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EST Sequencing of Meloidogyne javanica Infected Pineapple Root Tissues Reveals Changes in Gene Expression during Root-Knot Nematode Induced Gall Formation

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Abstract

An expressed sequence tag project has been performed to survey a range of expressed sequences in the vascular cylinder tissue of pineapple roots infected with the root-knot nematode Meloidogyne javanica. A total of 4,102 EST sequences were obtained, comprising of 1,298 early infection clones, 2,461 late infection clones and 343 non-infected root tip clones. Clone redundancy was 34.4 %, with the 4,102 EST sequences clustering into 2,976 contigs comprising of 286 clusters and 2,690 singletons. A comparison of the most abundant clones isolated from the early and late infection libraries revealed significant differences in the transcriptomes of the vascular cylinder at early and late infection stages. Northern analysis and quantitative real time PCR confirmed a variety of genes including a metallothinein-like protein, an alpha tubulin, a phosphoglyceratemutase, a glyceradehyde phosphate dehydrogenase, a mannose-binding lectin and four previously undiscovered sequences are differentially expressed during gall formation. Analysis of clone distribution by functional classification revealed that the late infection library contains a higher proportion of clones associated with oxidative stress responses and the detoxification of free radicals. The EST and contig sequence collection, bioinformatic data and functional classification information is available through an online pineapple database resource housed at http://genet.imb.uq.edu.au/Pineapple/index.html.

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References

  • Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical-scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Biophys Res Commun 323(1):72–78

    Article  CAS  PubMed  Google Scholar 

  • Barre A, Bourne Y, Van Damme EJ, Peumans WJ, Rouge P (2001) Mannose-binding plant lectins: different structural scaffolds for a common sugar-recognition process. Biochimie 83(7):645–651

    Article  CAS  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2003) GenBank. Nucleic Acids Res 31(1):23–27

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caillaud MC, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida Engler J, Abad P, Rosso MN, Favery B (2008) Root-knot nematodes manipulate plant cell functions during a compatible interaction. J Plant Physiol 165(1):104–113. doi:10.1016/j.jplph.2007.05.007

    Article  CAS  PubMed  Google Scholar 

  • Chitwood DJ (2003) Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Manag Sci 59(6–7):748–753

    Article  CAS  PubMed  Google Scholar 

  • Chubatsu LS, Meneghini R (1993) Metallothionein protects DNA from oxidative damage. Biochem J 291(Pt 1):193–198

    CAS  PubMed Central  PubMed  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81(7):1991–1995

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, Rosso MN, Abad P (2000) Nematode parasitism genes. Annu Rev Phytopathol 38:365–396

    Article  CAS  PubMed  Google Scholar 

  • de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38(1):12–26

    Article  PubMed  Google Scholar 

  • Fei J, Liao Z, Chai Y, Pang Y, Yao J, Sun X, Tang K (2003) Molecular cloning and characterization of a novel mannose-binding lectin gene from Amorphophallus konjac. Mol Biol Rep 30(3):177–183

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hu W et al (2003) Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 35(2):139–147

    Article  PubMed  Google Scholar 

  • Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, 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(3):447–458. doi:10.1111/j.1365-313X.2005.02532.x

    Article  CAS  PubMed  Google Scholar 

  • Jones MGK, Payne HL (1978) Early stages of nematode-induced giant-cell formation in roots of Impatiens balsamina. J Nematol 10:70–84

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kling PG, Olsson P (2000) Involvement of differential metallothionein expression in free radical sensitivity of RTG-2 and CHSE-214 cells. Free Radic Biol Med 28(11):1628–1637

    Article  CAS  PubMed  Google Scholar 

  • Koia JH, Moyle RL, Botella JR (2012) Microarray analysis of gene expression profiles in ripening pineapple fruits. BMC Plant Biol 12:240. doi:10.1186/1471-2229-12-240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, Van Criekinge W, De Meyer T, Gheysen G (2012) Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol 196(3):887–900. doi:10.1111/j.1469-8137.2012.04311.x

