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Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression

Published online by Cambridge University Press:  04 October 2007

C. Couldridge
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
H.J. Newbury
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
B. Ford-Lloyd
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
J. Bale
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
J. Pritchard*
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
*
*Author for correspondence Fax: 0121 414 5925 E-mail: [email protected]

Abstract

The aim of this study was to determine which Arabidopsis thaliana (L.) genes had significantly altered expression following 2–36 h of infestation by the aphid Myzus persicae (Sulzer). Six biological replicates were performed for both control and treatment at each time point, allowing rigorous statistical analysis of any changes. Only two genes showed altered expression after 2 h (one up- and one down-regulated) while two were down-regulated and twenty three were up-regulated at 36 h. The transcript annotation allowed classification of the significantly altered genes into a number of classes, including those involved in cell wall modification, carbon metabolism and signalling. Additionally, a number of genes were implicated in oxidative stress and defence against other pathogens. Five genes could not currently be assigned any function. The changes in gene expression are discussed in relation to current models of plant-insect interactions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

Abate, T., van Huis, A. & Ampofo, J.K.O. (2000) Pest management strategies in traditional agriculture: An African perspective. Annual Review of Entomology 45, 631659.CrossRefGoogle ScholarPubMed
Amann, K., Lezhneva, L., Wanner, G., Herrmann, R.G. & Meurer, J. (2004) Accumulation of photosystem one1, a member of a novel gene family, is required for accumulation of cluster-containing chloroplast complexes and antenna proteins. Plant Cell 16, 30843097.CrossRefGoogle ScholarPubMed
Barnes, A., Bale, J.S., Constantinidou, C., Ashton, P., Jones, A. & Pritchard, J. (2004) Determining protein identity from sieve element sap in Ricinus communis l. by quadrupole time of flight (Q-TOF) mass spectrometry. Journal of Experimental Botany 55, 14731481.CrossRefGoogle ScholarPubMed
Bassham, D.C., Gal, D., Conceicao, A.D. & Raikhel, N.V. (1995) An Arabidopsis syntaxin homologue isolated by functional complementation of a yeast pep12 mutant. Proceedings of the National Academy of Sciences of the United States of America 92, 72627266.CrossRefGoogle ScholarPubMed
Benjamini, V. & Hochberg, V. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 57, 289300.Google Scholar
Bergey, D.R. & Ryan, C.A. (1999) Wound- and systemin-inducible calmodulin gene expression in tomato leaves. Plant Molecular Biology 40, 815823.CrossRefGoogle ScholarPubMed
Borner, G.H.H., Lilley, K.S., Stevens, T.J. & Dupree, P. (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. a proteomic and genomic analysis. Plant Physiology 132, 568577.CrossRefGoogle ScholarPubMed
Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. & Gorlach, J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13, 14991510.Google Scholar
Cherqui, A. & Tjallingii, W.F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. Journal of Insect Physiology 46, 11771186.CrossRefGoogle ScholarPubMed
Custers, J.H.H.V., Harrison, S.J., Sela-Buurlage, M.B., Van Deventer, E., Lageweg, W., Howe, P.W., Van Der Meijs, P.J., Ponstein, A.S., Simons, B.H., Melchers, L.S. & Stuiver, M.H. (2004) Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. Plant Journal 39, 147160.CrossRefGoogle ScholarPubMed
De Ilarduya, O.M., Xie, Q.G. & Kaloshian, I. (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions 16, 699708.CrossRefGoogle Scholar
Delessert, C., Kazan, K., Wilson, I.W., Van Der Straeten, D., Manners, J., Dennis, E.S. & Dolferus, R. (2005) The transcription factor ataf2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant Journal 43, 745757.CrossRefGoogle ScholarPubMed
