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Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding

Published online by Cambridge University Press:  08 October 2008

A. Gutsche ,
T. Heng-Moss ,
G. Sarath ,
P. Twigg ,
Y. Xia ,
G. Lu  and
D. Mornhinweg
A. Gutsche
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
T. Heng-Moss*
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
G. Sarath
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
P. Twigg
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
Y. Xia
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
G. Lu
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
D. Mornhinweg
Affiliation:
Department of Entomology, University of Nebraska, 202 Entomology Hall, Lincoln, NE 68583, USA
*
*Author for correspondence Fax: 402-472-4687 E-mail: [email protected]
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Abstract

Aphids are, arguably, the single most damaging group of agricultural insect pests throughout the world. Plant tolerance, which is a plant response to an insect pest, is viewed as an excellent management strategy. Developing testable hypotheses based on genome-wide and more focused methods will help in understanding the molecular underpinnings of plant tolerance to aphid herbivory. As a first step in this process, we undertook transcript profiling with Affymetrix GeneChip Barley Genome arrays using RNA extracted from tissues of tolerant and susceptible genotypes collected at three hours, three days and six days after Diuraphis noxia introduction. Acquired data were compared to identify changes unique to the tolerant barley at each harvest date. Transcript abundance of 4086 genes was differentially changed over the three harvest dates in tolerant and susceptible barley in response to D. noxia feeding. Across the three harvest dates, the greatest number of genes was differentially expressed in both barleys at three days after aphid introduction. A total of 909 genes showed significant levels of change in the tolerant barley in response to D. noxia feeding as compared to susceptible plants infested with aphids. Many of these genes could be assigned to specific metabolic categories, including several associated with plant defense and scavenging of reactive oxygen species (ROS). Interestingly, two peroxidase genes, designated HvPRXA1 and HvPRXA2, were up-regulated to a greater degree in response to D. noxia feeding on tolerant barley plants, indicating that specific peroxidases could be important for the tolerance process. These findings suggest that the ability to elevate and sustain levels of ROS-scavenging enzymes could play an important role in the tolerant response.

Keywords

Russian wheat aphidmicroarray analysisperoxidasesplant resistance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 2 , April 2009 , pp. 163 - 173
Copyright
Copyright © 2008 Cambridge University Press

