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Patterns of Phytochemical Variation in Mimulus guttatus (Yellow Monkeyflower)

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Abstract

The search for general patterns in the production and allocation of plant defense traits will be facilitated by characterizing multivariate suites of defense, as well as by studying additional plant taxa, particularly those with available genomic resources. Here, we investigated patterns of genetic variation in phytochemical defenses (phenylpropanoid glycosides, PPGs) in Mimulus guttatus (yellow monkeyflower). We grew plants derived from several natural populations, consisting of multiple full-sibling families within each population, in a common greenhouse environment. We found substantial variation in the constitutive multivariate PPG phenotype and in constitutive levels of individual phytochemicals within plants (among leaves of different ages), within populations (among full-sibling families), and among populations. Populations consisting of annual plants generally, but not always, had lower concentrations of phytochemicals than did populations of perennial plants. Populations differed in their plastic response to artificial herbivory, both in the overall multivariate PPG phenotype and in the individual phytochemicals. The relationship between phytochemistry and another defense trait, trichomes, differed among populations. Finally, we demonstrated that one of the PPGs, verbascoside, acts as a feeding stimulant rather than a feeding deterrent for a specialist herbivore of M. guttatus, the buckeye caterpillar (Junonia coenia Nymphalidae). Given its available genetic resources, numerous, easily accessible natural populations, and patterns of genetic variation highlighted in this research, M. guttatus provides an ideal model system in which to test ecological and evolutionary theories of plant-herbivore interactions.

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References

  • Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85.

    Article  Google Scholar 

  • Agrawal, A. A. and Fishbein, M. 2006. Plant defense syndromes. Ecology 87:S132–S149.

    Article  PubMed  Google Scholar 

  • Agrawal, A. A., Salminen, J.-H., and Fishbein, M. 2009. Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution 63:663–673.

    Article  PubMed  CAS  Google Scholar 

  • Ali, J. G. and Agrawal, A. A. 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17:293–302.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, J. T. and Mitchell-Olds, T. 2011. Ecological genetics and genomics of plant defenses: evidence and approaches. Funct. Ecol. 25:312–324.

    Article  PubMed  Google Scholar 

  • Barton, K. E. and Koricheva, J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 175:481–493.

    Article  PubMed  Google Scholar 

  • Beardsley, P. M. and Olmstead, R. G. 2002. Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma. Am. J. Bot. 89:1093–1102.

    Article  PubMed  Google Scholar 

  • Becerra, J. X., Noge, K., and Venable, D. L. 2009. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proc. Natl. Acad. Sci. U. S. A. 106:18062–18066.

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. 2008. Facing the future of plant-insect interaction research: Le retour a` la “raison d'être.”. Plant Physiol. 146:804–811.

    Article  PubMed  CAS  Google Scholar 

  • Boege, K. and Marquis, R. J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:441–448.

    Article  PubMed  Google Scholar 

  • Bowers, M. D. 1984. Iridoid glycosides and host-plant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567–1577.

    Article  CAS  Google Scholar 

  • Bowers, M. D. and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14:319–334.

    Article  CAS  Google Scholar 

  • Camara, M. D. 1997. Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable? J. Chem. Ecol. 23:2093–2106.

    Article  CAS  Google Scholar 

  • Carmona, D., Lajeunesse, M. J., and Johnson, M. T. J. 2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25:358–357.

    Article  Google Scholar 

  • Carr, D. E. and Eubanks, M. D. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Schrophulariaceae). Evolution 56:22–30.

    PubMed  Google Scholar 

  • Carroll, M. J., Zangerl, A. R., and Berenbaum, M. R. 2000. Heritability estimates for octyl acetate and octyl butyrate in the mature fruit of the wild parsnip. J. Hered. 91:68–71.

    Article  PubMed  CAS  Google Scholar 

  • Clauss, M. J., Dietel, S., Schubert, G., and Mitchell-Olds, T. 2006. Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. J. Chem. Ecol. 32:2351–2373.

    Article  PubMed  CAS  Google Scholar 

  • Diezel, C., Ailmann, S., and Baldwin, I. T. 2011. Mechanisms of optimal defense patterns in Nicotiana attenuate: flowering attenuates herbivory-elicted ethylene and jasmonate signaling. J. Int. Plant Biol. 53:971–983.

    Article  CAS  Google Scholar 

  • Falconer, D. F. and Mackay, T. F. C. 1996. Introduction to Quantitative Genetics, 4th ed. Longman Group Ltd, England.

    Google Scholar 

  • Fenster, C. B. and Ritland, K. 1994. Quantitative genetics of mating system divergence in the yellow monkeyflower species complex. Heredity 73:422–435.

    Article  Google Scholar 

  • Franzyk, H., Husum, T. L., and Jensen, S. R. 1998. A caffeoyl phenylethanoid glycoside from Plantago myosuros. Phytochemistry 47:1161–1162.

    CAS  Google Scholar 

  • Geber, M. A. and Griffen, L. R. 2003. Inheritance and natural selection on functional traits. Int. J. Plant Sci. 164:S21–S42.

    Article  Google Scholar 

  • Hakes, A. S. and Cronin, J. T. 2011. Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): genetic variability, costs, and selection for multiple traits. Am. J. Bot. 98:1445–1455.

    Article  Google Scholar 

  • Hall, M. C. and Willis, J. H. 2006. Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60:2466–2477.

    PubMed  Google Scholar 

  • Harborne, J. B. 1993. Introduction to Ecological Biochemistry, 4th ed. Academic, London.

    Google Scholar 

  • Hegnauer, R. and Kooiman, P. 1978. Taxonomic significance of iridoids of Tubiflorae sensu Wettstein. Planta Med. 33:1–33.

