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Differences in gene expression amplitude overlie a conserved transcriptomic program occurring between the rapid and potent localized resistant reaction at the syncytium of the Glycine max genotype Peking (PI 548402) as compared to the prolonged and potent resistant reaction of PI 88788

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Abstract

Glycine max L. Merr. (soybean) resistance to Heterodera glycines Ichinohe occurs at the site of infection, a nurse cell known as the syncytium. Resistance is classified into two cytologically-defined responses, the G. max [Peking]- and G. max [PI 88788]-types. Each type represents a cohort of G. max genotypes. Resistance in G. max [Peking] occurs by a potent and rapid localized response, affecting parasitic second stage juveniles (p-J2). In contrast, resistance occurs by a potent but more prolonged reaction in the genotype G. max [PI 88788] that affects nematode development at the J3 and J4 stages. Microarray analyses comparing these cytologically and developmentally distinct resistant reactions reveal differences in gene expression in pericycle and surrounding cells even before infection. The differences include higher relative levels of the differentially expressed in response to arachidonic acid 1 gene (DEA1 [Gm-DEA1]) (+224.19-fold) and a protease inhibitor (+68.28-fold) in G. max [Peking/PI 548402] as compared to G. max [PI 88788]. Gene pathway analyses compare the two genotypes (1) before, (2) at various times during, (3) constitutively throughout the resistant reaction and (4) at all time points prior to and during the resistant reaction. The amplified levels of transcriptional activity of defense genes may explain the rapid and potent reaction in G. max [Peking/PI 548402] as compared to G. max [PI 88788]. In contrast, the shared differential expression levels of genes in G. max [Peking/PI 548402] and G. max [PI 88788] may indicate a conserved genomic program underlying the G. max resistance on which the genotype-specific gene expression programs are built off.

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Abbreviations

EST:

Expressed sequence tag

hpi:

Hours post inoculation

dpi:

Days post inoculation

SCN:

Soybean cyst nematode

J2:

Second stage juvenile

FS:

Farmer’s solution

LCM:

Laser capture microdissection

References

  • Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Ségurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915

    Article  PubMed  CAS  Google Scholar 

  • Acido JR, Dropkin VH, Luedders VD (1984) Nematode population attrition and histopathology of Heterodera glycines-Soybean associations. J Nematol 16:48–57

    Google Scholar 

  • Aist JR (1976) Papillae and related wound plugs of plant cells. Annu Rev Phytopathol 14:145–163

    Article  Google Scholar 

  • Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH, Meyer S, Knap HT, Khan R, Matthews BF (2006) Timecourse microarray analyses reveals global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838–852

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A, Shimada H, Kadowaki K (2002) Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32:401–408

    Article  PubMed  CAS  Google Scholar 

  • Bekal S, Craig JP, Hudson ME, Niblack TL, Domier LL, Lambert KN (2008) Genomic DNA sequence comparison between two inbred soybean cyst nematode biotypes facilitated by massively parallel 454 micro-bead sequencing. Mol Genet Genomics 279:535–543

    Article  PubMed  CAS  Google Scholar 

  • Blée E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–322

    Article  PubMed  Google Scholar 

  • Bostock RM, Kuc J, Laine RA (1981) Eicosapentaenoic and arachidonic acids from Phytophthora infestans elicit fungitoxic sesquiterpenes in the potato. Science 212:67–69

    Article  PubMed  CAS  Google Scholar 

  • Bostock RM, Schaeffer DA, Hammerschmidt R (1986) Comparison of elicitor activities of arachidonic acid, fatty acids and glucans from Phytopthora infestans in hypersensitivity expression in potato tuber. Physiol Mol Plant Pathol 29:349–360

    Article  CAS  Google Scholar 

  • Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Odum N, Jørgensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502

    Article  PubMed  CAS  Google Scholar 

  • Cai D, Kleine M, Kifle S, Hans-Joachim H, Sandal NN, Marcker KA, Klein-Lankhorst RM, Salentijn EMJ, Lange W, Stiekema WJ, Wyss U, Grundler FMW, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–834

    Article  PubMed  CAS  Google Scholar 

  • Caldwell BE, Brim CA, Ross JP (1960) Inheritance of resistance of soybeans to the soybean cyst nematode, Heterodera glycines. Agron J 52:635–636

    Article  Google Scholar 

  • Cambier V, Hance T, De Hoffmann E (2001) Effects of 1,4-benzoxazin-3-one derivatives from maize on survival and fecundity of Metopolophium dirhodum (Walker) on artificial diet. J Chem Ecol 27:359–370

    Article  PubMed  CAS  Google Scholar 

  • Chandra-Shekara AC, Venugopal SC, Barman SR, Kachroo A, Kachroo P (2007) Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc Natl Acad Sci USA 104:7277–7282