Desveaux, D., Marechal, A. & Brisson, N. (2005) Whirly transcription factors: Defense gene regulation and beyond. Trends in Plant Science 10, 95102.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.J. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923937.CrossRefGoogle ScholarPubMed
Dillwith, J.W., Berberet, R.C., Bergman, D.K., Neese, P.A., Edwards, R.M. & McNew, R.W. (1991) Plant biochemistry and aphid populations – Studies on the Spotted Alfalfa Aphid, Therioaphis maculata. Archives of Insect Biochemistry and Physiology 17, 235251.CrossRefGoogle Scholar
Dinant, S., Lark, A.M., Zhu, Y.M., Vilaine, F., Palauqui, J.C., Kusiak, C. & Thompson, G.A. (2003) Diversity of the superfamily of phloem lectins (phloem protein 2) in angiosperms. Plant Physiology 131, 114128.CrossRefGoogle ScholarPubMed
Divol, F., Vilaine, F., Thibivilliers, S., Amselem, J., Palauqui, J.C., Kusiak, C. & Dinant, S. (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Molecular Biology 57, 517540.CrossRefGoogle ScholarPubMed
Dixon, D.P., Skipsey, M., Grundy, N.M. & Edwards, R. (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiology 138, 22332244.CrossRefGoogle ScholarPubMed
Doering-Saad, C., Newbury, H.J., Bale, J.S. & Pritchard, J. (2002) Use of aphid stylectomy and RT-PCR for the detection of transporter mRNAs in sieve elements. Journal of Experimental Botany 53, 631637.CrossRefGoogle ScholarPubMed
Doering-Saad, C., Newbury, H.J., Couldridge, C.E., Bale, J.S. & Pritchard, J. (2006) A phloem-enriched cDNA library from Ricinus: insights into phloem function. Journal of Experimental Botany 57, 31833193.CrossRefGoogle ScholarPubMed
Dong, X. (2004) The role of membrane-bound ankyrin-repeat protein ACD6 in programmed cell death and plant defense. Science's STKE 221, 6.Google Scholar
Douglas, A.E. (2003) The nutritional physiology of aphids. Advances in Insect Physiology 31, 73140.CrossRefGoogle Scholar
Edwards, R., Brazier-Hicks, M., Dixon, D.P. & Cummins, I. (2005) Chemical manipulation of antioxidant defences in plants. Advances in Botanical Research Incorporating Advances in Plant Pathology 42, 132.CrossRefGoogle Scholar
Eulgem, T., Weigman, V.J., Chang, H.S., McDowell, J.M., Holub, E.B., Glazebrook, J., Zhu, T. & Dangl, J.L. (2004) Gene expression signatures from three genetically separable resistance gene signalling pathways for downy mildew resistance. Plant Physiology 135, 11291144.CrossRefGoogle ScholarPubMed
Ezaki, B., Suzuki, M., Motoda, H., Kawamura, M., Nakashima, S. & Matsumoto, H. (2004) Mechanism of gene expression of Arabidopsis glutathione S-transferase, atgst1, and atgst11 in response to aluminum stress. Plant Physiology 134, 16721682.CrossRefGoogle ScholarPubMed
Faivre-Nitschke, S.E., Grienenberger, J.M. & Gualberto, J.M. (1999) A prokaryotic-type cytidine deaminase from Arabidopsis thaliana – gene expression and functional characterization. European Journal of Biochemistry 263, 896903.CrossRefGoogle ScholarPubMed
Feys, B.J., Moisan, L.J., Newman, M.A. & Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO Journal 20, 54005411.CrossRefGoogle ScholarPubMed
Fidantsef, A.L., Stout, M.J., Thaler, J.S., Duffey, S.S. & Bostock, R.M. (1999) Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor ii, and pathogenesis-related protein p4 in the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology 54, 97114.CrossRefGoogle Scholar
Filkowski, J., Kovalchuk, O. & Kovalchuk, I. (2004) Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant Journal 38, 6069.CrossRefGoogle ScholarPubMed
Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E.E., Crute, I.R., Holub, E.B., Hammerschmidt, R. & Ausubel, F.M. (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146, 381392.CrossRefGoogle ScholarPubMed
Hale, B.K., Bale, J.S., Pritchard, J., Masters, G.I. & Brown, V.K. (2003) Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): A mechanistic analysis. Ecological Entomology 28, 666677.CrossRefGoogle Scholar
Hegedus, D., Yu, M., Baldwin, D., Gruber, M., Sharpe, A., Parkin, I., Whitwill, S. & Lydiate, D. (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Molecular Biology 53, 383397.CrossRefGoogle ScholarPubMed
