Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory

Journal of Chemical Ecology

Volumn 36, Issue 3, 2010, Pages 260-276

  Smith, Charles Michael ^a   Liu, Xuming ^a   Wang, Liang J ^b   Liu, Xiang ^c   Chen, Ming Shun ^d   Starkey, Sharon ^a   Bai, Jianfa ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b CLEMSON UNIVERSITY   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Diuraphis noxia; Insect; Microarray; Northern blot; Oxylipin signaling; Plant defense; Real time polymerase chain reaction (PCR); Russian wheat aphid; Triticum aestivum; Wheat

Indexed keywords

OXYLIPIN; PHEROMONE; REACTIVE OXYGEN METABOLITE;

ALLELOCHEMICAL; APHID; BARLEY; CHLOROPHYLL; CROP YIELD; ELECTROKINESIS; GENE EXPRESSION; HERBIVORY; PHYTOCHEMISTRY; PLANT DEFENSE; PLANT-INSECT INTERACTION; POLYMERASE CHAIN REACTION; REAL TIME; WHEAT;

ANIMAL; ANIMAL FOOD; APHID; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; METABOLISM; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME; WHEAT;

ANIMAL FEED; ANIMALS; APHIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; OXYLIPINS; PHENOTYPE; PHEROMONES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TIME FACTORS; TRITICUM;

APHIDIDAE; ARTHROPODA; DIURAPHIS NOXIA; HEXAPODA; HORDEUM; TRITICUM AESTIVUM;

EID: 77952321073     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-010-9756-8     Document Type: Article

References (94)

