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

  • Plant-Animal interactions - Original Paper
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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 (Populus tremula × 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.

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References

  • 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 30:1363–1379

    Article  CAS  PubMed  Google Scholar 

  • 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 47:349–357

    Article  CAS  PubMed  Google Scholar 

  • Barbehenn RV, Karowe DN, Spickard A (2004) Effects of elevated atmospheric CO2 on the nutritional ecology of C3 and C4 grass-feeding caterpillars. Oecologia 140:86–95

    Article  PubMed  Google Scholar 

  • 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 31:969–988

    Article  CAS  PubMed  Google Scholar 

  • Barbehenn RV, Jones CP, Karonen M, Salminen J-P (2006a) Tannin composition affects the oxidative activities of tree leaves. J Chem Ecol 32:2235–2251

    Article  CAS  PubMed  Google Scholar 

  • 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 32:2253–2267

    Article  CAS  PubMed  Google Scholar 

  • 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 154:129–140

    Article  PubMed  Google Scholar 

  • 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 55:297–304

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1511–1530

    Article  CAS  Google Scholar 

  • Bi JL, Murphy JB, Felton GW (1997) Antinutritive and oxidative components as mechanisms of induced resistance in cotton. J Chem Ecol 23:97–117

    Article  CAS  Google Scholar 

  • Brodeur-Campbell S, Vucetich JA, Richter DA, Waite TA, Rosemier JN, Tsai C-J (2006) Insect herbivory on low-lignin transgenic aspen. Environ Entomol 35:1696–1701

    Article  CAS  Google Scholar 

  • Cheeseman JM (2009) Seasonal patterns of leaf H2O2 content: reflections of leaf phenology, or environmental stress? Funct Plant Biol 36:721–731

    Article  CAS  Google Scholar 

  • 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 23:2357–2370

    Article  CAS  Google Scholar 

  • 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 54:712–720

    Article  CAS  PubMed  Google Scholar 

  • 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 6:241–249

    Article  CAS  PubMed  Google Scholar 

  • Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32:3–37

    Article  CAS  Google Scholar 

  • Felton GW (1996) Nutritive quality of plant protein: sources of variation and insect herbivore responses. Arch Insect Biochem Physiol 32:107–130

    Article  CAS  Google Scholar 

  • 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 38:277–285

    Article  CAS  Google Scholar 

  • 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 65:157–173

    Article  CAS  PubMed  Google Scholar 

  • Hagerman AE, Dean RT, Davies MJ (2003) Radical chemistry of epigallocatechin gallate and its relevance to protein damage. Arch Biochem Biophys 414:115–120

    Article  CAS  PubMed  Google Scholar 

  • 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 125:683–700

    Article  CAS  PubMed  Google Scholar 

  • Horton RA, Redak DR (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263–275

    Article  Google Scholar 

  • 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 31:995–1002

    Article  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • 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 522:105–112

    Article  CAS  Google Scholar 

  • 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 78:49–53

    Article  CAS  Google Scholar 

  • 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 132:1177–1185

    Article  CAS  PubMed  Google Scholar 

  • Lagrimini LM (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583

    Article  CAS  PubMed  Google Scholar 

  • 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 140:1022–1035

    Article  CAS  PubMed  Google Scholar 

  • Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory. Comparison of wound- and insect elicitor-induced gene expression. New Phytol 172:617–635

    Article  CAS  PubMed  Google Scholar 

  • 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 62:517–522

    Article  CAS  PubMed  Google Scholar 

  • 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 150:924–941

    Article  CAS  PubMed  Google Scholar 

  • 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 21:341–354

    Article  CAS  PubMed  Google Scholar 

  • 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 12:203–211

    Google Scholar 

  • 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 17:549–554

    Article  Google Scholar 

  • 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 96:6553–6557

    Article  Google Scholar 

  • 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 25:197–207

    Article  Google Scholar 

  • 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 15:1275–1297

    Article  PubMed  Google Scholar 

  • Robison DJ, Raffa KF (1997) Effects of constitutive and inducible traits of hybrid poplars on forest tent caterpillar feeding and population ecology. For Sci 43:252–267

    Google Scholar 

  • Rossiter M, Schultz JC, Baldwin IT (1988) Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277

    Article  CAS  Google Scholar 

  • 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 154:725–730

    Article  PubMed  Google Scholar 

  • SAS Institute (2003) The SAS system for Windows. Version 9.1. SAS Institute, Cary

    Google Scholar 

  • 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 723:81–94

    Article  CAS  Google Scholar 

  • Stout MJ, Workman KV, Duffey SS (1996) Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomol Exp Appl 79:255–271

    Article  Google Scholar 

  • Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3:207–219

    Article  CAS  Google Scholar 

  • 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 22:1767–1781

    Article  CAS  Google Scholar 

  • 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 120:481–487

    CAS  Google Scholar 

  • Tscharntke T, Boland W, Dolch R, Thiessen S (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Systemat Ecol 29:1025–1047

    Article  CAS  Google Scholar 

  • Wang J, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria) herbivory. Planta 220:87–96

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson L (2000) SYSTAT: the system for statistics. SYSTAT, Evanston

    Google Scholar 

  • Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2004-35302-14840 to R. V. B. and C. P. C. and 2007-35302-17803 to R. V. B. and J. P. S. We thank Akiyoshi Kawaoka for generously providing the PrxC1a construct, John Tanner for providing L. dispar eggs, Brad Binges for greenhouse help, and Michael M. Martin for outstanding suggestions for revising the manuscript.

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Authors and Affiliations

  1. Departments of Molecular, Cellular and Developmental Biology and Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109-1048, USA

    Raymond Barbehenn, Chris Dukatz, Chris Holt & Austin Reese

  2. Laboratory of Organic Chemistry and Chemical Biology, Department of Chemistry, University of Turku, 20014, Turku, Finland

    Olli Martiskainen & Juha-Pekka Salminen

  3. Centre for Forest Biology and Department of Biology, University of Victoria, P.O. Box 3020, Stn CSC, Victoria, BC, V8W 3N5, Canada

    Lynn Yip, Lan Tran & C. Peter Constabel

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  1. Raymond Barbehenn
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Correspondence to Raymond Barbehenn.

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Communicated by Richard Karban.

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Barbehenn, R., Dukatz, C., Holt, C. et al. Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164, 993–1004 (2010). https://doi.org/10.1007/s00442-010-1733-y

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