Abstract
Species of the Salicaceae produce phenolic compounds that may function as anti-herbivore defenses. Levels of these compounds have been reported to increase upon herbivory, but only rarely have these changes in phenolics been studied under natural conditions. We profiled the phenolics of old-growth black poplar (Populus nigra L.) and studied the response to gypsy moth (Lymantria dispar L.) herbivory in two separate field experiments. In a first experiment, foliar phenolics of 20 trees were monitored over 4 weeks after caterpillar infestation, and in a second experiment the bark and foliar phenolics of a single tree were measured over a week. Of the major groups of phenolics, salicinoids (phenolic glycosides) showed no short term response to caterpillar feeding, but after 4 weeks they declined up to 40 % in herbivore damaged and adjacent undamaged leaves on the same branch when compared to leaves of control branches. Flavonol glycosides, low molecular weight flavan-3-ols, and condensed tannins were not affected by herbivory in the first experiment. However, in the single-tree experiment, foliar condensed tannins increased by 10–20 % after herbivory, and low molecular weight flavan-3-ols decreased by 10 % in the leaves but increased by 10 % in the bark. Despite 15 % experimental leaf area loss followed by a 5-fold increase in foliar jasmonate defense hormones, we found no evidence for substantial induction of phenolic defense compounds in old growth black poplar trees growing in a native stand. Thus, if phenolics in these trees function as defenses against herbivory, our results suggest that they act mainly as constitutive defenses.
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References
Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552
Ayres MP, Clausen TP, Maclean SF, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712
Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen JP, Yip L, Tran L, Constabel CP (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164:993–1004
Barbehenn R, Weir Q, Salminen JP (2008) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34:748–756. doi:10.1007/s10886-008-9478-3
Barbehenn RV, Constabel CP (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565. doi:10.1016/j.phytochem.2011.01.040
Bingaman BR, Hart ER (1993) Clonal and leaf age variation in Populus phenolic glycosides: Implications for host selection by Chrysomela scripta (Coleoptera: Chrysomelidae). Environ Entomol 22:397–403
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509
Bourjot M, Leyssen P, Eydoux C, Guillemot JC, Canard B, Rasoanaivo P, Gueritte F, Litaudon M (2012) Flacourtosides A-F, phenolic glycosides isolated from Flacourtia ramontchi. J Nat Prod 75:752–758
Bryant JP, Kuropat PJ (1980) Selection of winter forage by subarctic browsing vertebrates: the role of plant chemistry. Annu Rev Ecol Syst 11:261–285
Clausen TP, Reichardt PB, Bryant JP, Werner RA, Post K, Frisby K (1989) Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J Chem Ecol 15:2335–2346
Constabel CP, Lindroth R (2010) The impact of genomics on advances in herbivore defense and secondary metabolism in Populus. In: Jansson S, Bhalaero R, Groover A, (eds.). Genetics and genomics of Populus. Springer Verlag, pp 279–305
Crawley MJ (2007) The R Book. John Wiley & Sons Ltd, Chichester
Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429
Ebert G (1994) Die Schmetterling Baden-Württembergs. Eugen Ulmer GmbH & Co., Stuttgart
Ekabo OA, Farnsworth NR, Santisuk T, Reutrakul V (1993) A phytochemical investigation of Homalium ceylanicum. J Nat Prod 56:699–707
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259
Fields MJ, Orians CM (2006) Specificity of phenolic glycoside induction in willow seedlings (Salix sericea) in response to herbivory. J Chem Ecol 32:2647–2656
Förster N, Ulrichs C, Zander M, Katzel R, Mewis I (2010) Factors influencing the variability of antioxidative phenolic glycosides in Salix species. J Agric Food Chem 58:8205–8210
Haukioja E, Koricheva J (2000) Tolerance to herbivory in woody vs. herbaceous plants. Evol Ecol 14:551–562
Heiska S, Tikkanen O-P, Rousi M, Julkunen-Tiitto R (2007) Bark salicylates and condensed tannins reduce vole browsing amongst cultivated dark-leaved willows (Salix myrsinifolia). Chemoecology 17:245–253
Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moth and forest tent caterpillars. Oecologia 103:79–88
Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85:267–280