1. Argandona, V. H., Chaman, M., Cardemil, L., Munoz, O., Zuniga, G. A., and Corchera, L. J. 2001. Ethylene production and peroxidase activities in aphid-infested barley. J. Chem. Ecol. 27: 53-68.
2. Bairoch, A., Apweiler, R., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M., Martin, M. J., Natale, D. A., O'Donovan, C., Redaschi, N., and Yeh, L. S. 2005. The universal protein resource (UniProt). Nucleic Acids Res. 33: D154-D159.
3. Basky, Z. 2003. Biotypic and pest status differences between Hungarian and South African populations of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae). Pest Manag. Sci. 59: 1152-1158.
4. Berzonsky, W., Shanower, T., Lamb, R., Mckenzie, R., Ding, H., Harris, M. O., Peairs, F., Haley, S., Porter, D., and Ratcliffe, R. H. 2003. Breeding wheat for resistance to insects. Plant Breed. Rev. 22: 221-296.
5. 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 Rep. 25: 41-54.
6. Boyko, E. V., Smith, C. M., Vankatappa, T., Bruno, J., Deng, Y., Starkey, S. R., and Klaahsen, D. 2006. The molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-like sequences modulate aphid-wheat interaction. J. Econ. Entomol. 99: 1430-1445.
7. Broeckling, C. D., Reddy, I. R., Duran, A. L., Zhao, X., and Sumner, L. W. 2006. MET-IDEA: a data extraction tool for mass spectrometry-based metabolomics. Anal. Chem. 78: 4334-4341.
8. Burd, J. D. and Elliott, N. C. 1996. Changes in chlorophyll α fluorescence induction kinetics in cereals infested with Russian wheat aphid (Homoptera: Aphididae). J. Econ. Entomol. 89: 1332-1337.
9. Burd, J. D., Porter, D. R., Puterka, G. J., Haley, S. D., and Peairs, F. B. 2006. Biotypic variation among North American Russian wheat aphid (Homoptera: Aphididae) populations. J. Econ. Entomol. 99: 1862-1866.
10. Camon, E., Magrane, M., Barrell, D., Binns, D., Fleischmann, W., Kersey, P., Mulder, N., Oinn, T., Maslen, J., Cox, A., and Apweiler, R. 2003. The gene ontology annotation (GOA) project: implementation of GO in SWISS-PROT, TrEMBL, and InterPro. Genome Res. 13: 662-672.
11. Chen, M.-S., Fellers, J. P., Stuart, J. J., Reese, J. C., and Liu, X. 2004. A group of related cDNAs encoding secreted proteins from Hessian fly [Mayetiola destructor (say)] salivary glands. Insect Mol. Biol. 13: 101-108.
12. Ciepiela, A. 1989. Biochemical basis of winter wheat resistance to the grain aphid, Sitobion avenae. Entomol. Exp. Appl. 51: 269-275.
13. Collinge, M. and Boller, T. 2001. Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol. Biol. 46: 521-529.
14. 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.
15. Devonshire, A. L. and Field, L. M. 1991. Gene amplification and insecticide resistance. Annu. Rev. Entomol. 36: 1-23.
16. Dhondt, S., Geoffroy, P., Stelmach, B. A., Legrand, M., and Heitz, T. 2000. Soluble phospholipase A(2) activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J. 23: 431-440.
17. 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: 517-540.
18. Dolatti, L., Ghareyazie, B., Moharramipour, S., and Noori-Daloii, M. R. 2005. Evidence for regional diversity and host adaptation in Iranian populations of the Russian wheat aphid. Entomol. Exp. Appl. 114: 171-180.
19. Dong, J., Chen, C., and Chen, Z. 2003. Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 51: 21-37.
20. Dong, H.-P., Peng, J., Bao, Z., Meng, X., Bonasera, J. M., Chen, G., Beer, S. V., and Dong, H. 2004. Downstream divergence of the ethylene signaling pathway for harpin-stimulated arabidopsis growth and insect defense. Plant Physiol. 136: 3628-3638.
21. Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogensis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54: 97-114.
22. Forslund, K., Perrersson, J., Bryngelsson, T., and Jonsson, L. 2000. Aphid infestation induces PR-proteins differentially in barley susceptible or resistant to the bird cherry-oat aphid. Physiol. Plant. 110: 496-502.
23. Gatehouse, A. M. R. and Boulter, D. 1983. Assessment of the antimetabolic effects of trypsin-inhibitors from cowpea (Vigna unguiculata) and other legumes on development of the bruchid beetle Callosobruchus maculatus. J. Sci. Food Agric. 34: 345-350.
24. Gaupels, F., Buhtz, A., Knauer, T., Deshmukh, S., Waller, F., van Bel, A. J. E., Kogel, K.-H., and Kehr, J. 2008. Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J. Exp. Bot. 59: 3297-3306.
25. Harvey, T. L. and Martin, T. J. 1990. Resistance to Russian wheat aphid Diuraphis noxia, in wheat (Triticum aestivum). Cereal Res. Commun. 18: 127-129.
26. Hein, G. L. 1992. Influence of plant growth on Russian wheat aphid, Diuraphis noxia (Homoptera: Aphididae). Reproduction and damage symptom expression. J. Kans. Entomol. Soc. 65: 369-376.
27. 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 cartenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J. Econ. Entomol. 96: 475-481.
28. Huang, X. and Madan, A. 1999. CAP3: a DNA sequence assembly program. Genome Res. 9: 868-877.
29. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. 2001. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209.
30. Kalde, M., Barth, M., Somssich, I. E., and Lippok, B. 2003. Members of Arabidopsis WRKY group III transcripton factors are a part of different plant defense signaling pathways. Mol. Plant-Microb. Interact. 16: 295-305.
