Plants synthesize a wide range of bioactive secondary metabolites to defend against pests and pathogens. Red alder (Alnus rubra) bark, root, and leaf extract have a long history of use in traditional medicine and hygiene. Diarylheptanoids, especially oregonin ((5S)-1,7-bis(3,4-dihydroxyphenyl)-5-(β-D-xylopyranosyloxy)-heptan-3-one), have been identified as major bioactive constituents. Diarylheptanoids have become a focus of research following reports of their antioxidant, antifungal, and anti-cancer activities. Recent data suggest that high oregonin concentration is associated with resistance of red alder leaves to western tent caterpillar (Malacosoma californicum) defoliation. Here we test effects of this compound directly on leaf-eating insects. Purified oregonin was examined in insect choice and toxicity tests using lepidopteran caterpillars. The compound exhibited significant anti-feedant activity against cabbage looper (Trichoplusia ni), white-marked tussock moth (Orgyia leucostigma), fall webworm (Hyphantria cunea), and M. californicum at concentrations corresponding to oregonin content of the most resistant alder clones in previous experiments. Toxicity tests were carried out with cabbage looper larvae only, but no contact or ingested toxicity was detected. Our results suggest that oregonin at levels found in red alder leaves early in the growing season may contribute to protecting red alder from leaf-eating insects.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Abedini A, Chollet S, Angelis A, Borie N, Nuzillard JM, Skaltsounis AL, Reynaud R, Gangloff SC, Renault JH, Hubert J (2016) Bioactivity-guided identification of antimicrobial metabolites in Alnus glutinosa bark and optimization of oregonin purification by centrifugal partition chromatography. J Chromatogr B 1029–1030:121–127. https://doi.org/10.1016/j.jchromb.2016.07.021
Akhtar Y, Yu Y, Isman MB, Plettner E (2010) Dialkoxybenzene and dialkoxyallylbenzene feeding and oviposition deterrents against the cabbage looper, Trichoplusia ni: potential insect behavior control agents. J Agric Food Chem 58:4983–4991. https://doi.org/10.1021/jf9045123
Akhtar Y, Isman MB, Niehaus LA, Lee CH, Lee HS (2012) Antifeedant and toxic effects of naturally occurring and synthetic quinones to the cabbage looper, Trichoplusia ni. Crop Prot 31:8–14. https://doi.org/10.1016/j.cropro.2011.09.009
Alberti Á, Riethmüller E, Béni S (2018) Characterization of diarylheptanoids: an emerging class of bioactive natural products. J Pharm Biomed Anal 147:13–34. https://doi.org/10.1016/j.jpba.2017.08.051
Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552. https://doi.org/10.1007/BF00984895
Appel HM, Martin MM (1990) Gut redox conditions in herbivorous lepidopteran larvae. J Chem Ecol 16:3277–3290. https://doi.org/10.1007/BF00982098
Barbehenn RV (2002) Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. J Chem Ecol 28:1329–1347. https://doi.org/10.1023/A:1016288201110
Barbehenn RV, Constabel C (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565. https://doi.org/10.1016/j.phytochem.2011.01.040
Barbehenn RV, Martin MM, Hagerman AE (1996) Reassessment of the roles of the peritrophic envelope and hydrolysis in protecting polyphagous grasshoppers from ingested hydrolyzable tannins. J Chem Ecol 22:1901–1919. https://doi.org/10.1007/BF02028511
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. https://doi.org/10.1007/s00442-007-0822-z
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. R Stat Soc 57:289–300
Boateng K, Hawkins BJ, Constabel CP, Yanchuk AD, Fellenberg C (2020) Red alder defense mechanisms against western tent caterpillar defoliation. Can J For Res (in press)
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509. https://doi.org/10.1016/j.phytochem.2011.01.038
Boeckler GA, Towns M, Unsicker SB, Mellway RD, Yip L, Hilke I, Gershenzon J, Constabel CP (2014) Transgenic upregulation of the condensed tannin pathway in poplar leads to a dramatic shift in leaf palatability for two tree-feeding Lepidoptera. J Chem Ecol 40:150–158. https://doi.org/10.1007/s10886-014-0383-7
