Journal of Chemical Ecology

, Volume 37, Issue 12, pp 1332–1340 | Cite as

Elevated CO2 Increases Constitutive Phenolics and Trichomes, but Decreases Inducibility of Phenolics in Brassica rapa (Brassicaceae)

Article

Abstract

Increasing global atmospheric CO2 has been shown to affect important plant traits, including constitutive levels of defensive compounds. However, little is known about the effects of elevated CO2 on the inducibility of chemical defenses or on plant mechanical defenses. We grew Brassica rapa (oilseed rape) under ambient and elevated CO2 to determine the effects of elevated CO2 on constitutive levels and inducibility of carbon-based phenolic compounds, and on constitutive trichome densities. Trichome density increased by 57% under elevated CO2. Constitutive levels of simple, complex, and total phenolics also increased under elevated CO2, but inducibility of each decreased. Induction of simple phenolics occurred only under ambient CO2. Although induction of complex and total phenolics occurred under both ambient and elevated CO2, the damage-induced increases were 64% and 75% smaller, respectively, under elevated CO2. Constitutive phenolic levels were positively correlated with leaf C:N ratio, and inducibility was positively correlated with leaf N and negatively correlated with leaf C:N ratio, as would be expected if inducibility were constrained by nitrogen availability under elevated CO2. We conclude that B. rapa is likely to exhibit higher constitutive levels of both chemical and mechanical defenses in the future, but is also likely to be less able to respond to herbivore damage by inducing phenolic defenses. To our knowledge, this is only the second study to report a negative effect of elevated CO2 on the inducibility of any plant defense.

