Anti-Herbivore Activity of Oregonin, a Diarylheptanoid Found in Leaves and Bark of Red Alder (Alnus rubra)

Abstract

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data Availability

NA

References

  1. 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

    CAS  Article  Google Scholar 

  2. 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

    CAS  Article  PubMed  Google Scholar 

  3. 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

    CAS  Article  Google Scholar 

  4. 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

    CAS  Article  PubMed  Google Scholar 

  5. Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552. https://doi.org/10.1007/BF00984895

    CAS  Article  PubMed  Google Scholar 

  6. Appel HM, Martin MM (1990) Gut redox conditions in herbivorous lepidopteran larvae. J Chem Ecol 16:3277–3290. https://doi.org/10.1007/BF00982098

    CAS  Article  PubMed  Google Scholar 

  7. 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

    CAS  Article  PubMed  Google Scholar 

  8. Barbehenn RV, Constabel C (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565. https://doi.org/10.1016/j.phytochem.2011.01.040

    CAS  Article  PubMed  Google Scholar 

  9. 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

    CAS  Article  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. R Stat Soc 57:289–300

    Google Scholar 

  12. 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)

  13. 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

    CAS  Article  PubMed  Google Scholar 

  14. 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

    CAS  Article  PubMed  Google Scholar 

  15. Borden JH (1969) Observations on the life history and habits of Alniphagus aspericollis (Coleoptera: Scolytidae) in southwestern British Columbia. Can Entomol 101:870–878

    Article  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

  18. 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

    CAS  Article  PubMed  Google Scholar 

  19. Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252. https://doi.org/10.1080/00401706.1964.10490181

    Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    CAS  Article  PubMed  Google Scholar 

  22. 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

    CAS  Article  Google Scholar 

  23. 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

    Google Scholar 

  24. 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

    CAS  Article  Google Scholar 

  25. Karchesy J (1974) Polyphenols of red alder: chemistry of the staining phenomenon. Dissertation, Oregonin State University

  26. 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

    CAS  Article  Google Scholar 

  27. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Article  Google Scholar 

  28. 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

  29. 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

    CAS  Article  PubMed  Google Scholar 

  30. 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

    CAS  Article  PubMed  Google Scholar 

  31. Levene H (1960) Robust tests for equality of variances. In: Journal of the American Statistical Association, pp 278–292

  32. 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

  33. Lingren PD, Green GL (1984) Suppression and management of cabbage looper populations. U.S. Department of Agriculture, Technical Bulletin No. 1684, 152p

  34. Lv H, She G (2012) Naturally occurring diarylheptanoids - a supplementary version. Nat Prod Commun 5:1687–1708. https://doi.org/10.1177/1934578x1000501035

    Article  Google Scholar 

  35. 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

    CAS  Article  PubMed  Google Scholar 

  36. 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

    CAS  Article  Google Scholar 

  37. 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

    CAS  Article  PubMed  Google Scholar 

  38. Muthigani P (1971) Insect defoliation studies on red alder (Alnus rubra bong) on Burnaby Mountain. Thesis, Simon Fraser University, B.C.

  39. 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

    Article  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

    Article  PubMed  PubMed Central  Google Scholar 

  42. 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

  43. 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

    CAS  Article  PubMed  Google Scholar 

  44. 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

  45. 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

    Article  PubMed  Google Scholar 

  46. Sati SC, Sati N, Sati OP (2011) Bioactive constituents and medicinal importance of genus Alnus. Pharmacogn Rev 5:174–183

  47. 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

    CAS  Article  Google Scholar 

  48. 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

  49. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55. https://doi.org/10.1086/367580

    Article  PubMed  Google Scholar 

  50. 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

    CAS  Article  PubMed  Google Scholar 

  51. 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

    Article  PubMed  Google Scholar 

  52. 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

    CAS  Article  Google Scholar 

  53. 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

    CAS  Google Scholar 

  54. 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

    CAS  Article  Google Scholar 

  55. Tukey JW (1997) Exploratory data analysis. Addison-Wesley Publishing Company, London, Amsterdam, pp 5–24

    Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Funding

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.

Author information

Affiliations

Authors

Contributions

NA

Corresponding author

Correspondence to C. Peter Constabel.

Ethics declarations

Conflict of Interest/Competing Interest

The authors declare no conflicts of interest.

Code Availability

NA

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Keywords

  • Phenolic
  • Antifeedant
  • Plant-insect-interaction
  • Herbivore
  • Lepidoptera