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References

Adie, B.A.T., Perez-Perez, J., Perez-Perez, M.M., Godoy, M., Sanchez-Serrano, J.J., Schmelz, E.A. & Solano, R. (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. The Plant Cell 19, 1665–1681.CrossRefGoogle ScholarPubMed
Anderson, G.R., Papa, D., Peng, J., Tahir, M. & Lapitan, L.N. (2003) Genetic mapping of Dn7, a rye gene conferring resistance to the Russian wheat aphid in wheat. Theoretical and Applied Genetics 107, 1297–1303.CrossRefGoogle Scholar
Apel, K. & Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.CrossRefGoogle ScholarPubMed
Argandona, V.H., Chaman, M., Cardemil, L., Munoz, O., Zuniga, G.E. & Corcuera, L.J. (2001) Ethylene production and peroxidase activity in aphid-infested barley. Journal of Chemical Ecology 27, 53–68.CrossRefGoogle ScholarPubMed
Boter, M., Ruiz-Rivero, O., Abdeen, A. & Prat, S. (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes and Development 18, 1577–1591.CrossRefGoogle ScholarPubMed
Botha, A.-M., Lacock, L., van Niekerk, C., Matsioloko, M.T., du Preez, F.B., Loots, S., Venter, E., Kunert, K.J. & 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.CrossRefGoogle ScholarPubMed
Boyko, E.V., Smith, C.M., Thara, V.K., Bruno, J.M., Deng, Y., Starkey, S.R. & Klaahsen, D. (2006) The 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). Journal of Economic Entomology 99, 1430–1445.CrossRefGoogle ScholarPubMed
Burd, J.D. & Elliott, N.C. (1996) Changes in chlorophyll a fluorescence induction kinetics in cereals infested with Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology 89, 1332–1337.CrossRefGoogle Scholar
Burd, J.D., Webster, J.A., Puterka, G.J., Hoxie, R.P. & Wellso, S.G. (1996) Effect of Russian wheat aphid on constituent and nonconstituent carbohydrate content in wheat seedlings. Southwestern Entomologist 21, 167–172.Google Scholar
Clifton, R., Millar, A.H. & Whelan, J. (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochimica Biophysica Acta – Bioenergetics 1757, 730–741.CrossRefGoogle ScholarPubMed
Couldridge, J.J., Newbury, H.J., Ford-Lloyd, B., Bale, J. & Pritchard, J. (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bulletin of Entomological Research 97, 523–532.CrossRefGoogle ScholarPubMed
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K. & Scheible, W. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5–17.CrossRefGoogle ScholarPubMed
De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Metraux, J.P., Van Loon, L.C., Dicke, M. & Pieterse, C.M. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923–937.CrossRefGoogle ScholarPubMed
Divol, F., Vilaine, F., Thibivilliers, S., Amselem, J., Palauqui, J.-C., Kusiak, K. & Dinant, S. (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Molecular Biology 57, 517–540.CrossRefGoogle ScholarPubMed
Dixon, D.P., Lapthorn, A. & Edwards, R. (2002) Plant glutathione transferases. Genome Biology 3, reviews3004.1–10.CrossRefGoogle ScholarPubMed
Eckardt, N. (2002) Probing the mysteries of lignin biosynthesis: the crystal structure of caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase provides new insights. Plant Cell 14, 1185–1189.CrossRefGoogle ScholarPubMed
Franzen, L.D., Gutsche, A.R., Heng-Moss, T.M., Higley, L.G., Sarath, G. & Burd, J.D. (2007) Physiological and biochemical responses of resistant and susceptible wheat to injury by the Russian wheat aphid, Diuraphis noxia (Mordvilko). Journal of Economic Entomology 100, 1692–1703.CrossRefGoogle Scholar
Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R. & Van Breusegem, F. (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiology 141, 436–445.CrossRefGoogle ScholarPubMed
Haile, F.J., Higley, L.G., Ni, X. & Quisenberry, S.S. (1999) Physiological and growth tolerance in wheat to Russian wheat aphid (Homoptera: Aphididae) injury. Environmental Entomology 28, 787–794.CrossRefGoogle Scholar
Heidel, A.J. & Baldwin, I.T. (2004) Microarray analysis of SA- and JA-signaling in Nicotiana attenuata's responses to attack by insects from multiple feeding guilds. Plant, Cell & Environment 27, 1362–1373.CrossRefGoogle Scholar
