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Root response to Fusarium solani f. sp . glycines: temporal accumulation of transcripts in partially resistant and susceptible soybean

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Abstract

Sudden death syndrome (SDS) of soybean is a complex of root rot disease caused by the semi-biotrophic fungus Fusarium solani f. sp. glycines (Fsg) and a leaf scorch disease caused by toxins produced by the pathogen in the roots. Development of partial rate-reducing resistance in roots to SDS was studied. The recombinant inbred line 23 (RIL23) that carried resistance conferred by six quantitative trait loci (QTL) derived from cultivars ‘Essex’ × ‘Forrest’ was compared to the susceptible cultivar Essex. Roots of RIL23 and its susceptible parent Essex were inoculated with Fsg. Transcript abundance (TA) of 191 ESTs was studied at five time points after inoculation. For most of the genes, there was an initial decrease in TA in the inoculated roots of both genotypes. By days 7 and 10 the inoculated roots of Essex failed to increase expression of the transcripts of defense-related genes. In RIL23 inoculated roots, the TA of 81 genes was increased by at least two-fold at day 3 (P=0.004), 88 genes at day 7 (P=0.0023) and 129 genes at day 10 (P=0.0026). A set of 35 genes maintained at least a two-fold higher abundance at all three time points. The increase in TA in RIL23 was in contrast to that observed in Essex where most of the ESTs showed either no change or a decreased TA. The ESTs with an increased TA had homology to the genes involved in resistance (analogs), signal transduction, plant defense, cell wall synthesis and transport of metabolites. Pathways that responded included the protein phosphorylation cascade, the phospholipase cascade and the phenolic natural products pathways, including isoflavone and cell wall synthesis.

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References

  • Aoki T, O’Donnell K, Homma Y, Lattanzi AR (2003) Sudden death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex—F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95:660–684

    Google Scholar 

  • Beynon JL (1997) Molecular genetics of disease resistance: an end to the gene-for-gene concept? In: Crute IR, Holub EB, Burdon JJ (eds) The gene-for-gene relationship in plant-parasite interactions. CAB International, New York, pp 359–377

    Google Scholar 

  • Bubeck DM, Goodman MM, Beavis WD, Grant D (1993) Quantitative trait loci controlling resistance to gray leaf spot in maize. Crop Sci 33:838–847

    Google Scholar 

  • Chen H, Wang S, Xing Y, Xu C, Hayes PM, Zhang Q (2003) Comparative analyses of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proc Natl Acad Sci USA 100:2544–2549

    Article  CAS  PubMed  Google Scholar 

  • Constabel CP (1999) In: Agrawal AA, Tuzun S, Bent E (eds) A survey of herbivore-inducible defensive proteins and phytochemicals. APS, St. Paul, pp 137–166

  • Cramer CL, Edwards K, Dron M, Liang X, Dildine SL, Bolwell GP, Dixon RA, Lamb CJ, Schuch W (1989) Phenylalanine ammonia-lyase gene organization and structure. Plant Mol Biol 12:367–383

    Google Scholar 

  • Dixon RA, Harrison MJ, Lamb CJ (1994) Early events in the activation of plant defense responses. Annu Rev Phytopathol 32:479–501

    Google Scholar 

  • Dixon RA, Harrison MJ, Paiva NL (1995) The isoflavonoid phytoalexin pathway: from enzymes to genes to transcription factors. Physiol Plantarum 93:385–392

    Google Scholar 

  • Dowd C, Wilson IW, McFadden H (2004) Gene expression profile in cotton root and hypocotyls tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microb Interact 17:654–667

    Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Google Scholar 

  • Gebhardt C, Valkonen JP (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102

    Article  CAS  PubMed  Google Scholar 

  • Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40:347–369

    Article  Google Scholar 

  • Hartwig EE, Epps JM (1973) Registration of Forrest soybeans. Crop Sci 13:287

    Google Scholar 

  • Hegeman CE, Good LL, Grabau EA (2001) Expression of D-myo-inositol-3-phosphate synthase in soybean. Implications for phytic acid biosynthesis. Plant Phys 125:1941–1948

    Google Scholar 

  • Hnetkovsky N, Chang SC, Doubler TW, Gibson PT, Lightfoot DA (1996) Genetic mapping of loci underlying field resistance to sudden death syndrome. Crop Sci 36:392–400

    Google Scholar 

  • Iqbal MJ, Meksem K, Njiti VN, Kassem MA, Lightfoot DA (2001) Microsatellite markers identify three additional quantitative trait loci for resistance to soybean sudden-death syndrome (SDS) in Essex × Forrest RILs. Theor Appl Genet 102:187–192

