Transcriptome analysis of soybean lines reveals transcript diversity and genes involved in the response to common cutworm (Spodoptera lituraFabricius) feeding

Plant, Cell and Environment

Volumn 37, Issue 9, 2014, Pages 2086-2101

  Wang, Yongli ^a   Wang, Hui ^a   Fan, Rui ^b   Yang, Qing ^a   Yu, Deyue ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b QUZHOU UNIVERSITY   (China)

Author keywords

Induced resistance; Microarray; Spatiotemporal analysis

Indexed keywords

GLYCINE MAX; HEXAPODA; SPODOPTERA; SPODOPTERA LITURA;

MESSENGER RNA;

ANALYSIS OF VARIANCE; ANIMAL; CLUSTER ANALYSIS; DOWN REGULATION; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT GENE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOYBEAN; SPATIOTEMPORAL ANALYSIS; SPODOPTERA; TIME; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; CLUSTER ANALYSIS; DOWN-REGULATION; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SOYBEANS; SPATIO-TEMPORAL ANALYSIS; SPODOPTERA; TIME FACTORS; UP-REGULATION;

EID: 84904976655     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12296     Document Type: Article

References (119)

1. Alborn H.T., Rose U.S.R. & McAuslane H.J. (1996) Systemic induction of feeding deterrents in cotton plants by feeding of Spodoptera spp Larvae. Journal of Chemical Ecology 22, 919-932.
2. Arimura G., Tashiro K., Kuhara S., Nishioka T., Ozawa R. & Takabayashi J. (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochemical and Biophysical Research Communications 277, 305-310.
3. Baldwin I.T. (1988) The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77, 378-381.
4. Baldwin I.T. & Schmelz E.A. (1996) Immunological 'memory' in the induced accumulation of nicotine in wild tobacco. Ecology 77, 236-246.
5. Baldwin I.T., Zhang Z.P., Diab N., Ohnmeiss T.E., McCloud E.S., Lynds G.Y. & Schmelz E.A. (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201, 397-404.
6. Baldwin I.T., Halitschke R., Kessler A. & Schittko U. (2001) Merging molecular and ecological approaches in plant-insect interactions. Current Opinion in Plant Biology 4, 351-358.
7. Beckers G.J.M. & Spoel S.H. (2006) Fine-tuning plant defense signalling: salicylate versus jasmonate. Plant Biology 8, 1-10.
8. Belle A., Tanay A., Bitincka L., Shamir R. & O'Shea E.K. (2006) Quantification of protein half-lives in the budding yeast proteome. Proceedings of the National Academy of Sciences of the United States of America 103, 13004-13009.
9. Beyer A., Hollunder J., Nasheuer H.P. & Wilhelm T. (2004) Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale. Molecular & Cellular Proteomics: MCP 3, 1083-1092.
10. Bostock R.M. (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytopathology 43, 545-580.
11. Botella M.A., Xu Y., Prabha T.N., Zhao Y., Narasimhan M.L., Wilson K.A. & Hasegawa P.M. (1996) Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiology 112, 1201-1210.
12. Bradley D.J., Kjellbom P. & Lamb C.J. (1992) Elicitor-and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70, 21-30.
13. Broadway R.M. (1996) Dietary proteinase inhibitors alter complement of midgut proteases. Archives of Insect Biochemistry and Physiology 32, 39-53.
14. Brodbeck B.V., Mizell R.F. & Andersen P.C. (1993) Physiological and behavioral adaptations of three species of leafhoppers in response to the dilute nutrient content of xylem fluid. Journal of Insect Physiology 39, 73-81.
15. Bryant J.P., Heitkönig I., Kuropat P. & Owen-Smith N. (1991) Effects of severe defoliation on the long-term resistance to insect attack and on leaf chemistry in six woody species of the southern African savanna. American Naturalist 137, 50-63.
16. Chen H., Seguin P., Archambault A., Constan L. & Jabaji S. (2009) Gene expression and isoflavone concentrations in soybean sprouts treated with chitosan. Crop Science 49, 224-236.
17. Constabel C.P. & Ryan C.A. (1998) A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47, 507-511.
18. Constabel C.P., Bergey D.R. & Ryan C.A. (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proceedings of the National Academy of Sciences of the United States of America 92, 407-411.
19. Constabel C.P., Yip L., Patton J.J. & Christopher M.E. (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiology 124, 285-296.
