Skip to main content
Log in

Comparative serial analysis of gene expression of transcript profiles of tomato roots infected with cyst nematode

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We analyzed global transcripts for tomato roots infected with the cyst nematode Globodera rostochiensis using serial analysis of gene expression (SAGE). SAGE libraries were made from nematode-infected roots and uninfected roots at 14 days after inoculation, and the clones including SAGE tags were sequenced. Genes were identified by matching the SAGE tags to tomato expressed sequence tags and cDNA databases. We then compiled a list of numerous genes according to the mRNA levels that were altered after cyst nematode infection. Our SAGE results showed significant changes in expression of many unreported genes involved in nematode infection. Of these, for discussion we selected five SAGE tags of RSI-1, BURP domain-containing protein, hexose transporter, P-rich protein, and PHAP2A that were activated by cyst nematode infection. Over 20% of the tags that were upregulated in the infected root have unknown functions (non-annotated), suggesting that we can obtain information on previously unreported and uncharacterized genes by SAGE. We can also obtain information on previously reported genes involved in nematode infection (e.g., multicystatin, peroxidase, catalase, pectin esterase, and S-adenosylmethionine transferase). To evaluate the validity of our SAGE results, seven genes were further analyzed by semiquantitative reverse transcriptase–polymerase chain reaction and Northern blot hybridization; the results agreed well with the SAGE data.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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. Nucl Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Asamizu E, Nakamura Y, Sato S, Tabata S (2005) Comparison of the transcript profiles from the root and the nodulation root of the model legume Lotus japonicus by serial analysis of gene expression. Mol Plant Microbe Interact 18:487–498

    PubMed  CAS  Google Scholar 

  • Bar-Or C, Kapulnik Y, Koltai H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. Eur J Plant Pathol 111:181–192

    Article  CAS  Google Scholar 

  • Barthels N, Van der Lee FM, Klap J, Goddijn OJM, Karimi M, Puzio P, Grundler FMW, Ohl SA, Lindsey K, Robertson L, Robertson WM, Montagu MW, Gheysen G, Sijmons PC (1997) Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures. Plant Cell 9:2119–2134

    Article  PubMed  CAS  Google Scholar 

  • Batchelor AK, Boutilier K, Miller SS, Hattori J, Bowman LA, Hu M, Lantin S, Johnson DA, Miki BLA (2002) SCB1, a BURP-domain protein gene, from developing soybean seed coats. Planta 215:523–532

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Truernit E, Baier K, Scholz-Starke J, Sontheim M, Lauterbach C, Huss VAR, Sauer N (2000) AtSTP3, a green leaf-specific, low affinity monosaccharide-H+ symporter of Arabidopsis thaliana. Plant Cell Environ 23:175–184

    Article  Google Scholar 

  • De Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL Jr, Inzé D, Van Montagu M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793–807

    Article  PubMed  Google Scholar 

  • De Meutter J, Robertson L, Parcy F, Mena M, Fenoll C, Gheysen G (2005) Differential activation of ABI3 and LEA genes upon plant parasitic nematode infection. Mol Plant Pathol 6:321–325

    Article  Google Scholar 

  • Ernst K, Kumar A, Kriseleit D, Kloos D-U, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst-nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136

    Article  PubMed  CAS  Google Scholar 

  • Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P (1998) RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO J 17:6799–6811

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Simon R, Brommonschenkel S, Arndt M, Phillips MS, Tanksley SD, Kumar A (1995) Genetic mapping of a wide spectrum nematode resistance gene (Hero) against Globodera rostochiensis in tomato. Mol Plant Microbe Interact 8:886–891

    PubMed  CAS  Google Scholar 

  • Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Goverse A, De Almeida Engler J, Verhees J, Van der Krol S, Helder J, Gheysen G (2000a) Cell cycle activation by plant parasitic nematodes. Plant Mol Biol 43:747–761

    Article  CAS  Google Scholar 

  • Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000b) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 10:1121–1129

    Google Scholar 

  • Gurr SJ, McPherson MJ, Scollan C, Atkinson HJ, Bowles DJ (1991) Gene expression in nematode-infected plant roots. Mol Gen Genet 226:361–366

    Article  PubMed  CAS  Google Scholar 

  • Hammes UZ, Schachtman DP, Berg RH, Nielsen E, Koch W, McIntyre LM, Taylor CG (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol Plant Microbe Interact 18:1247–1257

    PubMed  CAS  Google Scholar 

  • Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular–arbuscular (VA) mycorrhizal associations. Plant J 9:491–503

    Article  PubMed  CAS  Google Scholar 

  • He B, Magill C, Starr JL (2005) Laser capture microdissection and real-time PCR for measuring mRNA in giant cells induced by Meloidogyne javanica. J Nematol 37:308–312

    CAS  Google Scholar 

  • Hermsmeier D, Mazarei M, Baum TJ (1998) Differential display analysis of the early compatible interaction between soybean and the soybean cyst nematode. Mol Plant Microbe Interact 11:1258–1263

    CAS  Google Scholar 

  • Hermsmeier D, Hart JK, Byzova M, Rodermel SR, Baum TJ (2000) Changes in mRNA abundances within Heterodera schachtii-infected roots of Arabidopsis thaliana. Mol Plant Microbe Interact 13:309–315

    PubMed  CAS  Google Scholar 

  • Hoth S, Schneidereit A, Lauterbach C, Scholz-Starke J, Sauer N (2005) Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiol 138:383–392

    Article  PubMed  CAS  Google Scholar 

  • Jammes F, Lecomte P, De Almeida-Engler J, Bitton F, Martin-Magnitte M-L, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–458

