Abstract
Wheat and its relatives possess a number of resistance (R) genes specific for the Hessian fly (HF) [Mayetiola destructor (Say)]. HF populations overcome R gene resistance by evolving virulence. Virulent HF larvae manipulate the plant to produce a nutritionally enhanced feeding tissue and, probably, also suppress plant defense responses. Using two wheat R genes, H9 and H13, and three HF strains (biotypes) differing in virulence for H9 and H13, we conducted a genome-wide transcriptional analysis of gene expression during compatible interactions with virulent larvae and incompatible interactions with avirulent larvae. During both types of interactions, a large number of genes (>1,000) showed alterations in gene expression. Analysis of genes with known functions revealed that major targets for differential regulation were genes that encoded defense proteins or enzymes involved in the phenylpropanoid, cell wall, and lipid metabolism pathways. A combination of the enhancement of antibiosis defense, the evasion of nutrient metabolism induction, and the fortification and expansion of the cell wall are likely the collective mechanism for host-plant resistance observed during incompatible interactions. To overcome this resistance, virulent larvae appeared to suppress antibiosis defense while inducing nutrient metabolism, weakening cell wall, and inhibiting plant growth.
Similar content being viewed by others
References
Aarts, M. G. M., Keijzer, C. J., Stiekema, W. J., and Pereira, A. 1995. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127.
Anderson, K. G., and Harris, M. O. 2006. Does R gene resistance allow wheat to prevent plant growth effects associated with Hessian fly (Diptera: Cecidomyiidae) attack? J. Econ. Entomol. 99:1842–1853.
Berzonsky, W. A., Ding, H., Haley, S. D., Harris, M. O., Lamb, R. J., Mckenzie, R. I. H., Ohm, H. W., Patterson, F. L., Peairs, F., Porter, D. R., atcliffe, R. H., and Shanower, T. G. 2003. Breeding wheat for resistance to insects. Plant Breed. Rev. 22:221–296.
Bhattarai, K. K., Xie, Q. G., Pourshalimi, D., Younglove, T., and Kaloshian, I. 2007. Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Mol. Plant Micro. Interact. 20:276–282.
Byers, R. A., and Gallun, R. L. 1972. Ability of the Hessian fly to stunt winter wheat. I: effect of larval feeding on elongation of leaves. J. Econ. Entomol. 65:955–958.
Cook, R. J. 1998. The molecular mechanisms responsible for resistance in plant–pathogen interactions of the gene-for-gene type function more broadly than previously imagined. Proc. Natl. Acad. Sci. U.S.A. 95:9711–9712.
Chen, M. S., Fellers, J. P., Stuart, J. J., eese, J. C., and Liu, X.-M. 2004. A group of related cDNAs encoding secreted proteins from Hessian fly [Mayetiola destructor (Say)] salivary glands. Insect Mol. Biol. 13:101–108.
Chen, M. S., Fellers, J. P., Zhu, Y. C., Stuart, J. J., Hulbert, S., El-Bouhssini, M., and Liu, X.-M. 2006. A super-family of genes coding for secreted salivary gland proteins from the Hessian fly, Mayetiola destructor. J. Insect Sci. 6:12 (http://www.insectscience.org/6.12/).
Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Host–microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803–814.
Cosgrove, D. J. 2003. Expansion of the plant cell wall. Annual Plant Rev. 8:237–258.
Davin, L. B., and Lewis, N. G. 2005. Dirigent phenoxy radical coupling: advances and challenges. Curr. Opin. Biotechnol. 16:398–406.
Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., and eddy, M. S. S. 2002. The phenylpropanoid pathway and plant defence—a genomics perspective. Mol. Plant Pathol. 3:371–390.
Dodds, P. N., Lawrence, G. J., Catanzariti, A. M., The, T., Wang, C. I. A., Ayliffe, M. A., Kobe, B., and Ellis, J. G. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103:8888–8893.
Dogimont, C., Bendahmane, A., Pauquet, J., Burget, E., Desloire, S., Hagen, L., Caboche, M., and Pitrat, M. 2003. Map-based cloning of the Vat gene confers resistance to both aphid colonization and virus transmission. In Proceedings of the 11th International Congress on Molecular Plant–Microbe Interactions, July 2003, St. Petersburg, Russia.
Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95:14863–14868.
Ferre, H., Broberg, A., Duus, J. O., and Thomsen, K. K. 2000. A novel type of arabinoxylan arabinofuranohydrolase isolated from germinated barley: analysis of substrate preference and specificity by nano-probe NMR. Eur. J. Biochem. 267:6633–6641.
Flor, H. H. 1955. Host–parasite interaction in flax rust: its genetics and other implication. Phytopathology 42:680–685.
Garcia-Brugger, A., Lamotte, O., Vandelle, E., Bourque, S., Lecourieux, D., Poinssot, B., Wendehenne, D., and Pugin, A. 2006. Early signaling events induced by elicitor of plant defenses. Mol. Plant Microbe Interact. 19:711–724.