20. Couldridge C., 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.
21. Croxford A.C., Edwards P.J. & Wratten S.D. (1989) Temporal and spatial variation in palatability of soybean and cotton leaves following wounding. Oecologia 79, 520-525.
22. Cui Z.L. & Gai J.Y. (1997) A study of leaf-feeding insect species on soybeans in Nanjing area. Soybean Science 16, 12-20.
23. von Dahl C.C. & Baldwin I.T. (2007) Deciphering the role of ethylene in plant-herbivore interactions. Journal of Plant Growth Regulation 26, 201-209.
24. De Vos M., Van Zaanen W., Koornneef A., Korzelius J.P., Dicke M., Van Loon L.C. & Pieterse C.M. (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology 142, 352-363.
25. DeBoer K.D., Lye J.C., Aitken C.D., Su A.K.K. & Hamill J.D. (2009) The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis. Plant Molecular Biology 69, 299-312.
26. Dhaubhadel S., Kuflu K., Romero M.C. & Gijzen M. (2005) A soybean seed protein with carboxylate-binding activity. Journal of Experimental Botany 56, 2335-2344.
27. Du H., Huang Y. & Tang Y. (2010) Genetic and metabolic engineering of isoflavonoid biosynthesis. Applied Microbiology and Biotechnology 86, 1293-1312.
28. Edwards P.J., Wratten S.D. & Parker E.A. (1992) The ecological significance of rapid wound-induced changes in grazing and plant competition. Oecologia 91, 266-272.
29. Ehlting J., Chowrira S.G., Mattheus N., Aeschliman D.S., Arimura G.-I. & Bohlmann J. (2008) Comparative transcriptome analysis of Arabidopsis thaliana infested by diamond back moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signaling. BMC Genomics 9, 154.
30. Eulgem T. & Somssich I.E. (2007) Networks of WRKY transcription factors in defense signaling. Current Opinion in Plant Biology 10, 366-371.
31. Fan J., Chen C.X., Yu Q.B., Brlansky R.H., Li Z.G. & Gmitter F.G. (2011) Comparative iTRAQ proteome and transcriptome analyses of sweet orange infected by 'Candidatus Liberibacter asiaticus'. Physiologia Plantarum 143, 235-245.
32. Fan R., Wang H., Wang Y.L. & Yu D.Y. (2012) Proteomic analysis of soybean defense response induced by cotton worm (Prodenia litura, fabricius) feeding. Proteome Science 10, 16.
33. Fehr W.R., Burmood C.E. & Pennington D.T. (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill1. Crop Science 11, 929-931.
34. Glazebrook J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227.
35. Gordon A.J., Minchin F.R., Skot L. & James C.L. (1997) Stress-induced declines in soybean N2 fixation are related to nodule sucrose synthase activity. Plant Physiology 114, 937-946.
36. Green T.R. & Ryan C.A. (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175, 776-777.
37. Hall D.E., Robert J.A., Keeling C.I., Domanski D., Qesada A.L., Jancsik S., ... Bohlmann J. (2011) An integrated genomic, proteomic, and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes which are resistant or susceptible to white pine weevil. The Plant Journal 65, 936-948.
38. Hammerschmidt R., Lamport D.T.A. & Muldoon E.P. (1984) Cell wall hydroxyproline enhancement and lignin deposition as an early event in the resistance of cucumber to Cladosporium cucumerinum. Physiological Plant Pathology 24, 43-47.
39. Haukioja E. & Niemelä P. (1979) Birch leaves as a resource for herbivores: seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. Oecologia 39, 151-159.
40. Havill N.P. & Raffa K.F. (1999) Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera: Lymantriidae) development and feeding behavior. Oecologia 120, 295-303.
41. Heil M. & Ton J. (2008) Long-distance signalling in plant defence. Trends in Plant Science 13, 264-272.
42. Heim U., Weber H., Bäumlein H. & Wobus U. (1993) A sucrose-synthase gene of Vicia faba L.: expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta 191, 394-401.
43. Hermsmeier D., Schittko U. & Baldwin I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defence-related plant mRNAs. Plant Physiology 125, 683-700.
44. Huang J.F., Bantroch D.J., Greenwood J.S. & Staswick P.E. (1991) Methyl jasmonate treatment eliminates cell-specific expression of vegetative storage protein genes in soybean leaves. Plant Physiology 97, 1512-1520.
