Abstract
Gall-forming insects induce host plants to form specialized structures (galls) that provide immature life stages of the insect access to host plant nutrients and protection from natural enemies. Feeding by larvae of the Hessian fly (Mayetiola destructor Say) causes susceptible host wheat plants to produce a gall-like nutritive tissue that supports larval growth and development. To determine if changes in host plant free amino acid levels are associated with virulent Biotype L Hessian fly larval feeding, we quantified free amino acid levels in crown tissues of susceptible Newton wheat plants 1, 4, and 7 days after Hessian fly egg hatch. Hessian fly-infested susceptible plants were more responsive than resistant plants or uninfested controls, showing higher concentrations of alanine, glutamic acid, glycine, phenylalanine, proline, and serine 4 days after egg hatch. This 4-day post-hatch time point corresponds to the maturation of nutritive tissue cells in susceptible plants and the onset of rapid larval growth. By 7 days after egg hatch, when virulent second instars are actively feeding on the contents of nutritive tissue cells, the aromatic amino acids phenylalanine and tyrosine were more abundant compared to uninfested controls, but the levels of other free amino acids were no longer elevated. Changes in free amino acid abundance described in this report were associated with increased levels of mRNA encoded by wheat genes involved in amino acid synthesis and transport.
Similar content being viewed by others
References
Behmer, S. T., and Joern, A. 1994. The influence of proline on diet selection: sex-specific feeding preferences by the grasshoppers Ageneotettix deorum and Phoetaliotes nebrascensis (Orthoptera: Acrididae). Oecologia 98:76–82.
Bronner, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids, pp. 118–140, in J. D. Shorthouse, and O. Rohfritsch (eds.). Biology of Insect-Induced Galls Oxford University Press, Oxford.
Bursell, E. 1981. The role of proline in energy metabolism, pp. 135–154, in G. H. Downer (ed.). Energy Metabolism in Insects Plenum Press, New York.
Carter, C., Shafir, S., Yehonatan, L., Palmer, R. G., and Thornburg, R. 2006. A novel role for proline in plant floral nectars. Naturwissenschaften 93:72–79.
Cartwright, W. B., Caldwell, R. M., and Compton, L. E. 1959. Responses of resistant and susceptible wheats to Hessian fly attack. Agron. J. 51:529–531.
Caspi, R., Foerster, H., Fulcher, C. A., Hopkinson, R., Ingraham, J., Kaipa, P., Krummenacker, M., Paley, S., Pick, J., Rhee, S. Y., Tissier, C., Zhang, P., and Karp, P. D. 2006. MetaCyc: a multiorganism database of metabolic pathways and enzymes. Nuc. Acids Res. 34:D511–D516(database issue).
Dindo, M. L., Grenier, S., Sighinolfi, L., and Baronio, P. 2006. Biological and biochemical differences between in vitro- and in vivo-reared Exorista larvarum. Entomol. Exp. Appl. 120:167–174.
Eleftherianos, I., Vamvatsikos, P., Ward, D., and Gravanis, F. 2006. Changes in the levels of plant total phenols and free amino acids induced by two cereal aphids and effects on aphid fecundity. J. Appl. Entomol. 130:15–19.
Flor, H. H. 1955. Host–parasite interaction in flax rust—its genetics and other implications. Phytopathology 45:680–685.
Gäde, G., and Auerswald, L. 2002. Beetle’s choice—proline for energy output: control by AKHs. Comp. Biochem. Physiol. B 132:117–129.
Giovanini, M. P., Puthoff, D. P., Nemacheck, J. A., Mittapalli, O., Saltzmann, K. D., Ohm, H. W., Shukle, R. H., and Williams, C. E. 2006. Gene-for-gene defense of wheat against the Hessian fly lacks a classical oxidative burst. Mol. Plant-Microbe Interact 19:1023–1033.
Giovanini, M. P., Saltzmann, K. D., Puthoff, D. P., Gonzalo, M., Ohm, H. W., and Williams, C. E. 2007. A novel wheat gene encoding a putative chitin-binding lectin is associated with resistance against Hessian fly. Mol. Plant Pathol 8:69–82.
Gruys, K. J., and Sikorski, J. A. 1999. Inhibitors of tryptophan, phenylalanine, and tyrosine biosynthesis as herbicides, pp. 357–384, in B. K. Singh (ed.). Plant Amino Acids: Biochemistry and Biotechnology. New York: Marcel Dekker.
Hare, P. D., and Cress, W. A. 1997. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 21:79–102.
Harris, M. O., Stuart, J. J., Mohan, M., Nair, S., Lamb, R. J., and Rohfritsch, O. 2003. Grasses and gall midges: plant defense and insect adaptation. Annu. Rev. Entomol. 48:549–577.
Harris, M. O., Freeman, T. P., Rohfritsch, O., Anderson, K. G., Payne, S. A., and Moore, J. A. 2006. Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Ann. Entomol. Soc. Am. 99:305–316.
Hatchett, J. H., and Gallun, R. L. 1970. Genetics of the ability of the Hessian fly, Mayetiola destructor, to survive on wheat having different genes for resistance. Ann. Entomol. Soc. Am. 63:1400–1407.
Heady, S. E., Lambert, R. G., and Covell, C. V. Jr. 1982. Determination of free amino acids in larval insect and gall tissues of the goldenrod, Solidago canadensis L. Comp. Biochem. Physiol. B 73:641–644.
Kaloshian, I. 2004. Gene-for-gene disease resistance: Bridging insect pest and pathogen defense. J. Chem. Ecol. 30:2419–2438.
Lam, H.-M., Wong, P., Chan, H.-K., Yam, K.-M., Chen, L., Chow, C.-M., and Coruzzi, G. M. 2003. Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol. 132:926–935.
Liu, X., Bai, J., Huang, L., Zhu, L., Liu, X., Weng, N., Reese, J. C., Harris, M., Stuart, J. J., and Chen, M.-S. 2007. Gene expression of different wheat genotypes during attack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae. J. Chem. Ecol. 33:2171–2194.
Macchi, F. D., Shen, F. J., Keck, R. G., and Harris, R. J. 2000. Amino acid analysis, using postcolumn ninhydrin detection, in a biotechnology laboratory, pp. 9–30, in C. Cooper, N. Packer, and K. Williams (eds.). Methods in Molecular Biology, Vol. 159: Amino Acid Analysis Protocols Humana Press, Totawa, NJ.
McColloch, J. W. 1923. The Hessian fly in Kansas. Kans. Agr. Exp. Sta. Tech. Bul. 11:96.
Meon, S., Fisher, J. M., and Wallace, H. R. 1978. Changes in free proline following infection of plants with either Meloidogyne javanica or Agrobacterium tumefaciens. Physiol. Plant Pathol. 12:251–256.
Ozols, J. 1990. Amino acid analysispp. 587–601, in J. N. Abelson, M. I. Simon, and M. P. Deutscher (eds.). Methods in Enzymology, Vol. 182: Guide to Protein Purification Academic Press, San Diego.
Patterson, F. L., Maas, F. B. III, Foster, J. E., Ratcliffe, R. H., Cambron, S. E., Safranski, G., Taylor, P. L., and Ohm, H. W. 1994. Registration of eight Hessian fly resistant common winter wheat germplasm lines (Carol, Erin, Flynn, Iris, Joy, Karen, Lola, and Molly). Crop Sci. 34:315–316.
Puthoff, D. P., Sardesai, N., Subramanyam, S., Nemacheck, J. A., and Williams, C. E. 2005. Hfr-2, a wheat cytolytic toxin-like gene, is up-regulated by virulent Hessian fly larval feeding. Mol. Plant Pathol. 6:411–423.
