Oecologia

, Volume 164, Issue 4, pp 993–1004 | Cite as

Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance

  • Raymond Barbehenn
  • Chris Dukatz
  • Chris Holt
  • Austin Reese
  • Olli Martiskainen
  • Juha-Pekka Salminen
  • Lynn Yip
  • Lan Tran
  • C. Peter Constabel
Plant-Animal interactions - Original Paper

Abstract

Peroxidases (PODs) are believed to act as induced and constitutive defenses in plants against leaf-feeding insects. However, little work has examined the mode of action of PODs against insects. Putative mechanisms include the production of potentially antinutritive and/or toxic semiquinone free radicals and quinones (from the oxidation of phenolics), as well as increased leaf toughness. In this study, transgenic hybrid poplar saplings (Populustremula × Populus alba) overexpressing horseradish peroxidase (HRP) were produced to examine the impact of elevated HRP levels on the performance and gut biochemistry of Lymantria dispar caterpillars. HRP-overexpressing poplars were more resistant to L. dispar than wild-type (WT) poplars when the level of a phenolic substrate of HRP (chlorogenic acid) was increased, but only when leaves had prior feeding damage. Damaged (induced) leaves produced increased amounts of hydrogen peroxide, which was used by HRP to increase the production of semiquinone radicals in the midguts of larvae. The decreased growth rates of larvae that fed on induced HRP-overexpressing poplars resulted from post-ingestive mechanisms, consistent with the action of HRP in their midguts. The toughness of HRP-overexpressing leaves was not significantly greater than that of WT leaves, whether or not they were induced. When leaves were coated with ellagitannins, induced HRP leaves also produced elevated levels of semiquinone radicals in the midgut. Decreased larval performance on induced HRP leaves in this case was due to post-ingestive mechanisms as well as decreased consumption. The results of this study provide the first demonstration that a POD is able to oxidize phenolics within an insect herbivore’s gut, and further clarifies the chemical conditions that must be present for PODs to function as antiherbivore defenses.