45. Hui D.Q., Iqbal J., 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 herbivore-induced mRNAs. Plant Physiology 131, 1877-1893.
46. Hunter M.D. (1987) Opposing effects of spring defoliation on late season oak caterpillars. Ecological Entomology 12, 373-382.
47. Jongsma M.A. & Bolter C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology 3, 885-895.
48. Jouanin L., Bonadé-Bottino M., Girard C., Morrot G. & Giband M. (1998) Transgenic plants for insect resistance. Plant Science 131, 1-11.
49. Karban R. & Myers J.H. (1989) Induced plant responses to herbivory. Annual Review of Ecology and Systematics 20, 331-348.
50. Karban R., Agrawal A.A. & Mangel M. (1997) The benefits of induced defenses against herbivores. Ecology 78, 1351-1355.
51. 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 143, 849-865.
52. Kessler A. & Baldwin I.T. (2002) Plant response to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299-328.
53. Kim K.N., Cheong Y.H., Gupta R. & Luan S. (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiology 124, 1844-1853.
54. Ko J.H. & Han K.H. (2004) Arabidopsis whole-transcriptome profiling defines the features of coordinated regulations that occur during secondary growth. Plant Molecular Biology 55, 433-453.
55. Kogan M. (1972) Feeding and nutrition of insects associated with soybeans. 2. Soybean resistance and host preferences of the Mexican bean beetle, Epilachna varivest. Annals of the Entomological Society of America 65, 675-683.
56. Lippert D., Ralph S.G., Phillips M., White R., Smith D., Hardie D., ... Bohlmann J. (2009) Quantitative iTRAQ proteome and comparative transcriptome analysis of elicitor-induced Norway spruce (Picea abies) cells reveals elements of calcium signaling in the early conifer defense response. Proteomics 9, 350-367.
57. Luan S. (2009) The CBL-CIPK network in plant calcium signaling. Trends in Plant Science 14, 37-42.
58. McCloud E.S., Tallamy D.W. & Halaweish F.T. (1995) Squash beetle trenching behaviour: avoidance of cucurbitacin induction or mucilaginous plant sap? Ecological Entomology 20, 51-59.
59. McDowell J.M. & Dangl J.L. (2000) Signal transduction in the plant immune response. Trends in Biochemical Sciences 25, 79-82.
60. McPherson R.M. (2004) XVIII. Soybean insects. In Summary of Losses from Insect Damage and Cost of Control in Georgia 2004 (eds P. Gillebeau, N. Hinkle & P. Roberts ) pp. 37-38. Georgia Cooperative Extension Service, Athens.
61. Major I.T. & Constabel C.P. (2006) Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytologist 172, 617-635.
62. Marchetti S., Delledonne M., Fogher C., Chiaba C., Chiesa F., Savazzini F. & Giordano A. (2000) Soybean Kunitz, C-II and PI-IV inhibitor genes confer different levels of insect resistance to tobacco and potato transgenic plants. Theoretical and Applied Genetics 101, 519-526.
63. Mason H.S. & Mullet J.E. (1990) Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. The Plant Cell Online 2, 569-579.
64. Menke U., Renault N. & Mueller-Roeber B. (2000) StGCPRP, a potato gene strongly expressed in stomatal guard cells, defines a novel type of repetitive proline-rich proteins. Plant Physiology 122, 677-686.
65. Mozoruk J., Hunnicutt L.E., Cave R.D., Hunter W.B. & Bausher M.G. (2006) Profiling transcriptional changes in Citrus sinensis (L.) Osbeck challenged by herbivory from the xylem-feeding leafhopper Homalodisca coagulata (Say) by cDNA macroarray analysis. Plant Science 170, 1068-1080.
66. Nie L., Wu G. & Zhang W.W. (2006) Correlation of mRNA expression and protein abundance affected by multiple sequence features related to translational efficiency in Desulfovibrio vulgaris: a quantitative analysis. Genetics 174, 2229-2243.
67. Nogueira F.T., Schlögl P.S., Camargo S.R. & Fernandez J.H. (2005) SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Science 169, 93-106.
68. Nuruzzaman M., Manimekalai R., Sharoni A.M., Satoh K., Kondoh H., Ooka H. & Kikuchi S. (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465, 30-44.
69. Osier T.L. & Lindroth R.L. (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. Journal of Chemical Ecology 27, 1289-1313.
70. Panthee D.R., Yuan J.S., Wright D.L., Marois J.J., Mailhot D. & Stewart C.N. Jr. (2007) Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Functional & Integrative Genomics 7, 291-301.
