Skip to main content
SpringerLink
Log in

Role of Horizontal Gene Transfer in the Evolution of Plant Parasitism Among Nematodes

  • Protocol
Book cover Horizontal Gene Transfer

Part of the book series: Methods in Molecular Biology ((MIMB,volume 532))

Abstract

Horizontal gene transfer (HGT) implies the non-sexual exchange of genetic material between species – in some cases even across kingdoms. Although common among Bacteria and Archaea, HGTs from pro- to eukaryotes and between eukaryotes were thought to be extremely rare. Recent studies on intracellular bacteria and their hosts seriously question this view. Recipient organisms could benefit from HGT as new gene packages could allow them to broaden or change their diet, colonize new habitats, or survive conditions that previously would have been lethal.

About a decade ago, plant parasitic nematodes were shown to produce and secrete cellulases. Prior to this, animals were thought to fully depend on microbial symbionts for the breakdown of plant cell walls. This discovery prompted Keen and Roberts (1) to hypothesize that the ability of nematodes to parasitize plants was acquired by HGT from soil bacteria to (ancestral) bacterivorous nematodes. Since the identification of the first nematode cellulases, many more plant cell wall–degrading enzymes (CWDE) have been identified in a range of plant parasitic nematode species.

Here we discuss a number of criteria that can be used to underpin an HGT claim. HGT requires close physical contact between donor and recipient, and this could be achieved in, for example, a symbiont–host, or a trophic relationship. The former type of relationship was indeed shown to potentially result in the transfer of genetic material (e.g., Brugia malayi and Wolbachia). However, currently known endosymbionts of nematodes may not be the source of CWDEs. Remarkably, all cellulases discovered so far within the order Tylenchida belong to a single glycoside hydrolase family (GHF5). A range of soil bacteria harbours GHF5 cellulases, but of course nothing can be said about the gene content of soil bacteria at the time HGT took place (if at all). We suggest that characterisation of cellulases (and other CWDEs) and their genomic organisation in more basal (facultative) plant parasitic Tylenchida is needed to find out if CWDEs were indeed acquired via HGT from bacteria. A more complete picture about the evolution of CWDEs among plant parasitic Tylenchida will require a detailed characterisation of two – so far – fully unexplored basal suborders, Tylenchina and Criconematina. Finally, we performed a computational high-throughput identification of potential HGT candidates (including ones unrelated to CWDEs) in plant parasitic nematodes using a genomics approach.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Keen, N. T., Roberts, P. A. (1998) Plant parasitic nematodes: Digesting a page from the microbe book. Proc Natl Acad Sci U S A 95, 4789–90.

    Article  CAS  PubMed  Google Scholar 

  2. Lambshead, P. J., Brown, C., Ferrero, T., Hawkins, L., Smith, C., Mitchell, N. (2003) Biodiversity of nematode assemblages from the region of the clarion-clipperton fracture zone, an area of commercial mining interest. BMC Ecology 3, 1.

    Article  PubMed  Google Scholar 

  3. (1998) Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 282, 2012–8.

    Google Scholar 

  4. Agrios, G. N. (2005) Plant pathology, Academic Press, New York.

    Google Scholar 

  5. WHO (2005) Deworming for health and development. Report of the third global meeting of the partners for parasite control. World Health Organization, Geneva.

    Google Scholar 

  6. Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T., Thomas, W. K. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–5.

    Article  CAS  PubMed  Google Scholar 

  7. Holterman, M., Van Der Wurff, A., Van Den Elsen, S., Van Megen, H., Bongers, T., Holovachov, O., Bakker, J., Helder, J. (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 23, 1792–800.

    Article  CAS  PubMed  Google Scholar 

  8. Holterman, M., Rybarczyk, K., Van Den Elsen, S., Van Megen, H., Mooyman, P., Santiago, R. P., Bongers, T. O. M., Bakker, J., Helder, J. (2008) A ribosomal DNA-based framework for the detection and quantification of stress-sensitive nematode families in terrestrial habitats. Mol Ecol Res 8, 23–34.

    Article  CAS  Google Scholar 

  9. Smith, M. W., Feng, D. F., Doolittle, R. F. (1992) Evolution by acquisition: The case for horizontal gene transfers. Trends Biochem Sci 17, 489–93.

