Skip to main content
SpringerLink
Log in

Heterodera elachista the Japanese cyst nematode parasitizing corn in Northern Italy: integrative diagnosis and bionomics

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

The Japanese cyst nematode Heterodera elachista was detected parasitizing corn cv Rixxer in Bosco Mesola (Ferrara Province) in Northern Italy. The only previous report of this nematode was in Asia (Japan, China and Iran) attacking upland rice; being this work the first report of this cyst nematode in Europe, and confirmed corn as a new host plant for this species. Integrative morphological and molecular data for this species were obtained using D2-D3 expansion regions of 28S rDNA, ITS1-rDNA, the partial 18S rDNA, the protein-coding mitochondrial gene, cytochrome oxidase c subunit I (COI), and the heat-shock protein 90 (hsp90). Heterodera elachista identified in Northern Italy was morphologically and molecularly clearly separated from other cyst nematodes attacking corn (viz. H. avenae, H. filipjevi, H. delvii, H. oryzae, H. sacchari, H. sorghi, H. zeae, Punctodera chalcoensis, and Vittadera zeaphila) and rice (H. oryzae, H. sacchari). The phylogenetic relationships of H. elachista from Northern Italy with other cyst-nematodes using rDNA and mtDNA showed a separation of the genus Heterodera in various morphospecies groups based on vulval cone structures. The development and parasitic habit of H. elachista on naturally infected corn cv Rixxer confirmed a typical susceptible reaction, including multinucleate syncytial cells in parenchymatic cells. Under greenhouse conditions, H. elachista successfully reproduced on two crops widely used in Northern Italy, such as corn (cv PR 33) and rice (cv Baldo). Considering the limited host-range of this nematode, that include two of the three world’s most important crops, special attention is needed for avoiding the dispersal of this nematode into new areas, by movement of soil on equipment, water, and contaminated containers infested soil, or agricultural practices.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bernard, E. C., Handoo, Z. A., Powers, T. O., Donald, P. A., & Heinz, R. D. (2010). Vittatidera zeaphila (Nematoda: Heteroderidae), a new genus and species of cyst nematode parasitic on corn (Zea mays). Journal of Nematology, 42, 139–150.

    PubMed  Google Scholar 

  • Boutsika, K., Brown, D. J. F., Phillips, M. S., & Blok, V. C. (2004). Molecular characterisation of the ribosomal DNA of Paratrichodorus macrostylus, P. pachydermus, Trichodorus primitivus and T. similis (Nematoda: Trichodoridae). Nematology, 6, 641–654.

    Article  CAS  Google Scholar 

  • Castillo, P., & Vovlas, N. (2007). In D. J. Hunt & R. N. Perry (Eds.), Pratylenchus (Nematoda: Pratylenchidae): Diagnosis, biology, pathogenicity and control. Leiden: Brill. 529 pp.

    Chapter  Google Scholar 

  • Castillo, P., Vovlas, N., Subbotin, S., & Troccoli, A. (2003). A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in Southern Spain. Phytopathology, 93, 1093–1102.

    Article  PubMed  Google Scholar 

  • Coolen, W. A. (1979). Methods for extraction of Meloidogyne spp. and other nematodes from roots and soil. In F. Lamberti & C. E. Taylor (Eds.), Root-knot nematodes (Meloidogyne species). Systematics, biology and control (pp. 317–329). New York: Academic Press.

    Google Scholar 

  • Correia, F. J. S., & Abrantes, I. M. O. (2005). Characterization of Heterodera zeae populations from Portugal. Journal of Nematology, 37, 328–335.

    PubMed  CAS  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  PubMed  CAS  Google Scholar 

  • Derycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J., Vincx, M., et al. (2005). Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Marine Ecology Progress Series, 300, 91–103.

    Article  CAS  Google Scholar 

  • Di Vito, M., Vovlas, N., & Inserra, R. N. (1980). Influence of Meloidogyne incognita on growth of corn in pots. Plant Disease, 64, 1025–1026.

    Article  Google Scholar 

  • Ding, Z., Namphueng, J., He, X. F., Peng, D. L., & Huang, W. K. (2012). First report of the cyst nematode (Heterodera elachista) on rice in Hunan Province, China. Plant Disease, 96, 151–151.

    Article  Google Scholar 

  • Endo, B. Y. (1964). Penetration and development of Heterodera glycines in soybean roots and related anatomical changes. Phytopathology, 54, 79–88.