Heng-Moss, T.M., Ni, X., Macedo, T., Markwell, J.P., Baxendale, F.P., Quisenberry, S.S. & Tolmay, V. (2003) Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. Journal of Economic Entomology 96, 475–481.CrossRefGoogle ScholarPubMed
Heng-Moss, T.M., Sarath, G., Baxendale, F.P., Novak, D., Bose, S., Xinhi, N. & Quisenberry, S. (2004) Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus. Journal of Economic Entomology 97, 1086–1095.CrossRefGoogle ScholarPubMed
Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y. & Matsui, H. (2001) A large family of class III plant peroxidases. Plant and Cell Physiology 42, 462–468.CrossRefGoogle ScholarPubMed
Hui, D., Javeed, I., Lehmann, K., Gase, K., Saluz, H.P. & Baldwin, I.T. (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in the accumulations of herbivore-induced mRNAs. Plant Physiology 131, 1877–1893.CrossRefGoogle Scholar
Kawano, T. (2003) Roles of the reactive oxygen speices-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports 21, 829–837.CrossRefGoogle ScholarPubMed
Kazemi, M.H., Talebi-Chaichi, P., Shakiba, M.R. & Jafarloo, M.M. (2001) Biological responses of Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae) to different wheat varieties. Journal of Agriculture, Science, and Technology 3, 249–255.Google Scholar
Kotchoni, S.O. & Gachomo, E.W. (2006) The reactive oxygen species networkpathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. Journal of Bioscience 31, 389–404.CrossRefGoogle Scholar
Lauvergeat, V., Lacomme, C., Lacombe, E., Lasserre, E., Roby, D. & Grima-Pettenati, J. (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57, 1187–1195.CrossRefGoogle ScholarPubMed
Lee, K., Loros, J.J. & Dunlap, J.C. (2000) Interconnected feedback loops in the Neurospora circadian system. Science 289, 107–110.CrossRefGoogle ScholarPubMed
Liu, G., Sheng, X., Greenshields, D.L., Ogieglo, A., Kaminskyj, S., Selvaraj, G. & Wei, Y. (2005) Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Molecular Plant Microbe Interactions 18, 730–741.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-DeltaDeltaCT) method. Methods 25, 402–408.CrossRefGoogle Scholar
Lu, G., Nguyen, T.V., Xiao, Y. & Fromm, M. (2006) AffyMiner: mining differentially expressed genes and biological knowledge in GeneChip microarray data. BMC Bioinformatics 7, S26.CrossRefGoogle ScholarPubMed
Ma, Q.-H. (2007) Characterization of a cinnamoyl-CoA reductase that is associated with stem development in wheat. Journal of Experimental Botany 58, 2011–2021.CrossRefGoogle ScholarPubMed
Macedo, T. (2003) Physiological responses of plants to piercing–sucking arthropods. PhD Dissertation. University of Nebraska-Lincoln, Lincoln, NE, USA.Google Scholar
Macedo, T.B., Higley, L.G., Ni, X. & Quisenberry, S.S. (2003) Light activation of Russian wheat aphid-elicited physiological responses in susceptible wheat. Journal of Economic Entomology 96, 194–201.CrossRefGoogle ScholarPubMed
Miller, H., Porter, D.R., Burd, J.D., Mornhinweg, D.W. & Burton, R.L. (1994) Physiological effects of Russian wheat aphid (Homoptera: Aphididae) on resistant and susceptible barley. Journal of Economic Entomology 87, 493–499.CrossRefGoogle Scholar
Moran, P.J. & Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defence pathways. Plant Physiology 125, 1074–1085.CrossRefGoogle Scholar
Moran, P.J., Cheng, Y., Cassell, J.L. & Thompson, G.A. (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Archives of Insect Biochemistry and Physiology 51, 182–203.CrossRefGoogle ScholarPubMed
Mornhinweg, D.W., Porter, D.R. & Webster, J.A. (1995) Registration of STARS-9301B barley germplasm resistant to Russian wheat aphid. Crop Science 35, 602.Google Scholar
Ni, X. & Quisenberry, S. (2003) Possible roles of esterase glutathione S–transferase, and superoxide dismutase activities in understanding aphid–cereal interactions. Entomologia Experimentalis et Applicata 108, 187–195.CrossRefGoogle Scholar
Ni, X., Quisenberry, S.S., Heng-Moss, T., Markwell, J., Sarath, G., Klucas, R. & Baxendale, F. (2001) Oxidative responses of resistant and susceptible cereal leaves to symptomatic and non-symptomatic cereal aphid (Hemiptera: Aphididae) feeding. Journal of Economic Entomology 94, 743–751.CrossRefGoogle Scholar
