Abstract
Plants have been suggested to have an immunological memory comparable to animals. The evidence for this, however, is scarce. In our study with the mountain birch—Epirrita autumnata system, we demonstrated that birches exposed as long as 5 yr to feeding of E. autumnata larvae (delayed induced resistance, DIR), responded more strongly to a new challenge than trees without an herbivory history. Pupal weights remained lower, and the duration of the larval period was prolonged in the DIR trees, although immunity, measured as an encapsulation rate, was not affected. We further demonstrated that the effects of birch phenolics on performance of E. autumnata were different in the exposed (DIR) trees from naive control trees, although we found only one significant change in chemistry. The quercetin:kaemferol ratio was increased in DIR trees, suggesting that herbivory caused oxidative stress in birches. In DIR trees, phenolics, especially hydrolyzable tannins (HTs), affected pupal weights negatively, whereas in control trees, the effects were either nonsignificant or positive. HTs also prolonged the duration of the larval period of females, whereas peroxidase (POD) activity prolonged that of males. We suggest that the causal explanation for the induced resistance was an enhanced oxidation of phenolic compounds from the DIR trees in the larval digestive tract. Phenolic oxidation produces semiquinones, quinones, free radicals, and ROS, which may have toxic, antinutritive, and/or repellent properties against herbivores.
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References
Appel, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19:1521–1552.
Baldwin, I., and Schmelz, E. A. 1996. Immunological “memory” in the induced accumulation of nicotine in wild tobacco. Ecology 77:236–246.
Barbehenn, R. V., Jones, C. P., Hagerman, A. E., Karonen, M., and 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, J. L., and Felton, G. W. 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.
Bradford, M. M. 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.
Chan, T., Galati, G., and O’Brien, P. J. 1999. Oxygen activation during peroxidase catalysed metabolism of flavones or flavanones. Chem. -Biol. Interact. 122:15–25.
Danell, K., Haukioja, E., and Huss-Danell, K. 1997. Morphological and chemical responses of mountain birch leaves and shoots to winter browsing along a gradient of plant productivity. Ecoscience 4:296–303.
Felton, G. W., and Duffey, S. S. 1991. Protective action of midgut catalase in Lepidopteran larvae against oxidative plant defenses. J. Chem. Ecol. 17:1715–1732.
Felton, G. W., Donato, K., Del Vecchio, R. J., and Duffey, S. S. 1989. Activation of foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667–2694.
Gatehouse, J. A. 2002. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 156:145–169.
Gorman, M. J., Cornel, A. J., Collins, F. H., and Paskewitz, S. M. 1996. A shared genetic mechanism for melanotic encapsulation of CM-sepharex beads and the malaria parasite, Plasmodium cynomolgi B, in the mosquito Anopheles gambiae. Exp. Parasitol. 84:380–386.
Haukioja, E. 1982. Inducible defenses of white birch to a geometrid defoliator, Epirrita autumnata. pp. 199–203, in J. H. Visser and A. K. Minks (eds.). Proceedings of 5th International Symposium on Insect–Plant Relationship. Pudoc, Wageningen.
Haukioja, E. 2005. Plant defenses and population fluctuations of forest defoliators: mechanisms-based scenarios. Ann. Zool. Fenn. 42:313–325.
Haukioja, E. and Neuvonen, S. 1985. Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303–1308.
Haukioja, E., Suomela, J., and Nevonen, S. 1985. Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator. Oecologia 65:363–369.
Haukioja, E., Neuvonen, S., Hanhimäki, S., and Niemelä, P. 1988. The autumnal moth in Fennoscandia. pp. 163–178, in A. A. Berryman (ed.). Dynamics of Forest Insect Populations. Patterns, Causes, and Implications. Plenum Press, New York.
Haukioja, E., Ossipov, V., and Lempa, K. 2002. Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomol. Exp. Appl. 104:125–136.
Heim, K. E., Tagliaferro, A. R., and Bobilya, D. J. 2002. Flavonoid antioxidants: chemistry, metabolism and structure–activity relationship. J. Nutr. Biochem. 13:572–584.
Hoover, K., Lee, L. Y., Schulz, C. M., Rocke, D. M., Hammock, B. D., and Duffey, S. S. 1998a. Effects of plant identity and chemical constituents on the efficacy of a baculovirus against Heliothis virescens. J. Chem. Ecol. 24:221–252.