Borden JH (1969) Observations on the life history and habits of Alniphagus aspericollis (Coleoptera: Scolytidae) in southwestern British Columbia. Can Entomol 101:870–878
Brennan M, Fritsch C, Cosgun S, Dumarcay S, Colin F, Gérardin P (2020) Quantitative and qualitative composition of bark polyphenols changes longitudinally with bark maturity in Abies alba mill. Ann For Sci 77:1–14. https://doi.org/10.1007/s13595-019-0916-x
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Heidelberg, pp 253–270
Dong G-Z, Jeong JH, Lee Y-I, Lee SY, Zhao HY, Jeon R, Lee HJ, Ryu JH (2017) Diarylheptanoids suppress proliferation of pancreatic cancer PANC-1 cells through modulating shh-Gli-FoxM1 pathway. Arch Pharm Res 40:509–517. https://doi.org/10.1007/s12272-017-0905-2
Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252. https://doi.org/10.1080/00401706.1964.10490181
González-Hernández MP, Starkey EE, Karchesy J (2000) Seasonal variation in concentrations of fiber, crude protein, and phenolic compounds in leaves of red alder (Alnus rubra): nutritional implications for cervids. J Chem Ecol 26:293–301. https://doi.org/10.1023/A:1005462100010
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. https://doi.org/10.1034/j.1399-3054.2001.1120413.x
Hemming JDC, Lindroth RL (2000) Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environ Entomol 29:1108–1115. https://doi.org/10.1603/0046-225x-29.6.1108
Hibbs DE, DeBell DS (1994) Management of young red alder. In: DeBell DE, DeBell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, Corvallis, pp 202–215
Hu W, Wang M-H (2011) Antioxidative activity and anti-inflammatory effects of diarylheptanoids isolated from Alnus hirsuta. J Wood Sci 57:323–330. https://doi.org/10.1007/s10086-010-1170-x
Karchesy J (1974) Polyphenols of red alder: chemistry of the staining phenomenon. Dissertation, Oregonin State University
Konno K, Hirayama C, Yasui H, Nakamura M (1999) Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc Natl Acad Sci U S A 96:9159–9164
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621
Lea CS, Simhadri C, Bradbury SG et al (2020) Efficient purification of the diarylheptanoid oregonin from red alder (Alnus rubra) leaves and bark combining aqueous extraction, spray drying and flash-chromatography. Phytochem Anal:1–8. https://doi.org/10.1002/pca.3005
Lee WS, Kim J-R, Im K-R, Cho KH, Sok DE, Jeong TS (2005) Antioxidant effects of diarylheptanoid derivatives from Alnus japonica on human LDL oxidation. Planta Med 71:295–299. https://doi.org/10.1055/s-2005-864093
Lee O, Kim J, Choi YW, Lee M, Park G, Oh C (2013) Efficacy of oregonin investigated by non-invasive evaluation in a B16 mouse melanoma model. Exp Dermatol 22:842–844. https://doi.org/10.1111/exd.12277
Levene H (1960) Robust tests for equality of variances. In: Journal of the American Statistical Association, pp 278–292
Lindroth RL (2001) Adaptations of quaking aspen for defense against damage by herbivores and related environmental agents. USDA Forest Service Proceedings RMRS-P-18:273–284
Lingren PD, Green GL (1984) Suppression and management of cabbage looper populations. U.S. Department of Agriculture, Technical Bulletin No. 1684, 152p
Lv H, She G (2012) Naturally occurring diarylheptanoids - a supplementary version. Nat Prod Commun 5:1687–1708. https://doi.org/10.1177/1934578x1000501035
Mansfield JL, Curtis PS, Zak DR, Pregitzer KS (1999) Genotypic variation for condensed tannin production in trembling aspen (Populus tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. Am J Bot 86:1154–1159. https://doi.org/10.2307/2656979
McArthur C, Robbins CT, Hagerman AE, Hanley TA (1993) Diet selection by a ruminant generalist browser in relation to plant chemistry. Can J Zool 71:2236–2243. https://doi.org/10.1139/z93-314
Muilenburg VL, Phelan PL, Bonello P, Herms DA (2011) Inter- and intra-specific variation in stem phloem phenolics of paper birch (Betula papyrifera) and European white birch (Betula pendula). J Chem Ecol 37:1193–1202. https://doi.org/10.1007/s10886-011-0028-z
Muthigani P (1971) Insect defoliation studies on red alder (Alnus rubra bong) on Burnaby Mountain. Thesis, Simon Fraser University, B.C.
