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A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica

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Abstract

The root knot nematode Meloidogyne javanicaa plant parasite that is an agricultural pest, establishes and maintains a permanent feeding site within plant roots. In order to gain a broad view of gene expression in nematode feeding sites during the compatible response of tomato to root knot nematodes, we used the tomato spotted microarray chip, followed by real-time reverse transcription polymerase chain reaction (RT-PCR) validation. Cluster analysis and determination of the amplitude of gene expression suggested that the plant response at 5 days post-inoculation was not as vigorous as that at 10 days post-inoculation. In addition, by filtering the data for genes that were significantly up- or down-regulated during the interaction, we identified both the quantitative and qualitative differences between the two time points. Our microarray experiments demonstrated significant changes in the steady-state levels of transcripts of several functional categories, including pathogenesis-related genes, hormone-associated genes and development-associated transcription factors.

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Abbreviations

d.p.i:

days post-inoculation

EREBP:

ethylene-responsive element binding protein

GA:

gibberellin

PR:

pathogenesis related

qPCR:

real-time quantitative RT-PCR

RKN:

root knot nematode

RT-PCR:

reverse transcription-polymerase chain reaction

SAR:

systemic acquired resistance

References

  • J Almeida Engler Particlede V Vleesschauwer Particlede S Burssens JL Celenza ParticleJr D Inze M Montagu Particlevan G Engler G Gheysen (1999) ArticleTitleMolecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia Plant Cell 11 793–808 Occurrence Handle10330466

    PubMed  Google Scholar 

  • AF Bird (1971) ArticleTitleQuantitative studies on the growth of syncytia induced in plants by root knot nematodes International Journal of Parasitology 2 157–170

    Google Scholar 

  • DM Bird (1996) ArticleTitleManipulation of host gene expression by root-knot nematodes Journal of Parasitology 82 881–888 Occurrence Handle8973394 Occurrence Handle1:STN:280:DyaK2s7ivVymtg%3D%3D

    PubMed  CAS  Google Scholar 

  • DM Bird H Koltai (2000) ArticleTitlePlant parasitic nematodes: Habitats, hormones and horizontally-acquired genes Journal of Plant Growth Regulation 19 183–194 Occurrence Handle11038227 Occurrence Handle1:CAS:528:DC%2BD3cXnvF2hu78%3D

    PubMed  CAS  Google Scholar 

  • AF Bird BR Loveys (1980) ArticleTitleThe involvement of cytokinins in a host–parasite relationship between the tomato (Lycopersicon esculentum) and a nematode (Meloidogyne javanica) Parasitology 80 497–505 Occurrence Handle10.1017/S0031182000000962 Occurrence Handle1:CAS:528:DyaL3cXlt1yqsL8%3D

    Article  CAS  Google Scholar 

  • CS de Castro R DeSouza C Bloch ParticleJr (2002) ArticleTitleCa(II)-gamma-thionin complex: Interaction studies by differential pulse voltammetry and MALDI- TOF/MS Protein and Peptide Letters 9 45–52 Occurrence Handle12141923

    PubMed  Google Scholar 

  • JQ Chen Y Dong YJ Wang Q Liu JS Zhang SY Chen (2003) ArticleTitleAn AP2/EREBP-type transcription-factor gene from rice is cold-inducible and encodes a nuc1ear-localized protein Theoretical and Applied Genetics 107 972–979 Occurrence Handle12844217 Occurrence Handle1:CAS:528:DC%2BD3sXnvVCgt7c%3D

    PubMed  CAS  Google Scholar 

  • GA Churchill (2002) ArticleTitleFundamentals of experimental design for cDNA microarrays Nature Genetics 32 490–495 Occurrence Handle12454643 Occurrence Handle1:CAS:528:DC%2BD38XovFyqs7w%3D

    PubMed  CAS  Google Scholar 

  • GR Comelis F Gijsegem Particlevan (2000) ArticleTitleAssembly and function of type III secretory systems Annual Review of Microbiology 54 735–774