    Google Scholar 

  • Fenwick, D. W. (1940). Methods for the recovery and counting of cysts of Heterodera schachtii from soil. Journal of Helminthology, 18, 155–172.

    Article  Google Scholar 

  • Food and Agriculture Organization of the United Nations statistical database (FAOSTAT). 2011. Faostat production statistics of crops. Online database, http://faostat.fao.org/.

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98NT. Nucleic Acids Symposium Serial, 41, 95–98.

    CAS  Google Scholar 

  • Holterman, M., Karssen, G., van der Elsen, S., van Megen, H., Bakker, J., & Helder, J. (2008). Small subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology, 99, 227–235.

    Article  Google Scholar 

  • Hooper, D. J. (1986). Handling, fixing, staining and mounting nematodes. In J. Southey (Ed.), Laboratory methods for work with plant and soil nematodes (Ministry of Agriculture, Fisheries and Food 6th ed., pp. 59–80). London: Her Majesty’s Stationery Office.

    Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    Article  PubMed  CAS  Google Scholar 

  • Hussey, R. S., & Williamson, V. M. (1997). Physiological and molecular aspects of nematode parasitism. In K. R. Barker, G. A. Pederson, & G. L. Windham (Eds.), Plant and nematode interactions (pp. 87–108). Madison: American Society of Agronomy.

    Google Scholar 

  • Johansen, D. A. (1940). Plant microtechnique. New York: McGraw-Hill Book Co.

    Google Scholar 

  • Johnson, P. W., & Fushtey, S. G. (1966). The biology of the oat cyst nematode Heterodera avenae in Canada. II. Nematode development and related anatomical changes in roots of oats and corn. Nematologica, 12, 630–636.

    Article  Google Scholar 

  • Lewis, S. A. (1987). Nematode-plant compatibility. In J. A. Veech & D. W. Dickson (Eds.), Vistas on nematology (pp. 246–252). Hyattsville: The Society of Nematologists.

    Google Scholar 

  • Nobbs, J., Ibrahim, S. K., & Rowe, J. (1992). A morphological and biochemical comparison of the four cyst nematode species, Heterodera elachista, H. oryzicola, H. oryzae and H. sacchari (Nematoda: Heteroderidae) known to attack rice (Oryza sativa). Fundamental and Applied Nematology, 15, 551–562.

    Google Scholar 

  • Norton, D. C. (1984). Nematode parasites of corn. In W. R. Nickle (Ed.), Plant and insect nematodes (pp. 61–94). New York: Marcel Dekker, Inc.

    Google Scholar 

  • Ohshima, Y. (1974). Heterodera elachista n. sp., an upland rice cyst nematode from Japan. Japanese Journal of Nematology, 4, 51–56.

    Google Scholar 

  • Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357–358.

    PubMed  CAS  Google Scholar 

  • Seinhorst, J. W., & den Ouden, H. (1966). An improvement of Bijloo’s method for determining the eggs content of Heterodera cysts. Nematologica, 12, 170–171.

    Article  Google Scholar 

  • Siddiqi, M. R. (2000). Tylenchida parasites of plants and insects (2nd ed.). Wallingford: CABI Publishing.

    Book  Google Scholar 

  • Skantar, A. M., & Carta, L. K. (2005). Phylogenetic evaluation of nucleotide and protein sequences from the heat shock protein 90 gene of selected nematodes. Journal of Nematology, 36, 466–480.

    Google Scholar 

  • Skantar, A. M., Handoo, Z. A., Zanakis, G. N., & Tzortzakakis, E. A. (2012). Molecular and morphological characterization of the corn cyst nematode, Heterodera zeae, from Greece. Journal of Nematology, 44, 58–66.

    PubMed  CAS  Google Scholar 

  • Suarez, Z., Moss, C. S., & Inserra, R. N. (1985). Anatomical changes induced by Punctodera chalcoensis in corn roots. Journal of Nematology, 17, 242–244.

    PubMed  CAS  Google Scholar 

  • Subbotin, S. A., Vierstraete, A., De Ley, P., Rowe, J., Waeyenberge, L., Moens, M., et al. (2001). Phylogenetic relationships within the cyst-forming nematodes (Nematoda, Heteroderidae) based on analysis of sequences from the ITS regions of ribosomal DNA. Molecular Phylogenetics and Evolution, 21, 1–16.