Novaković M, Novaković I, Cvetković M, Sladić D, Tešević V (2015) Antimicrobial activity of the diarylheptanoids from the black and green alder. Rev Bras Bot 38:441–446. https://doi.org/10.1007/s40415-015-0151-0
O’Neal ME, Landis DA, Isaacs R (2009) An inexpensive, accurate method for measuring leaf area and defoliation through digital image analysis. J Econ Entomol 95:1190–1194. https://doi.org/10.1603/0022-0493-95.6.1190
Ochoa-López S, Villamil N, Zedillo-Avelleyra P, Boege K (2015) Plant defence as a complex and changing phenotype throughout ontogeny. Ann Bot 116:797–806. https://doi.org/10.1093/aob/mcv113
Park D, Kim HJ, Jung SY, Yook CS, Jin C, Lee YS (2010) A new diarylheptanoid glycoside from the stem bark of Alnus hirsuta and protective effects of diarylheptanoid derivatives in human HepG2 cells. Chem Pharm Bull 58:238–241. https://doi.org/10.1248/cpb.58.238
Ponomarenko J, Trouillas P, Martin N, Dizhbite T, Krasilnikova J, Telysheva G (2014) Elucidation of antioxidant properties of wood bark derived saturated diarylheptanoids: a comprehensive (DFT-supported) understanding. Phytochemistry 103:178–187. https://doi.org/10.1016/j.phytochem.2014.03.010
Ren X, He T, Chang Y, Zhao Y, Chen X, Bai S, Wang L, Shen M, She G (2017) The genus Alnus, a comprehensive outline of its chemical constituents and biological activities. Molecules 22(8):1383
Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K (2002) Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380–390. https://doi.org/10.1007/s00442-001-0826-z
Sati SC, Sati N, Sati OP (2011) Bioactive constituents and medicinal importance of genus Alnus. Pharmacogn Rev 5:174–183
Saxena G, Farmer S, Hancock REW, Towers GHN (1995) Antimicrobial compounds from Alnus rubra. Pharm Biol 33:33–36. https://doi.org/10.3109/13880209509088144
Sidda JD, Song L, Parker JL, Studholme DJ, Sambles C, Grant M (2020) Diversity of secoiridoid glycosides in leaves of UK and Danish ash provide new insight for ash dieback management. Sci Rep 10:19566. https://doi.org/10.1038/s41598-020-76140-z
Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55. https://doi.org/10.1086/367580
Sunnerheim K, Bratt K (2004) Identification of centrolobol as the platyphylloside metabolite responsible for the observed effect on in vitro digestibility of hay. J Agric Food Chem 52:5869–5872. https://doi.org/10.1021/jf040135e
Sunnerheim-Sjöberg K, Knutsson PG (1995) Platyphylloside: metabolism and digestibility reduction in vitro. J Chem Ecol 21:1339–1348. https://doi.org/10.1007/BF02027566
Telysheva G, Dizhbite T, Bikovens O, Ponomarenko J, Janceva S, Krasilnikova J (2011) Structure and antioxidant activity of diarylheptanoids extracted from bark of grey alder (Alnus incana) and potential of biorefinery-based bark processing of European trees. Holzforschung 65:623–629. https://doi.org/10.1515/HF.2011.096
Thompson DW, Kozak RA, Evans PD (2008) Thermal modification of color in red alder veneer. Part II. Effects of season, log storage time, and location of wood in stems. Wood Fiber Sci 40:80–90
Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29:1025–1047. https://doi.org/10.1016/S0305-1978(01)00048-5
Tukey JW (1997) Exploratory data analysis. Addison-Wesley Publishing Company, London, Amsterdam, pp 5–24
Vassão DG, Wielsch N, de MM GAM et al (2018) Plant defensive β-Glucosidases resist digestion and sustain activity in the gut of a lepidopteran herbivore. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.01389
Yang H, Sung SH, Kim J, Kim YC (2011) Neuroprotective diarylheptanoids from the leaves and twigs of Juglans sinensis against glutamate-induced toxicity in HT22 cells. Planta Med 77:841–845. https://doi.org/10.1055/s-0030-1250609
We thank Dr. Jacqueline Bede from McGill University, and Dr. Murray Isman from University of British Columbia for providing technical advice. We also thank Dr. Ori Granot from the UVic Chemistry Analytical Facility, and Dr. Christin Fellenberg and Dr. Kennedy Boateng from the Centre of Forest Biology for their help, as well as Brad Binges for greenhouse assistance. We acknowledge generous support from the Natural Sciences Engineering Research Council of Canada in the form of an Engage Grant, and a Mitacs Accelerate Grant for funding of this project.
This work was funded by the Natural Sciences and Engineering Council of Canada (NSERC) via an Engage Grant, as well as a Mitacs Accelerate Grant, to CPC.
Conflict of Interest/Competing Interest
The authors declare no conflicts of interest.
About this article
Cite this article
Lea, C.S., Bradbury, S.G. & Constabel, C.P. Anti-Herbivore Activity of Oregonin, a Diarylheptanoid Found in Leaves and Bark of Red Alder (Alnus rubra). J Chem Ecol 47, 215–226 (2021). https://doi.org/10.1007/s10886-021-01244-3