31. Kaloshian, I. 2004. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30: 2419-2438.
32. Kaloshian, I., Kinser, M. G., Ullman, D. E., and Willamson, V. M. 1997. The impact of Meu1-mediated resistance in tomato on longevity, fecundity, and behavior of the potato aphid, Macrosiphum euphorbiae. Entomol. Exp. Appl. 83: 181-187.
33. Kawano, T. 2003. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep. 21: 829-837.
34. Kempema, L. A., Xinping, C., Holzer, F. M., and Walling, L. L. 2007. Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol. 143: 850-865.
35. 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: 654-1662.
36. Klingler, J., Creasy, R., Gao, L., Nair, R. M., Calix, A. S., Jacob, H. S., Edwards, O. R., and Singh, K. B. 2005. Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiol. 137: 1445-1455.
37. Koornneef, A., Leon-Rayes, A., Ritsema, T., Verhage, A., Den Otter, F. C., van Loon, L. C., and Pieterse, C. M. J. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147: 1358-1368.
38. Lacock, L. C., van Niekerk, S., Loots, F., du Preez, F. B., and Botha, A. M. 2003. Functional and comparative analysis of expressed sequences from Diuraphis noxia infested wheat obtained utilizing the conserved nucleotide binding site. African J. Biotechnol. 2: 75-81.
39. 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 different categories of resistance. J. Econ. Entomol. 102: 1291-1300.
40. Li, J., Brader, G., and Palva, E. T. 2004. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: 319-331.
41. 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: 185-195.
42. Liechti, R. and Farmer, E. E. 2002. The jasmonate pathway. Science 296: 1649-1650.
43. Liu, X. M., Smith, C. M., Gill, B. S., and Tolmay, V. 2001. Microsatellite markers linked to six Russian wheat aphid resistance genes in wheat. Theor. Appl. Genet. 102: 504-510.
44. Liu, X. M., Smith, C. M., and Gill, B. S. 2005. Allelic relationships among Russian wheat aphid resistance genes. Crop Sci. 45: 2273-2280.
45. 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.
46. Lou, Y. and Baldwin, I. T. 2006. Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores. Plant Physiol. 140: 1126-1136.
47. Malinga, J. N., Kinuya, M. G., Kamau, A. W., Wanjama, J. K., Awalla, J. O., and Pathak, R. S. 2007. Biotypic and genetic variation within tropical populations of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae) in Kenya. J. Entomol. 4: 350-361.
48. Mao, P., Duan, W., Wei, C., and Li, Y. 2007. WRKY62 transcriptional factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. Plant Cell Physiol. 48: 833-842.
49. 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.
50. Miles, P. W. 1999. Aphid saliva. Biol. Rev. 74: 41-85.
51. Miller, H. L., Neese, P. A., Ketring, D. L., and Dillwith, J. W. 1994. Involvement of ethylene in aphid infestation of barley. J. Plant Growth Regul. 13: 167-171.
52. Miller, B., Madilao, L., Ralph, S., and Bohlmann, J. 2005. Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol. 137: 369-382.
53. Moraes, R. A., Sales, M. P., Pinto, M. S. P., Silva, L. B., Oliveira, A. E. A., Machado, O. L. T., Fernández, K. V. S., and Xavier-Filho, J. 2000. Lima bean (Phaseolus lunatus) seed coat phaseolin is detrimental to the cowpea weevil (Callosobruchus maculatus). Braz. J. Med. Biol. Res. 33: 191-198.
54. Moran, P. J. and Thompson, G. A. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125: 1074-1085.
55. Moran, P. J., Cheng, Y. F., 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.
56. Panda, N. and Khush, G. S. 1995. Host Plant Resistance to Insects. CAB/International Rice Research Institute, Wallingford.
57. Park, S. J., Huang, Y. H., and Ayoubi, P. 2006. Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 223: 932-947.
58. Park, D.-S., Yi, G.-H., Lee, J.-H., Kwak, D.-Y., Yeo, U.-S., Oh, B.-G., Nam, M.-H., Goo, Y.-C., and Kim, H.-Y. 2007. The identification of candidate rice genes that confer resistant to the brown planthopper (Nilaparvata lugens) through representational difference analysis. Theor. Appl. Genet. 115: 537-547.
59. Prinsloo, G. J. 2000. Host and host instar preference of Aphelinus sp. nr. varipes (Hymenoptera: Aphelinidae), a parasitoid of cereal aphids (Homoptera: Aphididae) in South Africa. Afr. Entomol. 8: 57-61.
60. Quick, J. S., Ellis, G. E., Normann, R. M., Stromberger, J. A., Shanahan, J. F., Peairs, F. B., Rudolph, J. B., and Lorenz, K. 1996. Registration of 'Halt' wheat. Crop Sci. 36: 210.
61. Quisenberry, S. S. and Peairs, F. B. 1998. A Response Model for an Introduced Pest-The Russian Wheat Aphid. Thomas Say Publications in Entomology, Entomol. Soc. Am., Lanham.
62. Reese, J. C., Schwenke, J. R., Lamont, P. S., and Zehr, D. D. 1994. Importance and quantification of plant tolerance in crop pest management programs for aphids: greenbug resistance in sorghum. J. Agric. Entomol. 11: 255-270.
63. Salzman, R. A., Brady, J. A., Finlayson, S. A., Buchanan, C. D., Summer, E. J., Sun, F., Klein, P. E., Klein, R. R., Pratt, L. H., Cordonnier-Pratt, M-M., and Mullet, J. E. 2005. Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol. 138: 352-368.