71. Paré P.W. & Tumlinson J.H. (1999) Plant volatiles as a defense against insect herbivores. Plant Physiology 121, 325-331.
72. Pieterse C.M.J., Leon-Reyes A., van der Ent S. & van Wees S.C.M. (2009) Networking by small-molecular hormones in plant immunity. Nature Chemical Biology 5, 308-316.
73. Pinheiro G.L., Marques C.S., Costa M.D.B.L., Reis P.A.B., Alves M.S., Carvalho C.M., ... Fontes E.P.B. (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444, 10-23.
74. Ralph S., Yueh H., Friedmann M.F., Aeschliman D., Zeznik J.A., Nelson C.C., ... Bohlmann J. (2006a) Conifer defense against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworm (Choristoneura occidentalis) or white pine weevil (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant, Cell & Environment 29, 1545-1570.
75. Ralph S., Oddy C., Cooper D., Yueh H., Jancsik S., Kolosova N. & Bohlmann J. (2006b) Genomics of hybrid poplar (Populus trichocarpa×deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Molecular Ecology 15, 1275-1297.
76. Reymond P., Weber H., Damond M. & Farmer E.E. (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. The Plant Cell 12, 707-719.
77. Reymond P., Bodenhausen N., Van Poecke R.M., Krishnamurthy V., Dicke M. & Farmer E.E. (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. The Plant Cell Online 16, 3132-3147.
78. Rojo E., Solano R. & Sánchez-Serrano J.J. (2003) Interactions between signaling compounds involved in plant defense. Journal of Plant Growth Regulation 22, 82-98.
79. Roland J. & Myers J.H. (1987) Improved insect performance from host-plant defoliation: winter moth on oak and apple. Ecological Entomology 12, 409-414.
80. Rozen S. & Skaletsky H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132, 365-386.
81. Rushton P.J. & Somssich I.E. (1998) Transcriptional control of plant genes responsive to pathogens. Current Opinion in Plant Biology 1, 311-315.
82. Ryan C.A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annual Review of Phytopathology 28, 425-449.
83. Ryan C.A. (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochimica et Biophysica Acta 1477, 112-121.
84. Ryan C.A. & Moura D.S. (2002) Systemic wound signaling in plants: a new perception. Proceedings of the National Academy of Sciences of the United States of America 99, 6519-6520.
85. Sano H., Seo S., Koizumi N., Niki T., Iwamura H. & Ohashi Y. (1996) Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant & Cell Physiology 37, 762-769.
86. SAS (1989) SAS/STAT User's Guide, SAS Institute, Cary, CA. 889 pp.
87. Schenk P.M., Kazan K., Wilson I., Anderson J.P., Richmond T., Somerville S.C. & Manners J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97, 11655-11660.
88. Schilmiller A.L. & Howe G.A. (2005) Systemic signaling in the wound response. Current Opinion in Plant Biology 8, 369-377.
89. Schwachtje J. & Baldwin I.T. (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiology 146, 845-851.
90. Seldal T., Andersen K.J. & Hogstedt G. (1994) Grazing-induced proteinase inhibitors: a possible cause for lemming population cycles. Oikos 70, 3-11.
91. Shinozaki K., Yamaguchi-Shinozaki K., Mizoguchi T., Urao T., Katagiri T., Nakashima K. & Mikami K. (1998) Molecular responses to water stress in Arabidopsis thaliana. Journal of Plant Research 111, 345-351.
92. Shoji T., Winz R., Iwase T., Nakajima K., Yamada Y. & Hashimoto T. (2002) Expression patterns of two tobacco isoflavone reductase-like genes and their possible roles in secondary metabolism in tobacco. Plant Molecular Biology 50, 427-440.
93. Singh A., Singh I.K. & Verma P.K. (2008) Differential transcript accumulation in Cicer arietinum L. in response to a chewing insect Helicoverpa armigera and defence regulators correlate with reduced insect performance. Journal of Experimental Botany 59, 2379-2392.
94. Skibbe M., Qu N., Galis I. & Baldwin I.T. (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. The Plant Cell 20, 1984-2000.
95. Smith C.M. & Boyko E.V. (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 1-16.
96. Spilatro S.R., Cochran G.R., Walker R.E., Cablish K.L. & Bittner C.C. (1996) Characterization of a new lectin of soybean vegetative tissues. Plant Physiology 110, 825-834.