Keywords

Herbivore Plant defense 

References

  1. Allison SD, Schultz JC (2004) Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.). J Chem Ecol 30:1363–1379CrossRefPubMedGoogle Scholar
  2. Barbehenn RV, Bumgarner SL, Roosen E, Martin MM (2001) Antioxidant defenses in caterpillars: role of the ascorbate recycling system in the midgut lumen. J Insect Physiol 47:349–357CrossRefPubMedGoogle Scholar
  3. Barbehenn RV, Karowe DN, Spickard A (2004) Effects of elevated atmospheric CO2 on the nutritional ecology of C3 and C4 grass-feeding caterpillars. Oecologia 140:86–95CrossRefPubMedGoogle Scholar
  4. Barbehenn RV, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midguts of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988CrossRefPubMedGoogle Scholar
  5. Barbehenn RV, Jones CP, Karonen M, Salminen J-P (2006a) Tannin composition affects the oxidative activities of tree leaves. J Chem Ecol 32:2235–2251CrossRefPubMedGoogle Scholar
  6. Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen J-P (2006b) Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. J Chem Ecol 32:2253–2267CrossRefPubMedGoogle Scholar
  7. Barbehenn RV, Jones CP, Yip L, Tran L, Constabel CP (2007) Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar. Oecologia 154:129–140CrossRefPubMedGoogle Scholar
  8. Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen J-P (2009) Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Physiol 55:297–304CrossRefPubMedGoogle Scholar
  9. Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530CrossRefGoogle Scholar
  10. Bi JL, Murphy JB, Felton GW (1997) Antinutritive and oxidative components as mechanisms of induced resistance in cotton. J Chem Ecol 23:97–117CrossRefGoogle Scholar
  11. Brodeur-Campbell S, Vucetich JA, Richter DA, Waite TA, Rosemier JN, Tsai C-J (2006) Insect herbivory on low-lignin transgenic aspen. Environ Entomol 35:1696–1701CrossRefGoogle Scholar
  12. Cheeseman JM (2009) Seasonal patterns of leaf H2O2 content: reflections of leaf phenology, or environmental stress? Funct Plant Biol 36:721–731CrossRefGoogle Scholar
  13. Dowd PF, Lagrimini LM (1997) Examination of different tobacco (Nicotiana spp.) types under- and overproducing tobacco anionic peroxidase for their leaf resistance to Helicoverpa zea. J Chem Ecol 23:2357–2370CrossRefGoogle Scholar
  14. Dowd PF, Lagrimini LM, Herms DA (1998a) Differential leaf resistance to insects of transgenic sweetgum (Liquidambar styraciflua) expressing tobacco anionic peroxidase. Cell Mol Life Sci 54:712–720CrossRefPubMedGoogle Scholar
  15. Dowd PF, Lagrimini LM, Nelsen TC (1998b) Relative resistance of transgenic tomato tissues expressing high levels of tobacco anionic peroxidase to different insect species. Nat Toxins 6:241–249CrossRefPubMedGoogle Scholar
  16. Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32:3–37CrossRefGoogle Scholar
  17. Felton GW (1996) Nutritive quality of plant protein: sources of variation and insect herbivore responses. Arch Insect Biochem Physiol 32:107–130CrossRefGoogle Scholar
  18. Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore. J Insect Physiol 38:277–285CrossRefGoogle Scholar
  19. Gant TW, Ramakrishna R, Mason RP, Cohen GM (1988) Redox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes. Chem Biol Interact 65:157–173CrossRefPubMedGoogle Scholar
  20. Hagerman AE, Dean RT, Davies MJ (2003) Radical chemistry of epigallocatechin gallate and its relevance to protein damage. Arch Biochem Biophys 414:115–120CrossRefPubMedGoogle Scholar
  21. Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700CrossRefPubMedGoogle Scholar
  22. Horton RA, Redak DR (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263–275CrossRefGoogle Scholar
  23. Hu Z-H, Shen Y-B, Shen F-Y, Su X-H (2009) Effects of feeding Clostera anachoreta on hydrogen peroxide accumulation and activities of peroxidase, catalase, and ascorbate peroxidase in Populus simonii x P. pyramidalis ‘Opera 8277’ leaves. Acta Physiol Plant 31:995–1002CrossRefGoogle Scholar
  24. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoGoogle Scholar
  25. Karonen M, Loponen J, Ossipov V, Pihlaja K (2004) Analysis of procyanidins in pine bark with reversed-phase and normal-phase high-performance liquid chromatography–electrospray ionization mass spectrometry. Anal Chim Acta 522:105–112CrossRefGoogle Scholar
  26. Kawaoka A, Kawamoto T, Moriki H, Murakami A, Murakami K, Yoshida K, Sekine M, Takano M, Shinmyo A (1994) Growth-stimulation of tobacco plant introduced the horseradish-peroxidase gene Prxc1a. J Ferment Bioeng 78:49–53CrossRefGoogle Scholar
  27. Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol 132:1177–1185CrossRefPubMedGoogle Scholar
  28. Lagrimini LM (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583CrossRefPubMedGoogle Scholar
  29. Maffei ME, Mithofer A, Arimura G-I, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022–1035CrossRefPubMedGoogle Scholar
  30. Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory. Comparison of wound- and insect elicitor-induced gene expression. New Phytol 172:617–635CrossRefPubMedGoogle Scholar
  31. Matsui T, Nakayama H, Yoshida K, Shinmyo A (2003) Vesicular transport route of horseradish C1a peroxidase is regulated by N- and C-terminal propeptides in tobacco cells. Appl Microbiol Biotechnol 62:517–522CrossRefPubMedGoogle Scholar
  32. Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941CrossRefPubMedGoogle Scholar
  33. Mohan R, Bajar AM, Kolattukudy PE (1993) Induction of tomato anionic peroxidase gene (tap1) by wounding in transgenic tobacco and activation of tap1/GUS and tap2/GUS chimeric gene fusions in transgenic tobacco by wounding and pathogen attack. Plant Mol Biol 21:341–354CrossRefPubMedGoogle Scholar
  34. Moilanen J, Salminen J-P (2008) Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 12:203–211Google Scholar
  35. Moore JP, Paul ND, Whittaker JB, Taylor JE (2003) Exogenous jasmonic acid mimics herbivore-induced sytemic increase in cell wall bound peroxidase activity and reduction in leaf expansion. Funct Ecol 17:549–554CrossRefGoogle Scholar
  36. Orozco-Cardena M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Nat Acad Sci USA 96:6553–6557CrossRefGoogle Scholar
  37. Osier TL, Hwang S-Y, Lindroth RL (2000) Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol Entomol 25:197–207CrossRefGoogle Scholar
  38. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N et al (2006) Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–1297CrossRefPubMedGoogle Scholar
  39. Robison DJ, Raffa KF (1997) Effects of constitutive and inducible traits of hybrid poplars on forest tent caterpillar feeding and population ecology. For Sci 43:252–267Google Scholar
  40. Rossiter M, Schultz JC, Baldwin IT (1988) Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277CrossRefGoogle Scholar
  41. Ruuhola T, Yang S, Ossipov V, Haukioja E (2008) Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Eppirita autumnata. Oecologia 154:725–730CrossRefPubMedGoogle Scholar
  42. SAS Institute (2003) The SAS system for Windows. Version 9.1. SAS Institute, CaryGoogle Scholar
  43. Shingfield KJ, Offer NW (1999) Simultaneous determination of purine metabolites, creatine and pseudouridine in ruminant urine by reversed-phase high performance liquid chromatography. J Chrom B 723:81–94CrossRefGoogle Scholar
  44. Stout MJ, Workman KV, Duffey SS (1996) Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomol Exp Appl 79:255–271CrossRefGoogle Scholar
  45. Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3:207–219CrossRefGoogle Scholar
  46. Thaler J, Stout MJ, Karban R, Duffey S (1996) Exogenous jasmonate simulates insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and the field. J Chem Ecol 22:1767–1781CrossRefGoogle Scholar
  47. Thiboldeaux RL, Lindroth RL, Tracy JW (1998) Effects of juglone (5-hydroxy-1, 4-naphthoquinone) on midgut morphology and glutathione status in saturniid moth larvae. Comp Biochem Physiol 120:481–487Google Scholar
  48. Tscharntke T, Boland W, Dolch R, Thiessen S (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Systemat Ecol 29:1025–1047CrossRefGoogle Scholar
  49. Wang J, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria) herbivory. Planta 220:87–96CrossRefPubMedGoogle Scholar
  50. Wilkinson L (2000) SYSTAT: the system for statistics. SYSTAT, EvanstonGoogle Scholar
  51. Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Raymond Barbehenn
    • 1
  • Chris Dukatz
    • 1
  • Chris Holt
    • 1
  • Austin Reese
    • 1
  • Olli Martiskainen
    • 2
  • Juha-Pekka Salminen
    • 2
  • Lynn Yip
    • 3
  • Lan Tran
    • 3
  • C. Peter Constabel
    • 3
  1. 1.Departments of Molecular, Cellular and Developmental Biology and Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Laboratory of Organic Chemistry and Chemical Biology, Department of ChemistryUniversity of TurkuTurkuFinland
  3. 3.Centre for Forest Biology and Department of BiologyUniversity of VictoriaVictoriaCanada

Personalised recommendations