    Article  PubMed  CAS  Google Scholar 

  • Juergensen K, Scholz-Starke J, Sauer N, Hess P, van Bel AJE, Grundler FMW (2003) The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia. Plant Physiol 131:61–69

    Article  PubMed  CAS  Google Scholar 

  • Jung S-H, Lee J-Y, Lee D-H (2003) Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Mol Biol 52:553–567

    Article  PubMed  CAS  Google Scholar 

  • Khan R, Alkharouf N, Beard H, MacDonald M, Chouikha I, Meyer S, Greffenstette J, Knap H, Matthews B (2004) Microarray analysis of gene expression in soybean roots susceptible to the soybean cyst nematode two days post invasion. J Nematol 36:241–248

    CAS  Google Scholar 

  • Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    Article  PubMed  CAS  Google Scholar 

  • Lee J-Y, Lee D-H (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE, Benfey PN (1997) Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci 2:390–396

    Article  Google Scholar 

  • Man MZ, Wang X, Wang Y (2000) POWER_SAGE: comparing statistical tests for SAGE experiments. Bioinformatics 16:953–959

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Nirasawa S, Terauchi R (1999) Transcript profiling in rice (Oryza sativa L.) seedling using serial analysis of gene expression (SAGE). Plant J 20:719–726

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, Winter P, Kahl G, Reuter M, Kruger DH, Terauchi R (2003) Gene expression analysis of host–pathogen interactions by SuperSAGE. Proc Natl Acad Sci USA 100:15718–15723

    Article  PubMed  CAS  Google Scholar 

  • Mazarei M, Puthoff DP, Hart JK, Rodermel SR, Baum TJ (2002) Identification and characterization of a soybean ethylene-responsive element-binding protein gene whose RNA expression changes during soybean cyst nematode infection. Mol Plant Microbe Interact 15:577–586

    PubMed  CAS  Google Scholar 

  • Mazarei M, Lennon KA, 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 

  • Medina-Fiho HP, Tanksley SD (1983) Breeding of nematode resistance. In: Evans DA, Sharp WR, Ammirato PV, Yamada Y (eds) Handbook of plant cell culture, vol 1. Macmillan, New York, pp904–923

    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 

  • Opperman CH, Taylor CG, Conkling MA (1994) Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221–223

    Article  CAS  Google Scholar 

  • Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33:911–921

    Article  PubMed  CAS  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 

  • Shibata D (2005) Genome sequencing and functional genomics approaches in tomato. J Gen Plant Pathol 71:1–7

    Article  CAS  Google Scholar 

  • Smant G, Stokkermans JPWG, Yang Y, De Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of β-1,4-endoglucanases from two species of plant–parasitic nematodes. Proc Natl Acad Sci USA 95:4906–4911

    Article  PubMed  CAS  Google Scholar 

  • Sobczak M, Avrova A, Jupowicz J, Phillips MS, Ernst K, Kumar A (2005) Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Mol Plant Microbe Interact 18:158–168

    PubMed  CAS  Google Scholar 

  • Takahashi H, Shimizu A, Arie T, Rosmalawati S, Fukushima S, Kikuchi M, Hikichi Y, Kanda A, Takahashi A, Kiba A, Ohnishi K, Ichinose Y, Taguchi F, Yasuda C, Kodama M, Egusa M, Masuta C, Sawada H, Shibata D, Hori K, Watanabe Y (2005) Catalog of Micro-Tom tomato responses to common fungal, bacterial, and viral pathogens. J Gen Plant Pathol 71:8–22

    Article  Google Scholar 

  • Takemoto D, Yoshioka H, Doke N, Kawakita K (2003) Disease stress-inducible genes of tobacco: expression profile of elicitor-responsive genes isolated by subtractive hybridization. Physiol Plant 118:545–553

    Article  CAS  Google Scholar 

  • Taylor BH, Scheuring CF (1994) A molecular marker for lateral root initiation: the RSI-1 gene of tomato (Lycopersicon esculentum Mill) is activated in early lateral root primordia. Mol Gen Genet 243:148–157

    PubMed  CAS  Google Scholar 

  • Truernit E, Schmid J, Epple P, Illing J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wound, elicitors and pathogen challenge. Plant Cell 8:2169–2182

    Article  PubMed  CAS  Google Scholar 

  • Velculescu VE, Zang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487

    Article  PubMed  CAS  Google Scholar 

  • Vercauteren I, De Almeida Engler J, De Groodt R, Gheysen G (2002) An Arabidopsis thaliana pectin acetylesterase gene is upregulated in nematode feeding sites induced by root-knot and cyst nematodes. Mol Plant Microbe Interact 15:404–407

    PubMed  CAS  Google Scholar 

  • Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745

    Article  PubMed  CAS  Google Scholar 

  • Yu S, Zhang L, Zuo K, Li Z, Tang K (2004) Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress. Physiol Plant 122:210–218

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to T. Narabu and K. Itou (National Agricultural Research Center for Hokkaido Region) and Y. Maruta (Lab Company Ltd.) for their valuable advice. We thank T. Yanagidate (Lab Company Ltd.) for excellent technical assistance. This study was supported in part by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 18780039).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Taketo Uehara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uehara, T., Sugiyama, S. & Masuta, C. Comparative serial analysis of gene expression of transcript profiles of tomato roots infected with cyst nematode. Plant Mol Biol 63, 185–194 (2007). https://doi.org/10.1007/s11103-006-9081-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-006-9081-3

Keywords

Navigation