Holeski LM, Vogelzang A, Stanosz G, Lindroth RL (2009) Incidence of Venturia shoot blight in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochem Syst Ecol 37:139–145
Hwang SY, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108
Julkunen-Tiitto R (1985) Chemotaxonomical screening of phenolic glycosides in northern willow twigs by capillary gas chromatography. J Chromatogr 324:129–139
Julkunen-Tiitto R, Bryant JP, Kuropat P, Roininen H (1995) Slight tissue wounding fails to induce consistent chemical defense in three willow (Salix spp.) clones. Oecologia 101:467–471
Kleiner KW, Ellis DD, Mccown BH, Raffa KF (2003) Leaf ontogeny influences leaf phenolics and the efficacy of genetically expressed Bacillus thuringiensis cry1A(a) d-endotoxin in hybrid poplar against gypsy moth. J Chem Ecol 29:2585–2602
Lindroth RL (1991) Biochemical ecology of aspen-Lepidoptera Interactions. J Kans Entomol Soc 64:372–380
Lindroth RL, Kinney KK (1998) Consequences of enriched atmospheric CO2 and defoliation for foliar chemistry and gypsy moth performance. J Chem Ecol 24:1677–1695
Lindroth RL, Peterson SS (1988) Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75:185–189
Mellway RD, Constabel CP (2009) Metabolic engineering and potential functions of proanthocyanidines in poplar. Plant Signal Behav 4:1–3
Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941
Meyer GA, Montgomery ME (1987) Relationships between leaf age and food quality of cottonwood foliage for the gypsy moth, Lymantria dispar. Oecologia 72:527–532
Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Microbe Interact 20:816–831
Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225
Mutikainen P, Walls M, Ovaska J, Keinanen M, Julkunen-Tiitto R, Vapaavuori E (2000) Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65
Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–1313
Palo RT (1984) Distribution of birch (Betula SPP.), willow (Salix SPP.) and poplar (Populus SPP.) secondary matabolites and their potential role as chemical defense against herbivores. J Chem Ecol 10:499–520
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 32:701–712
Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230
Roth S, Lindroth RL, Volin JC, Kruger EL (1998) Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance. Global Change Biol 4:419–430
Ruuhola TM, Sipura M, Nousiainen O, Tahvanainen J (2001) Systemic induction of salicylates in Salix myrsinifolia (Salisb.). Ann Bot 88:483–497
Schofield P, Mbugua DM, Pell AN (2001) Analysis of condensed tannins: a review. Anim Feed Sci Technol 91:21–40
Scioneaux AN, Schmidt MA, Moore MA, Lindroth RL, Wooley SC, Hagerman AE (2011) Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key. J Chem Ecol 37:57–70
Spalinger DE, Collins WB, Hanley TA, Cassara NE, Carnahan AM (2010) The impact of tannins on protein, dry matter, and energy digestion in moose (Alces alces). Can J Zool-Rev Can Zool 88:977–987
Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306
Thieme H, Benecke R (1971) Die Phenolglykoside der Salicaeen. 8. Mitteilung: Untersuchung über die Glykosidakkumulation in einigen mitteleuropäischen Populus-Arten. Pharmazie 26:227–231
Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithöfer A (2012) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in arabidopsis. Plant Physiol 159:1159–1175
Young B, Wagner D, Doak P, Clausen T (2010) Induction of phenolic glycosides by quaking aspen (Populus tremuloides) leaves in relation to extrafloral nectaries and epidermal leaf mining. J Chem Ecol 36:369–377
Zangerl AR (2003) Evolution of induced plant responses to herbivores. Basic Appl Ecol 4:91–103
Acknowledgments
We are grateful to Rick Lindroth, Bernd Schneider, and Peter Constabel for providing various phenolic standards, Sonja Löffler and Ralf Kätzel for help in establishing the field site, and Beate Rothe, Michael Reichelt, and Antje Zamella for technical assistance in the laboratory. Further, we thank Grit Kunert for advice on the statistical analysis and Peter Constabel for comments on an earlier version of the manuscript.
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Boeckler, G.A., Gershenzon, J. & Unsicker, S.B. Gypsy Moth Caterpillar Feeding has Only a Marginal Impact on Phenolic Compounds in Old-Growth Black Poplar. J Chem Ecol 39, 1301–1312 (2013). https://doi.org/10.1007/s10886-013-0350-8
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DOI: https://doi.org/10.1007/s10886-013-0350-8