    Article  PubMed  CAS  Google Scholar 

  • Hjältén, J. 2004. Simulating herbivory: problems and possibilities, pp. 243–255, in W. W. Weisser and E. Siemann (eds.), Ecological Studies-Analysis and Synthesis, Vol. 173. Springer-Verlag Press, Berlin.

    Google Scholar 

  • Holeski, L. M. 2007. Within and between generation variation in trichome density of Mimulus guttatus. J. Evol. Biol. 20:2092–2100.

    Article  PubMed  CAS  Google Scholar 

  • Holeski, L. M., Chase-alone, R., and Kelly, J. K. 2010. The genetics of phenotypic plasticity in plant defense: trichome production in Mimulus guttatus. Am. Nat. 175:391–400.

    Article  PubMed  Google Scholar 

  • Ivey, C. T., Carr, D. E., and Eubanks, M. D. 2009. Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus. Heredity 102:303–311.

    Article  PubMed  CAS  Google Scholar 

  • Kelly, J. K. and Arathi, H. S. 2003. Inbreeding and the genetic variance in floral traits of Mimulus guttatus. Heredity 90:77–83.

    Article  PubMed  CAS  Google Scholar 

  • Koricheva, J. 1999. Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 119:467–473.

    Article  Google Scholar 

  • Kruskal, J. B. 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–26.

    Article  Google Scholar 

  • Kursar, T. A. and Coley, P. D. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochem. Syst. Ecol. 8:929–949.

    Article  Google Scholar 

  • Lekberg, Y., Roskilly, B., Hendrick, M. F., Zabinkski, C. A., Barr, C. M., and Fishman, L. 2012. Phenotypic and genetic differentiation among yellow monkeyflower populations from thermal and non-thermal soils in Yellowstone National Park. Oecologia 170:111–122.

    Article  PubMed  Google Scholar 

  • Levine, J. M. 1999. Indirect facilitation: evidence and predictions from a riparian community. Ecology 80:1762–1769.

    Article  Google Scholar 

  • Levine, J. M. 2000. Local interactions, dispersal, and native and exotic plant diversity along a California stream. Oikos 95:397–408.

    Article  Google Scholar 

  • Mitchell-Olds, T. 2001. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16:693–700.

    Article  Google Scholar 

  • Mølgaard, P. 1986. Population genetics and geographical distribution of caffeic acid esters in leaves of Plantago major in Denmark. J. Ecol. 74:1127–1137.

    Article  Google Scholar 

  • Mølgaard, P. and Ravn, H. 1988. Evolutionary aspects of caffeoyl ester distribution in dicotyledons. Phytochemistry 27:2411–2421.

    Article  Google Scholar 

  • Mousseau, T. A. and ROFF, D. A. 1987. Natural selection and the heritability of fitness components. Heredity 59:181–197.

    Article  PubMed  Google Scholar 

  • Rausher, M. D. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12:212–217.

    Article  PubMed  CAS  Google Scholar 

  • Reymond, P., Bodenhausen, N., van Poecke, R. M. P., Krisnamurthy, V., Dicke, M., and Farmer, E. E. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.

    Article  PubMed  CAS  Google Scholar 

  • Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., and Manners, J. M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. U. S. A. 97:11655–11660.

    Article  PubMed  CAS  Google Scholar 

  • Stamp, N. 2003. Out of the quagmire of plant defense hypotheses. Quant. Rev. Biol. 78:23–55.

    Article  Google Scholar 

  • Stotz, H. U., Kroymann, J., and Mitchell-Olds, T. 1999. Plant-insect interactions. Curr. Opin. Plant Biol. 2:268–272.

    Article  PubMed  CAS  Google Scholar 

  • Tian, D., Peiffer, M., Shoemaker, E., Tooker, J., Haubruge, E., Francis, F., Luthe, D. S., and Felton, D. W. 2012. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168.

    Article  PubMed  CAS  Google Scholar 

  • van der Meijden, E., Wijn, M., and Verkaar, H. J. 1988. Defense and regrowth: alternative plant strategies in the struggle against herbivores. Oikos 51:355–363.

    Article  Google Scholar 

  • van der Putten, W. H. 2003. Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280.

    Article  Google Scholar 

  • Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W., and Willis, J. H. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100:220–230.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the Mimulus seed library (Duke University) and D. Lowry who generously provided some of the seeds used in this study. Thanks to E. Lewis and M. Crossley for help with sample processing and M. Arntz and R. Ecker for laboratory assistance. We are grateful for comments by several anonymous reviewers and J. Couture that substantially improved this manuscript. Z. HarnEnz was funded through the IBS-SRP (Integrated Biological Sciences Summer Research Program) at the University of Wisconsin, Madison. This work was supported in part by the National Science Foundation (grant numbers FIBR-0425908, DEB-0841609).

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Authors and Affiliations

  1. Department of Entomology, University of Wisconsin, Madison, WI, 53706, USA

    Liza M. Holeski, Ken Keefover-Ring, Zoe T. Harnenz & Richard L. Lindroth

  2. Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, 90187, Sweden

    Ken Keefover-Ring

  3. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    M. Deane Bowers

  4. Integrated Biological Sciences Summer Research Program, University of Wisconsin, Madison, WI, 53706, USA

    Zoe T. Harnenz

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  1. Liza M. Holeski
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Correspondence to Liza M. Holeski.

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Holeski, L.M., Keefover-Ring, K., Bowers, M.D. et al. Patterns of Phytochemical Variation in Mimulus guttatus (Yellow Monkeyflower). J Chem Ecol 39, 525–536 (2013). https://doi.org/10.1007/s10886-013-0270-7

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