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Glucosinolate and Trichome Defenses in a Natural Arabidopsis lyrata Population

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Abstract

Glucosinolates (GS) and trichomes contribute to plant resistance against insect herbivores in the model Arabidopsis thaliana. The functional and genetic characteristics of herbivore defense, however, can differ even between closely related species. In a quantitative genetic experiment with the out-crossing perennial Arabidopsis lyrata spp. petraea, we measured constitutive GS composition, trichome density, leaf thickness, and plant resistance in four different herbivore interactions. In a single population of A. lyrata, we found heritable variation for trichome density as well as GS amount and carbon side-chain elongation ratios associated with activity in methylthioalkylmalate synthase (MAM). Unexpectedly, heritabilities for indole GS in A. lyrata were high and less affected by differences in plant age and environment than aliphatic GS. We found significant heritability in plant resistance to the specialist Plutella xylostella and generalist Trichoplusia ni, but not to the specialists Pieris brassicae and Phyllotreta cruciferae. Analyses of phenotypic and genetic correlations between candidate defense traits and insect resistance suggested that A. lyrata resistance was conferred by a combination of indole GS amount and trichome density, and, to a lesser extent, aliphatic GS ratios and leaf thickness. Variation in the most abundant compound, the aliphatic 3-hydroxypropyl GS, had little impact on A. lyrata herbivore resistance. The contribution of defense traits to resistance depended on the experimental herbivory context, and resistances were weakly correlated. A diversified defense strategy is likely to be important for long-lived individuals of A. lyrata that are subject to attack by many different herbivores in nature.

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References

  • Agrawal, A. A. 1999. Induced responses to herbivory in wild radish: Effects on several herbivores and plant fitness. Ecology 80:1713–1723.

    Article  Google Scholar 

  • Agrawal, A. A. 2000. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813.

    Article  Google Scholar 

  • Agrawal, A. and Kurashige, N. 2003. A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J. Chem. Ecol. 29:1403–1415.

    Article  PubMed  CAS  Google Scholar 

  • Agrawal, A. A., Strauss, S. Y., and Stout, M. J. 1999. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–1104.

    Article  Google Scholar 

  • Agrawal, A., Conner, J., Johnson, M., and Wallsgrove, R. 2002. Ecological genetics of an induced plant defense against herbivores: Additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–2213.

    Article  PubMed  Google Scholar 

  • Agren, J. and Schemske, D. W. 1993. The cost of defense against herbivores: An experimental study of trichome production in Brassica rapa. Am. Nat. 141:338–350.

    Article  CAS  PubMed  Google Scholar 

  • Arany, A. M., De Jong, T. J., and Van der Meijden, E. 2005. Herbivory and abiotic factors affecting population dynamics of Arabidopsis thaliana in a sand dune area. Plant Biol. 7:1–7.

    Article  Google Scholar 

  • Bergelson, J. and Purrington, C. B. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536–558.

    Article  Google Scholar 

  • Bert, V., Meerts, P., Saumitou-Laprade, P., Salis, P., Gruber, W., and Verbruggen, N. 2003. Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18.

    Article  CAS  Google Scholar 

  • Brader, G., Tas, E., and Palva, E. T. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol.: 849–860.

  • Brown, P. D., Tokuhisa, J. G., Reichelt, M., and Gershenzon, J. 2003. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth, D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:379–384.

    Article  CAS  Google Scholar 

  • Charmantier, A. and Garant, D. 2005. Environmental quality and evolutionary potential: Lessons from wild populations. Proc. R. Soc. Lond., B Biol. Sci. 272:1415–1425.

    Article  Google Scholar 

  • Charmantier, A., Perrins, C., McCleery, R. H., and Sheldon, B. C. 2006. Age-dependent genetic variance in a life-history trait in the mute swan. Proc. R. Soc. Lond., B Biol. Sci. 273:225–232.

    Article  Google Scholar 

  • Chen, F., D’Auria, J. C., Tholl, D., Ross, J. R., Gershenzon, J., Noel, J. P., and Pichersky, E. 2003. An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36:577–588.

    Article  PubMed  CAS  Google Scholar 

  • Clauss, M. J. and Koch, M. 2006. Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci. 11:449–459.

