiological study of antifeedant mechanisms associated with polyhydroxyalkaloids. J Chem Ecol 16:3167–3196

    Article  CAS  PubMed  Google Scholar 

  67. Johnson ET, Dowd PF (2004) Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J Agric Food Chem 52:5135–5138

    Article  CAS  PubMed  Google Scholar 

  68. Lane GA, Sutherland ORW, Skipp RA (1987) Isoflavonoids as insect feeding deterrents and antifungal components from root of Lupinus angustifolius. J Chem Ecol 13:771–783

    Article  CAS  PubMed  Google Scholar 

  69. Simmonds MSJ, Stevenson PC (2001) Effects of isoflavonoids from Cicer on larvae of Helicoverpa armigera. J Chem Ecol 27:965–977

    Article  CAS  PubMed  Google Scholar 

  70. Renwick JAA, Zhang W, Haribal M, Attygalle AB, Lopez KD (2001) Dual chemical barriers protect a plant against different larval stages of an insect. J Chem Ecol 27:1575–1583

    Article  CAS  PubMed  Google Scholar 

  71. Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    Article  CAS  PubMed  Google Scholar 

  72. Karban R, Agrawal AA, Thaler JS, Adler LS (1999) Induced plant responses and information content about risk of herbivory. Trends Ecol Evol 14:443–447

    Article  CAS  PubMed  Google Scholar 

  73. Grob K, Matile PH (1979) Vacuolar location of glucosinolates in horseradish root cells. Plant Sci Lett 14:327–335

    Article  CAS  Google Scholar 

  74. Bennett RN, Wallsgrove RM (1994) Tansley review no. 72. Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633

    Article  CAS  PubMed  Google Scholar 

  75. Bodnaryk RP (1991) Developmental profile of sinalbin in mustard seedlings, Sinapis alba L., and its relationship to insect resistance. J Chem Ecol 17:1543–1556

    Article  CAS  PubMed  Google Scholar 

  76. Li Q, Eigenbrode SD, Stringham GR, Thingarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419

    Article  CAS  Google Scholar 

  77. Wink M (2012) Medicinal plants: a source of anti-parasitic secondary metabolites. Molecules 17:12771–12791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Wink M (2007) Molecular modes of action of cytotoxic alkaloids- from DNA intercalation, spindle poisoning, topoisomerase inhibition to apoptosis and multiple drug resistance. Alkaloids 64:1–48

    CAS  Google Scholar 

  79. Schmeller T, Latz-Brüning B, Wink M (1997) Biochemical activities of berberine, palmatine and sanguinarine mediating chemical defence against microorganisms and herbivores. Phytochemistry 44:257–266

    Article  CAS  PubMed  Google Scholar 

  80. Salminen JP, Lahtinen M, Lempa K, Kapari L, Haukioja E, Pihlaja K (2004) Metabolic modifications of birch leaf phenolics by an herbivorous insect: detoxification of flavonoid aglycones via glycosylation. Zeits für Naturfor 59:437–444

    Article  CAS  Google Scholar 

  81. Ferreres F, Valentao P, Pereira JA, Bento A, Noites A, Seabra RM et al (2008) HPLC-DAD MS/MS-ESI screening of phenolic compounds in Pieris brassicae L. reared on Brassica rapa var. rapa L. J Agri Food Chem 56:844–853

    Article  CAS  Google Scholar 

  82. Schramm K, Vassao DG, Reichelt M, Gershenzon J, Wittstock U (2011) Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Mol Biol 42:174–182

    Article  PubMed  CAS  Google Scholar 

  83. Heckel D (2013) Insect detoxification and sequestration strategies. In: Voelckel C, Jander G (eds) Plant insect interactions. Wiley, Chichester

    Google Scholar 

  84. Feyereisen R (2005) Insect cytochrome P450. In: Gilbert LI et al (eds) Comprehensive molecular insect science. Elsevier, Amsterdam, pp 1–77

    Google Scholar 

  85. Cianfrogna JA, Zangeri AR, Berenbaum MR (2002) Dietary and developmental influences on induced detoxification in an oligophage. J Chem Ecol 28:1349–1364

