Skip to main content
SpringerLink
Log in

Gene expression profiling of resistant and susceptible soybean lines infected with soybean cyst nematode

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Soybean cyst nematode (SCN) is the most devastating pathogen of soybean. Information about the molecular basis of soybean–SCN interactions is needed to assist future development of effective management tools against this pathogen. Toward this end, soybean transcript abundance was measured using the Affymetrix Soybean Genome Array in a susceptible and a resistant reaction of soybean to SCN infection. Two genetically related soybean sister lines TN02-226 and TN02-275, which are resistant and susceptible, respectively, to the SCN race 2 infection were utilized in these experiments. Pairwise comparisons followed by false discovery rate analysis indicated that the expression levels of 162 transcripts changed significantly in the resistant line, of which 84 increased while 78 decreased. However, in the susceptible line, 1,694 transcripts changed significantly, of which 674 increased while 1,020 decreased. Comparative analyses of these transcripts indicated that a total of 51 transcripts were in common between resistance and susceptible responses. In this set, 42 transcripts increased in the resistant line, but decreased in the susceptible line. Quantitative real-time reverse-transcription polymerase chain reaction confirmed the results of microarray analysis. Of the transcripts to which a function could be assigned, genes were associated with metabolism, cell wall modification, signal transduction, transcription, and defense. Microarray analyses examining two genetically related soybean lines against the same SCN population provided additional insights into the specific changes in gene expression of a susceptible and a resistant reaction beneficial for identification of genes involved in defense.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anand SC (1992) Hartwig soybean. Crop Sci 32:1069

    Article  Google Scholar 

  • Anand S, Newman T, Fisher J (2001) Anand soybean. Crop Sci 41:919

    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 reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 24:838–852

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer 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 

  • Arelli PR, Sleper DA, Yue P, Wilcox JA (2000) Soybean reaction to races 1 and 2 of Heterodera glycines. Crop Sci 40:824–826

    Article  Google Scholar 

  • Arelli PR, Wang D (2008) Inheritance of cyst nematode resistance in a new genetic source, Glycine max PI 494182. J Crop Sci Biotech 11:83–90

    Google Scholar 

  • Burton JW, Carter TE Jr, Huie EB (1996) Holladay soybean. Crop Sci 36:467

    Article  Google Scholar 

  • Buss GR, Camper HM Jr, Roane CW (1988) Registration of ‘Hutcheson’ soybean. Crop Sci 28:1024

    Article  Google Scholar 

  • Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29:23–39

    Article  PubMed  CAS  Google Scholar 

  • Caviness CE, Riggs RD, Walters HJ (1975) Registration of ‘Lee 74’ soybean. Crop Sci 15:100

    Article  Google Scholar 

  • Chong J, Baltz R, Schmitt C, Beffa R, Fritig B, Saindrenan P (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14:1093–1107

    Article  PubMed  CAS  Google Scholar 

  • Davis EL, Hussey RS, Mitchum MG, Baum TJ (2008) Parasitism proteins in nematode–plant interactions. Curr Opi Plant Biol 11:360–366

    Article  CAS  Google Scholar 

  • De Boer JM, Yan YT, Wang XH, Smant G, Hussey RS, Davis EL, Baum TJ (1999) Developmental expression of secretory beta-1,4-endoglucanases in the subventral esophageal glands of Heterodera glycines. Mol Plant Microbe Interact 12:663–669

    Article  PubMed  Google Scholar 

  • De Boer JM, McDermott JP, Davis EL, Hussey RS, Popeijus H, Smant G, Baum TJ (2002) Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. J Nematol 34:9–11

    PubMed  Google Scholar 

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

    Google Scholar 

  • Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11:65–70

    Article  PubMed  CAS  Google Scholar 

  • Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44

    Article  PubMed  CAS  Google Scholar 

  • Gheysen G, Mitchum MG (2009) Molecular insights in the susceptible plant response to nematode infection. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant Cell Monographs. Springer, Berlin, pp 45–81

    Chapter  Google Scholar 

  • Gillen AM, Shelton GW (2007) Uniform soybean tests, southern states, 2006. USDA-ARS, Stoneville

    Google Scholar 

  • Gillen AM, Shelton GW (2008) Uniform soybean tests, southern states, 2007. USDA-ARS, Stoneville

    Google Scholar 

  • Goellner M, Smant G, De Boer JM, Baum TJ, Davis EL (2000) Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. J Nematol 32:154–165

    PubMed  CAS  Google Scholar 

  • Goellner M, Wang XH, Davis EL (2001) Endo-beta-1,4-glucanase expression in compatible plant–nematode interactions. Plant Cell 13:2241–2255

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129

    Article  PubMed  CAS  Google Scholar 

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266

    Article  PubMed  Google Scholar 

  • Grunewald W, van Noorden G, Van Isterdael G, Beeckman T, Gheysen G, Mathesius U (2009b) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553–2562