    Article  CAS  PubMed  Google Scholar 

  10. Koonin, E. V., Makarova, K. S., Aravind, L. (2001) Horizontal gene transfer in prokaryotes: Quantification and classification. Annu Rev Microbiol 55, 709–42.

    Article  CAS  PubMed  Google Scholar 

  11. Lawrence, J. G., Hendrickson, H. (2003) Lateral gene transfer: When will adolescence end? Mol Microbiol 50, 739–49.

    Article  CAS  PubMed  Google Scholar 

  12. Brown, J. R. (2003) Ancient horizontal gene transfer. Nat Rev Genet 4, 121–32.

    Article  CAS  PubMed  Google Scholar 

  13. Andersson, J. O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62, 1182–97.

    Article  CAS  PubMed  Google Scholar 

  14. Blaxter, M. (2007) Symbiont genes in host genomes: Fragments with a future? Cell Host Microbe 2, 211–3.

    Article  CAS  PubMed  Google Scholar 

  15. Koski, L. B., Golding, G. B. (2001) The closest BLAST hit is often not the nearest neighbor. J Mol Evol 52, 540–2.

    CAS  PubMed  Google Scholar 

  16. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860–921.

    Google Scholar 

  17. Stanhope, M. J., Lupas, A., Italia, M. J., Koretke, K. K., Volker, C., Brown, J. R. (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411, 940–4.

    Article  CAS  PubMed  Google Scholar 

  18. Ford Doolittle, W. (1998) You are what you eat: A gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14, 307–11.

    Article  Google Scholar 

  19. Hotopp, J. C. D., Clark, M. E., Oliveira, D. C. S. G., Foster, J. M., Fischer, P., Torres, M. C. M., Giebel, J. D., Kumar, N., Ishmael, N., Wang, S., Ingram, J., Nene, R. V., Shepard, J., Tomkins, J., Richards, S., Spiro, D. J., Ghedin, E., Slatko, B. E., Tettelin, H., Werren, J. H. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–6.

    Article  Google Scholar 

  20. Shepherd, A. M., Clark, S. A., Kempton, A. (1973) Spermatogenesis and sperm ultrastructure in some cyst nematodes, Heterodera spp.. Nemaiologica 19, 551–60.

    Article  Google Scholar 

  21. Chang, H. P., Musgrave, A. J. (1972) Multiple symbiosis in a leafhopper, Helochara communis Fitch (cicadellidae: Homoptera): Envelopes, nucleoids and inclusions of the symbiotes. J Cell Sci 11, 275–93.

    CAS  PubMed  Google Scholar 

  22. Zchori-Fein, E., Perlman, S. J. (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13, 2009–16.

    Article  CAS  PubMed  Google Scholar 

  23. Noel, G. R., Atibalentja, N. (2006) ‘Candidatus Paenicardinium endonii’, an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. Int J Syst Evol Microbiol 56, 1697–702.

    Article  CAS  PubMed  Google Scholar 

  24. Adams, R. E., Eichenmuller, J. J. (1963) A bacterial infection of Xiphenema americanum. Phytopathology 53, 745.

    Google Scholar 

  25. Vandekerckhove, T. T. M., Willems, A., Gillis, M., Coomans, A. (2000) Occurrence of novel verrucomicrobial species, endosymbiotic and associated with parthenogenesis in Xiphinema americanum-group species (Nematoda, Longidoridae). Int J Syst Evol Microbiol 50, 2197–205.

    PubMed  Google Scholar 

  26. Smant, G., Stokkermans, J. P., Yan, Y., De Boer, J. M., Baum, T. J., Wang, X., Hussey, R. S., Gommers, F. J., Henrissat, B., Davis, E. L., Helder, J., Schots, A., Bakker, J. (1998) Endogenous cellulases in animals: Isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A 95, 4906–11.

    Article  CAS  PubMed  Google Scholar 

  27. Popeijus, H., Overmars, H. A., Jones, J. T., Blok, V. C., Goverse, A., Helder, J., Schots, A., Bakker, J., Smant, G. (2000) Degradation of plant cell walls by a nematode. Nature 406, 36–7.

    Article  CAS  PubMed  Google Scholar 

  28. Kudla, U., Milac, A.-L., Qin, L., Overmars, H., Roze, E., Holterman, M., Petrescu, A.-J., 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  CAS  PubMed  Google Scholar 

  29. Jaubert, S., Laffaire, J. B., Abad, P., Rosso, M. N. (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett 522, 109–12.

