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

Volumn 97, Issue 5, 2007, Pages 523-532

  Couldridge, C ^a   Newbury, H J ^a   Ford Lloyd, B ^a   Bale, J ^a   Pritchard, J ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Aphid feeding; Defence; Functional genomics; Microarray Arabidopsis thaliana; Myzus persicae; Phloem; Sieve element

Indexed keywords

ARABIDOPSIS PROTEIN;

ANGIOSPERM; APHID; FEEDING; GENE EXPRESSION; METABOLISM; PHLOEM; PLANT DEFENSE; SIGNALING;

ANIMAL; APHID; ARABIDOPSIS; ARTICLE; CALCIUM SIGNALING; CARBOHYDRATE METABOLISM; CELL WALL; CLASSIFICATION; DNA MICROARRAY; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATIVE STRESS; PARASITOLOGY; PHLOEM; PHYSIOLOGY;

ANIMALS; APHIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM SIGNALING; CARBOHYDRATE METABOLISM; CELL WALL; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PHLOEM;

APHIDIDAE; ARABIDOPSIS; ARABIDOPSIS THALIANA; HEXAPODA; MYZUS PERSICAE;

EID: 34548741060     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S0007485307005160     Document Type: Article

References (96)

1. Abate, T., van Huis, A. & Ampofo, J.K.O. (2000) Pest management strategies in traditional agriculture: An African perspective. Annual Review of Entomology 45, 631-659.
2. 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, 3084-3097.
3. 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, 1473-1481.
4. 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, 7262-7266.
5. 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, 289-300.
6. Bergey, D.R. & Ryan, C.A. (1999) Wound- and systemin-inducible calmodulin gene expression in tomato leaves. Plant Molecular Biology 40, 815-823.
7. 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, 568-577.
8. 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, 1499-1510.
9. Cherqui, A. & Tjallingii, W.F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. Journal of Insect Physiology 46, 1177-1186.
10. 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, 147-160.
11. 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, 699-708.
12. 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, 745-757.
13. Desveaux, D., Marechal, A. & Brisson, N. (2005) Whirly transcription factors: Defense gene regulation and beyond. Trends in Plant Science 10, 95-102.
14. 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, 923-937.
15. 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, 235-251.
16. 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, 114-128.
17. 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, 517-540.
18. Dixon, D.P., Skipsey, M., Grundy, N.M. & Edwards, R. (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiology 138, 2233-2244.
19. 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, 631-637.
20. 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, 3183-3193.
21. Dong, X. (2004) The role of membrane-bound ankyrin-repeat protein ACD6 in programmed cell death and plant defense. Science's STKE 221, 6.
22. Douglas, A.E. (2003) The nutritional physiology of aphids. Advances in Insect Physiology 31, 73-140.
23. 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, 1-32.
24. 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, 1129-1144.
25. 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, 1672-1682.
26. 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, 896-903.
27. 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, 5400-5411.
28. 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, 97-114.
29. 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, 60-69.
30. 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, 381-392.
31. 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, 666-677.
32. 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, 383-397.
33. 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, 769-779.
34. 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, 4203-4213.
35. 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, 447-458.
36. 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, 636-641.
37. 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.
38. 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, 613-620.
39. Lamport, D.T.A. & Kieliszewski, M.J. (2005) Stress upregulates periplasmic arabinogalactan-proteins. Plant Biosystems 139, 60-64.
40. 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, 9834-9839.
41. 2+ calmodulin in Arabidopsis thaliana. Molecular and General Genetics 258, 412-419.
42. Li, X.C., Schuler, M.A. & Berenbaum, M.R. (2002) Jasmonate and salicylate induce expression of herbivore cytochrome p450 genes. Nature 419, 712-715.
43. 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, 750-757.
44. Mahalingam, R., Shah, N., Scrymgeour, A. & Fedoroff, N. (2005) Temporal evolution of the Arabidopsis oxidative stress response. Plant Molecular Biology 57, 709-730.
45. 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, 231-239.
46. Miles, P.W. (1999) Aphid saliva. Biological Reviews 74, 41-85.
47. Miles, P.W. & Oertli, J.J. (1993) The significance of antioxidants in the aphid-plant interaction - the redox hypothesis. Entomologia Experimentalis et Applicata 67, 275-283.
48. 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, 74-84.
49. 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, 182-203.
50. 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, 4097-4105.
51. 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, 187-195.
52. 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, 743-751.
53. 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, 45248-45254.
54. Ogawa, K. (2005) Glutathione-associated regulation of plant growth and stress responses. Antioxidants & Redox Signaling 7, 973-981.
55. 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, 239-247.
56. Oparka, K.J. (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends in Plant Science 9, 33-41.
57. Pavlidis, P., Qinghong, L. & Stafford Nobel, W. (2003) The effect of replication on gene expression microarray experiments. Bioinformatics 19, 1620-1627.
58. 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, 1927-1934.
59. 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, 203-210.
60. 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, 1-9.
61. Prado, E. & Tjallingii, W.F. (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis et Applicata 82, 189-200.
62. 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.
63. 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, 145-152.
64. Reddy, V.S. & Reddy, A.S.N. (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65, 1745-1776.
65. 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, 2105-2110.
66. 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, 1558-1569.
67. 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, 33-40.
68. 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, 432-438.
69. 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, 31-44.
70. 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, 279-292.
71. 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, 6281-6292.
72. Sjölund, R.D. (1997) The phloem sieve element: a river runs through it. Plant Cell 9, 1137-1146.
73. 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, 1213-1222.
74. 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, 433-442.
75. 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 benoxacorand copper-treated seedlings. Journal of Biological Chemistry 279, 26098-26104.
76. 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, 65-73.
77. Thompson, G.A. & Goggin, F.L. (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany 57, 755-766.
78. Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 139-745.
79. Tjallingii, W.F. & Hogen Esch, T. (1993) Fine-structure of aphid stylet routes in plant-tissues in correlation with EPG signals. Physiological Entomology 18, 317-328.
80. 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, 197-203.
81. Van Bel, A.J.E. (2003) The phloem, a miracle of ingenuity. Plant Cell and Environment 26, 125-149.
82. Vasconcelos, I.M. & Oliveira, J.T.A. (2004) Antinutritional properties of plant lectins. Toxicon 44, 385-403.
83. Vijayan, M. & Chandra, N. (1999) Lectins. Current Opinion in Structural Biology 9, 707-714.
84. 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.
85. 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, 515-532.
86. Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195-216.
87. Will, T. & van Bel, A.J.E. (2006) Physical and chemical interactions between aphids and plants. Journal of Experimental Botany 57, 729-737.
88. 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, 193-202.
89. 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, 700-704.
90. 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, 987-991.
91. 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, 223-233.
92. Zhou, J.M. & Goldsbrough, P.B. (1993) An Arabidopsis gene with homology to glutathione S-transferases is regulated by ethylene. Plant Molecular Biology 22, 517-523.
93. 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, 1021-1030.
94. Zhu, T. (2003) Global analysis of gene expression using GeneChip microarrays. Current Opinion in Plant Biology 6, 418-425.
95. 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, 221-242.
96. 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, 420-431.