    Article  PubMed  CAS  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  PubMed  CAS  Google Scholar 

  • Cole RA (1984) Phenolic acids associated with the resistance of lettuce cultivars to the lettuce root aphid. Ann Appl Biol 105:129–145

    Article  CAS  Google Scholar 

  • Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK (2002) Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant Microbe Interact 15411–15420

  • Colgrove AL, Niblack TL (2008) Correlation of female indices from virulence assays on inbred lines and field populations of Heterodera glycines. J Nematol 40:39–45

    PubMed  CAS  Google Scholar 

  • Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131

    Article  CAS  Google Scholar 

  • Edens RM, Anand SC, Bolla RI (1995) Enzymes of the phenylpropanoid pathway in soybean infected with Meloiodiogyne incognita or Heterodera glycines. J Nematol 27:292–303

    PubMed  CAS  Google Scholar 

  • Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang Z, Goldstein SR, Weiss RA, Liotta LA (1996) Laser capture microdissection. Science 274:998–1001

    Article  PubMed  CAS  Google Scholar 

  • Endo BY (1964) Penetration and development of Heterodera glycines in soybean roots and related and related anatomical changes. Phytopathology 54:79–88

    Google Scholar 

  • Endo BY (1965) Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines. Phytopathology 55:375–381

    CAS  Google Scholar 

  • Endo BY (1991) Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines. Rev Nematol 14:73–94

    Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Starr J, Göbel C, Engelberth J, Feussner I, Tumlinson J, Kolomiets M (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. MPMI 21:98–109

    Article  PubMed  CAS  Google Scholar 

  • Glover KD, Wang D, Arelli PR, Carlson SR, Cianzio SR, Diers BW (2004) Near isogenic lines confirm a soybean cyst nematode resistance gene from PI 88788 on linkage group. J Crop Sci 44:936–941

    Article  Google Scholar 

  • Golden AM, Epps JM, Riggs RD, Duclos LA, Fox JA, Bernard RL (1970) Terminology and identity of infraspecific forms of the soybean cyst nematode (Heterodera glycines). Plant Dis Rep 54:544–546

    Google Scholar 

  • Halbrendt J, Lewis S, Shipe E (1992) A technique for evaluating Heterodera glycines development in susceptible and resistant soybean. J Nematol 24:84–91

    PubMed  CAS  Google Scholar 

  • Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8:63

    Article  PubMed  Google Scholar 

  • Hartwig EE, Epps JM (1978) Registration of Bedford soybeans. Crop Sci 18:915

    Article  Google Scholar 

  • He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115

    Article  PubMed  CAS  Google Scholar 

  • Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222

    Article  PubMed  CAS  Google Scholar 

  • Isenberg G, Bielser W, Meier-Ruge W, Remy E (1976) Cell surgery by laser micro-dissection: a preparative method. J Microsc 107:19–24

    Article  PubMed  CAS  Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793

    Article  PubMed  CAS  Google Scholar 

  • Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15:2952–2965

    Article  PubMed  CAS  Google Scholar 

  • Kachroo A, Fu DQ, Havens W, Navarre D, Kachroo P, Ghabrial SA (2008) An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol Plant Microbe Interact 21:564–575

    Article  PubMed  CAS  Google Scholar 

  • Kim KS, Riggs RD (1992) Cytopathological reactions of resistant soybean plants to nematode invasion. In: Wrather JA, Riggs RD (eds) Biology and management of the soybean cyst nematode. APS Press, St. Paul, pp 157–168

    Google Scholar 

  • Kim YH, Riggs RD, Kim KS (1987) Structural changes associated with resistance of soybean to Heterodera glycines. J Nematol 19:177–187

    PubMed  CAS  Google Scholar 

  • Klink VP, MacDonald M, Alkharouf N, Matthews BF (2005) Laser capture microdissection (LCM) and expression analyses of Glycine max (soybean) syncytium containing root regions formed by the plant pathogen Heterodera glycines (soybean cyst nematode). Plant Mol Biol 59:969–983

    Article  Google Scholar 

  • Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF (2007a) Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean roots infected by soybean cyst nematode (Heterodera glycines). Planta 226:1389–1409

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF (2007b) A comparative microarray analysis of an incompatible and compatible disease response by soybean (Glycine max) to soybean cyst nematode (Heterodera glycines) infection. Planta 226:1423–1447

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, MacDonald MH, Martins VE, Park S-C, Kim K-H, Baek S-H, Matthews BF (2008) MiniMax, a new diminutive Glycine max variety, with a rapid life cycle, embryogenic potential and transformation capabilities. Plant Cell Tissue Organ Cult 92:183–195

    Article  CAS  Google Scholar 

  • Klink VP, Hosseini P, Matsye P, Alkharouf N, Matthews BF (2009a) A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Mol Biol 71:525–567