    Article  CAS  PubMed  Google Scholar 

  30. Kikuchi, T., Shibuya, H., Jones, J. T. (2005) Molecular and biochemical characterization of an endo-beta-1,3-glucanase from the pinewood nematode Bursaphelenchus xylophilus acquired by horizontal gene transfer from bacteria. Biochem J 389, 117–25.

    Article  CAS  PubMed  Google Scholar 

  31. Mitreva-Dautova, M., Roze, E., Overmars, H., De Graaff, L., Schots, A., Helder, J., Goverse, A., Bakker, J., Smant, G. (2006) A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita. Mol Plant Microbe Interact 19, 521–9.

    Article  CAS  PubMed  Google Scholar 

  32. Qin, L., Kudla, U., Roze, E. H. A., Goverse, A., Popeijus, H., Nieuwland, J., Overmars, H., Jones, J. T., Schots, A., Smant, G., Bakker, J., Helder, J. (2004) Plant degradation: A nematode expansin acting on plants. Nature 427, 30.

    Article  CAS  PubMed  Google Scholar 

  33. Ding, X., Shields, J., Allen, R., Hussey, R. S. (1998) A secretory cellulose-binding protein cDNA cloned from the root-knot nematode (Meloidogyne incognita). Mol Plant Microbe Interact 11, 952–9.

    Article  CAS  PubMed  Google Scholar 

  34. Gao, B., Allen, R., Davis, E. L., Baum, T. J., Hussey, R. S. (2004) Molecular characterisation and developmental expression of a cellulose-binding protein gene in the soybean cyst nematode Heterodera glycines. Int J Parasitol 34, 1377–83.

    Article  CAS  PubMed  Google Scholar 

  35. Stein, L. D., Bao, Z., Blasiar, D., Blumenthal, T., Brent, M. R., Chen, N., Chinwalla, A., Clarke, L., Clee, C., Coghlan, A., et al. (2003) The genome sequence of Caenorhabditis briggsae: A platform for comparative genomics. PLoS Biol 1, E45.

    Article  PubMed  Google Scholar 

  36. Andersson, J. O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62, 1182–97.

    Article  CAS  PubMed  Google Scholar 

  37. Walton, J. D. (1994) Deconstructing the cell wall. Plant Physiol 104, 1113–8.

    CAS  PubMed  Google Scholar 

  38. Lynd, L. R., Weimer, P. J., Van Zyl, W. H., Pretorius, I. S. (2002) Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol Mol Biol Rev 66, 506–77.

    Article  CAS  PubMed  Google Scholar 

  39. Davison, A., Blaxter, M. (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22, 1273–84.

    Article  CAS  PubMed  Google Scholar 

  40. Lo, N., Watanabe, H., Sugimura, M. (2003) Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc Biol Sci 270 Suppl 1, S69–72.

    Article  PubMed  Google Scholar 

  41. Kikuchi, T., Jones, J. T., Aikawa, T., Kosaka, H., Ogura, N. (2004) A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett 572, 201–5.

    Article  CAS  PubMed  Google Scholar 

  42. Henrissat, B., Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293, 781–8.

    CAS  PubMed  Google Scholar 

  43. Jones, J. T., Furlanetto, C., Kikuchi, T. (2003) Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7, 641–6.

    Article  Google Scholar 

  44. Mccarter, J., Dautova Mitreva, M., Martin, J., Dante, M., Wylie, T., Rao, U., Pape, D., Bowers, Y., Theising, B., Murphy, C. V., Kloek, A. P., Chiapelli, B. J., Clifton, S. W., Bird, M. D., Waterston, R. (2003) Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol 4, R26: 1–19.

    Article  Google Scholar 

  45. Scholl, E. H., Thorne, J. L., Mccarter, J. P., Bird, D. M. (2003) Horizontally transferred genes in plant-parasitic nematodes: A high-throughput genomic approach. Genome Biol 4, R39.

    Article  PubMed  Google Scholar 

  46. Wylie, T., Martin, J., Dante, M., Mitreva, M., Clifton, S. W., Chinwalla, A., Waterston, R. H., Wilson, R. K., Mccarter, J. P. (2004) Nematode.Net: A tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res 32, D423–6.