Hong, Z.L., Zhang, Z.M., Olson, J.M. & Verma, D.P.S. (2001) A novel udp-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13, 769779.CrossRefGoogle ScholarPubMed
Hunt, E.J., Pritchard, J., Bennett, M.J., Zhu, X., Barrett, D.A., Allen, T., Bale, J.S. & Newbury, H.J. (2006) The Arabidopsis thaliana/Myzus persicae model system demonstrates that a single gene can influence the interaction between a plant and a sap-feeding insect. Molecular Ecology 15, 42034213.CrossRefGoogle Scholar
Jammes, F., Lecompte, P., de Almida-Engler, J., Bitton, F., Martin-Magniette, M-L., Renou, J.P., Abad, P. & Favery, B. (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. The Plant Journal 44, 447458.CrossRefGoogle ScholarPubMed
Kallberg, Y., Oppermann, U., Jornvall, H. & Persson, B. (2002) Short-chain dehydrogenase/reductase (SDR) relationships: a large family with eight clusters common to human, animal, and plant genomes. Protein Science 11, 636641.CrossRefGoogle ScholarPubMed
Kempema, L.A., Cui, X., Holzer, F.M. & Walling, L.L. (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology, in press.CrossRefGoogle ScholarPubMed
Kim, H.G., Kim, B.C., Park, E.H. & Lim, C.J. (2005) Stress-dependent regulation of a monothiol glutaredoxin gene from Schizosaccharomyces pombe. Canadian Journal of Microbiology 51, 613620.CrossRefGoogle ScholarPubMed
Lamport, D.T.A. & Kieliszewski, M.J. (2005) Stress upregulates periplasmic arabinogalactan-proteins. Plant Biosystems 139, 6064.CrossRefGoogle Scholar
Lee, M.T., Kuo, F.C., Whitmore, G.A. & Sklar, J. (2000) Importance of replication in microarray gene expression studies: Statistical methods and evidence from repetitive cDNA hybridizations. Proceedings of the National Academy of Sciences 97, 98349839.CrossRefGoogle ScholarPubMed
León, J., Rojo, E., Titarenko, E. & Sanchez-Serrano, J.J. (1998) Jasmonic acid-dependent and -independent wound signal transduction pathways are differentially regulated by Ca2+ calmodulin in Arabidopsis thaliana. Molecular and General Genetics 258, 412419.CrossRefGoogle ScholarPubMed
Li, X.C., Schuler, M.A. & Berenbaum, M.R. (2002) Jasmonate and salicylate induce expression of herbivore cytochrome p450 genes. Nature 419, 712715.CrossRefGoogle ScholarPubMed
Lieberherr, D., Wagner, U., Dubuis, P.H., Metraux, J.P. & Mauch, F. (2003) The rapid induction of glutathione S-transferases atgstf2 and atgstf6 by a virulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signalling. Plant and Cell Physiology 44, 750757.CrossRefGoogle Scholar
Mahalingam, R., Shah, N., Scrymgeour, A. & Fedoroff, N. (2005) Temporal evolution of the Arabidopsis oxidative stress response. Plant Molecular Biology 57, 709730.CrossRefGoogle ScholarPubMed
Mang, H.G., Kang, E.O., Shim, J.H., Kim, S.Y., Park, K.Y., Kim, Y.S., Bahk, Y.Y. & Kim, W.T. (2004) A proteomic analysis identifies glutathione S-transferase isoforms whose abundance is differentially regulated by ethylene during the formation of early root epidermis in Arabidopsis seedlings. Biochimica et Biophysica Acta-Gene Structure and Expression 1676, 231239.CrossRefGoogle ScholarPubMed
Miles, P.W. (1999) Aphid saliva. Biological Reviews 74, 4185.CrossRefGoogle Scholar
Miles, P.W. & Oertli, J.J. (1993) The significance of antioxidants in the aphid-plant interaction – the redox hypothesis. Entomologia Experimentalis et Applicata 67, 275283.CrossRefGoogle Scholar
Mittler, T.E. (1958) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) ii, the nitrogen and sugar composition of ingested phloem sap and excreted honeydew. Journal of Experimental Biology 35, 7484.CrossRefGoogle Scholar
Moran, P.J., Cheng, Y.F., 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, 182203.CrossRefGoogle ScholarPubMed
Nagano, Y., Furuhashi, H., Inaba, T. & Sasaki, Y. (2001) A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. Nucleic Acids Research 29, 40974105.CrossRefGoogle ScholarPubMed
Ni, X.Z. & Quisenberry, S.S. (2003) Possible roles of esterase, glutathione s-transferase, and superoxide dismutase activities in understanding aphid-cereal interactions. Entomologia Experimentalis et Applicata 108, 187195.CrossRefGoogle Scholar
Ni, X.Z., 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 nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. Journal of Economic Entomology 94, 743751.CrossRefGoogle ScholarPubMed
Nühse, T.S., Boller, T. & Peck, S.C. (2003) A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. Journal of Biological Chemistry 278, 4524845254.CrossRefGoogle Scholar
Ogawa, K. (2005) Glutathione-associated regulation of plant growth and stress responses. Antioxidants & Redox Signaling 7, 973981.CrossRefGoogle ScholarPubMed
Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci, P., Hayashizaki, Y., Suzuki, K., Kojima, K., Takahara, Y., Yamamoto, K. & Kikuchi, S. (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10, 239247.CrossRefGoogle ScholarPubMed
Oparka, K.J. (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends in Plant Science 9, 3341.CrossRefGoogle ScholarPubMed
Pavlidis, P., Qinghong, L. & Stafford Nobel, W. (2003) The effect of replication on gene expression microarray experiments. Bioinformatics 19, 16201627.CrossRefGoogle ScholarPubMed
Pegadaraju, V., Knepper, C., Reese, J. & Shah, J. (2005) Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiology 139, 19271934.CrossRefGoogle ScholarPubMed
Ponder, K.L., Pritchard, J., Harrington, R. & Bale, J.S. (2000) Difficulties in location and acceptance of phloem sap combined with reduced concentration of phloem amino acids explain lowered performance of the aphid Rhopalosihum padi on nitrogen deficient barley (Hordeum vulgare) seedlings. Entomologia Experimentalis et Applicata 97, 203210.CrossRefGoogle Scholar
Ponder, K.L., Pritchard, J., Harrington, R. & Bale, J.S. (2001) Feeding behaviour of the aphid Rhopalosiphum padi (Hemiptera: Aphididae) on nitrogen and water stressed barley (Hordeum vulgare) seedlings. Bulletin of Entomological Research 91, 19.CrossRefGoogle ScholarPubMed
Prado, E. & Tjallingii, W.F. (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis et Applicata 82, 189200.CrossRefGoogle Scholar
Pritchard, J., Griffiths, B. & Hunt, E.J. (2007) Can the effect of climate change on the performance of phloem-feeding insect herbivores be predicted? Global Change Biology. in press.Google Scholar
Qubbaj, T., Reineke, A. & Zebitz, C.P.W. (2005) Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata 115, 145152.CrossRefGoogle Scholar
Reddy, V.S. & Reddy, A.S.N. (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65, 17451776.CrossRefGoogle ScholarPubMed
Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C.Z., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J.Z., Ghandehari, D., Sherman, B.K. & Yu, C.L. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 21052110.CrossRefGoogle ScholarPubMed
Sanderfoot, A.A., Assaad, F.F. & Raikhel, N.V. (2000) The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiology 124, 15581569.CrossRefGoogle ScholarPubMed
Sandström, J., Telang, A. & Moran, N.A. (2000) Nutritional enhancement of host plants by aphids – a comparison of three aphid species on grasses. Journal of Insect Physiology 46, 3340.CrossRefGoogle ScholarPubMed
Satoh, S., Sturm, A., Fujii, T. & Chrispeels, M.J. (1992) cDNA cloning of an extracellular dermal glycoprotein of carrot and its expression in response to wounding. Planta 188, 432438.CrossRefGoogle ScholarPubMed
Sauvion, N., Charles, H., Febvay, G. & Rahbe, Y. (2004) Effects of jackbean lectin (conA) on the feeding behaviour and kinetics of intoxication of the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 110, 3144.CrossRefGoogle Scholar
Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y. & Shinozaki, K. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant Journal 31, 279292.CrossRefGoogle ScholarPubMed
Shang, C.W., Shibahara, T., Hanada, K., Iwafune, Y. & Hirano, H. (2004) Mass spectrometric analysis of posttranslational modifications of a carrot extracellular glycoprotein. Biochemistry 43, 62816292.CrossRefGoogle ScholarPubMed
Sjölund, R.D. (1997) The phloem sieve element: a river runs through it. Plant Cell 9, 11371146.CrossRefGoogle Scholar
Slosser, J.E. (1993) Influence of planting date and insecticide treatment on insect pest abundance and damage in dryland cotton. Journal of Economic Entomology 86, 12131222.CrossRefGoogle Scholar