Ni, X., Quisenberry, S.S., Heng-Moss, T., Markwell, J., Higley, L., Baxendale, F., Sarath, G. & Klucas, R. (2002) Dynamic change in photosynthetic pigments and chlorophyll degradation elicited by cereal aphid feeding. Entomologia Experimentalis et Applicata 105, 43–53.CrossRefGoogle Scholar
Park, J.-H., Halitschke, R., Kim, H.B., Baldwin, I.T., Feldmann, K.A. & Feyereisen, R. (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant Journal 31, 1–12.CrossRefGoogle ScholarPubMed
Park, S.-J., Huang, Y. & Ayoubi, P. (2005) Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 223, 932–947.CrossRefGoogle ScholarPubMed
Passardi, F., Cosio, C., Penel, C. & Dunand, C. (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Reports 24, 255–265.CrossRefGoogle ScholarPubMed
Pitzschke, A., Forzani, C. & Hirt, H. (2006) Reactive oxygen species signaling in plants. Antioxidants & Redox Signaling 8, 1757–1764.CrossRefGoogle ScholarPubMed
Quisenberry, S.S. & Peairs, F.B. (Eds) (1998) Response model for an introduced pest: the Russian wheat aphid. 442 pp. MD, Entomological Society of America.CrossRefGoogle Scholar
Rafi, M.M., Zemetra, R.S. & Quisenberry, S.S. (1997) Feeding damage of Russian wheat aphid on resistant and susceptible wheat genotypes. Cereal Research Communications 25, 63–68.CrossRefGoogle Scholar
Rampino, P., Spano, G., Pataleo, S., Mita, G., Napier, J.A., Di Fonzo, N., Shewry, P.R. & Perrotta, C. (2006) Molecular analysis of a durum wheat “stay green” mutant: expression pattern of photosynthesis-related genes. Journal of Cereal Science 43, 160–168.CrossRefGoogle Scholar
Remans, R., Spaepen, S. & Vanderleyden, J. (2006) Auxin signaling in plant defense. Science 313, 171.CrossRefGoogle ScholarPubMed
Reymond, P., Weber, H., Damond, M. & Farmer, E.E. (2000) Differential gene expression in respone to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707–719.CrossRefGoogle Scholar
Rodriguez-Lopez, M., Baroja-Fernandezm, E., Zandueta-Criado, A. & Pozueta-Romero, J. (2000) Adenosine diphosphate glucose pyrophosphatase: a plastidial phosphodiesterase that prevents starch biosynthesis. Proceedings of the National Academy of Science USA 97, 8705–8710.CrossRefGoogle ScholarPubMed
Smith, C.M. (2005) Plant resistance to arthropods: molecular and coventional approaches. 423 pp. Netherlands, Springer.CrossRefGoogle Scholar
Smith, C.M. & Boyko, E.V. (2007) The molecular bases of plant resistance and defense to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 1–16.CrossRefGoogle Scholar
Strassner, J., Schaller, F., Frick, U.B., Howe, G., Weiler, E.W., Amrhein, N., Macheroux, P. & Schaller, A. (2002) Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. The Plant Journal 32, 585–601.CrossRefGoogle ScholarPubMed
Sugimoto, K., Takeda, S. & Hirochika, H. (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell 12, 2511–2528.CrossRefGoogle ScholarPubMed
Telang, A., Sandström, J., Dyreson, E. & Moran, N.A. (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomologia Experimentalis et Applicata 91, 403–412.CrossRefGoogle Scholar
Urao, T., Yamaguchi-Shinozaki, K., Urao, S. & Shinozaki, K. (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. The Plant Cell 5, 1529–1539.Google Scholar
Voelckel, C., Weisser, W.W. & Baldwin, I.T. (2004) An analysis of plant–aphid interactions by different microarray hybridization strategies. Molecular Ecology 13, 3187–3195.CrossRefGoogle ScholarPubMed
Webster, J.A., Baker, C.A. & Porter, D.R. (1991) Detection and mechanisms of Russian wheat aphid (Homoptera: Aphididae) resistance in barley. Journal of Economic Entomology 84, 669–673.CrossRefGoogle Scholar
Yanhui, C., Xiaoyuan, Y., Kun, H., Meihua, L., Jigang, L., Zhaofeng, G., Zhiqiang, L., Yunfei, Z., Xiaoxiao, W., Xiaoming, Q., Yunping, S., Li, Z., Xiaohui, D., Jingchu, L., Xing-Wang, D., Zhangliang, C., Hongya, G. & Li-Jia, Q. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular Biology 60, 107–124.CrossRefGoogle ScholarPubMed
Zhu-Salzman, K., Salzman, R.A., Ahn, J.-E. & Koiwa, H. (2004) Transcriptional regulation of sorghum defence determinants against a phloem-feeding aphid. Plant Physiology 134, 420–431.CrossRefGoogle ScholarPubMed
Zierold, U., Scholz, U. & Schweizer, P. (2005) Transcriptome analysis of mlo-mediated resistance in the epidermis of barley. Molecular Plant Pathology 6, 139–151.CrossRefGoogle ScholarPubMed