    Google Scholar 

  • ME Daykin RS Hussey (1985) Staining and histopathological techniques in nematology KR Barker CC Carter JN Sasser (Eds) An Advanced Treatise on Meloidogyne Biology and Control. Vol. I North Carolina State University Raleigh, NC, USA 19–35

    Google Scholar 

  • C Dowd IW Wilson H McFadden (2004) ArticleTitleGene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Molecular Plant Microbe Interaction 17 654–667 Occurrence Handle1:CAS:528:DC%2BD2cXktlOmurs%3D

    CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO and Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the USA 95: 14863–14868

    Google Scholar 

  • B Favery A Complainville JM Vinardell P Lecomte D Vaubert P Mergaert A Kondorosi E Kondorosi M Crespi P Abad (2002) ArticleTitleThe endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic-nematode interactions in Medicago truncatula Molecular Plant Microbe Interactions 15 1008–1013 Occurrence Handle12437298 Occurrence Handle1:CAS:528:DC%2BD38XnvFGjtL4%3D

    PubMed  CAS  Google Scholar 

  • G Gheysen C Fenoll (2002) ArticleTitleGene expression in nematode feeding sites Annual Review of Phytopathology 40 191–219 Occurrence Handle12147759 Occurrence Handle1:CAS:528:DC%2BD38Xos1Cltb8%3D

    PubMed  CAS  Google Scholar 

  • DG Ginzinger (2002) ArticleTitleGene quantification using real-time quantitative PCR: An emerging technology hits the mainstream Experimental Hematology 30 503–512 Occurrence Handle12063017 Occurrence Handle1:CAS:528:DC%2BD38XksFOksb8%3D

    PubMed  CAS  Google Scholar 

  • I Glazer D Orion A Apelbaum (1983) ArticleTitleInterrelationships between ethylene production, gall formation and root-knot nematode development in tomato plants infected with Meloidogyne javanica Journal of Nematology 15 539–544 Occurrence Handle1:CAS:528:DyaL2cXot12isw%3D%3D

    CAS  Google Scholar 

  • I Glazer D Orion A Apelbaum (1984) ArticleTitleEffect of inhibitors and stimulators of ethylene production on gall development in Meloidogyne javanica infected tomato roots Journal of Nematology 17 145–149

    Google Scholar 

  • M Goellner X Wang EL Davis (2001) ArticleTitleEndo-beta-1,4-glucanase expression in compatible plant-nematode interactions Plant Cell 13 2241–2255 Occurrence Handle11595799 Occurrence Handle1:CAS:528:DC%2BD3MXotVehu7c%3D

    PubMed  CAS  Google Scholar 

  • S Gopalan W Wei SY He (1996) ArticleTitlehrp gene-dependent induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal Plant Journal 10 591–600 Occurrence Handle8893538 Occurrence Handle1:CAS:528:DyaK28XmvF2lurc%3D

    PubMed  CAS  Google Scholar 

  • A Goverse H Overmars J Engelbertink A Schots J Bakker J Helder (2000) ArticleTitleBoth induction and morphogenesis of cyst nematode feeding cells are mediated by auxin Molecular Plant Microbe Interactions 13 1121–1129 Occurrence Handle11043473 Occurrence Handle1:CAS:528:DC%2BD3cXntVarsrY%3D

    PubMed  CAS  Google Scholar 

  • D Hermsmeier JK Hart M Byzova SR Rodermel TJ Baum (2000) ArticleTitleChanges in mRNA abundance within Heterodera schachtii-infected roots of Arabidopsis thaliana Molecular Plant Microbe Interactions 13 309–315 Occurrence Handle10707356 Occurrence Handle1:CAS:528:DC%2BD3cXht1ymur4%3D

    PubMed  CAS  Google Scholar 

  • RS Hussey KR Barker (1973) ArticleTitleA comparison of methods of collecting inocula of Meloidogyne spp., including a new technique Plant Disease Reporter 57 1025–1028

    Google Scholar 

  • RS Hussey FMW Grundler (1998) Nematode parasitism of plants. RN Perry DJ Wright (Eds) The Physiology and Biochemistry of Free-Living and Plant-Parasitic Nematodes CABI Publishing Wallingford, UK 213–243