    Google Scholar 

  • Iqbal MJ, Yaegashi S, Njiti VN, Ahsan R, Cryder KL, Lightfoot DA (2002a) Resistance locus pyramids alter transcript abundance in soybean roots inoculated with Fusarium solani f.sp. glycines. Mol Genet Genomics 268:407–417

    Google Scholar 

  • Iqbal MJ, Afzal AJ, Yaegashi S, Ruben E, Triwitayakorn K, Njiti VN, Ahsan R, Wood AJ, Lightfoot DA (2002b) A pyramid of loci for partial resistance to Fusarium solani f.sp. glycines maintains myo-inositol-1-phosphate synthase expression in soybean roots. Theor Appl Genet 105:1115–1123

    Google Scholar 

  • Jaeck E, Dumas B, Geoffroy P, Favet N, Inze D, Van Montagu M, Fritig B, Legrand M (1992) Regulation of enzymes involved in lignin biosynthesis: induction of O-methyltransferase mRNAs during the hypersensitive reaction of tobacco to tobacco mosaic virus. Mol Plant Microbe Interact 5:294–300

    Google Scholar 

  • Jin H, Hartman GL, Nickell CD, Widholm JM (1996) Characterization and purification of a phytotoxin produced by Fusarium solani, the causal agent of soybean sudden death syndrome. Phytopathology 86:277–282

    Google Scholar 

  • Keates SE, Kostman TA, Anderson JD, Bailey BA (2003) Altered gene expression in three plant species in response to treatment with nep1, a fungal protein that causes necrosis. Plant Physiol 132:1610–1622

    Article  CAS  PubMed  Google Scholar 

  • Kim JA, Agrawal GK, Rakwal R, Han KS, Kim KN, Yun CH, Heu S, Park SY, Lee YH, Jwa NS (2003) Molecular cloning and mRNA expression analysis of a novel rice (Oryzasativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochem Biophys Res Commun 300:868–876

    Google Scholar 

  • Kumar A, Ellis BE (2001) The phenylalanine ammonia-lyase gene family in raspberry: structure, expression, and evolution. Plant Physiol 127:230–239

    Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol 48:251–275

    Article  CAS  PubMed  Google Scholar 

  • Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Knapp SJ, Salamini F, Gebhardt C (1994) Quantitative resistance to Phytophthora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77

    Google Scholar 

  • Liu Y, Jin H, Yang KY, Kim CY, Baker B, Zhang S (2003) Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J 34:149–160

    Google Scholar 

  • Meindl T, Boller T, Felix G (1998) The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10:1561–1570

    Article  CAS  PubMed  Google Scholar 

  • Meksem K, Doubler TW, Chancharoenchai K, Njiti VN, Chang SJC, Rao-Areli AP, Cregan PE, Gray LE, Gibson PT, Lightfoot DA (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142

    Google Scholar 

  • Meksem K, Pantazopoulos P, Njiti VN, Hyten LD, Arelli PR, Lightfoot DL (2001) ‘Forrest’ resistance to the soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. Theor Appl Genet 103:710–717

    Google Scholar 

  • Melgar J, Roy KW, Abney TS (1994) Sudden death syndrome of soybean: etiology, symptomatology and effects of irrigation and Heterodera glycines on incidence and severity under field conditions. Can J Bot 72:1647–1653

    Google Scholar 

  • Morris ER, Walker JC (2003) Receptor-like protein kinases: the keys to response. Curr Opin Plant Biol 6:339–342

    Google Scholar 

  • Moy P, Qutob D, Chapman BP, Atkinson I, Gijzen M (2004) Patterns of gene expression upon infection soybean plants by Phytophthora sojae. Mol Plant Microb Interact 17:1051–1062

    Google Scholar 

  • Nair TM, Zheng CL, Fink JL, Stuart RO, Gribskov M (2003) Rival penalized competitive learning (RPCL): a topology-determining algorithm for analyzing gene expression data. Comput Biol Chem 27:565–574

    Google Scholar 

  • Njiti VN, Gray LE, Lightfoot DA (1997) Rate-reducing resistance to Fusarium solani f.sp. phaseoli underlies field resistance to soybean sudden death syndrome (SDS). Crop Sci 37:1–12

    Google Scholar 

  • Njiti VN, Douler TW, Suttner RJ, Gray LE, Gibson PT, Lightfoot DA (1998) Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycine in near-isogenic lines. Crop Sci 38:472–477

    Google Scholar 

  • Njiti VN, Johnson JE, Torto TA, Gray LE, Lightfoot DA (2001) Inoculum rate influences selection for field resistance to soybean sudden death syndrome in the greenhouse. Crop Sci 41:1726–1731