64. Sardesai, N., Subramanyam, S., Nemacheck, J., and Williams, C. E. 2005. Modulation of defense-response gene expression in wheat during Hessian fly larval feeding. J. Plant Interact. 1: 39-50.
65. SAS Institute Inc. 2001. SAS/STAT Software Version 9. 1. SAS Institute, Cary, NC.
66. Scharrenberg, C., Falk, J., Quast, S., Haussuhl, K., Humbeck, K., and Krupinska, K. 2003. Isolation of senescence-related cDNAs from flag leaves of field grown barley plants. Physiol. Plant. 118: 278-288.
67. Schmelz, E. A., Engelberth, J., Tumlinson, J. H., Block, A., and Alborn, H. T. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J. 39: 790-808.
68. Schmidt, D. D., Voelckel, C., Hartl, M., Schmidt, S., and Baldwin, I. T. 2005. Specificity in ecological Interactions. Attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two solanaceous host plants. Plant Physiol. 138: 1763-1773.
69. Smith, C. M. 1989. Plant Resistance to Insects: A Fundamental Approach. Wiley, New York.
70. Smith, C. M. 2004. Plant resistance against pests: issues and strategies, pp. 147-167, in O. Koul, G. S. Dhaliwal, and G. Cuperus (eds.). Integrated Pest Management: Potential, Constraints and Challenges. CABI Publ., Oxon.
71. Smith, C. M. 2005. Plant Resistance to Arthropods-Molecular and Conventional Approaches. Springer, The Netherlands.
72. Smith, C. M. and Boyko, E. V. 2006. Mini Review: the molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol. Exp. Appl. 122: 1-16.
73. Smith, C. M., Schotzko, D. J., Zemetra, R. S., Souza, E. J., and Schroeder-Teeter, S. 1991. Identification of Russian wheat aphid (Homoptera, Aphididae) resistance in wheat. J. Econ. Entomol. 84: 328-332.
74. Smith, C. M., Belay, T., Stauffer, C., Stary, P., Kubeckova, I., and Starkey, S. 2004. Identification of Russian wheat aphid (Homoptera: Aphididae) biotypes virulent to the Dn4 resistance gene. J. Econ. Entomol. 97: 112-117.
75. Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J. P., van Pelt, J. A., Mueller, M. J., Buchala, A. J., Metraux, J.-P., Brown, R., and Kazan, K., et al. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770.
76. Stintzi, A., Weber, H., Reymond, P., Browse, J., and Farmer, E. E. 2001. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl. Acad. Sci. U. S. A. 98: 12837-12842.
77. Taki, N., Sasaki-Sekimoto, Y., Obayashi, T., Kikuta, A., Kobayashi, K., Ainai, T., Yagi, K., Sakurai, N., Suzuki, H., Masuda, T., Takamiya, K., Shibata, D., Kobayashi, Y., and Ohta, H. 2005. 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol. 139: 1268-1283.
78. Theodoulou, F. L., Job, K., Slocombe, S. P., Footitt, S., Holdsworth, M., Baker, A., Larson, T. R., and Graham, I. A. 2005. Jasmonic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol. 137: 835-840.
79. 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.
80. Tolmay, V. L., Lindeque, R. C., and Prinsloo, G. L. 2007. Preliminary evidence of a resistance-breaking biotype of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), in South Africa. Afr. Entomol. 15: 228-230.
81. Turner, J. G., Ellis, C., and Devoto, A. 2002. The jasmonate signal pathway. Plant Cell 14(suppl): S153-S164.
82. Urbanska, A., Tjallingii, W. F., Dixon, A. F. G., and Leszczynski, B. 1998. Phenol oxidizing enzymes in the grain aphid's saliva. Entomol. Exp. Appl. 86: 197-203.
83. van de Ven, W. T. G., Levesque, C. S., Perring, T. M., and Walling, L. L. 2000. Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12: 1409-1423.
84. van Loon, L. C., Rep, M., and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44: 135-162.
85. 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.
86. Voothuluru, P., Meng, J., Khajuria, C., Louis, J., Zhu, L., Starkey, S., Wilde, G. E., Baker, C. A., and Smith, C. M. 2006. Categories and inheritance of resistance to Russian wheat aphid (Homoptera: Aphididae) Biotype 2 in a selection from wheat cereal introduction 2401. J. Econ. Entomol. 99: 1854-1861.
87. Vos, P., Simons, G., Jesse, T., Wijbrandi, J., and Heinen, L. et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16: 1315-1316.
88. Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19: 195-216.
89. Wang, L. and Zhang, Y. 2004. Data integration and target selection for Medicago genomics, pp. 275-288, in A. Hopkins, Z.-Y. Wang, R. Mian, M. Sledge, and R. E. Barker (eds.). Developments in Plant Breeding: Molecular Breeding of Forage and Turf. Kluwer Academic Publishers, Dordrecht.
90. Xiong, L. Z., Lee, M. W., Qi, M., and Yang, Y. N. 2001. Identification of defense-relate rice genes by suppression subtractive hybridization and differential screening. Mol. Plant Microbe Interact. 14: 685-692.
91. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D. A., and Raskin, I. 1991. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809-818.
92. Zhang, H., Sreenivasulu, N., Weschke, W., Stein, N., Rudd, S., Radchuk, V., Potokina, E., Scholz, U., Schweizer, P., Zierold, U., Langridge, P., Varshney, R. K., Wobus, U., and Graner, U. 2004. Large-scale analysis of the barley transcriptome based on expressed sequence tags. Plant J. 40: 276-290.
93. Zhu, J. K. 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53: 247-273.
94. Zhu-Salzman, K., Salzman, R. A., Ahn, J., and Koiwa, H. 2004. Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol. 134: 420-431.