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, Hosseini P, MacDonald MH, Alkharouf N, Matthews BF (2009b) Population-specific gene expression in the plant pathogenic nematode Heterodera glycines exists prior to infection and during the onset of a resistant or susceptible reaction in the roots of the Glycine max genotype Peking. BMC Genomics 10:111

    Article  PubMed  Google Scholar 

  • Klink VP, Kim K-H, Martins VE, MacDonald MH, Beard HS, Alkharouf NW, Park S-C, Matthews BF (2009c) A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of the formation of female Heterodera glycines cysts during infection of Glycine max. Planta 230:53–71

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, Hosseini P, Matsye P, Alkharouf N, Matthews BF (2010a) Syncytium gene expression in Glycine max [PI 88788] roots undergoing a resistant reaction to the parasitic nematode Heterodera glycines. Plant Physiol Biochem 48:176–193

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF (2010b) Microarray detection calls as a means to compare transcripts expressed within syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). J Biomed Biotechnol 2010:491217 (1–30)

  • Kosma DK, Nemacheck JA, Jenks MA, Williams CE (2010) Changes in properties of wheat leaf cuticle during interactions with Hessian fly. Plant J 63:31–43

    PubMed  CAS  Google Scholar 

  • Lauritis JA, Rebois R, Graney LS (1983) Development of Heterodera glycines Ichinohe on soybean, Glycine max (L.) Merr., under gnotobiotic conditions. J Nematol 15:272–280

    PubMed  CAS  Google Scholar 

  • Leszczynski B, Wright LC, Bakowski T (1989) Effect of secondary plant substances on winter wheat resistance to grain aphid. Entomol Exp Appl 52:135–139

    Article  CAS  Google Scholar 

  • Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107:496–501

    Article  PubMed  CAS  Google Scholar 

  • Mahalingham R, Skorupska HT (1996) Cytological expression of early response to infection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:986–998

    Article  Google Scholar 

  • Mahalingham R, Wang G, Knap HT (1999) Polygalacturonase and polygalacturonase inhibitor protein: gene isolation and transcription in Glycine maxHeterodera glycines interactions. Mol Plant Microbe Interact 12:490–498

    Article  Google Scholar 

  • Matson AL, Williams LF (1965) Evidence of a fourth gene for resistance to the soybean cyst nematode. Crop Sci 5:477

    Article  Google Scholar 

  • McElver J, Tzafrir I, Aux G, Rogers R, Ashby C, Smith K, Thomas C, Schetter A, Zhou Q, Cushman MA, Tossberg J, Nickle T, Levin JZ, Law M, Meinke D, Patton D (2001) Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159:1751–1763

    PubMed  CAS  Google Scholar 

  • Meier-Ruge W, Bielser W, Remy E, Hillenkamp F, Nitsche R, Unsold R (1976) The laser in the Lowry technique for microdissection of freeze-dried tissue slices. Histochem J 8:387–401

    Article  PubMed  CAS  Google Scholar 

  • Melito S, Heuberger AL, Cook D, Diers BW, MacGuidwin AE, Bent AF (2010) A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1locus LRR-kinase on soybean cyst nematode resistance. BMC Plant Biol 10:104

    Article  PubMed  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  PubMed  CAS  Google Scholar 

  • Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, Bak S (2008) Beta-glucosidases as detonators of plant chemical defense. Phytochemistry 69:1795–1813

    Article  PubMed  CAS  Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    Article  PubMed  CAS  Google Scholar 

  • Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf JH, Schmitt DP, Shannon JG, Tylka GL (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol 34:279–288

    PubMed  CAS  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2008) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23:80–92

    Article  PubMed  Google Scholar 

  • Rao-Arelli AP (1994) Inheritance of resistance to Heterodera glycines race 3 in soybean accessions. Plant Dis 78:898–900

    Article  Google Scholar 

  • Reina-Pinto JJ, Voisin D, Kurdyukov S, Faust A, Haslam RP, Michaelson LV, Efremova N, Franke B, Schreiber L, Napier JA, Yephremov A (2009) Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis epidermis induces cell death and suggests a critical role for phospholipase A2 in this process. Plant Cell 21:1252–1272

    Article  PubMed  CAS  Google Scholar 

  • Ricker KE, Bostock RM (1992) Evidence for release of the elicitor arachidonic acid and its metabolites from sporangia of Phytophthora infestans during infection of potato. Physiol Mol Plant Pathol 41:61–72

    Article  CAS  Google Scholar 

  • Riggs RD (1988) Races of Heterodera glycines. Nematropica 18:163–170

    Google Scholar 

  • Riggs RD (1992) Chapter 10: Host range. In: Riggs RD, Wrather JA (eds) Biology and management of the soybean cyst nematode. APS Press, St Paul, pp 107–114

