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Genetic Variation in Primary Metabolites of Pastinaca sativa; Can Herbivores Act as Selective Agents?

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Abstract

Although insect herbivory has been shown to act as a selective agent on plant secondary metabolism, whether primary metabolites contribute to resistance and can respond to selection by herbivores remains untested. In the wild parsnip (Pastinaca sativa), its principal herbivore, Depressaria pastinacella, acts as a selective agent on furanocoumarin resistance factors. In this study, we determined whether webworms can, by causing differential reductions in fitness, act as selective agents on parsnip primary metabolites. Estimates of narrow-sense heritabilities were significantly different from zero for C18 fatty acids in buds and developing fruits, fructose and sorbitol in buds, fructose, myoinositol, bergapten, and psoralen in fruits. Wild parsnips protected from webworms by insecticide produced 2.5 times as much seed biomass as unsprayed plants; that webworms accounted for this difference in plant fitness was indicated by a significant negative relationship between reproductive effort and an index of webworm damage. Only a handful of metabolites influenced resistance to webworms; these included osthol, sorbitol, and protein in developing fruits as well as previously documented furanocoumarins. Osthol, a coumarinic compound, enhanced resistance, as did protein content, while sorbitol lowered resistance. Other primary metabolites may affect resistance to webworms but their effect was context-dependent, that is, their effect depended on concentrations of other metabolites (epistasis). Susceptible plant phenotypes were found to have average chemical compositions. Although there was genetic variation in some of the primary metabolites in parsnips, the epistatic nature of their involvement in resistance and the lack of genetic variation in some suggest that selection on them from webworms will be either inconsistent or ineffective.

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REFERENCES

  • Auclair, J. L., Maltais, J. B., and Cartier, J. J. 1957. Factors in resistance of peas to the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera: Aphididae). II. Amino acids. Can. Entomol. 89:457–464.

    Google Scholar 

  • Aucoin, R. R., Fields, P., Lewis, M. A., PhilogÈne, B. J. R., and Arnason, J. T. 1990. The protective effect of antioxidants to a phototoxin-sensitive insect herbivore, Manduca sexta. J. Chem. Ecol. 16:2913–2924.

    Google Scholar 

  • Axtell, J. D. 1981. Breeding for improved nutritional quality, pp. 365–432, in K. J. Frey (ed.). Plant Breeding II. Iowa State University Press, Ames.

    Google Scholar 

  • Bajaj, K. L., Kaur, G., and Sukhija, B. S. 1980. Chemical composition and some plant characteristics in relation to quality of some promising cultivars of carrot (Daucus carota L.). Qual. Plant Food Hum. Nutr. 30:97–107.

    Google Scholar 

  • Becker, W. A. 1984. Manual of Quantitative Genetics. Academic Enterprises, Pullman, WA.

    Google Scholar 

  • Berenbaum, M. R. 1995. Turnabout is fair play: Secondary roles for primary compounds. J. Chem. Ecol. 21:925–940.

    Google Scholar 

  • Berenbaum, M. R., Zangerl, A. R., and Lee, K. 1989. Chemical barriers to adaptation by a specialist herbivore. Oecologia 80:501–506.

    Google Scholar 

  • Berenbaum, M. R., Zangerl, A. R., and Nitao, J. K. 1986. Constraints of chemical coevolution: Wild parsnips and the parsnip webworm. Evolution 40:1215–1228.

    Google Scholar 

  • Brandle, J. E., Court, W. A., and Roy, R. C. 1993. Heritability of seed yield, oil concentration and oil quality among wild biotypes of Ontario evening primrose. Can. J. Plant. Sci. 73:1067–1070.

    Google Scholar 

  • Caradus, J. R. 1992. Heritability of, and relationships between phosphorus and nitrogen concentration in shoot, stolon and root of white clover (Trifolium repens L.). Plant Soil 146:209–217.

    Google Scholar 

  • Clancy, K. M. 1992. The role of sugars in western spruce budworm nutritional ecology. Ecol. Entomol. 17:189–197.

    Google Scholar 

  • Dreyer, D. L., Jones, K. C., Jurd, L., and Campbell, B. C. 1987. Feeding deterrency of some 4-hydroxycoumarins and related compounds: Relationship to hostplant resistance of alfalfa toward pea aphid (Acrythosiphon pisum). J. Chem. Ecol. 13:925–930.

    Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense. Rec. Adv. Phytochem. 10:1–40.

    Google Scholar 

  • Freeman, R. E. and Simon, P. W. 1983. Evidence for simple genetic control of sugar type in carrot (Daucus carota L.). J. Am. Soc. Hort. Sci. 108:50–54.

    Google Scholar 

  • Gathman, A. C. and Bemis, W. P. 1983. Heritability of fatty acid composition of buffalo gourd seed oil. J. Heredity 74:199–200.

    Google Scholar 

  • Green, E. and Berenbaum, M. R. 1994. Phototoxicity of citral to Trichoplusia ni Lepidoptera: Noctuidae) and its amelioration by vitamin A. Photochem. Photobiol. 60:459–462

    Google Scholar 

  • Hansen, J. L., Viands, D. R., Steffens, J. C., and Sniffen, C. J. 1992. Heritability and improvement of protein and nitrogen concentrations in wilted alfalfa forage. Crop Sci. 32:879–883.

    Google Scholar 

  • Hodges, R. W. 1974. Gelechioidea Oecophoridae, pp. 142, in R. B. Dominick, D. C. Ferguson, J. F. Franclemont, R. R. W. Hodges, and E. G. Munroe (eds.) The Moths of America North of Mexico. Fascicle 6.2. E.W. Classey, London.

    Google Scholar 

  • Janzen, D. H. 1977. How southern cowpea weevil larvae (Bruchidae: Callosobruchus maculatus)die on nonhost seeds. Ecology 58:921–927.

    Google Scholar 

  • Kinman, M. L. 1972. Breeding for lipid and amino acid composition in sunflower. J. Am. Oil. Chem. Soc. 49:36–37.

    Google Scholar 

  • Knowles, P. F. and Mutwakil, A. 1963. Inheritance of low iodine value of safflower selections from India. Econ. Bot. 17:139–145.

    Google Scholar 

  • Kondra, Z. P. and Wilson, T. W. 1976. Selection for oleic, linoleic, and linolenic acid content in F2 populations of rape. Can. J. Plant Sci. 56:961–966.

    Google Scholar 

  • Lundberg, P. and Astrom, M. 1990. Low nutritive quality as a defense against optimally foraging herbivores. Am. Nat. 135:547–562.

    Google Scholar 

  • Maltais, J. B. and Auclair, J. L. 1957. Factors in resistance to the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera:Aphididae). I. The sugar-nitrogen ratio. Can. Entomol. 89:365–370.

    Google Scholar 

  • Mcferson, J. K. and Frey, K. J. 1991. Recurrent selection for protein yield of oat. Crop Sci. 31:1–8.

    Google Scholar 

  • Moran, N. and Hamilton, W. D. 1980. Low nutritive quality as defense against herbivores. J. Theor. Biol. 86:247–254.

    Google Scholar 

  • Moser, H. S. and Frey, K. J. 1993. Effects of S1-recurrent selection for protein yield on seven agronomic traits of oat. Euphytica 70:141–150.

    Google Scholar 

  • Mozafar, A. 1994. Plant Vitamins: Agronomic, Physiological and Nutritional Aspects. CRC Press, Boca Raton, FL.

  • Neuvonen, S. and Haukioja, E. 1984. Low nutritive quality as defence against herbivores: Induced responses in birch. Oecologia 63:71–74.

    Google Scholar 

  • Nitao, J. K. and Zangerl, A. R. 1987. Floral development and chemical defense allocation in wild parsnip (Pastinaca sativa). Ecology 68:521–529.

    Google Scholar 

  • Parrish, J. A. D. and Bazzaz, F. A. 1985. Nutrient content of Abutilon theophrasti seeds and the competitive ability of the resulting plants. Oecologia 65:247–251.

    Google Scholar 

  • Patton, C. A., Ranney, T. G., Burton, J. D., and Walgenbach, J. F. 1997. Natural pest resistance of Prunus taxa to feeding by adult japanese beetles-role of endogenous allelochemicals in host plant resistance. J. Am. Soc. Hort. Sci. 122:668–672.