    Google Scholar 

  • Pakusch AE, Matern U (1991) Kinetic characterization of caffeoyl-coenzyme A-specific 3-O-methyltransferase from elicited parsley cell suspensions. Plant Phys 96:327–330

    Google Scholar 

  • Parlevliet JE (1979) Components of resistance that reduce the rate of epidemic development. Annu Rev Phytopathol 17:203–222

    Article  Google Scholar 

  • Pe ME, Gianfranceschi L, Taramino G, Tarchini R, Angelini P, Dani M, Binelli G (1993) Mapping quantitative trait loci for resistance to Giberella zeae infection in maize. Mol Gen Genet 241:11–16

    Google Scholar 

  • Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129:1076–1085

    Google Scholar 

  • Roy KW, Rupe JC, Hershman DE, Abney TS (1998) Sudden death syndrome of soybean. Plant Dis 81:1100–1111

    Google Scholar 

  • Schultheiss H, Dechert C, Kogel KH, Huckelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36:589–601

    Article  CAS  PubMed  Google Scholar 

  • Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry 64:153–161

    Google Scholar 

  • Shoemaker R, Keim P, Vodkin L, Retzel E, Clifton SW, Waterson R, Smoller D, Coryell V, Khanna A, Erpelding J, Gai X, Brendel V, Raph-Schmidt C, Shoop EG, Vielweber CJ, Schmatz M, Pape D, Bowers Y, Theising B, Martin J, Dante M, Wylie T, Granger C (2002) A compilation of soybean ESTs: generation and analysis. Genome 45:329–338

    Google Scholar 

  • Smart CD, Myers KL, Restrepo S, Martin GB, Fry WE (2003) Partial resistance of tomato to Phytophthora infestans is not dependent upon ethylene, jasmonic acid, or salicylic acid signaling pathways. Mol Plant Microbe Interact 16:141–148

    Google Scholar 

  • Smith TJ, Camper HM (1973) Registration of Essex soybeans. Crop Sci 13:495

    Google Scholar 

  • Taylor JL, Fritzemeier KH, Hauser I, Kombrink E, Rohwer F, Schroder M, Strittmatter G, Hahlbrock K (1999) Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Mol Plant Microbe Interact 3:72–77

    Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  CAS  PubMed  Google Scholar 

  • Tooley PW, Grau CR (1982) Identification and quantitative characterization of rate-reducing resistance to Phytophthora megasperma f.sp. glycinea in soybean seedlings. Phytopathology 72:727–733

    Google Scholar 

  • Triwitayakorn K, Njiti VN, Iqbal MJ, Yaegashi S, Town C, Lightfoot DA (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome 48:125−138

    Google Scholar 

  • Wang GL, Mackill DJ, Bonman MJ (1994) RFLP mapping of genes conferring complete and partial resistance to blast in a durably resistant rice cultivar. Genetics 136:1421–1430

    CAS  PubMed  Google Scholar 

  • Wrather JA, Sleper DA, Steven WE, Shannon JG, Wilson RF (2003) Planting date and cultivar effects on soybean yield, seed quality, and Phomopsis sp. seed infection. Plant Dis 87:529–532

    Google Scholar 

  • Xu P, Blancaflor EB, Roossinck MJ (2003) In spite of induced multiple defense responses, tomato plants infected with Cucumber mosaic virus and D satellite RNA succumb to systemic necrosis. Mol Plant Microbe Interact 16:467–476

    Google Scholar 

  • Young ND, Manacio-Hautea D, Danesh NS, Kumar L (1994) Mapping oligogenic resistance to powdery mildew in mung bean with RFLPs. Theor Appl Genet 87:243–249

    Google Scholar 

  • Yu I, Fengler KA, Clough SJ, Bent AF (2000) Identification of Arabidopsis mutants exhibiting an altered hypersensitive response in gene-for-gene disease resistance. Mol Plant Microbe Interact 13:277–286

    Google Scholar 

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Acknowledgements

The research was funded in part by grants from the United Soybean Board to M.J.I and D.A.L (projects 2228 and 3218). Any opinions and findings are of authors and USB is not responsible for the contents. The continued support of the Dean of the College of Agriculture, SIUC and the office of the VC for Research, SIUC is appreciated. The authors appreciate Chet Langin for help in statistical analysis. We also thank Dr. T.M. Nair for doing the rival penalized competitive learning (RPCL) cluster analysis presented in the Supplementary Information.

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Correspondence to M. J. Iqbal.

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Iqbal, M.J., Yaegashi, S., Ahsan, R. et al. Root response to Fusarium solani f. sp . glycines: temporal accumulation of transcripts in partially resistant and susceptible soybean. Theor Appl Genet 110, 1429–1438 (2005). https://doi.org/10.1007/s00122-005-1969-9

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