Skip to main content

Advertisement

Log in

Wheat Gene Expression is Differentially Affected by a Virulent Russian Wheat Aphid Biotype

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

An improved understanding of the complex interactions between plants and aphids is emerging. Recognition of aphid feeding in plant tissues involves production of several defense response signaling pathways and downstream production of defense and detoxification compounds. Feeding by Russian wheat aphid, Diuraphis noxia (Kurdjumov), a serious pest of cereal crops worldwide, induces foliar deformity and chlorophyll loss during compatible wheat-D. noxia interactions. Experiments described here revealed significant differences in level and pattern of gene expression in defense response signaling and metabolic pathways between compatible and incompatible D. noxia-wheat interactions. The jasmonate (JA)-signaling genes LOX, AOS, and AOC were significantly more upregulated (~3- to 7 fold) in incompatible interactions than in compatible interactions (~2.5 to 3.5 fold) as early as 1 h post D. noxia infestation (hpi). Cellulose synthase, responsible for strengthening plant cell walls via cellulose production, was also more upregulated in incompatible interactions (4 to 7 fold) than in compatible interactions (1 to 3.5 fold). In contrast, glycolysis and citric acid cycle genes were significantly downregulated (~1.5 to 2 fold) in incompatible interactions and upregulated or less downregulated in compatible interactions from 6 to 72 hpi. Differences in expression of JA-signaling genes between feeding site tissues and non-feeding site tissues suggest that D. noxia defense response signals in wheat are restricted primarily to aphid feeding sites in the initial 6 hpi. This is the first report of differential upregulation of plant genes at 1 hpi in incompatible interactions involving aphid herbivory. Early wheat plant defense responses in incompatible D. noxia interactions at 1, 3, and 6 hpi appear to be important aspects of D. noxia resistance in wheat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alborn, H. T., Hansen, T. V., Jones, T. H., Bennett, D. C., Tumlinson, J. H., Schmelz, E. A., and Teal, P. E. A. 2007. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc. Natl. Acad. Sci. U. S. A. 104:12976–12981.

    Article  PubMed  CAS  Google Scholar 

  • Balbi, V., and Devoto, A. 2008. Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytologist 177:301–318.

    Article  PubMed  CAS  Google Scholar 

  • Bonaventure, G. and Baldwin, I. T. 2010. New insights into the early biochemical activation of jasmonic acid biosynthesis in leaves. Plant Signaling & Behavior 5:1–3.

    Article  Google Scholar 

  • Botha, A-M., Lacock, L., Niekerk, C. V., Matsioloko, M. T., Du Preez, F. B., Loots, S., Venter, E., Kunert, K. J., and Cullis, C. A. 2006. Is photosynthetic transcriptional regulation in Triticum aestivum L. cv. ‘TugelaDN’ a contributing factor for tolerance to Diuraphis noxia (Homoptera: Aphididae)? Plant Cell Reports 25:41–54.

  • Boyko, E. V., Smith, C. M., Thara, V. K., Bruno, J. M., Deng, Y. P., Starkey, S. R., and Klaahsen, D. L. 2006. Molecular basis of plant gene expression during aphid invasion: Wheat Pto- and Pti-like sequences are involved in interactions between wheat and Russian wheat aphid (Homoptera : Aphididae). J. Econ. Entomol. 99:1430–1445.

    Article  PubMed  CAS  Google Scholar 

  • Burd, J. D., and Elliot, N. C. 1996. Changes in chlorophyll a flourescence induction kinetics in cereals infested with Russian wheat aphid (Homoptera: Aphididae). J. Econ. Entomol. 89:1332–1337.

    Google Scholar 

  • Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J. M., Lorenzo, O., García-Casado, G., López-Vidriero, I., Lozano, F. M., Ponce, M. R., Micol, J. L. and Solano, R. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–71.

    Article  PubMed  CAS  Google Scholar 

  • Cho, S. K., Jung, K. W., Jeung, J. U., Kang, K. H., Shim, K. S., You, M. K., Yoo, K. S., Ok, S. H., and Shin, J. S. 2005. Analysis of differentially expressed transcripts from planthopper-infested wild rice (Oryza minuta). Plant Cell Rep. 24:59–67.

    Article  PubMed  CAS  Google Scholar 

  • Couldridge, C., Newbury, H. J., Ford-Lloyd, B., Bale, J., and PRITCHARD, J. 2007. Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bull. Entomol. Res. 97:523–532.

    Article  PubMed  CAS  Google Scholar 

  • Divol, F., Vilaine, F., Thibivilliers, S., Amselem, J., Palauqui, J. C., Kusiak, C., and DINANT, S. 2005. Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Mol. Biol. 57:517–40.

    Article  PubMed  CAS  Google Scholar 

  • Doss, R. P., Oliver, J. E., Proebsting, W. M., Potter, S. W., Kuy, S. R., Clement, S. L., Williamson, R. T., Carney, J. R., and DEVILBISS, E. D. 2000. Bruchins: insect-derived plant regulators that stimulate neoplasm formation. Proc. Natl. Acad. Sci. U. S. A. 97:6218–6223.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, C., Karafyllidis, I., and TURNER, J. G. 2002a. Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphae cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant Microbe Interact. 15:1025–1030.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, C., Karafyllidis, I.,Wasternack, C., and TURNER, J. G. 2002b. The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–66.

    Article  PubMed  CAS  Google Scholar 

  • Forslund, K., Pettersson, J., Bryngelsson, T., and JONSSON, L. 2000. Aphid infestation induces PR proteins differentially in barley susceptible or resistant to the bird cherry-oat aphid. Physiologia Plantarum 110:496–502.

    Article  CAS  Google Scholar 

  • Gao, L.-L., Klingler, J. P., Anderson, J. P., Edwards, O. R., and SINGH, K. B. 2008. Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol. 146:996–1009.

    Article  PubMed  CAS  Google Scholar 

  • Hatcher, P. E., Moore, J., Taylor, J. E., Tinney, G. W., and PAUL, N. D. 2004. Phytohormones and plant-herbivore-pathogen interactions: Integrating the molecular with the ecological: Phytohormonal ecology. Ecology 85:59–69.

    Article  Google Scholar 

  • Heng-Moss, T. M., Ni, X., Macedo, T., Markwell, J. P., Baxendale, F. P., Quisenberry, S. S., and TOLMAY, V. 2003. Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J. Econ. Entomol. 96:475–481.

    Article  PubMed  CAS  Google Scholar 

  • HOWE, G. A., and JANDER, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 2008. 59:41–66

  • KALOSHIAN, I. 2004. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30:2419–2438.

    Article  PubMed  CAS  Google Scholar 

  • KALOSHIAN, I., and WALLING, L. 2005. Hemipterans as pathogens. Annu. Rev. Phytopathol. 43:491–521.

    Article  PubMed  CAS  Google Scholar 

  • KAZAN, K., and MANNERS, J. M. 2008. Jasmonate signaling: Toward an integrated view. Plant Physiol. 146:1459–1468.

    Article  PubMed  CAS  Google Scholar 

  • KESSLER, A., and BALDWIN, I. T. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Physiol. 53:299–328.

    CAS  Google Scholar 

  • Khan, S. A., Murugan, M., Starkey, S., Manley, A., and SMITH, C. M. 2009. Inheritance and categories of resistance in wheat to Russian wheat aphid (Hemiptera: Aphididae) biotype 1 and biotype 2. J. Econ. Entomol. 102:1654–1662.

    Article  PubMed  CAS  Google Scholar 

  • KOORNNEEF, A., and PIETERSE C.M.J. 2008. Cross talk in defense signaling. 2008. Plant Physiol. 146: 839–844 doi:10.1104/pp.107.112029.

  • Lazzari, S., Starkey, S., Reese, J., Ray-Chandler, A., and SMITH, C. M. 2009. Feeding behavior of Russian wheat aphid (Hemiptera: Aphididae) biotype 2 in response to wheat genotypes exhibiting antibiosis and tolerance. J. Econ. Entomol. 102:1291–1300.

    Article  PubMed  CAS  Google Scholar 

  • LEE, H., LEON, J., and RASKIN, I. 1995. Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. U. S. A. 92:4076–4079.

    Article  PubMed  CAS  Google Scholar 

  • Li, L., Li, C., Lee, G. I., and HOWE, G. A. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response in tomato. Proc. Natl. Acad. Sci. U. S. A. 99:6416–6421.