97. Staswick P.E., Huang J.F. & Rhee Y. (1991) Nitrogen and methyl jasmonate induction of soybean vegetative storage protein genes. Plant Physiology 96, 130-136.
98. Stotz H.U., Pittendrigh B.R., Kroymann J., Weniger K., Fritsche J., Bauke A. & Mitchell-Olds T. (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiology 124, 1007-1017.
99. Stotz H.U., Koch T., Biedermann A., Weniger K., Boland W. & Mitchell-Olds T. (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214, 648-652.
100. Stratmann J.W. (2003) Long distance run in the wound response-jasmonic acid is pulling ahead. Trends in Plant Science 8, 247-250.
101. Tahara S. (2007) A journey of twenty-five years through the ecological biochemistry of flavonoids. Bioscience, Biotechnology, and Biochemistry 71, 1387-1404.
102. Tamagnone L., Merida A., Parr A., Mackay S., Culianez-Macia F.A., Roberts K. & Martin C. (1998) The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. The Plant Cell Online 10, 135-154.
103. Tan Z., Liu R., Hu Y. & Lin Z. (2012) Production of isoflavone genistein in transgenic IFS tobacco roots and its role in stimulating the development of arbuscular mycorrhiza. Acta Physiologiae Plantarum 34, 1863-1871.
104. 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.
105. Underwood N.C. (1998) The timing of induced resistance and induced susceptibility in the soybean - Mexican bean beetle system. Oecologia 114, 376-381.
106. Walling L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195-216.
107. Wang H., Gao Z.J., Fan R., Zhang Y.S., Wu Q. & Yu D.Y. (2011) Evaluation of resistance of soybean germplasm to common cutworm based on three resistance mechanisms. Soybean Science 30, 8-14.
108. Wilson R.F. (2008) Chapter 1 Soybean: market driven research needs. In Genetics and Genomics of Soybean (ed. G. Stacey ) pp. 3-15. Springer, New York.
109. Wu J.J., Wu Q., Wu Q.J., Gai J.Y. & Yu D.Y. (2008) Constitutive overexpression of AOS-like gene from soybean enhanced tolerance to insect attack in transgenic tobacco. Biotechnology Letters 30, 1693-1698.
110. Wu Q., Wu J., Sun H., Zhang D. & Yu D.Y. (2011) Sequence and expression divergence of the AOC gene family in soybean: insights into functional diversity for stress responses. Biotechnology Letters 33, 1351-1359.
111. Yamaguchi-Shinozaki K. & Shinozaki K. (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Molecular & General Genetics: MGG 238, 17-25.
112. Yauk C. & Berndt M. (2007) Review of the literature examining the correlation among DNA microarray technologies. Environmental and Molecular Mutagenesis 48, 80-394.
113. Yi J., Derynck M.R., Li X., Telmer P., Marsolais F. & Dhaubhadel S. (2010) A single-repeat MYB transcription factor, GmMYB176, regulates CHS8 gene expression and affects isoflavonoid biosynthesis in soybean. The Plant Journal 62, 1019-1034.
114. Zangerl A.R. & Berenbaum M.R. (1995) Spatial, temporal, and environmental limits on xanthotoxin induction in wild parsnip foliage. Chemoecology 5/6, 37-42.
115. Zavala J.A., Patankar A.G., Gase K., Hui D. & Baldwin I.T. (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiology 134, 81-1190.
116. Zhan Q.W., Gai J.Y., Zhang Y.M. & Sun Z.D. (2001) Development and expression process of inheritance of resistance to cotton worm (prodinia litura) in soybeans. Yi Chuan Xue Bao=Acta Genetica Sinica 28, 956-963.
117. Zhang P.J., Shu J.P., Fu C.X., Zhou Y., Hu Y., Zalucki M.P. & Liu S.S. (2008) Trade-offs between constitutive and induced resistance in wild crucifers shown by a natural, but not an artificial, elicitor. Oecologia 157, 83-92.
118. Zhu-Salzman K., Ahn J.E., Salzman R.A., Koiwa H., Shade R.E. & Balfe S. (2003) Fusion of a soybean cysteine protease inhibitor and a legume lectin enhances anti-insect activity synergistically. Agricultural and Forest Entomology 5, 317-323.
119. Zulak K.G., Lippert D.N., Kuzyk M., Domanski D., Chou T., Borchers C.H. & Bohlmann J. (2009) Targeted proteomics using selected reaction monitoring (SRM) reveals the induction of specific terpene synthases in a multi-level study of methyl jasmonate treated Norway spruce (Picea abies). The Plant Journal 60, 1015-1030.