    Article  PubMed  CAS  Google Scholar 

  • Hartwig EE, Epps JM, Edwards CJ Jr (1971) Registration of ‘Pickett 71’ soybean. Crop Sci 11:603

    Article  Google Scholar 

  • Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093

    Article  PubMed  CAS  Google Scholar 

  • Hussey R (1990) Staining nematodes in plant tissue. In: Zuckerman BM, Mai WF, Krusberg LR (eds) Plant nematology laboratory manual. The University of Massachusetts Agricultural Experiment Station, Amherst, pp 190–193

    Google Scholar 

  • Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Aust J Plant Physiol 26:221–231

    Article  CAS  Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007a) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305

    Article  PubMed  CAS  Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007b) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20:510–525

    Article  PubMed  CAS  Google Scholar 

  • Jasmer DP, Goverse A, Smant G (2003) Parasitic nematode interactions with mammals and plants. Annu Rev Phytopathol 41:245–270

    Article  PubMed  CAS  Google Scholar 

  • Jones MGK (1981) Host cell responses to endoparasitic nematode attack: Structure and function of giant cells and syncytia. Ann Appl Biol 97:353–372

    Article  CAS  Google Scholar 

  • Kazi S, Shultz J, Afzal J, Hashmi R, Jasim M, Bond J, Arelli PR, Lightfoot DA (2010) Iso-lines and inbred-lines confirmed loci that underlie resistance from cultivar ‘Hartwig’ to three soybean cyst nematode populations. Theor Appl Genet 120:633–644

    Article  PubMed  Google Scholar 

  • Klink VP, Matthews BF (2009) Emerging approaches to broaden resistance of soybean to soybean cyst nematode as supported by gene expression studies. Plant Physiol 151:1017–1022

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, Hosseini P, Matsye P, Alkharouf NW, Matthews BF (2009) 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, Matsye P, Alkharouf NW, Matthews BF (2010) 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 

  • Kudla U, Milac AL, Qin L, Overmars H, Roze E, Holterman M, Petrescu AJ, Goverse A, Bakker J, Helder J, Smant G (2007) Structural and functional characterization of a novel, host penetration related pectate lyase from the potato cyst nematode Globodera rostochiensis. Mol Plant Pathol 8:293–305

    Article  PubMed  CAS  Google Scholar 

  • Langlois-Meurinne M, Gachon CM, Saindrenan P (2005) Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol 139:1890–1901

    Article  PubMed  CAS  Google Scholar 

  • Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey R, Bennett M, Mitchum MG (2011) The novel cyst nematode effector protein 19C07 interacts with the arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–880

    Article  PubMed  CAS  Google Scholar 

  • Lee BJ, Kim SK, Choi SB, Bae J, Kim KJ, Kim YJ, Paek KH (2009) Pathogen-inducible CaUGT1 is involved in resistance response against TMV infection by controlling salicylic acid accumulation. FEBS Lett 583:2315–2320

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Fester T, Taylor CG (2009) Transcriptomic analysis of nematode infestation. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant Cell Monographs. Springer, Berlin, pp 189–220

    Chapter  Google Scholar 

  • Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247

    Article  PubMed  CAS  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  PubMed  CAS  Google Scholar 

  • Lorenc-Kukuła K, Zuk M, Kulma A, Czemplik M, Kostyn K, Skala J, Starzycki M, Szopa J (2009) Engineering flax with the GT Family 1 Solanum sogarandinum glycosyltransferase SsGT1 confers increased resistance to Fusarium infection. J Agric Food Chem 57:6698–6705

    Article  PubMed  Google Scholar 

  • Mazarei M, Elling AA, Maier TR, Puthoff DP, Baum TJ (2007) GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis. Mol Plant Microbe Interact 20:107–119

    Article  PubMed  CAS  Google Scholar 

  • Mazarei M, Lennon KL, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530

    Article  PubMed  CAS  Google Scholar 

  • Mitchum MG, Baum TJ (2008) Genomics of the soybean cyst nematode–soybean interaction. In: Stacey G (ed) Genetics and genomics of soybean. Springer, New York, pp 321–341

    Chapter  Google Scholar 

  • Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf J, 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 

  • Paris RL, Shelton GW (2005) Uniform soybean tests, southern states, 2004. USDA-ARS, Stoneville

    Google Scholar 

  • Paris RL, Shelton GW (2006) Uniform soybean tests, southern states, 2005. USDA-ARS, Stoneville

    Google Scholar 

  • Panthee D, Marois JJ, Wright DL, Narváez D, Yuan JS, Stewart CN Jr (2009) Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific. Theor Appl Genet 118:359–370

    Article  PubMed  CAS  Google Scholar 

  • Puthoff DP, Ehrenfried ML, Vinyard BT, Tucker ML (2007) GeneChip profiling of transcriptional responses to soybean cyst nematode, Heterodera glycines, colonization of soybean roots. J Exp Bot 58:3407–3418

    Article  PubMed  CAS  Google Scholar 

  • Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H, Nieuwland J, Overmars H, Jones JT, Schots A, Smant G, Bakker J, Helder J (2004) A nematode expansin acting on plants. Nature 427:30–130

    Article  PubMed  CAS  Google Scholar 

  • Ross J, Nam KH, D’Auria JC, Pichersky E (1999) S-Adenosyl-l-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys 367:9–16

    Article  PubMed  CAS  Google Scholar 

  • Sandhu D, Tasma IM, Frasch R, Bhattacharyya MK (2009) Systemic acquired resistance in soybean is regulated by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol 9:105

    Article  PubMed  Google Scholar 

  • Schaff JE, Nielsen DM, Smith CP, Scholl EH, Bird DM (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol 144:1079–1092

    Article  PubMed  CAS  Google Scholar 

  • Schmitt DP, Shannon JG (1992) Differentiating soybean responses to Heterodera glycines races. Crop Sci 32:275–277

    Article  Google Scholar 

  • Simonetti E, Veronico P, Melillo MT, Delibes A, Andrés MF, López-Braña I (2009) Analysis of class III peroxidase genes expressed in roots of resistant and susceptible wheat lines infected by Heterodera avenae. Mol Plant Microbe Interact 22:1081–1092

    Article  PubMed  CAS  Google Scholar 

  • Sleper DA, Poehlman JM (2006) Breeding field crops, 5th edn. Blackwell, USA

    Google Scholar 

  • Sobczak M, Golinowski W (2009) Structure of cyst nematode feeding sites. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant Cell Monographs. Springer, Berlin, pp 153–187

    Chapter  Google Scholar 

  • Tomczak A, Koropacka K, Smant G, Goverse A, Bakker E (2009) Resistant plant responses. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant Cell Monographs. Springer, Berlin, pp 83–113

    Chapter  Google Scholar 

  • Vanholme B, Van Thuyne W, Vanhouteghem K, De Meutter J, Cannoot B, Gheysen G (2007) Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Mol Plant Pathol 8:267–278

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Wang Y, Wang Q, Luo G, Zhang Z, He C, He SJ, Zhang J, Gai J, Chen S (2004) Characterization of an NBS-LRR resistance gene homologue from soybean. J Plant Physiol 161:815–822

    Article  PubMed  CAS  Google Scholar 

  • Weigel RR, Pfitzner UM, Gatz C (2005) Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17:1279–1291

    Article  PubMed  CAS  Google Scholar 

  • Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, Cosgrove DJ, Kreil DP, Puzio PS, Bohlmann H, Grundler FM (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48:98–112

    Article  PubMed  CAS  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Wubben MJE II, Su H, Rodermel SR, Baum TJ (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol Plant Microbe Interact 14:1206–1212

    Article  PubMed  CAS  Google Scholar 

  • Wubben MJE II, Rodermel SR, Baum TJ (2004) Mutation of a UDP glucose-4-epimerase alters nematode susceptibility and ethylene responses in Arabidopsis roots. Plant J 40:712–724

    Article  PubMed  CAS  Google Scholar 

  • Young LD (2001) Fowler soybean. Crop Sci 41:257

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge funding by the Tennessee Soybean Promotion Board and funds from a USDA-NIFA grant and the Tennessee Agricultural Experiment Station. We sincerely acknowledge Julia Gouffon at the Affymetrix Core Center of the University of Tennessee for help in conducting the microarray experiment, Dana Pekarchick and Lisa Fritz at USDA-ARS, Jackson, TN for technical assistance. Minimum information about a microarray experiment (MIAME) guidelines were followed in this study.

Author information

Author notes

  1. Hani Al-Ahmad

    Present address: Department of Biology and Biotechnology, An-Najah National University, P.O. Box 7, Nablus, Palestine

Authors and Affiliations

  1. Department of Plant Sciences, The University of Tennessee, 252 Ellington Plant Sciences, 2431 Joe Johnson Dr., Knoxville, TN, 37996, USA

    Mitra Mazarei, Wusheng Liu, Hani Al-Ahmad, Vincent R. Pantalone & C. Neal Stewart Jr

  2. Crop Genetics Research Unit, USDA-ARS, 605 Airways Blvd, Jackson, TN, 38301, USA

    Prakash R. Arelli

Authors
  1. Mitra Mazarei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wusheng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hani Al-Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Prakash R. Arelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vincent R. Pantalone
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Neal Stewart Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mitra Mazarei.

Additional information

Communicated by D. Lightfoot.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mazarei, M., Liu, W., Al-Ahmad, H. et al. Gene expression profiling of resistant and susceptible soybean lines infected with soybean cyst nematode. Theor Appl Genet 123, 1193–1206 (2011). https://doi.org/10.1007/s00122-011-1659-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1659-8

Keywords

Search

Navigation