    Google Scholar 

  • P Hutangura U Mathesius MGK Jones BG Rolfe (1999) ArticleTitleAuxin 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 Australian Journal of Plant Physiology 26 221–231 Occurrence Handle1:CAS:528:DyaK1MXktlKht7c%3D Occurrence Handle10.1071/PP98157

    Article  CAS  Google Scholar 

  • N Jain J Thatte T Braciale K Ley M O’Connell JK Lee (2003) ArticleTitleLocal-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays Bioinformatics 19 1945–1951 Occurrence Handle10.1093/bioinformatics/btg264 Occurrence Handle1:CAS:528:DC%2BD3sXot1Crs78%3D Occurrence Handle14555628

    Article  CAS  PubMed  Google Scholar 

  • H Koltai M Dhandaydham JF Thomas C Opperman DMcK Bird (2001) ArticleTitleOverlapping plant signal transduction pathways induced by a parasitic-nematode and a rhizobial endosymbiont Molecular Plant Microbe Interactions 14 1168–1177 Occurrence Handle11605956 Occurrence Handle1:CAS:528:DC%2BD3MXnsVeltLs%3D

    PubMed  CAS  Google Scholar 

  • KN Lambert BJ Ferrie G Nombela ED Brenner VM Williamson (1999) ArticleTitleIdentification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection Physiological and Molecular Plant Pathology 55 341–348 Occurrence Handle1:CAS:528:DC%2BD3cXosFam

    CAS  Google Scholar 

  • Lee S, Kim SY, Chung E, Joung YH, Pai HS, Hur CG, Choi D (2004) EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Functional and Integrative Genomics [Epub ahead of print].

  • DR Lester JJ Ross JJ Smith RC Elliott JB Reid (1999) ArticleTitleGibberellin 2-oxidation and the SLN gene of Pisum sativum Plant Journal 19 65–73 Occurrence Handle10417727 Occurrence Handle1:CAS:528:DyaK1MXls1Wgtrs%3D

    PubMed  CAS  Google Scholar 

  • DP Lohar JE Schaff JG Laskey JJ Kieber KD Bilyeu DM. Bird (2004) ArticleTitleCytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses Plant Journal 38 203–214 Occurrence Handle15078325 Occurrence Handle1:CAS:528:DC%2BD2cXkt1Kksrw%3D

    PubMed  CAS  Google Scholar 

  • K Maleck A Levine T Eulgem A Morgan J Schmid KA Lawton JL Dangl RA Dietrich (2000) ArticleTitleThe transcriptome of Arabidopsis thaliana during systemic acquired resistance Nature Genetics 26 403–410 Occurrence Handle11101835 Occurrence Handle1:CAS:528:DC%2BD3cXptVWgsbk%3D

    PubMed  CAS  Google Scholar 

  • M Mazarei DP Puthoff JK. Hart SR Rodermel TJ Baum (2002) ArticleTitleIdentification and characterization of a soybean ethylene-responsive element-binding protein gene whose mRNA expression changes during soybean cyst nematode infection Molecular Plant Microbe Interactions 15 577–586 Occurrence Handle12059106 Occurrence Handle1:CAS:528:DC%2BD38XktlSntrc%3D

    PubMed  CAS  Google Scholar 

  • M Moreno A Segura F Garcia-Olmedo (1994) ArticleTitlePseudothionin-St1, a potato peptide active against potato pathogens European Journal of Biochemistry 223 135–139 Occurrence Handle8033886 Occurrence Handle1:CAS:528:DyaK2cXlsFemsb0%3D

    PubMed  CAS  Google Scholar 

  • DP Puthoff D Nettleton SR Rodermel TJ Baum (2003) ArticleTitleArabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles Plant Journal 33 911–921 Occurrence Handle12609032 Occurrence Handle1:CAS:528:DC%2BD3sXis1GlsLw%3D

