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Journal of Chemical Ecology

, 35:1326 | Cite as

Induced Responses to Herbivory and Jasmonate in Three Milkweed Species

  • Sergio Rasmann
  • M. Daisy Johnson
  • Anurag A. Agrawal
Article

Abstract

We studied constitutive and induced defensive traits (latex exudation, cardenolides, proteases, and C/N ratio) and resistance to monarch caterpillars (Danaus plexippus) in three closely related milkweed species (Asclepias angustifolia, A. barjoniifolia and A. fascicularis). All traits showed significant induction in at least one of the species. Jasmonate application only partially mimicked the effect of monarch feeding. We found some correspondence between latex and cardenolide content and reduced larval growth. Larvae fed cut leaves of A. angustifolia grew better than larvae fed intact plants. Addition of the cardenolide digitoxin to cut leaves reduced larval growth but ouabain (at the same concentration) had no effect. We, thus, confirm that latex and cardenolides are major defenses in milkweeds, effective against a specialist herbivore. Other traits such as proteases and C/N ratio additionally may be integrated in the defense scheme of those plants. Induction seems to play an important role in plants that have an intermediate level of defense, and we advocate incorporating induction as an additional axis of the plant defense syndrome hypothesis.

Keywords

Multiple defenses Secondary metabolites Latex Cardenolides Monarch (Danaus plexippusProteases Asclepias 

Notes

Acknowledgments

We thank Amy Hastings for laboratory assistance, Rayko Halitschke for help with chemical analysis, Jennifer Thaler for providing jasmonic acid, Susan Cook, Rayko Halitschke and Mike Stastny for comments on the manuscript, and Steve Malcolm for providing seeds of A. barjoniifolia. Chemical analyses were conducted in the Cornell Chemical Ecology Core Facility, with support from Paul Feeny, New Life Sciences Initiative, College of Agriculture and Life Sciences, Center for a Sustainable Future, Boyce Thompson Institute, and Departments of Ecology & Evolutionary Biology, Neurobiology & Behavior, Entomology, Plant Biology, and Horticulture. Our research was supported by NSF-DEB 0447550 to AAA, and postdoctoral fellowship from Swiss National Science Foundation PA0033-121483 to SR.

References

  1. Ackery, P. R., and Vane-Wright, R. I. 1984. Milkweed butterflies: their cladistics and biology, pp. 201–205. Cornell University Press, Ithaca, NY, USA.Google Scholar
  2. Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201–1202.CrossRefPubMedGoogle Scholar
  3. Agrawal, A.A. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol. Ecol. Res. 7:651–667.Google Scholar
  4. Agrawal, A.A., and Fishbein, M. 2006. Plant defense syndromes. Ecology 87:S132–S149.CrossRefPubMedGoogle Scholar
  5. Agrawal, A. A., and Fishbein, M. 2008. Phylogenetic escalation and decline of plant defense strategies. Proc. Natl. Acad. Sci. USA 105:10057–10060.CrossRefPubMedGoogle Scholar
  6. Agrawal, A. A., and Konno, K. 2009. Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu. Rev. Plant Biol. Google Scholar
  7. Agrawal, A. A. and Van Zandt, P. A. 2003. Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. J. Ecol. 91:1049–1059.CrossRefGoogle Scholar
  8. Agrawal, A. A., Lajeunesse, M. J., and Fishbein, M. 2008. Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomol. Exp. Appl. 128:126–138.CrossRefGoogle Scholar
  9. Agrawal, A. A., Fishbein, M., Jetter, R., Salminen, J. P., Goldstein, J. B., Freitag, A. E., and Sparks, J. P. 2009. Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol. 183:848–867.CrossRefPubMedGoogle Scholar
  10. Arima, K., Uchikoba, T., Yonezawa, H., Shimada, M., and Kaneda, M. 2000. Cucumisin-like protease from the latex of Euphorbia supina. Phytochemistry 53:639–644.CrossRefPubMedGoogle Scholar
  11. Arribere, M.C., Cortadi, A.A., Gattuso, M.A., Bettiol, M.P., Priolo, N.S., and Caffini, N.O. 1998. Comparison of asclepiadaceae latex proteases and characterization of Morrenia brachystephana Griseb. Cysteine peptidases. Phytochem. Anal. 9:267–273.CrossRefGoogle Scholar
  12. Behmer, S. T. 2009. Insect herbivore nutrient regulation. Annu. Rev. Entomol. 54:165–187.CrossRefPubMedGoogle Scholar
  13. Bennett, R. N., and Wallsgrove, R. M. 1994. Secondary metabolites in plant defense-mechanisms. New Phytol. 127:617–633.CrossRefGoogle Scholar
  14. Berenbaum, M. R., Zangerl, A. R., and Nitao, J. K. 1986. Constraints on chemical coevolution—wild parsnips and the parsnip webworm. Evolution 40:1215–1228.CrossRefGoogle Scholar
  15. Berenbaum, M. R., Nitao, J. K., and Zangerl, A. R. 1991. Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae). J. Chem. Ecol. 17:207–215.CrossRefGoogle Scholar
  16. Broadway, R. M., Duffey, S. S., Pearce, G., and Ryan, C. A. 1986. Plant proteinase inhibitors: a defence against herbivorous insects? Entomol. Exp. Appl. 41:33–38.CrossRefGoogle Scholar
  17. Brower, L. P., Williams, K. L., McEvoy, P. B., and Flannery, M. A. 1972. Variation in cardiac glycoside content of monarch butterflies from natural populations in Eastern North-America. Science 177:426.CrossRefPubMedGoogle Scholar
  18. Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J. M., Lorenzo, O., Garcia-Casado, G., Lopez-Vidriero, I., Lozano, F. M., and Ponce, M. R., et al. 2007. The JAZ family of repressors is the missing link in jasmonate signaling. Nature 448:666–U4.CrossRefPubMedGoogle Scholar
  19. Coley, P.D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr. 53:209–233.CrossRefGoogle Scholar
  20. Constabel, C. P., Bergey, D. R., and Ryan, C. A. 1995. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. USA 92:407–411.CrossRefPubMedGoogle Scholar
  21. David, G. 2007. 585. Asclepias barjoniifolia. Curtis’s Bot. Mag. 24:93–100.CrossRefGoogle Scholar
  22. De Bruxelles, G. L., and Roberts, M. R. 2001. Signals regulating multiple responses to wounding and herbivores. Crit. Rev. Plant Sci. 20:487–521.CrossRefGoogle Scholar
  23. Duffey, S. S., and Scudder, G. G. E. 1974. Cardiac glycosides in Oncopeltus fasciatus (Dallas) (Hemiptera-Lygaeidae) .1. Uptake and distribution of natural cardenolides in body. Can. J. Zool. 52:283–290.CrossRefGoogle Scholar
  24. Duffey, S. S., and Stout, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3–37.CrossRefGoogle Scholar
  25. Dussourd, D. E., and Denno, R. F. 1991. Deactivation of plant defense: correspondence between insect behavior and secretory canal architecture. Ecology 72:1383–1396.CrossRefGoogle Scholar
  26. Dussourd, D. E., and Eisner, T. 1987. Vein-cutting behavior: Insect counterplay to the latex defense of plants. Science 237:898–901.CrossRefPubMedGoogle Scholar
  27. Fishbein, M., Chuba, D., Ellison, C., Mason-Gamer, R., and Lynch, S.P. 2009. Phylogenetic relationships of Asclepias (Apocynaceae) estimated from non-coding cpDNA sequences. Systemat. Botany.Google Scholar
  28. Frick, C., and Wink, M. 1995. Uptake and sequestration of ouabain and other cardiac-glycosides in Danaus plexippus (Lepidoptera, Danaidae)—evidence for a carrier-mediated process. J. Chem. Ecol. 21:557–575.CrossRefGoogle Scholar
  29. Holzinger, F., and Wink, M. 1996. Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+, K+-ATPase. J. Chem. Ecol. 22:1921–1937.CrossRefGoogle Scholar
  30. Howe, G.A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66.CrossRefPubMedGoogle Scholar
  31. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. The University of Chicago Press, Chicago.Google Scholar
  32. Konno, K., Hirayama, C., Nakamura, M., Tateishi, K., Tamura, Y., Hattori, M., and Kohno, K. 2004. Papain protects papaya trees from herbivorous insects: Role of cysteine proteases in latex. Plant J. 37:370–378.CrossRefPubMedGoogle Scholar
  33. Light, A., Frater, R., Kimmel, J. R., and Smith, E. L. 1964. Current status of structure of papain—linear sequence active sulfhydryl group + disulfide bridges. Proc. Natl. Acad. Sci. USA 52:1279.CrossRefGoogle Scholar
  34. Malcolm, S. B. 1991. Cardenolide-mediated interactions between plants and herbivores. pp. 251–296 in G. A. Rosenthal, and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Metabolites. 2nd ed. Academic, San Diego, CA, USAGoogle Scholar
  35. Malcolm, S. B., and Zalucki, M. P. 1996. Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol. Exp. Appl. 80:193–196.CrossRefGoogle Scholar
  36. Malcolm, S. B., Cockrell, B. J., and Brower, L. P. 1989. Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. J. Chem. Ecol.15:819–853.CrossRefGoogle Scholar
  37. Matsuki, S. and Koike, T. 2006. Comparison of leaf life span, photosynthesis and defensive traits across seven species of deciduous broad-leaf tree seedlings. Ann. Bot. 97:813–817.CrossRefPubMedGoogle Scholar
  38. Mattson, W. J. 1980. Herbivory in relation to plant nitrogen-content. Annu. Rev. Ecol. Syst. 11:119–161.CrossRefGoogle Scholar
  39. Rasmann, S., and Agrawal, A. A. 2009. Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr. Op. Plant Biol. 12:473–478.CrossRefGoogle Scholar
  40. Rasmann, S., Agrawal, A. A., Cook, C. S., and Erwin, C. A. 2009. Cardenolides, induced responses in shoots and roots, and interactions between above and belowground herbivores in the milkweeds (Asclepias spp) Ecology 90:2393–2404.CrossRefPubMedGoogle Scholar
  41. Romeo, J. T., Saunders, J. A., and Barbosa, P., eds. 1996. Phytochemical Diversity and Redundancy in Ecological Interactions. Plenum, New York, New York, USA.Google Scholar
  42. Seiber, J. N., Tuskes, P. M., Brower, L. P., and Nelson, C. J. 1980. Pharmacodynamics of some individual milkweed cardenolides fed to larvae of the monarch butterfly (Danaus plexippus L). J. Chem. Ecol. 6:321–339.CrossRefGoogle Scholar
  43. Sgarbieri, V. C., Kramer, D. E., Whitaker, J. R., and Gupte, S. M. 1964. Ficus enzymes .I. Separation of proteolytic enzymes of Ficus carica + Ficus glabrata latices. J. Biol. Chem. 239:2170.PubMedGoogle Scholar
  44. Stout, M. J., and Duffey, S. S. 1996. Characterization of induced resistance in tomato plants. Entomol. Exp. Appl. 79:273–283.CrossRefGoogle Scholar
  45. Stout, M. J., Workman, K. V., and Duffey, S. S. 1996. Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomol. Exp. Appl. 79:255–271.CrossRefGoogle Scholar
  46. Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81.CrossRefGoogle Scholar
  47. Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767–1781.CrossRefGoogle Scholar
  48. Thaler, J. S., Farag, M. A., Pare, P. W., and Dicke, M. 2002. Jasmonate–deficient plants have reduced direct and indirect defences against herbivores. Ecol. Lett. 5:764–774.CrossRefGoogle Scholar
  49. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G. H., Nomura, K., He, S. Y., Howe, G. A., and Browse, J. 2007. JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661–U2.CrossRefPubMedGoogle Scholar
  50. Tomar, R., Kumar, R., and Jagannadham, M. V. 2008. A stable serine protease, wrightin, from the latex of the plant Wrightia tinctoria (Roxb.) r. br.: Purification and biochemical properties. J. Agri. Food Chem. 56:1479–1487.CrossRefGoogle Scholar
  51. Van Zandt, P. A., and Agrawal, A. A. 2004. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629.CrossRefGoogle Scholar
  52. Woodson, R. E. 1954. The North American species of Asclepias L. Ann. Mo. Bot. Gard. 41:1–211.CrossRefGoogle Scholar
  53. Wright, S. E. 1960. The Metabolism of Cardiac Glycosides: A Review of the Absorption, Metabolism and Excretion of Clinically Important Cardiac Glycosides. Blackwell Scientific Publications, Oxford.Google Scholar
  54. Zalucki, M. P., and Brower, L. P. 1992. Survival of first instar larvae of Danaus plexippus (Lepidoptera: Danainae) in relation to cardiac glycoside and latex content of Asclepias humistrata (Asclepiadaceae). Chemoecology 3:81–93.CrossRefGoogle Scholar
  55. Zalucki, M. P., and Malcolm, S. B. 1999. Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. J. Chem. Ecol. 25:1827–1842.CrossRefGoogle Scholar
  56. Zalucki, M. P., Brower, L. P., and Malcolm, S. B. 1990. Oviposition by Danaus plexippus in relation to cardenolide content of 3 Asclepias species in the Southeastern USA. Ecol. Entomol. 15:231–240.CrossRefGoogle Scholar
  57. Zalucki, M. P., Brower, L. P., and Alonso, A. 2001a. Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecol. Entomol. 26:212–224.CrossRefGoogle Scholar
  58. Zalucki, M. P., Malcolm, S. B., Paine, T. D., Hanlon, C. C., Brower, L. P., and Clarke, A. R. 2001b. It’s the first bites that count: survival of first-instar monarchs on milkweeds. Austral Ecol. 26:547–555.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Sergio Rasmann
    • 1
  • M. Daisy Johnson
    • 1
  • Anurag A. Agrawal
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA

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