Smith, A.P., Nurizadeh, S.D., Peer, W.A., Xu, J.H., Bandyopadhyay, A., Murphy, A.S. & Goldsbrough, P.B. (2003) Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant Journal 36, 433442.CrossRefGoogle ScholarPubMed
Smith, A.P., Deridder, B.P., Guo, W.J., Seeley, E.H., Regnier, F.E. & Goldsbrough, P.B. (2004) Proteomic analysis of Arabidopsis glutathione S-transferases from benoxacor- and copper-treated seedlings. Journal of Biological Chemistry 279, 2609826104.CrossRefGoogle ScholarPubMed
Stoger, R., Williams, S., Christou, P., Down, R.E. & Gatehouse, J.A. (1999) Expression of the insecticidal lectin from snowdrop (Galanthus nivalis agglutinin; GNA) in transgenic wheat plants: effects on predation by the grain aphid Sitobion avenae. Molecular Breeding 5, 6573.CrossRefGoogle Scholar
Thompson, G.A. & Goggin, F.L. (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany 57, 755766.CrossRefGoogle ScholarPubMed
Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 139745.CrossRefGoogle ScholarPubMed
Tjallingii, W.F. & Hogen Esch, T. (1993) Fine-structure of aphid stylet routes in plant-tissues in correlation with EPG signals. Physiological Entomology 18, 317328.CrossRefGoogle Scholar
Urbanska, A., Tjallingii, W.F., Dixon, A.F.G. & Leszczynski, B. (1998) Phenol oxidising enzymes in the grain aphid's saliva. Entomologia Experimentalis et Applicata 86, 197203.CrossRefGoogle Scholar
Van Bel, A.J.E. (2003) The phloem, a miracle of ingenuity. Plant Cell and Environment 26, 125149.CrossRefGoogle Scholar
Vasconcelos, I.M. & Oliveira, J.T.A. (2004) Antinutritional properties of plant lectins. Toxicon 44, 385403.CrossRefGoogle ScholarPubMed
Vijayan, M. & Chandra, N. (1999) Lectins. Current Opinion in Structural Biology 9, 707714.CrossRefGoogle ScholarPubMed
Voelckel, C., Weisser, W.W. & Baldwin, I.T. (2004) An analysis of plant-aphid interactions by different microarray hybridization strategies. Molecular Ecology 13, 31873195.CrossRefGoogle ScholarPubMed
Wagner, U., Edwards, R., Dixon, D.P. & Mauch, F. (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Molecular Biology 49, 515532.CrossRefGoogle ScholarPubMed
Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195216.CrossRefGoogle ScholarPubMed
Will, T. & van Bel, A.J.E. (2006) Physical and chemical interactions between aphids and plants. Journal of Experimental Botany 57, 729737.CrossRefGoogle ScholarPubMed
Yan, J., Wang, J. & Zhang, H. (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. The Plant Journal 29, 193202.CrossRefGoogle Scholar
Yang, K.Y., Kim, E.Y., Kim, C.S., Guh, J.O., Kim, K.C. & Cho, B.H. (1998) Characterization of a glutathione S-transferase gene AtGST1 in Arabidopsis thaliana. Plant Cell Reports 17, 700704.CrossRefGoogle Scholar
Yang, K.Y., Im, Y.J., Chung, G.C. & Cho, B.H. (2002) Activity of the Arabidopsis blue copper-binding protein gene promoter in transgenic tobacco plants upon wounding. Plant Cell Reports 20, 987991.CrossRefGoogle Scholar
York, W.S., Qin, Q.A. & Rose, J.K.C. (2004) Proteinaceous inhibitors of endo-beta-glucanases. Biochimica et Biophysica Acta-Proteins and Proteomics 1696, 223233.CrossRefGoogle ScholarPubMed
Zhou, J.M. & Goldsbrough, P.B. (1993) An Arabidopsis gene with homology to glutathione S-transferases is regulated by ethylene. Plant Molecular Biology 22, 517523.CrossRefGoogle ScholarPubMed
Zhou, N., Tootle, T.L., Tsui, F., Klessig, D.F. & Glazebrook, J. (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10, 10211030.CrossRefGoogle ScholarPubMed
Zhu, T. (2003) Global analysis of gene expression using GeneChip microarrays. Current Opinion in Plant Biology 6, 418425.CrossRefGoogle ScholarPubMed
Zhu, T., Budworth, P., Han, B., Brown, D., Chang, H-S., Zou, G. & Wang, X. (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: Parallel analysis of 8300 genes by a high-density oligonucleotide probe array. Plant Physiology and Biochemistry 39, 221242.CrossRefGoogle Scholar
Zhu-Salzman, K., Salzman, R.A., Ahn, J.E. & Koiwa, H. (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiology 134, 420431.CrossRefGoogle ScholarPubMed