    PubMed  CAS  Google Scholar 

  • A Reiner D Yekutieli Y Benjamini (2003) ArticleTitleIdentifying differentially expressed genes using false discovery rate controlling procedures Bioinformatics 19 368–375 Occurrence Handle12584122 Occurrence Handle1:CAS:528:DC%2BD3sXit1ygt7s%3D

    PubMed  CAS  Google Scholar 

  • Y Tao Z Xie W Chen J Glazebrook HS Chang B Han T Zhu G Zou F Katagiri (2003) ArticleTitleQuantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae Plant Cell 15 317–330 Occurrence Handle10.1105/tpc.007591 Occurrence Handle1:CAS:528:DC%2BD3sXhtlOmtLY%3D Occurrence Handle12566575

    Article  CAS  PubMed  Google Scholar 

  • Thomas SG, Phillips AL and Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proceedings of the National Academy of Sciences of the USA 96: 4698–4703

    Google Scholar 

  • P Tornero V Conejero P Vera (1996) ArticleTitlePhloem-specific expression of a plant homeobox gene during secondary phases of vascular development Plant Journal 9 639–648 Occurrence Handle8653114 Occurrence Handle1:CAS:528:DyaK28XjvVSmu7o%3D

    PubMed  CAS  Google Scholar 

  • I Vercauteren JD Engler R De Groodt G Gheysen (2002) ArticleTitleAn Arabidopsis thaliana pectin acetylesterase gene is up-regulated in nematode feeding sites induced by root-knot and cyst nematodes Molecular Plant Microbe Interactions 15 404–407 Occurrence Handle12026180 Occurrence Handle1:CAS:528:DC%2BD38XivV2mtLw%3D

    PubMed  CAS  Google Scholar 

  • A Vignutelli C Wasternack K Apel H Bohlmann (1998) ArticleTitleSystemic and local induction of an Arabidopsis thionin gene by wounding and pathogens Plant Joumal 14 285–295 Occurrence Handle1:CAS:528:DyaK1cXjslOmu7o%3D

    CAS  Google Scholar 

  • J Wan FM Dunning AF Bent (2002) ArticleTitleProbing plant-pathogen interactions and downstream defense signaling using DNA microarrays Functional and Integrative Genomics 2 259–273 Occurrence Handle12444419 Occurrence Handle1:CAS:528:DC%2BD38XovVWns78%3D

    PubMed  CAS  Google Scholar 

  • SC Wees ParticleVan HS Chang T Zhu J Glazebrook (2003) ArticleTitleCharacterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling Plant Physiology 132 606–617 Occurrence Handle12805591

    PubMed  Google Scholar 

  • VM Williamson CA Gleason (2003) ArticleTitlePlant -nematode interactions Current Opinion in Plant Biology 6 327–333 Occurrence Handle12873526 Occurrence Handle1:CAS:528:DC%2BD3sXlsValtL8%3D

    PubMed  CAS  Google Scholar 

  • VM Williamson RS Hussey (1996) ArticleTitleNematode pathogenesis and resistance in plants Plant Cell 8 1735–1745 Occurrence Handle8914324 Occurrence Handle1:CAS:528:DyaK28Xmsl2mtLk%3D

    PubMed  CAS  Google Scholar 

  • MJ Wubben 2II H Su SR Rodermel TJ Baum (2001) ArticleTitleSusceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana Molecular Plant Microbe Interaction 14 1206–1212

    Google Scholar 

  • YR Yang T Speed (2002) ArticleTitleDesign issues for cDNA microarray experiments Nature Reviews Genetics 8 579–588

    Google Scholar 

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Authors and Affiliations

  1. Departments of Genomics, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Carmiya Bar-Or & Hinanit Koltai

  2. Departments of Agronomy and Natural Resources, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Yoram Kapulnik

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  1. Carmiya Bar-Or
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  2. Yoram Kapulnik
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  3. Hinanit Koltai
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Correspondence to Hinanit Koltai.

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Bar-Or, C., Kapulnik, Y. & Koltai, H. 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 (2005). https://doi.org/10.1007/s10658-004-2134-z

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