Abstract
Induced resistance of the mountain birch against its main defoliator Epirrita autumnata is a well-characterized phenomenon. The causal mechanism for this induced deterioration, however, has not been unequivocally explained, and no individual compound or group of traditional defensive compounds has been shown to explain the phenomenon. Phenolic compounds are the main secondary metabolites in mountain birch leaves, and the biological activity of phenolics usually depends on their oxidation. In this study, we found that the activity of polyphenoloxidases (PPOs), enzymes that oxidize o-diphenols to o-diquinones, was induced in trees with introduced larvae, and bioassays showed that both growth and consumption rates of larvae were reduced in damaged trees. PPO activity was negatively associated with both larval growth and consumption rates in trees with bagged larvae, but not in control trees. Our results suggest that the oxidation of phenolics by PPOs may be a causal explanation for the rapidly induced resistance of mountain birch against E. autumnata. This finding also helps to explain why correlations between insect performance and phenolics (without measuring indices explaining their oxidation) may not produce consistent results.
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References
Appel H (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552
Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen J-P (2006) Ellagitannins have greater oxidative activities than condensed tannins and galloylglucoses at high pH: potential impact on caterpillars. J Chem Ecol 32:2253–2267
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
Bi JL, Murphy JB, Felton GW (1997a) Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J Chem Ecol 23:97–117
Bi JL, Felton GW, Murphy JB, Howles PA, Dixon RA, Lamb CJ (1997b) Do plant phenolics confer resistance to specialist and generalist insect herbivore? J Agric Food Chem 45:4500–4504
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle protein–dye binding. Anal Biochem 72:248–254
Bryant JB, Chapin III FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368
Constabel CP (1999) A survey of herbivore-inducible defense proteins and phytochemicals, In: Agrawal AA, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores. Biochemistry, ecology and agriculture. APS, St Paul, Minn., pp 137–166
Constabel CP, Yip C, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295
Dietrich R, Ploss K, Heil M (2004) Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant Cell Environ 27:896–906
Edwards PJ, Wratten SD (1982) Wound-induced changes in palatability in birch (Betula pubescens Ehr. ssp. pubescens). Am Nat 120:816–818
Feeny P (1968) Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. J Insect Physiol 14:805–817
Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581
Felton GW, Duffey SS (1991) Protective action of midgut catalase in lepidopteran larvae against oxidative plant defenses. J Chem Ecol 17:1715–1732
Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694
Hanhimäki S, Senn J (1992) Sources of variation in rapidly inducible responses to leaf damage in the mountain birch–insect herbivore system. Oecologia 91:318–331
Haukioja E (1982) Inducible defences of white birch to a geometrid defoliator, Epirrita autumnata. In: Visser JH, Minks AK (eds) Proceedings of the 5th International Symposium on Insect–Plant Relationships. Pudoc, Wageningen, pp 199–203
Haukioja E (2005) Plant defenses and population fluctuations of forest defoliators: mechanisms-based scenarios. Ann Zool Fenn 42:313–325
Haukioja E, Hanhimäki S (1985) Rapid wound-induced resistance in white birch (Betula pubescens) foliage to the geometrid Epirrita autumnata: a comparison of trees and moths within and outside the outbreak range of the moth. Oecologia 65:223–228
Haukioja E, Neuvonen S (1985) Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303–1308
Haukioja E, Suomela J, Neuvonen S (1985) Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator. Oecologia 65:363–369
Haruta M, Pedersen JA, Constabel CP (2001) Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol Plant 112:552–558
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Hoover K, Kishida KT, Digiorgio LA, Workman J, Alaniz SA, Hammock BD, Duffey SS (1998) Inhibition of baculovirus disease by plant-mediated peroxidase activity and free radical generation. J Chem Ecol 24:1949–2001
Kaitaniemi P, Ruohomäki K (2001) Sources of variability in plant resistance against insects: free caterpillars show strongest effects. Oikos 95:461–470
Kaitaniemi P, Neuvonen S, Nyyssönen T (1999) Effects of cumulative defoliations on the growth, reproduction and insect resistance in mountain birch. Ecology 80:524–532
Kallio P, Lehtonen J (1973) Birch forest damage caused by Oporinia autumnata (Bkh.) (Lep., Geometridae) in 1965–66 in Utsjoki, N. Finland. Rep Kevo Subarct Res Stn 10:55–69
Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Defoliating insect immune defense interacts with induced plant defense during a population cycle. Ecology 87:291–296