Hoover, K., Kishida, K. T., DiGiorgio, L. A., Workman, J., Alaniz, S. A., Hammock, B. D., and Duffey, S. S. 1998b. Inhibition of baculoviral disease by plant-mediated peroxidase activity and free radical generation. J. Chem. Ecol. 24:1949–2001.
Kaitaniemi, P., Ruohomäki, K., and Haukioja, E. 1997. Consequences of defoliation on phenological interaction between Epirrita autumnata and its host plant, mountain birch. Funct. Ecol. 11:199–208.
Kaitaniemi, P., Ruohomäki, K., Ossipov, V., Haukioja, E., and Pihlaja, K. 1998. Delayed induced changes in the biochemical composition of host plants leaves during an insect outbreak. Oecologia 116:182–190.
Kapari, L., Haukioja, E., Rantala, M. J., and Ruuhola T. 2006. Defoliating insect immune defense interacts with induced plant defenses during a population outbreak. Ecology 87:291–296.
Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.
Karban, R., and Myers, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331–348.
Karban, R., and Niiho, C. 1995. Induced resistance and susceptibility to herbivory: plant memory and altered plant development. Ecology 76:1220–1225.
Kause, A., Ossipov, V., Haukioja, E., Lempa, K., Hanhimäki, S., and Ossipova S. 1999. Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112.
Klemola, N., Klemola, T., Rantala, M. J., and Ruuhola, T. 2007. Natural host plant quality affects immune defense of the insect herbivore. Entomol. Exp. Appl. 123:167–176.
Lempa, K., Agrawal, A. A., Salminen, J. -P., Turunen, T., Ossipov, V., Ossipova, S., Haukioja, E., and Pihlaja, K. 2004. Rapid herbivore-induced changes in mountain birch phenolics and nutritive compounds and their effects on performance of the major defoliator, Epirrita autumnata. J. Chem. Ecol. 30:303–321.
Levine, A., Tenhaken, R., Dixon, R., and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593.
Liu, L., Gittz, D. C., and Mclure, J. W. 1995. Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. Physiol. Plant. 93:725–733.
Markham, K. R., Ryan, K. G., Bloor, S. J., and Mitchell, K. A. 1998a. An increase in the luteolin:apigenin ratio in Marchantia polymorpha on UV-B enhancement. Phytochemistry 48:791–794.
Markham, K. R., Tanner, G. J., Caasi-lit, M., Whitecross, M. I., Nayudu, M., and Mitchell, K. A. 1998b. Possible protective role of 3′4′ -dihydroxyflavones induced by enhanced UV-B in a UV-tolerant rice cultivar. Phytochemistry 49:1913–1919.
Martin, J. S., Martin, M. M., and Bernays, E. A. 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.
Myers, J. H. 1998. Synchrony in outbreaks of forest Lepidoptera: a possible example of the Moran effect. Ecology 79:1111–1117.
Nappi, A. J., Vass, E., Frey, F., and Carton, Y. 1995. Superoxidase anion generation in Drosophila during melanotic encapsulation of parasites. Eur. J. Cell Biol. 68:450–456.
Olsson, L. C., Veit, M., and Bornman, J. F. 1999. Epidermal transmittance and phenolic composition in leaves of atrazine-tolerant and atrazine-sensitive cultivars of Brassica napus grown under enhanced UV-B radiation. Physiol. Plant. 107:259–266.
Orozco-Cárdenas, M. L., Nárvaez-Vásquez, J., and Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin and methyl jasmonate. Plant Cell 13:179–191.
Ossipov, V., Haukioja, E., Ossipova, S., Hanhimäki, S., and Pihlaja, K. 2001. Phenolic and phenolic-related factors as determinants of suitability of mountain birch leaves to an herbivorous insect. Biochem. Syst. Ecol. 29:223–240.
Paskewitz, S., and Riehle, M. A. 1994. Response of plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated Sephadex beads. Dev. Comp. Immunol. 18:369.
Pourcel, L., Routaboul, J. -M., Cheynier, V., Lepiniec, L., and Debeaujon, I. 2006. Flavonoid oxidation in plants: biochemical properties to physiological functions. Trends Plant Sci. 12:29–36.
Rantala, M. J., and Roff, D. A. 2005. An analysis of trade-off in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct. Ecol. 19:323–330.