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.
Goggin, F. L., Williamson, V. M., and Ullman, D. E. 2001. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environ. Entomol. 30:101–106.
Goggin, F. L., Shah, G., Williamson, V. M., and Ullman, D. E. 2004. Developmental regulation of Mi-mediated aphid resistance is independent of Mi-1.2 transcript levels. Mol. Plant Micro. Interact. 17:532–536.
Goggin, F. L., Jia, L., Shah, G., Hebert, S., Williamson, V. M., and Ullman, D. E. 2006. Heterologous expression of the Mi-1.2 gene from tomato confers resistance against nematodes but not aphids in eggplant. Mol. Plant Micro. Interact. 19:383–388.
Hammond-Kosack, K. E., and Jones, J. D. G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791.
Harris, M. O., Stuart, J. J., Mohan, M., Nair, S., Lamb, R. J., and ohfritsch, O. 2003. Grasses and gall midges: plant defense and insect adaptation. Ann. Rev. Entomol. 48:549–577.
Harris, M. O., Freeman, T. P., ohfritsch, 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 wheats having different genes for resistance. Ann. Entomol. Soc. Am. 63:1400–1407.
Hatchett, J. H., Kreitner, G. L., and Elzinga, R. J. 1990. Larval mouthparts and feeding mechanism of the Hessian fly (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 83:1137–1147.
Iwai, H., Masaoka, N., Ishii, T., and Satoh, S. 2002. A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem. Proc. Natl. Acad. Sci. U.S.A. 99:16319–16324.
Jang, C. S., Kim, J. Y., Haam, J. W., Lee, M. S., Kim, D. S., Li, Y. W., and Seo, Y. W. 2003. Expressed sequence tags from a wheat-rye translocation line (2BS/2RL) infested by larvae of Hessian fly [Mayetiola destructor (Say)]. Plant Cell Rep. 22:150–158.
Kalashian, I. 2004. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30:2419–2438.
Kaloshian, I., and Walling, L. L. 2005. Hemipterans as plant pathogens. Ann. Rev. Phytopathol. 43:491–521.
Kaygun, H., and Marzluff, W. F. 2005. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 12:794–800.
Keen, N. T. 1990. Gene-for gene complementarity in plant–pathogen interactions. Ann. Rev. Genet. 24:447–463.
Kobayashi, I., and Hakuno, H. 2003. Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta. 217:340–345.
Kobayashi, Y., Kobayashi, I., Fuaki, Y., Fujimoto, S., Takemoto, T., and Kunoh, H. 1997. Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J. 11:525–537.
Liu, X. M., Fritz, A. K., eese, J. C., Wilde, G. E., Gill, B. S., and Chen, M. S. 2005a. H9, H10, and H11 compose a cluster of Hessian fly-resistance genes in the distal gene-rich region of wheat chromosome 1AS. Theor. Appl. Genet. 110:1473–1480.
Liu, X. M., Gill, B. S., and Chen, M. S. 2005b. Hessian fly resistance gene H13 is mapped to a distal cluster of R genes in chromosome 6DS of wheat. Theor. Appl. Genet. 111:243–249.
Liu, X. M., Fellers, J. P., Zhu, Y. C., Mutti, N. S., El-Bouhssini, M., and Chen, M. S. 2006. Cloning and characterization of cDNAs encoding carboxypeptidase-like proteins from the gut of Hessian fly [Mayetiola destructor (Say)] larvae. Insect Biochem. Mol. Biol. 36:665–673.
Lobo, N. F., Behura, S. K., Aggarwal, R., Chen, M. S., Collins, F. H., and Stuart, J. J. 2006. Genomic analysis of a 1 Mb region near the telomere of Hessian fly chromosome X2 and avirulence gene vH13. BMC Genomics 7:7.
Martin, G. B., Bogdanove, A. J., and Sessa, G. 2003. Understanding the functions of plant disease resistance proteins. Ann. Rev. Plant Biol. 54:23–61.
Milligan, S. B., Bordeau, J., Yaghoobi, J., Kaloshian, I., and Williamson, V. M. 1998. The root-knot nematode resistance gene Mi from tomato is a member of leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319.
Moreno, J., Altabella, T., and Maarten, J. 1990. Characterization of α-amylase-inhibitor, a lectin-like protein in the seeds of Phaseolus vulgaris. Plant Physiol. 92:703–709.
Murdock, L. L., Shade, R. E., and Pomeroy, M. A. 1988. Effects of E-64, a cysteine proteinase-inhibitor, on cowpea weevil growth, development, and fecundity. Environ. Entomol. 17:467–469.
Natella, F., Nardini, M., Felice, M. D., and Scaccini, C. 1999. Benzoic and cinnamic acid derivatives as antioxidants: structure-activity relation. J. Agric. Food Chem. 47:1453–1459.