    Article  PubMed  CAS  Google Scholar 

  • Subbotin, S. A., Sturhan, D., Chizhov, V. N., Vovlas, N., & Baldwin, J. G. (2006). Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology, 8, 455–474.

    Article  CAS  Google Scholar 

  • Subbotin, S. A., Mundo-Ocampo, M., & Baldwin, J. G. (2010). In D. J. Hunt & R. N. Perry (Eds.), Systematics of cyst nematodes (Nematoda: Heteroderinae). Nematology monographs and perspectives 8B. Leiden: Brill. 512 pp.

    Google Scholar 

  • Swofford, D. L. (2003). PAUP*: Phylogenetic analysis using parsimony (and Other Methods) Version 4.0b 10. Sunderland, Massachusetts: Sinauer Associates.

  • Tanha Maafi, Z., Subbotin, S. A., & Moens, M. (2003). Molecular identification of cyst-forming nematodes (Heteroderidae) from Iran and a phylogeny based on ITS-rDNA sequences. Nematology, 5, 99–111.

    Article  Google Scholar 

  • Tanha Maafi, Z., Sturhan, D., Kheiri, A., Geraert, E., Subbotin, S. A., & Moens, M. (2004). Morphology of some cyst-forming nematodes from Iran. Russian Journal of Nematology, 12, 59–78.

    Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  • Troccoli, A. (2002). Aspetti pratici e comparativi di alcune metodologie tradizionali applicate all’identificazione dei nematodi da quarantena. Nematologia mediterranea, 30, 107–110.

    Google Scholar 

  • Windham, G. L. (1998). Corn. In K. R. Barker, G. A. Pederson, & G. L. Windham (Eds.), Plant and nematode interactions (pp. 335–357). Madison: American Society of Agronomy.

    Google Scholar 

  • Zhuo, K., Wang, H., Ye, W., Peng, D., & Liao. (2013). Heterodera hainanensis n. sp. (Nematoda: Heteroderinae) from bamboo in Hainan Province, China – a new cyst nematode in the Afenestrata group. Nematology, 15, 303–314.

    Article  Google Scholar 

Download references

Acknowledgments

Authors thank Dr. Valerio Finetti of Bayer Crop Science Srl., Milan, Italy; Mr. Antonio Carella of Horto Service, Noicattaro (BA), Italy, and Dr. J.A. Navas-Cortés (IAS-CSIC) for critical reading of the manuscript before submission. The present work was supported with funds provided by the Italian Ministry of Economy and Finance to the National Research Council for the project “Innovazione e Sviluppo del Mezzogiorno-Conoscenze Integrate per Sostenibilità ed Innovazione del Made in Italy Agroalimentare-Legge n. 191/2009, and partially by grant AGR-136 from ‘Consejería de Economía, Innvovación y Ciencia’ from Junta de Andalucía and the European Social Fund.

Author information

Authors and Affiliations

  1. Istituto per la Protezione delle Piante (IPP), Consiglio Nazionale delle Ricerche (CNR), U.O.S. di Bari, Via G. Amendola 122/D, 70126, Bari, Italy

    Francesca De Luca, Nicola Vovlas, Alberto Troccoli, Vincenzo Radicci & Elena Fanelli

  2. Horto Service, Via S.Pietro, 3, 70016, Noicattaro, BA, Italy

    Giuseppe Lucarelli

  3. Instituto de Agricultura Sostenible (IAS), Consejo Superior de Investigaciones Científicas (CSIC), Apdo. 4084, Campus de Excelencia Internacional Agroalimentario, ceiA3, 14080, Córdoba, Spain

    Carolina Cantalapiedra-Navarrete & Pablo Castillo

  4. Department of Forest Pathology, Forestry and Forest Products Research Institute (FFPRI), Tsukuba, 305-8687, Ibaraki, Japan

    Juan E. Palomares-Rius

Authors
  1. Francesca De Luca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicola Vovlas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giuseppe Lucarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alberto Troccoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vincenzo Radicci
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elena Fanelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carolina Cantalapiedra-Navarrete
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Juan E. Palomares-Rius
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pablo Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo Castillo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Luca, F., Vovlas, N., Lucarelli, G. et al. Heterodera elachista the Japanese cyst nematode parasitizing corn in Northern Italy: integrative diagnosis and bionomics. Eur J Plant Pathol 136, 857–872 (2013). https://doi.org/10.1007/s10658-013-0212-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-013-0212-9

Keywords

Search

Navigation