    Article  CAS  PubMed  Google Scholar 

  47. Mitreva, M., Mccarter, J. P., Martin, J., Dante, M., Wylie, T., Chiapelli, B., Pape, D., Clifton, S. W., Nutman, T. B., Waterston, R. H. (2004) Comparative genomics of gene expression in the parasitic and free-living nematodes Strongyloides stercoralis and Caenorhabditis elegans. Genome Res 14, 209–20.

    Article  PubMed  Google Scholar 

  48. Li, Z., Wang, L., Zhong, Y. (2005) Detecting horizontal gene transfer with t-rex and rhom programs. Brief Bioinform 6, 394–401.

    Article  CAS  PubMed  Google Scholar 

  49. Ledger, T. N., Jaubert, S., Bosselut, N., Abad, P., Rosso, M.-N. (2006) Characterization of a new beta-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 382, 121–8.

    Article  CAS  PubMed  Google Scholar 

  50. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J. (1990) Basic local alignment search tool. J Mol Biol 215, 403–10.

    CAS  PubMed  Google Scholar 

  51. Gish, W. (1996–2002) http://blast.wustl.edu.

  52. Zdobnov, E. M., Apweiler, R. (2001) Interproscan – an integration platform for the signature-recognition methods in interpro. Bioinformatics 17, 847–8.

    Article  CAS  PubMed  Google Scholar 

  53. The Gene Ontology Consortium (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25, 25–9.

    Google Scholar 

  54. Enright, A. J., Van Dongen, S., Ouzounis, C. A. (2002) An efficient algorithm for large-scale detection of protein families. Nucl Acids Res 30, 1575–84.

    Article  CAS  PubMed  Google Scholar 

  55. Van Sluys, M. A., De Oliveira, M. C., Monteiro-Vitorello, C. B., Miyaki, C. Y., Furlan, L. R., Camargo, L. E. A., Da Silva, A. C. R., Moon, D. H., Takita, M. A., Lemos, E. G. M., Machado, M. A., Ferro, M. I. T., Da Silva, F. R., Goldman, M. H. S., Goldman, G. H., Lemos, M. V. F., El-Dorry, H., Tsai, S. M., Carrer, H., Carraro, D. M., De Oliveira, R. C., Nunes, L. R., Siqueira, W. J., Coutinho, L. L., Kimura, E. T., Ferro, E. S., Harakava, R., Kuramae, E. E., Marino, C. L., Giglioti, E., Abreu, I. L., Alves, L. M. C., Do Amaral, A. M., Baia, G. S., Blanco, S. R., Brito, M. S., Cannavan, F. S., Celestino, A. V., Da Cunha, A. F., Fenille, R. C., Ferro, J. A., Formighieri, E. F., Kishi, L. T., Leoni, S. G., Oliveira, A. R., Rosa, V. E., Jr., Sassaki, F. T., Sena, J. A. D., De Souza, A. A., Truffi, D., Tsukumo, F., Yanai, G. M., Zaros, L. G., Civerolo, E. L., Simpson, A. J. G., Almeida, N. F., Jr., Setubal, J. C., Kitajima, J. P. (2003) Comparative analyses of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol 185, 1018–26.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, Washington University School of Medicine, St. Louis, MO, USA

    Makedonka Mitreva

  2. Department of Plant Sciences, Laboratory of Nematology, Wageningen University, Wageningen, Netherlands

    Geert Smant & Johannes Helder

Authors
  1. Makedonka Mitreva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geert Smant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johannes Helder
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Connecticut, 968 Warrenville Road, Mansfield Center, CT 06250, USA

    Maria Boekels Gogarten

  2. Dept. Molecular & Cell Biology, University of Connecticut, 91 North Eagleville Rd., Storrs, CT 06269-3125, USA

    Johann Peter Gogarten

  3. Biology Department, St. Lawrence University, 23 Romoda Drive, Canton, NY 13617, USA

    Lorraine C. Olendzenski

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Mitreva, M., Smant, G., Helder, J. (2009). Role of Horizontal Gene Transfer in the Evolution of Plant Parasitism Among Nematodes. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_30

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-853-9_30

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

  • Online ISBN: 978-1-60327-853-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation