Characterisation of the transcriptome of Aphelenchoides besseyi and identification of a GHF 45 cellulase

in Nematology
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While the majority of Aphelenchoides species are fungivorous, some species are plant parasites that have retained the ability to feed on fungi. Aphelenchoides besseyi is an important and widespread pathogen that causes ‘white tip’ disease on rice. This migratory endoparasitic nematode makes a significant contribution to the estimated $US 16 billion worth of damage caused by nematodes to rice crops. Here we describe a small-scale analysis of the transcriptome of A. besseyi. After sequencing, QC and assembly, approximately 5000 contigs were analysed. Bioinformatic analysis allowed 375 secreted proteins to be identified, including orthologues of proteins known to be secreted by other nematodes. One contig could encode an A. besseyi orthologue of a GHF45 cellulase, similar to those present in Bursaphelenchus xylophilus. No transcripts similar to GHF5 cellulases were present in this dataset.

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  • BendtsenJ.D.NielsenH.von HeijneG.BrunakS. (2004). Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340783-795.

    • Search Google Scholar
    • Export Citation
  • ChevreuxB.WetterT.SuhaiS. (1999). Genome sequence assembly using trace signals and additional sequence information. Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 9945-56.

    • Search Google Scholar
    • Export Citation
  • CockP.J.A.AntaoT.ChangJ.T.ChapmanB.A.CoxC.J.DalkeA.FriedbergI.HamelryckT.KauffF.WilczynskiB. (2009). Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 251422-1423.

    • Search Google Scholar
    • Export Citation
  • DuncanL.W.MoensM. (2006). Migratory endoparasitic nematodes. In: PerryR.N.MoensM. (Eds). Plant nematology. Wallingford, UKCAB International pp.  123-152.

    • Search Google Scholar
    • Export Citation
  • FuZ.AgudeloP.WellsC.E. (2012). Differential expression of a β-1,4-Endoglucanase induced by diet change in the foliar nematode Aphelenchoides fragariae. Phytopathology 102804-811.

    • Search Google Scholar
    • Export Citation
  • FurlanettoC.CardleL.BrownD.J.F.JonesJ.T. (2005). Analysis of expressed sequence tags from the ectoparasitic nematode Xiphinema index. Nematology 795-104.

    • Search Google Scholar
    • Export Citation
  • GaoB.AllenR.MaierT.DavisE.L.BaumT.J.HusseyR.S. (2003). The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 16720-726.

    • Search Google Scholar
    • Export Citation
  • GoecksJ.NekrutenkoA.TaylorJ. & The Galaxy Team (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology 11R86.

    • Search Google Scholar
    • Export Citation
  • HaegemanA.JacobJ.VanholmeB.KyndtT.GheysenG. (2008). A family of GHF5 endo-1,4-beta-glucanases in the migratory plant-parasitic nematode Radopholus similis. Plant Pathology 57581-590.

    • Search Google Scholar
    • Export Citation
  • HaegemanA.JacobJ.VanholmeB.KyndtT.MitrevaM.GheysenG. (2009). Expressed sequence tags of the peanut pod nematode Ditylenchus africanus: The first transcriptome analysis of an Anguinid nematode. Molecular and Biochemical Parasitology 16732-40.

    • Search Google Scholar
    • Export Citation
  • HaegemanA.JonesJ.T.DanchinE. (2011a). Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant-Microbe Interactions 24879-887.

    • Search Google Scholar
    • Export Citation
  • HaegemanA.JosephS.GheysenG. (2011b). Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Molecular and Biochemical Parasitology 1787-14.

    • Search Google Scholar
    • Export Citation
  • HocklandS. (2004). Aphelenchoides besseyi. EPPO Bulletin 34303-308.

  • HsiehS.H.LinC.J.ChenP. (2012). Sexual compatibility among different host-originated isolates of Aphelenchoides besseyi and the inheritance of the parasitism. PLoS ONE 7e40886.

    • Search Google Scholar
    • Export Citation
  • HuangG.Z.GaoB.L.MaierT.AllenR.DavisE.L.BaumT.J.HusseyR.S. (2003). A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 16376-381.

    • Search Google Scholar
    • Export Citation
  • HuntD.J. (1993). Aphelenchida Longidoridae and Trichodoridae: their systematics and bionomics. Wallingford, UKCAB International.

  • JacobJ.VanholmeB.HaegemanA.GheysenG. (2007). Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: Members of an extensive nematode-specific family. Gene 4029-19.

    • Search Google Scholar
    • Export Citation
  • JonesJ.T.FurlanettoC.KikuchiT. (2005). Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7641-646.

    • Search Google Scholar
    • Export Citation
  • JonesJ.T.KumarA.PylypenkoL.A.ThirugnanasambandamA.CastelliL.ChapmanS.CockP.J.A.GrenierE.LilleyC.J.PhillipsM.S. (2009). Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida. Molecular Plant Pathology 10815-828.

    • Search Google Scholar
    • Export Citation
  • KikuchiT.JonesJ.T.AikawaT.KosakaH.OguraN. (2004). A family of GHF45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Letters 572201-205.