Kranthi S, Kranthi KR, Wanjari RR (2003) Influence of semilooper damage on cotton host-plant resistance to Helicoverpa armigera (Hub). Plant Sci 164:157–163
Loomis WE (1932) Growth-differentiation balance vs. carbohydrate–nitrogen ratio. Proc Am Soc Hortic Sci 29:240–245
Myers JH (1998) Synchrony in outbreaks of forest Lepidoptera: a possible example of the Moran effect. Ecology 79:1111–1117
Niemelä P (1980) Dependence of Oporinia autumnata (Lep., Geometridae) outbreaks on summer temperature. Rep Kevo Subarct Res Stn 16:27–30
Nurmi K, Ossipov V, Haukioja E, Pihlaja K (1996) Variation of total phenolic content and individual low-molecular-weight phenolics in foliage of mountain birch trees (Betula pubescens ssp. tortuosa). J Chem Ecol 22:2023–2040
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251
Ruohomäki K, Hanhimäki S, Haukioja E, Iso-Iivari L, Niemelä P, Suomela J (1992) Variability in the efficacy of delayed inducible resistance in mountain birch. Entomol Exp Appl 62:107–115
Ruohomäki K, Chapin III FS, Haukioja E, Neuvonen S, Suomela J (1996) Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 27:2302–2311
Ruohomäki K, Tanhuanpää M, Ayres MP, Kaitaniemi P, Tammaru T, Haukioja E (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Popul Ecol 42:211–223
Ruuhola T, Yang S (2006) Wound-induced oxidative responses in mountain birch leaves. Ann Bot 97:29–37
Ruuhola T, Salminen J-P, Haviola S, Yang S, Rantala MJ (2007) Immunological memory of mountain birches: the effects of phenolics on the performance of the autumnal moth depend on the herbivory history of trees. J Chem Ecol (in press)
Salminen J-P, Ossipov V, Loponen J, Haukioja E, Pihlaja K (1999) Characterisation of hydrolysable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry. J Chromatogr 864:283–291
Sánchez M, Queijeiro E, Revilla G, Zarra I (1997) Changes in ascorbic acid levels in apoplastic fluid during the growth of pine hypocotyls. Effect on activities associated with cell walls. Physiol Plant 101:815–820
Stout MJ, Workman KV, Workman JS, Duffey SS (1996) Temporal and ontogenetic aspects of protein induction in foliage of the tomato, Lycopersicon esculetum. Biochem Syst Ecol 24:811–825
Tanhuanpää M, Ruohomäki K, Turchin P, Ayres MP, Bylund H, Kaitaniemi P, Tammaru T, Haukioja E (2002) Population cycles of the autumnal moth in Fennoscandia. In: Berryman AA (ed) Population cycles. The case for trophic interactions. Oxford University Press, New York, pp 142–154
Tenow O (1972) The outbreaks of Oporinia autumnata Bkh. and Operophtera spp. (Lep: Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1968. Zool Bridr Uppsala 2[Suppl]:1–107
Tenow O, Bylund H, Nilssen AC, Karlsson PS (2005) Long-term influence of herbivores on northern birch forest. In: Wiegolaski FE, Karlsson PS, Neuvonen S, Thannheiser D (eds) Plant ecology, herbivory, and human impact in nordic mountain birch forests. Springer, Berlin, pp 165–181
Thaler JS (2002) Effects of jasmonate-induced plant responses on the natural enemies of herbivores. J Anim Ecol 71:141–150
Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324
Thipyapong P, Hunt MD, Steffens JC (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220:105–117
Tscharntke T, Thiessen S, Dolch R, Doland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29:1025–1047
Vaarama A, Valanne T (1973) On the taxonomy, biology and origin of Betula tortuosa Ledeb. Rep Kevo Subarct Res Stn 10:70–84
Valanne N, Valanne T (1984) The development of the photosynthetic apparatus during the bud burst and leaf opening in two subspecies of Betula pubescens. Rep Kevo Subarct Res Stn 19:1–10
Wratten SD, Edwards PJ, Dunn I (1984) Wound-induced changes in the palatability of Betula pubescens and Betula pendula. Oecologia 61:372–375
Yang S, Ruuhola T, Haviola S, Rantala MJ (2007) Temperature as a modifier of plant–herbivore interaction. J Chem Ecol 33:463–475
Acknowledgements
We wish to express our great gratitude to the Departments of Plant Physiology, Molecular Biology and Animal Physiology, for providing the facilities for our enzymatic measurements. We also want to thank the staff of the Kevo Subarctic Research Station for their help with the study. Finally, we thank our field assistants: Pauliina Wäli, Tanja Kyykkä, Fia Haavisto, Jenny Koivisto and Rauno Varjonen. Ellen Valle kindly checked the English of the manuscript. The study was supported financially by the Academy of Finland (project nos. 29885301, 207294, 206144) and Emil Aaltonen Foundation. Our experiments comply with the current laws of Finland.
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Communicated by Julia Koricheva.
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Ruuhola, T., Yang, S., Ossipov, V. et al. Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata . Oecologia 154, 725–730 (2008). https://doi.org/10.1007/s00442-007-0869-x
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DOI: https://doi.org/10.1007/s00442-007-0869-x