    Article  CAS  PubMed  Google Scholar 

  86. Li X, Berenbaum MR, Schular MA (2002) Plant allelochemicals differentially regulate Helicoverpa zea cytochrome P450 genes. Insect Mol Biol 11:343–351

    Article  CAS  PubMed  Google Scholar 

  87. Stevens JL, Snyder MJ, Koener JF, Feyereisen R (2000) Inducible P450s of the CYP9 family from larval Manduca sexta midgut. Insect Biochem Mol Biol 30:559–568

    Article  CAS  PubMed  Google Scholar 

  88. Li X, Schular MA, Berenbaum MR (2002) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419:712–715

    Article  CAS  PubMed  Google Scholar 

  89. Danielson PB, Frank MR, Fogleman JC (1994) Comparison of larval and adult P-450 activity levels for alkaloid metabolism in desert Drosophila. J Chem Ecol 20:1893–1906

    Article  CAS  PubMed  Google Scholar 

  90. Yu SJ (2000) Allelochemical induction of hormone-metabolizing microsomal monooxygenases in the fall armyworm. Zool Studies 39(3):243–249

    CAS  Google Scholar 

  91. Berenbaum MR (1991) Comparative processing of allelochemicals in the Papilionidae (Lepidoptera). Arch Insect Biochem Physiol 17:213–221

    Article  CAS  Google Scholar 

  92. Ma R, Cohen MB, Berenbaum MR, Schuler MA (1994) Black swallowtail (Papilio polyxenes) alleles encode cytochrome P450s that selectively metabolize linear furanocoumarins. Arch Biochem Biophys 310:332–340

    Article  CAS  PubMed  Google Scholar 

  93. Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, Svatos A, Halkier BA, Glawischnig E (2006) CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 141:1248–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Andersen JF, Walding JK, Evans PH, Bowers WS, Feyereisen R (1997) Substrate specificity for the epoxidation of terpenoids and active site topology of house fly cytochrome P450 6A1. Chem Res Toxicol 10(2):156–164

    Article  CAS  PubMed  Google Scholar 

  95. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotech 25:1307–1313

    Article  CAS  Google Scholar 

  96. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci U S A 105:8855–8860

    Article  CAS  Google Scholar 

  97. McLaughlin LA, Niazi U, Bibby J, David JP, Vontas J, Hemingway J, Ranson H, Sutcliffe MJ, Paine MJ (2008) Characterization of inhibitors and substrates of Anopheles gambiae CYP6Z2. Insect Mol Biol 17:125–135

    Article  CAS  PubMed  Google Scholar 

  98. Sutherland TD, Unnithan GC, Andersen JF, Evans PH, Murataliev MB, Szabo LZ, Mash EA, Bowers WS, Feyereisena R (1998) Cytochrome P450 terpenoid hydroxylase linked to the suppression of insect juvenile hormone synthesis. Proc Natl Acad Sci U S A 95:12884–12889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Seybold SJ, Huber DPW, Lee JC, Graves AD, Bohlmann J (2006) Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochem Rev 5:143–178

    Article  CAS  Google Scholar 

  100. Yu SJ (1996) Insect glutathione S-transferases. Zool Stud 35:9–19

    CAS  Google Scholar 

  101. Feng Q, Davey KG, Pang ASD, Ladd TR, Retnakaran A, Tomkins BL et al (2001) Developmental expression and stress induction of glutathione S-transferase in the spruce budworm, Choristoneura fumiferana. J Insect Physiol 47:1–10

    Article  CAS  PubMed  Google Scholar 

  102. Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:3–8

    Article  CAS  PubMed  Google Scholar 

  103. Francis F, Vanhaelen N, Haubruge E (2005) Glutathione S-transferases in the adaptation to plant secondary metabolites in the Myzus persicae aphid. Arch Insect Biochem Physiol 58:166–174

    Article  CAS  PubMed  Google Scholar 

  104. Vanhaelen N, Haubruge E, Lognay G, Francis F (2001) Hoverfly glutathione S-transferases and effect of Brassicaceae secondary metabolites. Pestic Biochem Physiol 71:170–177

