Root herbivores can affect plant fitness, and roots often contain the same secondary metabolites that act as defenses in shoots, but the ecology and evolution of root chemical defense have been little investigated. Here, we investigated genetic variance, heritability, and correlations among defensive phenolic compounds in shoot vs. root tissues of common evening primrose, Oenothera biennis. Across 20 genotypes, there were roughly similar concentrations of total phenolics in shoots vs. roots, but the allocation of particular phenolics to shoots vs. roots varied along a continuum of genotype growth rate. Slow-growing genotypes allocated 2-fold more of the potential pro-oxidant oenothein B to shoots than roots, whereas fast-growing genotypes had roughly equivalent above and belowground concentrations. Phenolic concentrations in both roots and shoots were strongly heritable, with mostly positive patterns of genetic covariation. Nonetheless, there was genotype-specific variation in the presence/absence of two major ellagitannins (oenothein A and its precursor oenothein B), indicating two different chemotypes based on alterations in this chemical pathway. Overall, the presence of strong genetic variation in root defenses suggests ample scope for the evolution of these compounds as defenses against root herbivores.
Allocation Below-ground Chemical defense Growth Phenolics Roots Trade-off
We thank Alex Smith, Marc Johnson, Mike Stastny, Kailen Mooney, Scott McArt, Susan Cook-Patton, Alexis Erwin, Jennifer Thaler, Piia Koskinen, and Marc Lajeunesse for discussions or assisting with field and laboratory work. This work was supported by NSF-DEB 1118783 (A.A.A.).
Carmona, D., Lajeunesse, M. J., and Johnson, M. T. J. 2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25:358–367.CrossRefGoogle Scholar
Johnson, M. T. J. 2011. The contribution of evening primrose (Oenothera biennis) to a modern synthesis of evolutionary ecology. Pol. Ecol. 53:9–21.Google Scholar
Johnson, M. T. J., Agrawal, A. A., Maron, J. L., and Salminen, J. P. 2009. Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. J. Evol. Biol. 22:1295–1307.PubMedCrossRefGoogle Scholar
Kaplan, I., Halitschke, R., Kessler, A., Sardanelli, S., and Denno, R. F. 2008. Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406.PubMedCrossRefGoogle Scholar
Karonen, M., Parker, J. D., Agrawal, A. A., and Salminen, J. P. 2010. First evidence of hexameric and heptameric ellagitannins in plants detected by liquid chromatography/electrospray ionisation mass spectrometry. Rapid Commun. Mass Sp. 24:3151–3156.CrossRefGoogle Scholar
Koricheva, J. 2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190.CrossRefGoogle Scholar
Parker, J. D., Salminen, J. P., and Agrawal, A. A. 2010. Herbivory enhances positive effects of plant genotypic diversity. Ecol. Lett. 13:553–563.PubMedCrossRefGoogle Scholar
Rasmann, S. and Agrawal, A. A. 2008. In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol. 146:875–880.PubMedCrossRefGoogle Scholar
Salminen, J. P. and Karonen, M. 2011. Chemical ecology of tannins and other phenolics: We need a change in approach. Funct. Ecol. 25:325–338.CrossRefGoogle Scholar
Van Dam, N. M. 2009. Belowground herbivory and plant defenses. Annu. Rev. Ecol. Evol. Syst. 40:373–391.CrossRefGoogle Scholar