    Article  PubMed  CAS  Google Scholar 

  • Clauss, M. J. and Mitchell-Olds, T. 2003. Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history. Mol. Ecol. 12:1287–1299.

    Article  PubMed  CAS  Google Scholar 

  • Clauss, M. J. and Mitchell-Olds, T. 2006. Population genetic structure of Arabidopsis lyrata in Europe. Mol. Ecol. 15:2753–2766.

    Article  PubMed  CAS  Google Scholar 

  • Clauss, M. J., Cobban, H., and Mitchell-Olds, T. 2002. Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaceae). Mol. Ecol. 11:591–601.

    Article  PubMed  CAS  Google Scholar 

  • Conner, J. K., Franks, R., and Stewart, C. 2003. Expression of additive genetic variances and covariances for wild radish floral traits: Comparison between field and greenhouse environments. Evolution 57:487–495.

    Article  Google Scholar 

  • Fahey, J. W., Zalcmann, A. T, and Talalay, P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51.

    Article  PubMed  CAS  Google Scholar 

  • Falconer, D. S. 1989. Introduction to Quantitative Genetics, 3rd edn. Longman, NY, USA.

  • Giamoustaris, A. and Mithen, R. 1996. Genetics of aliphatic glucosinolates. IV. Side-chain modification in Brassica oleracea. Theor. Appl. Genet. 93:1006–1010.

    Article  CAS  Google Scholar 

  • Grubb, C. D. and Abel, S. 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11:89–100.

    Article  PubMed  CAS  Google Scholar 

  • Hauser, M. T., Harr, B., and Schlotterer, C. 2001. Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: Molecular analysis of the candidate gene GLABROUS1. Mol. Biol. Evol. 18:1754–1763.

    PubMed  CAS  Google Scholar 

  • Heidel, A., Clauss, M., Kroymann, J., Savolainen, O., and Mitchell-Olds, T. 2006. Natural variation in MAM within and between populations of Arabidopsis lyrata determines glucosinolate phenotype. Genetics 173:1629–1636.

    Article  PubMed  CAS  Google Scholar 

  • Hogge, L. R., Reed, D. W., Underhill, E. W., and Haughn, G. W. 1988. HPLC separation of glucosinolates from leaves and seeds of Arabidopsis thaliana and their identification using thermospray liquid chromatography-mass spectrometry. J. Chrom. Sci. 26:551–556.

    CAS  Google Scholar 

  • Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics. 6:65–70.

    Google Scholar 

  • Hopkins, R. J., Griffiths, D. W., Birch, A. N. E., and McKinlay, R. G. 1998. Influence of increasing herbivore pressure on modification of glucosinolate content of swedes (Brassica napus spp. rapifera). J. Chem. Ecol. 24:2003–2019.

    Article  CAS  Google Scholar 

  • Hougen-Eitzman, D. and Rausher, M. 1994. Interactions between herbivorous insects and plant–insect coevolution. Am. Nat. 143:677–697.

    Article  Google Scholar 

  • Jander, G., Cui, J., Nhan, B., Pierce, N. E., and Ausubel, F. M. 2001. The TASTY locus on chromosome 1 of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni. Plant Physiol. 126:890–898.

    Article  PubMed  CAS  Google Scholar 

  • Karkkainen, K. and Agren, J. 2002. Genetic basis of trichome production in Arabidopsis lyrata. Hereditas 136:219–226.

    Article  PubMed  Google Scholar 

  • Karkkainen, K., Loe, G., and Agren, J. 2004. Population structure in Arabidopsis lyrata: Evidence for divergent selection on trichome production. Evolution 58:2831–2836.

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein, D. J., Gershenzon, J., and Mitchell-Olds, T. 2001a. Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159:359–370.

    PubMed  CAS  Google Scholar 

  • Kliebenstein, D. J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J., and Mitchell-Olds, T. 2001b. Genetic control of natural variation in Arabidopsis thaliana glucosinolate accumulation. Plant Physiol. 126:811–825.

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein, D. J., Lambrix, V. M., Reichelt, M., Gershenzon, J., and Mitchell-Olds, T. 2001c. Gene duplication in the diversification of secondary metabolism: Tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:681–693.

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein, D. J., Pedersen, D., Barker, B., and Mitchell-Olds, T. 2002. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161:325–332.