Nimchuk, Z., Eulgem, T., Holt, B. F. III, and Dangl, J. L. 2003. Recognition and response in the plant immune system. Ann. Rev. Genet. 37:579–609.
Nombela, G., Williamson, V. M., and Muniz, M. 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Benisia tabaci. Mol. Plant Micro. Interact. 16:645–649.
Panda, N., and Khush, G. S. 1995. Host plant resistance to insects. CAB Int., Wallingford, UK.
Patterson, F. L., Mass, F. B. III, Foster, J. E., atcliffe, R. H., Cambron, S., 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.
Perrin, R. M., Derocher, A. E., Bar-Peled, M., Zeng, W., Norambuena, L., Orellana, A., aikhle, N. V., and Keegstra, K. 1999. Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284:1976–1979.
Peumans, W. J., and Van Damme, E. J. M. 1995. Lectins as plant defense proteins. Plant Physiol. 109:347–352.
Puthoff, D. P., Sardesa, N., Subramany, A. M. S., Nemacheck, J. A., and Williams, C. E. 2005. Hfr-2, a wheat cytolytic toxin-Like gene, is up-regulated by virulent Hessian fly larvae and feeding. Plant Mol. Biol. 6:411–423.
Quisenberry, S. S., and Clement, S. L. 2002. Conservation and use of global plant genetic resources for insect resistance. Aust. J. Agric. Res. 53:865–872.
Rasmussen, S., and Dixon, R. A. 1999. Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Physiol. 115:137–149.
Ratcliffe, R. H., and Hatchett, J. H. 1997. Biology and genetics of the Hessian fly and resistance in wheat, pp. 47–56, in New Developments in EntomologyResearch Signpost, Trivandrum, India.
Rohfritsch, O. 1992. Patterns in gall development, pp. 60–86, in Biology of insect-induced gallsOxford University Press, New York.
Rossi, M. F., Goggin, L., Milligan, S. B., Kaloshian, I., Ullman, D. E., and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. U.S.A. 95:9750–9754.
Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. U.S.A. 103:8894–8899.
Subramanyam, S., Sardesai, N., Puthoff, D. P., Meyer, J. M., Gonzalo, M., and Williams, C. E. 2006. Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci. 170:90–103.
Thompson, G. A., and Goggin, F. L. 2006. Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J. Exp. Botany 57:755–766.
Vercauteren, I., De Almeida Engler, J., De Groodt, R., and Gheysen, G. 2002. An Arabidopsis thaliana pectin acetylesterase gene is upregulated in nematode feeding sites induced by root-knot and cyst nematodes. Mol. Plant Micro. Interact. 15:404–407.
Widstrom, N. W., and Snook, M. E. 1998. A gene controlling biosynthesis of isoorientin, a compound in corn silks antibiotic to the corn earworm. Entomol. Exp. Appl. 89:119–124.
Williams, C. E., Collier, C. C., Nemacheck, J., Liang, C., and Cambron, S. E. 2002. A lectin-like wheat gene responds systemically to attempted feeding by avirulent first-instar Hessian fly larvae. J. Chem. Ecol. 28:1411–1428.
Zhu, Y. C., Liu, X. M., Maddur, A. A., Oppert, B., and Chen, M. S. 2005. Cloning and characterization of chymotrypsin- and trypsin-like cDNAs from the gut of the Hessian fly [Mayetiola destructor (Say)]. Insect Biochem. Mol. Biol. 35:23–32.
Zhu, L., Liu, X. M., Liu, X., Jeannotte, R., eese, J. C., Harris, M., Stuart, J. J., and Chen, M. S. 2007. Hessian Fly (Mayetiola Destructor) attack causes dramatic shift in carbon/nitrogen metabolism in wheat. Mol. Plant Micro. Interact (in press).
Acknowledgment
This work was supported by two grants from the National Research Initiative Competitive Grant program, the US Department of Agriculture (USDA 04-35607-14861 and USDA2005-35302-16254). This paper is contribution no. 07-81-J from the Kansas Agricultural Experiment Station. Hessian fly voucher specimens (no. 150) are located in the KSU Museum of Entomological and Prairie Arthropod Research, Kansas State University, Manhattan, Kansas. The microarray chips were processed with the Affymetrix GCS 3000 system in the Gene Expression Facility, Kansas State University. The system was purchased through the NSF Major Research Instrumentation grant DBI-0421427. The authors thank Dr. Subbaratnam Muthukrishnan, Dr. Guihua Bai, and Dr. Scot Hulbert for reviewing an earlier version of the manuscript. Mention of commercial or proprietary product does not constitute endorsement by the USDA.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, X., Bai, J., Huang, L. et al. Gene Expression of Different Wheat Genotypes During Attack by Virulent and Avirulent Hessian Fly (Mayetiola destructor) Larvae. J Chem Ecol 33, 2171–2194 (2007). https://doi.org/10.1007/s10886-007-9382-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-007-9382-2