    Article  CAS  Google Scholar 

  105. Hu F, Ye K, Lu YJ, Thakur K, Jiang L (2018) Identification and expression profiles of twenty-six glutathione S-transferase genes from rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae). Int J Biol Macromol 120:1063–1071

    Article  CAS  PubMed  Google Scholar 

  106. Barbehenn R, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut fluids of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988

    Article  CAS  PubMed  Google Scholar 

  107. Donkor D, Mirzahosseini Z, Bede J, Bauce E, Despland E (2018) Detoxification of host plant phenolic aglycones by the spruce budworm. bioRxiv 472308. https://doi.org/10.1101/472308

  108. Usmani KA, Knowles CO (2001) DEF sensitive esterases in homogenates of larval and adult Helicoverpa zea, Spodoptera frugiperda, and Agrotis ipsilon (Lepidoptera: Noctuidae). J Econ Entomol 94:884–891

    Article  CAS  PubMed  Google Scholar 

  109. Yang Z, Zhang F, He Q, He G (2005) Molecular dynamics of detoxification and toxin tolerance genes in brown plant hopper (Nilaparvata lugens Stal., Homoptera: Delphacidae) feeding on resistant rice plants. Arch Insect Biochem Physiol 59:59–66

    Article  CAS  PubMed  Google Scholar 

  110. Mackenzie PI, Bock KW, Burchell B, Guillemette C, Ikushiro S, Iyanagi T, Miners JO, Owens IS, Nebert DW (2005) Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 15:677–685

    Article  CAS  PubMed  Google Scholar 

  111. Ahmad SA, Hopkins TL (1993) β-Glycosylation of plant phenolics by phenol B-glucosyltransferase in larval tissues of the tobacco hornworm, Manduca sexta (L.). Insect Biochem Mol Biol 23:581–589

    Article  CAS  Google Scholar 

  112. Luque T, Okano K, O’Reilly DR (2002) Characterization of a novel silkworm (Bombyx mori) phenol UDP-glucosyltransferase. Eur J Biochem 269:819–825

    Article  CAS  PubMed  Google Scholar 

  113. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 1960:421–425

    Article  Google Scholar 

  114. Gripenberg S, Roslin T (2007) Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos 116:181–188

    Article  Google Scholar 

  115. Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92

    Article  CAS  PubMed  Google Scholar 

  116. Swain T (1977) Secondary compounds as protective agents. Ann Rev Plant Phys 28:479–501

    Article  CAS  Google Scholar 

  117. van Veen FJF (2015) Plant-modified trophic interactions. Curr Opin Insect Sci 8:29–33

    Article  PubMed  Google Scholar 

  118. Marsh NA, Clarke CA, Rothschild M, Kellett DN (1977) Hypolimnas bolina (L.), a mimic of danaid butterflies, and its model Euploea core (cram.) store cardioactive substances. Nature 268:726–728

    Article  CAS  PubMed  Google Scholar 

  119. Abe F, Yamauchi T, Minato K (1996) Presence of cardenolides and ursolic acid from oleander leaves in larvae and frass of Daphnis nerii. Phytochemistry 42:45–49

    Article  CAS  Google Scholar 

  120. Petschenka G, Dobler S (2009) Target-site sensitivity in a specialized herbivore towards major toxic compounds of its host plant: the Na+K+-ATPase of the oleander hawk moth (Daphnis nerii) is highly susceptible to cardenolides. Chemoecology 19:235–239

    Article  CAS  Google Scholar 

  121. Bramer C, Dobler S, Deckert J, Stemmer M, Petschenka G (2015) Na/K ATPase resistance and cardenolide sequestration: basal adaptations to host plant toxins in the milkweed bugs (Hemiptera: Lygaeidae: Lygaeinae). Proc Biol Sci 282:1805

    Article  CAS  Google Scholar 

  122. Aardema ML, Zhen Y, Andolfatto P (2012) The evolution of cardenolide-resistant forms of Na+, K+-ATPase in Danainae butterflies. Mol Ecol 21:340–349