    PubMed  CAS  Google Scholar 

  • Kliebenstein, D. J., Kroymann, J., and Mitchell-Olds, T. 2005. The glucosinolate–myrosinase system in an ecological and evolutionary context. Curr. Opin. Plant Biol. 8:264–271.

    Article  PubMed  CAS  Google Scholar 

  • Koch, M., Haubold, B., and Mitchell-Olds, T. 2001. Molecular systematics of the Brassicaceae: Evidence from coding plastidic matK and nuclear Chs sequences. Am. J. Bot. 88:534–544.

    PubMed  CAS  Google Scholar 

  • Koornneef, M., Alonso-Blanco, C., and Vreugdenhil, D. 2004. Naturally occurring genetic variation in Arabidopsis thaliana. Annu. Rev. Plant Biol. 55:141–172.

    Article  PubMed  CAS  Google Scholar 

  • Kroymann, J., Textor, S., Tokuhisa, J. G., Falk, K. L., Bartram, S., Gershenzon, J., and Mitchell-Olds, T. 2001. A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol. 127:1077–1088.

    Article  PubMed  CAS  Google Scholar 

  • Kroymann, J., Donnerhacke, S., Schnabelrauch, D., and Mitchell-Olds, T. 2003. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl. Acad. Sci. U. S. A. 1073:1–10.

    Google Scholar 

  • Lambdon, P. W., Hassall, M., Boar, R. R., and Mithen, R. 2003. Asynchrony in the nitrogen and glucosinolate leaf-age profiles of Brassica: Is this a defensive strategy against generalist herbivores? Agric. Ecosyst. Environ. 97:205–214.

    Article  CAS  Google Scholar 

  • Lambrix, V., Reichelt, M., Mitchell-Olds, T., Kliebenstein, D. J., and Gershenzon, J. 2001. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13:2793–2807.

    Article  PubMed  CAS  Google Scholar 

  • Littell, R., Milliken, G., Stroup, W., and Wolfinger, R. 1996. SAS System for Mixed Models. SAS Institute, Cary, NC, USA.

  • LØe, G. 2006. Ecology and evolution of resistance to herbivory: Trichome production in Arabidopsis lyrata. Ph.D. dissertation, Uppsala University, Sweden.

  • Mauricio, R. 1998. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am. Nat. 151:20–28.

    Article  CAS  PubMed  Google Scholar 

  • Mauricio, R. and Rausher, M. D. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444.

    Article  Google Scholar 

  • Mauricio, R., Stahl, E. A., Korves, T., Tian, D., Kreitman, M., and Bergelson, J. 2003. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163:735–746.

    PubMed  CAS  Google Scholar 

  • Mikkelsen, M. D., Petersen, B. L., Glawischnig, E., Jensen, A. B., Andreasson, E., and Halkier, B. A. 2003. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 131:298–308.

    Article  PubMed  CAS  Google Scholar 

  • Nasrallah, M. E., Liu, P., and Nasrallah, J. B. 2002. Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata. Science 297:247–249.

    Article  PubMed  CAS  Google Scholar 

  • O’Kane, S. L. and Al-Shehbaz, I. A. 1997. A synopsis of Arabidopsis (Brassicaceae). Novon 7:323–327.

    Article  Google Scholar 

  • Pilson, D. 1996. Two herbivores and constraints on selection for resistance in Brassica rapa. Evolution 50:1492–1500.

    Article  Google Scholar 

  • Rask, L., Andreasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., and Meijer, J. 2000. Myrosinase: Gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42:93–113.

    Article  PubMed  CAS  Google Scholar 

  • Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T., and Kroymann, J. 2002. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. U. S. A. 99:11223–11228.

    Article  PubMed  CAS  Google Scholar 

  • Raybould, A. F. and Moyes, C. L. 2001. The ecological genetics of aliphatic glucosinolates. Heredity 87:383–391.

    Article  PubMed  CAS  Google Scholar 

  • Reichelt, M., Brown, P. D., Schneider, B., Oldham, N. J., Stauber, E., Tokuhisa, J., Kliebenstein, D. J., Mitchell-Olds, T., and Gershenzon, J. 2002. Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59:663–671.