    Google Scholar 

  • Riggs RD, Schmitt DP (1988) Complete characterization of the race scheme for Heterodera glycines. J Nematol 20:392–395

    PubMed  CAS  Google Scholar 

  • Riggs RD, Schmitt DP (1991) Optimization of the Heterodera glycines race test procedure. J Nematol 23:149–154

    PubMed  CAS  Google Scholar 

  • Riggs RD, Kim KS, Gipson I (1973) Ultrastructural changes in Peking soybeans infected with Heterodera glycines. Phytopathology 63:76–84

    Article  Google Scholar 

  • Ross JP (1958) Host–Parasite relationship of the soybean cyst nematode in resistant soybean roots. Phytopathology 48:578–579

    Google Scholar 

  • Ross JP (1962) Physiological strains of Heterodera glycines. Plant Dis Rep 46:766–769

    Google Scholar 

  • Sardanelli S, Kenworthy WJ (1997) Soil moisture control and direct seeding for bioassay of Heterodera glycines on soybean. J Nematol 29(suppl):625–634

    PubMed  CAS  Google Scholar 

  • Sasai H, Ishida M, Murakami K, Tadokoro N, Ishihara A, Nishida R, Mori N (2009) Species-specific glucosylation of DIMBOA in larvae of the rice Armyworm. Biosci Biotechnol Biochem 73:1333–1338

    Article  PubMed  CAS  Google Scholar 

  • Sass JE (1958) Botanical microtechnique. Iowa State College Press, Ames

    Google Scholar 

  • Sasser JN, Freckman DW (1987) A world perspective on nematology: the role of the society. In: Veech JA, Dickerson DW (eds) Vistas on nematology. Society of Nematologists, Hyattsville, pp 7–14

    Google Scholar 

  • Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC, Vingron M, Slusarenko AJ, Hoheisel JD (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277:10555–105561

    Article  PubMed  CAS  Google Scholar 

  • Schmelzer E (2002) Cell polarization, a crucial process in fungal defence. Trends Plant Sci 7:411–415

    Article  PubMed  CAS  Google Scholar 

  • Shannon JG, Arelli PR, Young LD (2004) Breeding for resistance and tolerance. In: Schmitt DP, Wrather JA, Riggs RD (eds) Biology and management of soybean cyst nematode, 2nd edn. Schmitt & Associates of Marceline, Marceline, pp 155–180

    Google Scholar 

  • Sobolev VS, Neff SA, Gloer JB (2010) New dimeric stilbenoids from fungal-challenged peanut (Arachis hypogaea) seeds. J Agric Food Chem 58:875–881

    Article  PubMed  CAS  Google Scholar 

  • The Gene Ontology Consortium (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  Google Scholar 

  • Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D (2001) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135:1206–1220

    Article  Google Scholar 

  • Wang Y, Cai QN, Zhang QW, Han Y (2006) Effect of the secondary substances from wheat on the growth and digestive physiology of cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae). Eur J Entomol 103:255–258

    Google Scholar 

  • Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006a) A circadian rhythm-regulated tomato gene is induced by Arachidonic acid and Phytophthora infestans infection. Plant Physiol 140:235–248

    Article  PubMed  CAS  Google Scholar 

  • Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006b) DEA1, a circadian- and cold-regulated tomato gene, protects yeast cells from freezing death. Plant Mol Biol 62:547–559

    Article  PubMed  CAS  Google Scholar 

  • Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003–2005. J Nematol 38:173–180

    PubMed  Google Scholar 

  • Wrather JA, Stienstra WC, Koenning SR (2001) Soybean disease loss estimates for the United States from 1996 to 1998. Can J Plant Pathol 23:122–131

    Article  Google Scholar 

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Acknowledgments

VPK is a recipient of the Research Initiation Program Grant at Mississippi State University and thankfully acknowledges support provided by the Mississippi Soybean Promotion Board. The authors thank Dr. David Munroe, Nina Bubunenko and Nicole Lum at the Laboratory of Molecular Technology, SAIC-Frederick, National Cancer Institute at Frederick, Frederick, Maryland 21701, USA for the Affymetrix® soybean GeneChip® array hybridizations and data acquisition. Dr. Gary Lawrence Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University provided helpful insight into the analysis of the resistance responses of G. max [Peking/PI 548402] and G. max [PI 88788].

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Klink, V.P., Hosseini, P., Matsye, P.D. et al. Differences in gene expression amplitude overlie a conserved transcriptomic program occurring between the rapid and potent localized resistant reaction at the syncytium of the Glycine max genotype Peking (PI 548402) as compared to the prolonged and potent resistant reaction of PI 88788. Plant Mol Biol 75, 141–165 (2011). https://doi.org/10.1007/s11103-010-9715-3

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