Rhodes, D., Verslues, P. E., and Sharp, R. E. 1999. Role of amino acids in abiotic stress resistance, pp. 319–356, in B. K. Singh (ed.). Plant Amino Acids: Biochemistry and Biotechnology Marcel Dekker, New York.
Robinson, R. J., Miller, B. S., Miller, H. L., Mussman, H. C., Johnson, J. A., and Jones, E. 1960. Chloroplast number in leaves of normal wheat plants and those infested with Hessian fly or treated with maleic hydrazine. J. Econom. Entomol. 53:560–566.
Rossomando, E. F. 1990. Ion-Exchange Chromatography, pp. 309–316, in J. N. Abelson, M. I. Simon, and M. P. Deutscher (eds.). Methods in Enzymology, Vol. 182: Guide to Protein Purification Academic Press, San Diego.
Sacktor, B., and Childress, C. C. 1967. Metabolism of proline in insect flight muscle and its significance in stimulating the oxidation of pyruvate. Arch. Biochem. Biophys. 120:583–588.
Sardesai, N., Subramanyam, S., Nemacheck, J., and Williams, C. W. 2005. Modulation of defense-response gene expression in wheat during Hessian fly larval feeding. J. Plant Interact. 1:39–50.
Sandström, J., Telang, A., and Moran, N. A. 2000. Nutritional enhancement of host plants by aphids – a comparison of three aphid species on grasses. J. Insect Physiol. 46:33–40.
Subramanyam, S., Sardesai, N., Puthoff, D., Meyer, J. M., Nemacheck, J. A., Gonzalo, M., and Williams, C. W. 2006. Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci. 170:90–103.
Subramanyam, S., Smith, D. F., Clemens, J. C., Webb, M. A., Sardesai, N., and Williams, C. W. 2008. Hessian fly larvae induce production of HFR-1, a high mannose N-glycan-specific wheat lectin. Plant Physiol. 147, July 2008.
Telang, A., Sandström, J., Dyreson, E., and Moran, N. A. 1999. Feeding damage by Diuraphis noxia results in nutritionally enhanced phloem diet. Entomol. Exp. Appl. 91:403–412.
Tooker, J. F., and De Moraes, C. M. 2007. Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defenses. Ecol. Entomol. 32:153–161.
Verma, D. P. S., and Zhang, C.-S. 1999. Regulation of proline and arginine biosynthesis in plants, pp. 249–265, in B. K. Singh (ed.). Plant Amino Acids: Biochemistry and Biotechnology Marcel Dekker, New York.
Zhu, L., Liu, X., Liu, X., Jeannotte, R., Reese, J. C., Harris, M., Stuart, J. J., and Chen, M.-S. 2008. Hessian fly (Mayetiola destructor) attack causes a dramatic shift in carbon and nitrogen metabolism in wheat. Mol. Plant-Microbe Interact. 21:70–78.
Acknowledgements
This work is a joint contribution by the USDA Agricultural Research Service and Purdue University, was supported by USDA CRIS number 3602-22000-014-00D and is Purdue University agricultural experiment station journal article number 2007-18245. M. P. Giovanini received a research fellowship from the CAPES program (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) at the Ministry of Education of Brazil. The authors thank Dr. Herbert Ohm for providing Newton and H9-Iris wheat seeds, Dr. Subhashree Subramanyam, Jill Nemacheck, and Stephen Baluch for critical reading of the manuscript, Sue Cambron for maintaining Hessian fly stocks, and Jill Nemacheck for assistance with Affymetrix micorarray probe set annotation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Use of commercial or proprietary products to the exclusion of others does not constitute endorsement by the USDA.
Rights and permissions
About this article
Cite this article
Saltzmann, K.D., Giovanini, M.P., Zheng, C. et al. Virulent Hessian Fly Larvae Manipulate the Free Amino Acid Content of Host Wheat Plants. J Chem Ecol 34, 1401–1410 (2008). https://doi.org/10.1007/s10886-008-9544-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-008-9544-x