    Article  PubMed  CAS  Google Scholar 

  • Renwick, J. A. A. 2002. The chemical world of crucivores: Lures, treats and traps. Entomol. Exp. Appl. 104:35–42.

    Article  CAS  Google Scholar 

  • Renwick, J. A. A. and Lopez, K. 1999. Experience-based food consumption by larvae of Pieris rapae: Addiction to glucosinolates? Entomol. Exp. Appl. 91:51–58.

    Article  CAS  Google Scholar 

  • Reymond, P., Bodenhausen, N., Van Poecke, R. M. P., Krishnamurthy, 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 

  • Rotem, K., Agrawal, A. A., and Kott, L. 2003. Parental effects in Pieris rapae in response to variation in food quality: Adaptive plasticity across generations? Ecol. Entomol. 28:211–218.

    Article  Google Scholar 

  • Shelton, A. M., Cooley, R. J., Kroening, M. K., Wilsey, W. T., and Eigenbrode, S. D. 1991. Comparative analysis of two rearing procedures for diamond-back moth (Lepidoptera: Plutellidae). J. Entomol. Sci. 26:17–26.

    Google Scholar 

  • Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M., and Bergelson, J. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667–671.

    Article  PubMed  CAS  Google Scholar 

  • Strauss, S. Y., Watson, W., and Allen, M. T. 2003. Predictors of male and female tolerance to insect herbivory in Raphanus raphanistrum. Ecology 84:2074–2082.

    Google Scholar 

  • Symonds, V. V., Godoy, A. V., Alconada, T., Botto, J. F., Juenger, T. E., Casal, J. J., and Lloyd, A. M. 2005. Mapping quantitative trait loci in multiple populations of Arabidopsis thaliana identifies natural allelic variation for trichome density. Genetics 169:1649–1658.

    Article  PubMed  CAS  Google Scholar 

  • Traw, M. B. 2002. Is induction response negatively correlated with constitutive resistance in black mustard? Evolution 56:2196–2205.

    Article  PubMed  Google Scholar 

  • Traw, M. B. and Dawson, T. E. 2002a. Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532.

    Article  Google Scholar 

  • Traw, M. B. and Dawson, T. E. 2002b. Reduced performance of two specialist herbivores (Lepidoptera : Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ. Entomol. 31:714–722.

    Article  Google Scholar 

  • Weinig, C., Stinchcombe, J. R., and Schmitt, J. 2003a. Evolutionary genetics of resistance and tolerance to natural herbivory in Arabidopsis thaliana. Evolution 57:1270–1280.

    Article  PubMed  Google Scholar 

  • Weinig, C., Stinchcombe, J. R., and Schmitt, J. 2003b. QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments. Mol. Ecol. 12:1153–1163.

    Article  PubMed  CAS  Google Scholar 

  • Windsor, A. J., Reichelt, M., Figuth, A., Svatos, A., Kroymann, J., Kliebenstein, D. J., Gershenzon, J., and Mitchell-Olds, T. 2005. Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66:1321–1333.

    Article  PubMed  CAS  Google Scholar 

  • Wittstock, U. and Halkier, B. A. 2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7:263–270.

    Article  PubMed  CAS  Google Scholar 

  • Wittstock, U., Agerbirk, N., Stauber, E. J., Olsen, C. E., Hippler, M., Mitchell-Olds, T., Gershenson, J., and Vogel, H. 2004. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc. Natl. Acad. Sci. USA. 101:4859–4864.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank D. Kliebenstein, M. Reichelt and A. Figuth for technical advice, and J. Bishop and J. DeMeaux for helpful comment on an earlier version of the manuscript. Financial support was provided by the Max-Planck Gesellschaft.

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  1. Thomas Mitchell-Olds

    Present address: Department of Biology, Duke University, Durham, NC, 27708, USA

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  1. Max Planck Institute of Chemical Ecology, 07745, Jena, Germany

    Maria J. Clauss, Sylke Dietel, Grit Schubert & Thomas Mitchell-Olds

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  1. Maria J. Clauss
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Clauss, M.J., Dietel, S., Schubert, G. et al. Glucosinolate and Trichome Defenses in a Natural Arabidopsis lyrata Population. J Chem Ecol 32, 2351–2373 (2006). https://doi.org/10.1007/s10886-006-9150-8

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