Rantala, M. J. and Roff, D. A. 2007. Inbreeding and extreme outbreeding causes sex differences in immune defense and life history traits in Epirrita autumnata. Heredity 98:329–336.
Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A., and Suhonen, J. 2002. Do pheromones reveal male immunocompetence. Proc. R. Soc. Lond. B. 269:1681–1685.
Rantala, M. J., Roff D. A., and Rantala, L. M. 2007. Forceps size and immune function in the European earwig Forficula auricularia. Biol. J. Linn. Soc. 90:509–516.
Riipi, M., Ossipov, V., Lempa, K., Haukioja, E., Koricheva, J., Ossipova, S., and Pihlaja, K. 2002. Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380–390.
Ruohomäki, K., Chapin, III, F. S., Haukioja, E., Neuvonen, S., and Suomela, J. 1996. Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 77:2302–2311.
Ruohomäki, K., Tanhuanpää, M., Ayres, M. P., Kaitaniemi, P., Tammaru, T., and Haukioja, E. 2000. Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Pop. Ecol. 42:211–223.
Ruuhola, T. and Yang, S. 2006. Wound-induced oxidative responses in mountain birch leaves. Ann. Bot. 97:29–37.
Ryan, C. A. 2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477:112–121.
Ryan, K. G., Markham, K. R., Bloor, S. J. Bradley, J. M., Mitchell, K. A., and Jordan, B. R. 1998. UV-B radiation induced increase in quercetin:kaemferol ratio in wild-type and transgenic lines of Petunia. Photochem. Photobiol. 68:323–330.
Salminen, J. -P., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolyzable tannins from leaves of Betula pubescens by high-performance liquid chromatography-mass spectrometry. J. Chromatogr. A 864:283–291.
Salminen, J. -P., Ossipov, V., Haukioja, E., and Pihlaja, K. 2001. Seasonal variation in the content of hydrolyzable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22.
Salminen, J. -P., Ossipov, V., and Pihlaja, K. 2002. Distribution of hydrolyzable tannins in the foliage of Finnish birch species. Z. Naturforsch. 57c:248–256.
Schweigert, N., Zehnder, A. J. B., and Eggen, R. I. L. 2001. Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammal. Environ. Microbiol. 3:81–91.
Seppänen, E. J. 1970. Suomen suurperhostoukkien ravintokasvit (The food-plants of the larvae of the Macrolepidoptera of Finland). Animalia Fennica 14, Werner Söderström.
Söderhäll, K., and Cerenius, L. 1998. Role of the phenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol. 10:23–28.
Tallamy, D. W., and Raupp, M. J. 1991. Phytochemical induction by herbivores. John Wiley and Sons Inc., New York.
Tammaru, T. 1998. Determination of adult size in a folivorous moth: constraints at instar level? Ecol. Entomol. 23:80–89.
Tenow, O. 1972. The outbreaks of Oporinia antumnata Bkh. and Operophtera spp. (Lep: Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1986. PhD Thesis. Zool. Bridr. Uppsala, Suppl. 2:1–107.
Vaarama, A., and Valanne, T. 1973. On the taxonomy, biology and origin of Betula tortuosa Ledeb. Rep. Kevo Subarctic Res. Stat. 10:70–84.
Wielgolaski, F. E. 2005. History and environment of the Nordic mountain birch. pp. 3–18, in F. E. Wielgolaski (ed.). Plant Ecology, Herbivory, and Human Impact in Nordic Mountain Birch Forests. Springer-Verlag, Berlin.
Zar, J. H. 1999. Biostatistical Analysis. Prentice Hall Int. Inc., London.
Acknowledgements
The research was conducted in Kevo Subarctic Research Station, and we thank the staff for help and co-work. We also thank the department of Physiology and Genetics for providing the facilities for the enzymatic assays. We also thank our field assistants Ulla Anttila, Tia Lampela, Liisa Rantala and Mikko Oikamo, and Piia Saarinen for doing the phenolic analyses. Salla-Riikka Vesterlund kindly checked the English language. The study was supported financially by the Academy of Finland, Kone and Emil Aaltonen Foundation.
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Ruuhola, T., Salminen, JP., Haviola, S. et al. Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees. J Chem Ecol 33, 1160–1176 (2007). https://doi.org/10.1007/s10886-007-9308-z
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DOI: https://doi.org/10.1007/s10886-007-9308-z