    Article  CAS  PubMed  Google Scholar 

  123. Holzinger F, Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+, K+-ATPase. J Chem Ecol 22:1921–1937

    Article  CAS  PubMed  Google Scholar 

  124. Dobler S, Petschenka G, Wagschal V, Flacht L (2015) Convergent adaptive evolution — how insects master the challenge of cardiac glycoside-containing host plants. Entomol Exp Appl 157:30–39

    Article  CAS  Google Scholar 

  125. Groeneveld HW, Steijl H, Berg B, Elings JC (1990) Rapid, quantitative HPLC analysis of Asclepias fruticosa L. and Danaus plexippus L. cardenolides. J Chem Ecol 16:3373–3382

    Article  CAS  PubMed  Google Scholar 

  126. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Ann Rev Plant Biol 57:303–333

    Article  CAS  Google Scholar 

  127. Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, Gershenzon J, Vogel H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101:4859–4864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci U S A 99:11223–11228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Opitz SE, Jensen SR, Müller C (2010) Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defense against ants. J Chem Ecol 36:148–157

    Article  CAS  PubMed  Google Scholar 

  130. Müller C, Boevé JL, Brakefield PM (2002) Host plant derived feeding deterrence towards ants in the turnip sawfly Athalia rosae. Entomol Exp Appl 104:153–157

    Article  Google Scholar 

  131. Müller C, Brakefield PM (2003) Analysis of a chemical defense in sawfly larvae: easy bleeding targets predatory wasps in late summer. J Chem Ecol 29:2683–2694

    Article  PubMed  Google Scholar 

  132. Kos M, Kabouw P, Noordam R, Hendriks K, Vet LEM, Loon JJA, Dicke M (2011) Prey-mediated effects of glucosinolates on aphid predators. Ecol Entomol 36:377–388

    Article  Google Scholar 

  133. Abdalsamee MK, Müller C (2012) Effects of indole glucosinolates on performance and sequestration by the sawfly Athalia rosae and consequences of feeding on the plant defense system. J Chem Ecol 38:1366–1375

    Article  CAS  PubMed  Google Scholar 

  134. Discher S, Burse A, Tolzin-Banasch K, Heinemann SH, Pasteels JM, Boland W (2009) A versatile transport network for sequestering and excreting plant glycosides in leaf beetles provides an evolutionary flexible defense strategy. Chembiochem 10:2223–2229

    Article  CAS  PubMed  Google Scholar 

  135. Vetter J (2000) Plant cyanogenic glycosides. Toxicon 38:11–36

    Article  CAS  PubMed  Google Scholar 

  136. Zagrobelny M, Bak S, Rasmussen AV, Jørgensen B, Naumann CM, Møller BL (2004) Cyanogenic glucosides and plant– insect interactions. Phytochemistry 65:293–306

    Article  CAS  PubMed  Google Scholar 

  137. Pentzold S, Zagrobelny M, Roelsgaard PS, Møller BL, Bak S (2014) The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS One 9:e91337

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Glauser G, Marti G, Villard N, Doyen GA, Wolfender J, Turlings TCJ, Erb M (2011) Induction and detoxification of maize 1,4- benzoxazin-3-ones by insect herbivores. Plant J 68:901–911

    Article  CAS  PubMed  Google Scholar 

  139. Wouters FC, Reichelt M, Glauser G, Bauer E, Erb M, Gershenzon J, Vassaão DG (2014) Reglucosylation of the benzoxazinoid DIMBOA with inversion of stereochemical configuration is a detoxification strategy in lepidopteran herbivores. Angew Chem 126:11502–11506

    Article  Google Scholar 

  140. Strauss AS, Peters S, Boland W, Burse A (2013) ABC transporter functions as a pacemaker for sequestration of plant glucosides in leaf beetles. elife 2:e01096

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Kumar P, Pandit SS, Steppuhn A, Baldwin IT (2014) Natural history driven, plant-mediated RNAi-based study reveals CYP6B46’s role in a nicotine-mediated antipredator herbivore defense. Proc Natl Acad Sci U S A 111:1245–1252

    Article  CAS  PubMed  Google Scholar 

  142. Morris CE (1983) Uptake and metabolism of nicotine by the CNS of a nicotine-resistant insect, the tobacco hornworm (Manduca sexta). J Insect Physiol 29:807–817

    Article  CAS  Google Scholar 

  143. Kojima W, Fujii T, Suwa M, Miyazawa M, Ishikawa Y (2010) Physiological adaptation of the asian corn borer Ostrinia furnacalis to chemical defenses of its host plant, maize. J Insect Physiol 56:1349–1355.