    Google Scholar 

  • Poehlman, J. M. 1979. Breeding Field Crops, 2nd edn. AVI, Westport, CT.

  • Price, P. W., Bouton, C. E., Mcpheron, B. A., Thompson, J. N., and Weis, A. E. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41–65.

    Google Scholar 

  • Rahman, M. A. and Goodman, P. J. 1983. Effect of seed nitrogen on response to applied nitrogen in six spring barley (Hordeum vulgare L.) cultivars in a glasshouse. Plant Soil 73:203–209.

    Google Scholar 

  • Rhoades, D. F. and Cates, R. G. 1976. Toward a general theory of plant antiherbivore chemistry. Rec. Adv. Phytochem. 10:168–213.

    Google Scholar 

  • Simon, P. W., Peterson, C. E., and Lindsay, R. C. 1982. Genotype, soil, and climate effects on sensory and objective components of carrot flavor. J. Am. Soc. Hort. Sci. 107:644–648.

    Google Scholar 

  • Simpson, S. J. and Simpson, C. L. 1990. The mechanisms of nutritional compensation by phytophagous insects, pp. 111–160, in E. A. Bernays (ed.). Insect-Plant Interactions, Vol. II. CRC Press, Boca Raton.

    Google Scholar 

  • Slansky, F. 1992. Allelochemical-nutrient interactions in herbivore nutritional ecology, pp. 135–174, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores, Their Interactions with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • Slansky, F. and Feeny, P. 1977. Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol. Monogr. 47:209–228.

    Google Scholar 

  • Slansky, F. and Rodriguez, J. G. 1987. Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. Wiley, New York.

    Google Scholar 

  • Slansky, F. and Wheeler, G. S. 1992. Caterpillar's compensatory feeding response to diluted nutrients leads to toxic allelochemical dose. Entomol. Exp. Appl. 65:171–186.

    Google Scholar 

  • Stommel, J. R. and Simon, P. W. 1989. Phenotypic recurrent selection and heritability estimates for total dissolved solids and sugar type in carrot. J. Am. Soc. Hort. Sci. 114:695–699.

    Google Scholar 

  • Sullivan, J. G. and Bliss, F. A. 1983. Recurrent mass selection for increased seed yield and seed protein percentage in the common bean (Phaseolus vulgaris L.) using a selection index. J. Am. Soc. Hort. Sci. 108:42–46.

    Google Scholar 

  • Varis, S. and George, R. A. T. 1985. The influence of mineral nutrition on fruit yield, seed yield and quality in tomato. J. Hort. Sci. 60:373–376.

    Google Scholar 

  • Widstrom, N. W. and Jellum, M. D. 1975. Inheritance of kernel fatty acid composition among six maize inbreds. Crop Sci. 15:44–46

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R. 1990. Furanocoumarin induction in wild parsnip: Genetics and populational variation. Ecology 71:1933–1940.

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R. 1993. Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47–54.

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R. 1997. Cost of chemically defending seeds: Furanocoumarins and Pastinaca sativa. Am. Nat. 150:491–504.

    Google Scholar 

  • Zangerl, A. R., Green, E. S., Lampman, R. L., and Berenbaum, M. R. 1997. Phenological changes in primary and secondary chemistry of reproductive parts in wild parsnip. Phytochemistry 44:825–831.

    Google Scholar 

  • Zangerl, A. R. and Nitao, J. K. 1998. Optimal defence, kin conflict and the distribution of fura-nocoumarins among offspring of wild parsnip. Evol. Ecol. 12:443–457.

    Google Scholar 

  • Zou, J. and Cates, R. G. 1994. Role of Douglas fir (Pseudotsuga menziesii) carbohydrates in resistance to budworm (Choristoneura occidentalis). J. Chem. Ecol. 20:395–405.

    Google Scholar 

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  1. Department of Entomology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin, Urbana, Illinois, 61801, USA

    Arthur R. Zangerl & May R. Berenbaum

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  1. Arthur R. Zangerl
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Zangerl, A.R., Berenbaum, M.R. Genetic Variation in Primary Metabolites of Pastinaca sativa; Can Herbivores Act as Selective Agents?. J Chem Ecol 30, 1985–2002 (2004). https://doi.org/10.1023/B:JOEC.0000045590.28631.00

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