    • Search Google Scholar
    • Export Citation
  • KikuchiT.AikawaT.KosakaH.PritchardL.OguraN.JonesJ.T. (2007). EST analysis of the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus. Molecular and Biochemical Parasitology 1559-17.

    • Search Google Scholar
    • Export Citation
  • KikuchiT.CottonJ.A.DalzellJ.J.HasegawaK.KanzakiN.McVeighP.TakanashiT.TsaiI.J.AssefaS.A.CockP.J.A. (2011). Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 7e1002219.

    • Search Google Scholar
    • Export Citation
  • KroghA.LarssonB.von HeijneG.SonnhammerE. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305567-580.

    • Search Google Scholar
    • Export Citation
  • LilleyC.J.KyndtT.GheysenG. (2011). Nematode resistant GM crops in industrialised and developing countries. In: JonesJ.T.GheysenG.FenollC.F. (Eds). Genomics and molecular genetics of plant-nematode interactions. Heidelberg, GermanySpringer pp.  517-541.

    • Search Google Scholar
    • Export Citation
  • MardisE.R. (2008). The impact of next-generation sequencing technology on genetics. Trends in Genetics 24133-141.

  • MartinJ.AbubuckerS.HeizerE.TaylorC.M.MitrevaM. (2012). Nematode.net update 2011: addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Research 2012 40 (Database issue) D720-8.

    • Search Google Scholar
    • Export Citation
  • MilneI.StephenG.BayerM.CockP.J.A.PritchardL.CardleL.ShawP.D.MarshallD. (2013). Using Tablet for visual exploration of second-generation sequencing data. Briefings in Bioinformatics 14193-202.

    • Search Google Scholar
    • Export Citation
  • NicolP.GillR.Fosu-NyarkoJ.JonesM.G.K. (2012). De novo analysis and functional classification of the transcriptome of the root lesion nematode Pratylenchus thornei after 454 GS FLX sequencing. International Journal for Parasitology 42225-237.

    • Search Google Scholar
    • Export Citation
  • PetersenT.N.BrunakS.von HeijneG.NielsenH. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8785-786.

    • Search Google Scholar
    • Export Citation
  • RagsdaleE.J.NgoP.T.CrumJ.EllismanM.H.BaldwinJ.G. (2011). Reconstruction of the pharyngeal corpus of Aphelenchus avenae (Nematoda: Tylenchomorpha), with implications for phylogenetic congruence. Zoological Journal of the Linnean Society 1611-30.

    • Search Google Scholar
    • Export Citation
  • RehmanS.PostmaW.TytgatT.PrinsP.QinL.OvermarsH.VossenJ.SpiridonL.N.PetrescuA.J.GoverseA. (2009). A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Molecular Plant-Microbe Interactions 22330-340.

    • Search Google Scholar
    • Export Citation
  • RiggesR.D. (1991). Resistance-breaking races of plant parasitic nematodes. In: NickleW.R. (Ed.). Manual of agricultural nematology. New York, NY, USAMarcel Dekker pp.  827-854.

    • Search Google Scholar
    • Export Citation
  • Rybarczyk-MydłowskaK.MooymanP.van MegenH.van den ElsenS.VervoortM.VeenhuizenP.van DoornJ.DeesR.KarssenG.BakkerJ. (2012a). Small subunit ribosomal DNA-based phylogenetic analysis of foliar nematodes (Aphelenchoides spp.) and their quantitative detection in complex DNA backgrounds. Phytopathology 1021153-1160.

    • Search Google Scholar
    • Export Citation
  • Rybarczyk-MydłowskaK.Ruvimbo MaborekeH.van MegenH.van den ElsenS.MooymanP.SmantG.BakkerJ.HelderJ. (2012b). Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes. BMC Evolutionary Biology 12221.

    • Search Google Scholar
    • Export Citation
  • SultanaT.KimJ.LeeS.H.HanH.KimS.MinG.S.NadlerS.A.NadlerS.A. (2013). Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes. BMC Evolutionary Biology 1312.

    • Search Google Scholar
    • Export Citation
  • van MegenH.van den ElsenS.HoltermanM.KarssenG.MooymanP.BongersT.HolovachovO.BakkerJ.HelderJ. (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11927-950.

    • Search Google Scholar
    • Export Citation
  • YuP.C.TsayT.T. (2004). Occurrence of a foliar nematode disease of fern in Taiwan. Plant Pathology Bulletin 1335-44.

Figures
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    Contig length distribution histogram showing numbers of contigs of various lengths. Contig lengths are pooled in bins of 20.

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    Orthologues of Aphelenchoides besseyi sequences in Bursaphelenchus xylophilus and Meloidogyne incognita predicted proteins.

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    Alignment of predicted GHF45 cellulase from Aphelenchoides besseyi with top matches from Bursaphelenchus xylophilus. Residues conserved in all three proteins are shaded, predicted signal peptides are underlined and the GHF45 signature sequence is boxed. Bx seq 1: B. xylophilus eng-1 (Kikuchi et al., 2004); Bx seq 2: a further B. xylophilus endoglucanase (Accession number ACD12136); A. besseyi seq: the new sequence reported here.

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