    Article  CAS  PubMed  Google Scholar 

  144. Sasai H, Ishida M, Murakami K, Tadokoro N, Ishihara A, Nishida R, Mori N (2009) Species-specific glucosylation of DIMBOA in larvae of the rice armyworm. Biosci Biotechnol Biochem 73:1333–1338

    Article  CAS  PubMed  Google Scholar 

  145. Loayza-Muro R, Figueroa CC, Niemeyer HM (2000) Effect of two wheat cultivars differing in hydroxamic acid concentration on detoxification metabolism in the aphid Sitobion avenae. J Chem Ecol 26:2725–2736

    Article  CAS  Google Scholar 

  146. Miller NJ, Zhao Z (2015) Transcriptional responses of Diabrotica virgifera virgifera larvae to benzoxazinoids. J Appl Entomol 139:416–423

    Article  CAS  Google Scholar 

  147. Campos F, Atkinson J, Arnason JT, Philogéne BJR, Morand P, Werstiuk NH, Timmins G (1989) Toxicokinetics of 2,4- dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) in the European corn borer, Ostrinia nubilalis (Hubner). J Chem Ecol 15:1989–2001

    Article  CAS  PubMed  Google Scholar 

  148. Eswaran SV, Jindal A (2013) Grasshoppers — generalists to specialists? Resonance 18:810–816

    Article  Google Scholar 

  149. Martin JS, Martin MM, Bernays EA (1987) Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J Chem Ecol 13:605–621

    Article  CAS  PubMed  Google Scholar 

  150. Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552

    Article  CAS  PubMed  Google Scholar 

  151. Barbehenn RV (2003) Antioxidants in grasshoppers: higher levels defend the midgut tissues of a polyphagous species than a graminivorous species. J Chem Ecol 29:683–702

    Article  CAS  PubMed  Google Scholar 

  152. Krishnan N, Sehnal F (2006) Compartmentalization of oxidative stress and antioxidant defense in the larval gut of Spodoptera littoralis. Arch Insect Biochem Physiol 63:1–10

    Article  CAS  PubMed  Google Scholar 

  153. Henn M (1999) The changes of polyphenols as a result of the passage through the gut of the gypsy moth Lymantria dispar (Lep., Lymantriidae): influence on the growth of the larvae. J App Entomol 123:391–395

    Article  CAS  Google Scholar 

  154. Kopper BJ, Jakobi VN, Osier TL, Lindroth RL (2002) Effects of paper birch condensed tannin on white marked tussock moth (Lepidoptera: Lymantriidae) performance. Env Entomol 31:10–14

    Article  CAS  Google Scholar 

  155. Bernays EA, Chamberlain DJ (1980) A study of tolerance of ingested tannin in Schistocerca gregaria. J Insect Physiol 26:415–420

    Article  CAS  Google Scholar 

  156. Peñaflor MF, Erb M, Robert CA, Miranda LA, Werneburg AG, Dossi FC, Turlings TC, Bento JM (2011) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–215

    Article  PubMed  CAS  Google Scholar 

  157. Xiao Y, Wang Q, Erb M, Turlings TC, Ge L, Hu L, Li J, Han X, Zhang T, Lu J, Zhang G, Lou Y (2012) Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett 15:1130–1139

    Article  CAS  PubMed  Google Scholar 

  158. Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, Gershenzon J, Vogel H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101:4859–4864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Engler HS, Spencer KC, Gilbert LE (2000) Preventing cyanide release from leaves. Nature 406:144–145

    Article  CAS  PubMed  Google Scholar 

  160. Seigler DS (1998) Plant secondary metabolism. Chapman & Hall, London

    Book  Google Scholar 

  161. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  162. Agrawal AA, Gorski PM, Tallamy DW (1999) Polymorphism in plant defense against herbivory: constitutive and induced resistance in Cucumis sativus. J Chem Ecol 25:2285–2304