Key Words

Elevated CO2 Inducibility Phenolics Plant defense Trichomes Brassicaceae 

References

  1. Agrell, J., Anderson, P., Oleszek, W., Stochmal, A., and Agrell, C. 2004. Combined effects of elevated CO2 and herbivore damage on alfalfa and cotton. J. Chem. Ecol. 30:2309–2324.PubMedCrossRefGoogle Scholar
  2. Alley, R., Berntsen, T., Bindoff, N., Chen, Z., Chidthaisong, A., Friedlingstein, P., Gregory, J., Hegerl, G., Heimann, M., Hewitson, B., Hoskins, B., Joos, F., Jouzel, J., Kattsov, V., Lohmann, U., Manning, M., Matsuno, T., Molina, M., Nicholls, N., Overpeck, J., Qin, D., Raga, G., Ramaswamy, V., Ren, J., Rusticucci, M., Solomon, S., Somerville, R., Stocker, T., Stott, P., Stouffer, R., Whetton, P., Wood, R., and Wratt, D. 2007. Climate Change 2007: The Physical Science Basis, Summary for Policymakers. Intergovernmental Panel on Climate Change. Paris, France.Google Scholar
  3. Bazin, A., Goverde, M., Erhardt, A., and Shykoff, J. 2002. Influence of atmospheric CO2 enrichment on induced defense and growth compensation after herbivore damage in Lotus corniculatus. Ecol. Entomol. 27:271–278.CrossRefGoogle Scholar
  4. Bidart-Bouzat, M., Mithen, R., and Berenbaum, M. 2005. Elevated CO2 influences herbivory-induced defense responses of Arabidopsis thaliana. Oecologia. 145:415–424.PubMedCrossRefGoogle Scholar
  5. Boege, K. and Marquis, R. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:441–448.PubMedCrossRefGoogle Scholar
  6. Conway, T. and Tans, P. 2011. NOAA/ESRL (www.esrl.noaa.gov/gmd/ccgg/trends/).
  7. Cotrufo, M. F., Ineson, P., and Scott, A. 1998. Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biol. 4:43–54.CrossRefGoogle Scholar
  8. Gayler, S., Grams, T., Heller, W., Treutter, D., and Priesack, E. 2008. A dynamical model of environmental effects on allocation to carbon-based secondary compounds in juvenile trees. Ann. Bot. 101:1089–1098.PubMedCrossRefGoogle Scholar
  9. Ghasemzadeh, A., Jaafar, H., and Rahmat, A. 2010. Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in Malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules. 15:7907–7922.PubMedCrossRefGoogle Scholar
  10. Goverde, M., Erhardt, A., and Stöcklin, J. 2004. Genotype-specific response of a lycaenid herbivore to elevated carbon dioxide and phosphorus availability in calcareous grassland. Oecologia. 139:383–391.PubMedCrossRefGoogle Scholar
  11. Hartley, S., Jones, C., Couper, G., and Jones, T. 2000. Biosynthesis of plant phenolic compounds in elevated atmospheric CO2. Global Change Biol. 6:497–506.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. Haviola, S., Kapari, L., Ossipov, V., Rantala, M., Ruuhola, T., and Haukioja, E. 2007. Foliar phenolics are differently associated with Epirrita autumna growth and immunocompetence. J. Chem. Ecol. 33:1013–1023.PubMedCrossRefGoogle Scholar
  14. Howe, G. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66.Google Scholar
  15. Kaplan, I., Halitschke, R., Kessler, A., Sardanelli, S., and Denno, R. 2008. Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology. 89:392–406. PubMedCrossRefGoogle Scholar
  16. Karban, R. and Baldwin, I. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois, USA.Google Scholar
  17. Karowe, D. 1989. Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant anti-herbivore chemistry. Oecologia. 80:507–512.CrossRefGoogle Scholar
  18. Karowe, D. 2007. Are legume-feeding herbivores buffered against direct effects of elevated CO2 on host plants? A test with the sulfur butterfly, Colias philodice. Global Change Biol. 13:2045–2051.CrossRefGoogle Scholar
  19. Karowe, D., Seimens, D., and Mitchell-Olds, T. 1997. Species-specific response of glucosinolate content to elevated atmospheric CO2. J. Chem. Ecol. 23:2569–2582.CrossRefGoogle Scholar
  20. Lake, J. and Wade, R. 2009. Plant-pathogen interactions and elevated CO2: morphological changes in favour of pathogens. J. Exp. Bot. 60:3123–3131.PubMedCrossRefGoogle Scholar
  21. Lau, J., Strengbom, J., Stone, L., Reich, P., and Tiffin, P. 2008. Direct and indirect effects of CO2, nitrogen, and community diversity on plant-enemy interactions. Ecology. 89:226–236.PubMedCrossRefGoogle Scholar
  22. Lindroth, R. 2010. Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J. Chem. Ecol. 36:2–21.PubMedCrossRefGoogle Scholar
  23. Lindroth, R. and Kinney, K. 1998. Consequences of enriched atmospheric CO2 and defoliation for foliar chemistry and gypsy moth performance. J. Chem. Ecol. 24:1677–1695.CrossRefGoogle Scholar
  24. Littell, R., Henry, P., and Ammerman, C. 1998. Statistical analysis of repeated measures data using SAS procedures. J. Anim. Sci. 76:1216–1231.PubMedGoogle Scholar
  25. Lou, Y. and Baldwin, I. 2004. Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses in Nicotiana attenuata. Plant Physiol. 135:496–506.PubMedCrossRefGoogle Scholar
  26. Marks, M. 1997. Molecular genetic analysis of trichome development in Arabidopsis. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48:137–163.PubMedCrossRefGoogle Scholar
  27. Musser, R., Farmer, E., Peiffer, M., Williams, S., and Felton, G. 2006. Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect-plant interactions. J. Chem. Ecol. 32:981–992.PubMedCrossRefGoogle Scholar
  28. O’neill, B., Zangerl, A., Dermody, O., Bilgin, D., Casteel, C., Zavala, J., Delucia, E., and Berenbaum, M. 2010. Impact of elevated levels of atmospheric CO2 and herbivory on flavonoids of soybean (Glycine max Linnaeus). J. Chem. Ecol. 36:35–45.PubMedCrossRefGoogle Scholar
  29. 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. Sys. Eco. 29:223–240.CrossRefGoogle Scholar
  30. Paoletti, E., Seufert, G., Della Rocca, G., and Thomsen, H. 2007. Photosynthetic responses to elevated CO2 and O3 in Quercus ilex leaves at a natural CO2 spring. Environ. Pollut. 147:516–524.PubMedCrossRefGoogle Scholar
  31. Peñuelas, J., Estiarte, M., and Llusià, J. 1997. Carbon-based secondary compounds at elevated CO2. Photosynthetica. 33:313–316.CrossRefGoogle Scholar
  32. Plett, J., Wilkins, O., Campbell, M., Ralph, S., and Regan, S. 2010. Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth. Plant J. 64:419–432.PubMedCrossRefGoogle Scholar
  33. Pritchard, S., Rogers, H., Prior, S., and Peterson, C. 1999. Elevated CO2 and plant structure: a review. Global Change Biol. 5:807–837.CrossRefGoogle Scholar
  34. Ralph, S., Yueh, H., Friedmann, M., Aeschliman, D., Zeznik, J., Nelson, C., Butterfield, Y., Kirkpatrick, R., Liu, J., Jones, S., Marra, M., Douglas, C., Ritland, K., and Bohlman, J. 2006. Conifer defence against insects: Microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ. 29:1545–1570.PubMedCrossRefGoogle Scholar
  35. Raymer, P. 2002. Canola: An emerging oilseed crop, pp. 122–126, in J. Janick and A. Whipkey (eds.), Trends in New Crops and New Uses. ASHS Press, Alexandria, Virginia, USA.Google Scholar
  36. Reymond, P., Weber, H., Damond, M., and Farmer, E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell. 12:707–719.PubMedCrossRefGoogle Scholar
  37. Riikonen, J., Percy, K., Kivimaenpaa, M., Kubiske, M., Nelson, N., Vapaavuori, E., and Karnosky, D. 2010. Leaf size and surface characteristics of Betula papyrifera exposed to elevated CO2 and O3. Environ. Pollut. 158:1029–1035.PubMedCrossRefGoogle Scholar
  38. Rossi, A., Stiling, P., Moon, D., Cattell, M., and Drake, B. 2004. Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO2. J. Chem. Ecol. 30:1143–1152.PubMedCrossRefGoogle Scholar
  39. Roth, S., Lindroth, R., Volin, J., and Kruger, E. 1998. Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance. Global Change Biol. 4:419–430.CrossRefGoogle Scholar
  40. SAS Institute. 2000. The SAS system for Windows Version 8e. SAS Institute, Cary, North Carolina, USA.Google Scholar
  41. Simmons, A. and Gurr, G. 2005. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric. For. Entomol. 7:265–276.CrossRefGoogle Scholar
  42. Stiling, P. and Cornelissen, T. 2007. How does elevated carbon dioxide (CO2) affect plant-herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biol. 13:1823–1842.CrossRefGoogle Scholar
  43. Traw, M. and Dawson, T. 2002. Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ. Entomol. 31:714–722.CrossRefGoogle Scholar
  44. Tuchman, N., Wahtera, K., Wetzel, R., Russo, N., Kilbane, G., Sasso, L., and Teeri, J. 2003. Nutritional quality of leaf detritus altered by elevated atmospheric CO2: effects on development of mosquito larvae. Freshwater Biol. 48:1432–1439.CrossRefGoogle Scholar
  45. Vannette, R. and Hunter, M. 2011. Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2. Global Change Biol. 17:1277–1288.CrossRefGoogle Scholar
  46. Zavala, J., Casteel, C., Delucia, E., and Berenbaum, M. 2008. Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects. Proc. Natl. Acad. Sci. U. S. A. 105:5129–5133.PubMedCrossRefGoogle Scholar
  47. Zvereva, E. and Kozlov, M. 2006. Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Global Change Biol. 12:27–41CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Biological SciencesWestern Michigan UniversityKalamazooUSA
  2. 2.School of Natural Resources and EnvironmentUniversity of MichiganAnn ArborUSA

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