    Article  CAS  PubMed  Google Scholar 

  • Li J, Todd TC, Lee J, Trick HN (2011) Biotechnological application of functional genomics towards plant-parasitic nematode control. Plant Biotechnol J 9(9):936–944. doi:10.1111/j.1467-7652.2011.00601.x

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32(Web Server issue):W327–W331. doi:10.1093/nar/gkh454

    Article  CAS  PubMed Central  PubMed  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(4):513–530

    Article  CAS  PubMed  Google Scholar 

  • Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR (2005a) Developing pineapple fruit has a small transcriptome dominated by metallothionein. J Exp Bot 56(409):101–112

    CAS  PubMed  Google Scholar 

  • Moyle RL, Crowe ML, Ripi-Koia J, Fairbairn DJ, Botella JR (2005b) PineappleDB: an online pineapple bioinformatics resource. BMC Plant Biol 5:21

    Article  PubMed Central  PubMed  Google Scholar 

  • Neuteboom LW, Kunimitsu WY, Webb D, Christopher DA (2002) Characterization and tissue-regulated expression of genes involved in pineapple (Ananas comosus L.) root development. Plant Sci 163:1021–1035

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45

    Google Scholar 

  • Portillo M, Cabrera J, Lindsey K, Topping J, Andres MF, Emiliozzi M, Oliveros JC, Garcia-Casado G, Solano R, Koltai H, Resnick N, Fenoll C, Escobar C (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytol 197(4):1276–1290. doi:10.1111/nph.12121

    Article  CAS  PubMed  Google Scholar 

  • Potenza C, Thomas SH, Sengupta-Gopalan C (2001) Genes induced during early response to Meloidogyne incognita in roots of resistant and susceptible alfalfa cultivars. Plant Sci 161(2):289–299

    Article  CAS  PubMed  Google Scholar 

  • Rao KV, Rathore KS, Hodges TK, Fu X, Stoger E, Sudhakar D, Williams S, Christou P, Bharathi M, Bown DP, Powell KS, Spence J, Gatehouse AM, Gatehouse JA (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant J 15(4):469–477

    Article  CAS  PubMed  Google Scholar 

  • Rhee SY et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31(1):224–228

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sasser JN (1980) Root-knot nematodes: a global menace to crop production. Plant Dis 64(1):36–41. doi:10.1094/PD-64-36

    Article  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(2):1079–1092. doi:10.1104/pp. 106.090241

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schoof H, Zaccaria P, Gundlach H, Lemcke K, Rudd S, Kolesov G, Arnold R, Mewes HW, Mayer KF (2002) MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome. Nucleic Acids Res 30(1):91–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schoof H, Ernst R, Nazarov V, Pfeifer L, Mewes HW, Mayer KF (2004) MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource for plant genomics. Nucleic Acids Res 32(Database issue):D373–D376

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tirumalaraju SV, Jain M, Gallo M (2011) Differential gene expression in roots of nematode-resistant and -susceptible peanut (Arachis hypogaea) cultivars in response to early stages of peanut root-knot nematode (Meloidogyne arenaria) parasitization. J Plant Physiol 168(5):481–492. doi:10.1016/j.jplph.2010.08.006

    Article  CAS  PubMed  Google Scholar 

  • Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302(5643):296–299

    Article  CAS  PubMed  Google Scholar 

  • Yao JH, Zhao XY, Liao ZH, Lin J, Chen ZH, Chen F, Song J, Sun XF, Tang KX (2003) Cloning and molecular characterization of a novel lectin gene from Pinellia ternata. Cell Res 13(4):301–308

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Jose R. Botella.

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Communicated by: Schuyler S. Korban

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Moyle, R.L., Botella, J.R. EST Sequencing of Meloidogyne javanica Infected Pineapple Root Tissues Reveals Changes in Gene Expression during Root-Knot Nematode Induced Gall Formation. Tropical Plant Biol. 7, 43–52 (2014). https://doi.org/10.1007/s12042-014-9136-6

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  • DOI: https://doi.org/10.1007/s12042-014-9136-6

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