    Article  CAS  Google Scholar 

  163. Siemens DH, Keck AG, Ziegenbein S (2010) Optimal defense in plants: assessment of resource allocation costs. Evol Ecol 24:1291–1305

    Article  Google Scholar 

  164. Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605

    Article  CAS  PubMed  Google Scholar 

  165. Agrawal AA, Karban R (1999) Why induced defenses may be favored over constitutive strategies in plants. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 45–61

    Google Scholar 

  166. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307

    Article  PubMed  Google Scholar 

  167. Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction–immunity trade-offs in insects. Annu Rev Entomol 61:239–256

    Article  CAS  PubMed  Google Scholar 

  168. Forister ML, Dyer LA, Singer MS, Stireman JO, Lill JT (2012) Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions. Ecology 93:981–991

    Article  CAS  PubMed  Google Scholar 

  169. Brower LP, Moffitt CM (1974) Palatability dynamics of cardenolides in the monarch butterfly. Nature 249:280–283

    Article  CAS  PubMed  Google Scholar 

  170. Paradise CJ, Stamp NE (1991) Prey recognition time of praying mantids (Dictyoptera: Mantidae) and consequent survivorship of unpalatable prey (Hemiptera: Lygaeidae). J Insect Behav 4:265–273

    Article  Google Scholar 

  171. Petschenka G, Bramer C, Pankoke H, Dobler S (2011) Evidence for a deterrent effect of cardenolides on Nephila spiders. Basic App Ecol 12:260–267

    Article  CAS  Google Scholar 

  172. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398

    Article  PubMed  Google Scholar 

  173. Colvin SM, Yeargan KV (2013) Effects of milkweed host species on interactions between Aphis nerii (Hemiptera: Aphididae) and its parasitoids. J Kansas Entomol Soc 86:193–205

    Article  Google Scholar 

  174. War AR, Sharma HC (2014) Induced resistance in plants and counter- adaptation by insect pests. In: Chandrasekar R, Tyagi BK, Gui ZZ, Reeck GR (eds) Short views insect biochemistry and molecular biology. International Book Mission, Manhattan, Kansas State, USA, pp 533–547

    Google Scholar 

Download references

Acknowledgment

Funding for this review was provided by the Australian Centre for International Agricultural Research (ACIAR) through the project on International Mungbean Improvement Network (CIM-2014-079) and strategic long-term donors to the World Vegetable Center: Republic of China (Taiwan), UK aid from the UK government, United States Agency for International Development (USAID), Germany, Thailand, Philippines, Korea, and Japan. Thanks are also due to Dr. Paola Sotelo-Cardona (Scientist-Entomology), World Vegetable Center, Taiwan, for her critical review on the manuscript.

Author information

Authors and Affiliations

  1. World Vegetable Center, South Asia, Hyderabad, Telangana, India

    Abdul Rasheed War & Ramakrishnan M. Nair

  2. Entomology Division, Department of Zoology, University of Kashmir, Srinagar, Jammu and Kashmir, India

    Abdul Ahad Buhroo & Tariq Ahmad

  3. Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Srinagar, India

    Barkat Hussain

  4. Division of Entomology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Medak, Telangana, India

    Hari C. Sharma

Authors
  1. Abdul Rasheed War
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdul Ahad Buhroo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barkat Hussain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tariq Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ramakrishnan M. Nair
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hari C. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdul Rasheed War .

Editor information

Editors and Affiliations

  1. Faculty of Pharmaceutical Sciences, Institute of Vine and Wine Sciences, University of Bordeaux, Villenave d'Ornon, France

    Jean-Michel Mérillon

  2. Department of Botany, University College of Science, M. L. Sukhadia University, Udaipur, Rajasthan, India

    Kishan Gopal Ramawat

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

War, A.R., Buhroo, A.A., Hussain, B., Ahmad, T., Nair, R.M., Sharma, H.C. (2020). Plant Defense and Insect Adaptation with Reference to Secondary Metabolites. In: Mérillon, JM., Ramawat, K. (eds) Co-Evolution of Secondary Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-96397-6_60

Download citation

Publish with us

Policies and ethics

Search

Navigation