    Article  PubMed  CAS  Google Scholar 

  • Li, Y., Zou, J., Li, M., Bilgin, D. D., Vodkin, L. O., Hartman, G. L., and CLOUGH, S. J. 2008. Soybean defense responses to the soybean aphid. New Phytol. 179:85–195.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Liu, X., Marshall, J. L., Stary, P., Edwards, O., Puterka, G., Dolatti, L., Bouhssini, M. E., Malinga, J., and SMITH, C. M. 2010. Global phylogenetics of an invasive aphid species: Evidence for multiple invasions into North America. J. Econ. Entomol. 103:958–965. doi:10.1603/EC09376.

    Article  PubMed  Google Scholar 

  • LIVAK, K. J., and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆Ct method. Methods 25:402–408.

    Article  PubMed  CAS  Google Scholar 

  • Martinez De Ilarduya, O., Nombela, G., Hwang, C. F., Williamson, V. M., Muniz, M., and KALOSHIAN, I. 2004. Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Mol. Plant Microbe Interact. 17:55–61.

  • MITHOFER A., and BOLAND W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiol. 146:825–831.

  • Moran, P. J., Cheng, Y., Cassell, J. L., and THOMPSON, G. A. 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 51: 182–203.

    Article  PubMed  CAS  Google Scholar 

  • PFAFFL. M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.

  • QUISENBERRY, S. S., and PEAIRS, F. B. 1998. A response model for an introduced pest- the Russian wheat aphid. in Thomas Say Publications in Entomology. Entomol. Soc. Am., Lanham, MD.

  • SAS Institute Inc. 2001. SAS/STAT Software version 9.1. SAS Institute, Cary, NC.

  • Scheible, W.-R., Eshed, R., Richmond, T., Delmer, D., and SOMERVILLE, C. 2001. Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis ixr1 mutants. Proc. Natl. Acad. Sci. USA. 98:10079–10084.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • SMITH, C. M., and BOYKO, E. V. 2007. The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol. Exp. Appl. 122:1–16.

    Article  CAS  Google Scholar 

  • SMITH, C. M., LIU, X. M., WANG, L. J., LIU, X., CHEN, M.-S., STARKEY, S., and BAI, J. 2010. Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. J. Chem. Ecol. 36: 260–276. doi 10.1007/s10886-010-9756-8.

    Article  PubMed  CAS  Google Scholar 

  • Telang, A., Sandstrom, J., Dyreson, E., and MORAN, N. A. 1999 Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol. Exp. Appl. 91:403–412.

    Article  Google Scholar 

  • Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G. A., and BROWSE, J. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–65.

  • THOMPSON, G. A., and GOGGIN, F. L. 2006. Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J. Exp. Bot. 57:755–766.

    Article  PubMed  CAS  Google Scholar 

  • TJALLINGII, W. F., and HOGEN ESCH, T. 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18:317–328.

    Google Scholar 

  • TURNER, J. G., ELLIS, C., and DEVOTO, A. 2002. The jasmonate signal pathway. Plant Cell 14: (suppl.), S153-S164.

  • VOELCKEL, C., WEISSER, W. W., and BALDWIN, I. T. 2004. An analysis of plant–aphid interactions by different microarray hybridization strategies. Mol. Ecol. 13:3187–3195.

    Article  PubMed  CAS  Google Scholar 

  • WALLING, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regulation 19:195–216.

    CAS  Google Scholar 

  • Wildermuth, M.C., Dewdney, J., Wu, G., and AUSUBEL, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565.

  • Zhu, L., Liu, X., Liu, X., Jeannotte, R., Reese, J., Harris, M., Stuart, 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.

    Article  PubMed  Google Scholar 

  • Zhu-Salzman, K., Salzman, R. A., Ahn, J.-E., and KOIWA, H. 2004. Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol. 134: 420–431.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Murugan Marimuthu and Paola Sotelo for helpful comments in discussion of the data and Ming-Shun Chen and Subbarat Muthukrishnan for critical reviews of an early draft of the manuscript. This research was supported by grants to CMS from the Kansas Wheat Commission, the USDA CSREES NC-IPM program and the Kansas Agricultural Experiment Station. This is contribution No. 10-304-J of the Kansas Agricultural Experiment Station. This research was performed in the Gene Expression Facility at Kansas State University, which is supported through the National Science Foundation grant, DBI 0421427.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles Michael Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, X., Meng, J., Starkey, S. et al. Wheat Gene Expression is Differentially Affected by a Virulent Russian Wheat Aphid Biotype. J Chem Ecol 37, 472–482 (2011). https://doi.org/10.1007/s10886-011-9949-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-9949-9

Key Words

Navigation