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Morphological and Molecular Characterization of Heterodera schachtii and the Newly Recorded Cyst Nematode, H. trifolii Associated with Chinese Cabbage in Korea

  • Mwamula, Abraham Okki (Department of Ecological Science, Kyungpook National University) ;
  • Ko, Hyoung-Rai (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Youngjoon (Department of Ecological Science, Kyungpook National University) ;
  • Kim, Young Ho (Department of Ecological Science, Kyungpook National University) ;
  • Lee, Jae-Kook (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lee, Dong Woon (Department of Ecological Science, Kyungpook National University)
  • Received : 2017.12.23
  • Accepted : 2018.03.13
  • Published : 2018.08.01

Abstract

The sugar beet cyst nematode, Heterodera schachtii is a well known pathogen on Chinese cabbage in the highland fields of Korea. However, a race of cyst forming nematode with close morphological resemblance to H. trifolii was recently isolated from the same Chinese cabbage fields. Morphological species differentiation between the two cyst nematodes is challenging, with only minor differences between them. Thus, this study described the newly intercepted H. trifolii population, and reviewed morphological and molecular characteristics conceivably essential in differentiating the two nematode species. A comparison of morphometric measurements of both infective juveniles and vulval cones of cysts showed significant differences between the two cyst nematodes. When total RNA and genomic DNA were extracted from a mixed field population, COI genes and ITS regions were clearly amplified with primers of the two Heterodera species, suggesting that Heterodera population collected from the Chinese cabbage field consisted of a mixture of two species. COI and ITS of H. trifolii were predominantly amplified from nucleotides prepared from H. trifolii monoxenic population whereas those of H. schachtii were strongly detected in H. schachtii monoxenic cultures. Thus, this study confirms the coexistence of the two species in some Chinese cabbage fields; and the presence of H. trifolii in Korea is reported here for the first time.

Keywords

References

  1. Abawi, G. S., Foster, J. and Mai, W. F. 1973. Differentiation of cysts of Heterodera schachtii and H. trifolii by fenestral length. J. Nematol. 5:74-75.
  2. Ambrogioni, L. and Irdani, T. 2001. Identifcation of Heterodera schachtii group species in Italy by morphometrics and RAPD-PCR. Nematol. Medit. 29:159-168.
  3. Ambrogioni, L., Cotroneo, A., Moretti, F., Tacconi, R. and Irdani, T. 1999. First record of the yellow beet cyst nematode (Heterodera trifolii) in Italy. Nematol. Medit. 27:151-158.
  4. Amiri, S., Subbotin, S. A. and Moens, M. 2001. An efficient method for identification of the Heterodera schachtii sensu stricto group using PCR with specific primers. Nematol. Medit. 29:241-246.
  5. Amiri, S., Subbotin, S. A. and Moens, M. 2002. Identifcation of the beet cyst nematode Heterodera schachtii by PCR. Eur. J. Plant Pathol. 108:497-506. https://doi.org/10.1023/A:1019974101225
  6. Amiri, S., Subbotin, S. A. and Moens, M. 2003. Comparative morphometrics and RAPD studies of Heterodera schachtii and H. betae populations. Russ. J. Nematol. 11:91-99.
  7. Andersson, S. 1984. First record of a yellow beet cyst nematode (Heterodera trifolii) in Sweden. Vaextskyddsnotiser 48:93-95.
  8. Baldwin, J. G. and Mundo-Ocampo, M. 1991. Heteroderinae, cyst and non-cyst forming nematodes. In: A manual of agricultural Nematology, ed. by W. R. Nickel, pp. 275-362. Marcel Dekker Inc., New York, NY, USA.
  9. Caswell-Chen, E. P., Williamson, V. M. and Wu, F. F. 1992. Random amplified polymorphic DNA analysis of Heterodera cruciferae and H. schachtii populations. J. Nematol. 24:343-351.
  10. Chang, H. W., Kim, K. H., Nam, Y. D., Roh, S. W., Kim, M. S., Jeon, C. O. and Bae, J. W. 2008. Analysis of yeast and archaeal population dynamics in kimchi using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 126:159-166. https://doi.org/10.1016/j.ijfoodmicro.2008.05.013
  11. Cui, J. K., Erginbas-Orakci, G., Peng, H., Huang, W. K., Liu, S., Qiao, F. and Peng, D. L. 2016. First report of sugar beet nematode, Heterodera schachtii Schmidt, 1871 (Nemata: Heteroderidae) in sugar beet growing areas of Sanliurfa, Turkey. Turk. Entomol. Derg. 40:303-314.
  12. Derycke, S., Remerie, T., Vierstraete, A., Backeliau, T., Vanfleteren, J., Vincx, M. and Moens, T. 2005. Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar. Ecol. Prog. Ser. 300:91-103. https://doi.org/10.3354/meps300091
  13. EPPO. 2013. PM 7/119 (1) Nematode extraction. EPPO Bulletin 43:471-495. https://doi.org/10.1111/epp.12077
  14. Evans, K. and Rowe, J. A. 1998. Distribution and economic importance. In: The cyst nematodes, ed. by S. B. Sharma, pp. 1-30. Kluwer Academic Publishers, London, UK.
  15. Goodey, J., Franklin, M. T. H. and David, J. 1965. The nematode parasites of plants catalogued under their hosts. Commonwealth Agricultural Bureaux, England.
  16. Haidar, A. M., Al-Assas, K. M. and Dawabah, A. A. 2015. Preva- lence, distribution and intraspecifc variation of Heterodera schachtii populations from semiarid environment. Saudi J. Biol. Sci. 23:293-299.
  17. Inserra, R. N., Vovlas, N., Walker, S. and Dunn, R. A. 1993. The clover cyst nematode, Heterodera trifolii, a potential pest of clover and vegetable crops in Florida. Nematology Circular 204:1-4.
  18. Iwahori, H., Kanzaki, N. and Futai, K. 2000. A simple, polymerase chain reaction-restriction fragment length polymorphism-aided diagnosis method for pine wilt disease. For. Pathol. 30:157-164. https://doi.org/10.1046/j.1439-0329.2000.00201.x
  19. Joyce, S. A., Reid, A., Driver, F. and Curran, J. 1994. Application of polymerase chain reaction (PCR) methods to identifcation of entomopathogenic nematodes. In: Cost biotechnology, Vol. 812, eds. by A. M. Burnell, R. U. Ehlers and J. P. Masson, pp. 178-187.
  20. Kang, H., Eun, G., Ha, J., Kim, Y., Park, N., Kim, D. and Choi, I. 2016. New cyst nematode, Heterodera sojae n. sp. (Nematoda: Heteroderidae) from soybean in Korea. J. Nematol. 48:280-289. https://doi.org/10.21307/jofnem-2017-036
  21. Kim, H. I., Hong, C. P., Im, S., Choi, S. R. and Lim, Y. P. 2014. Development of molecular markers and application for breeding in Chinese cabbage. Korean J. Hortic. Sci. Technol. 32:745-752 (in Korean). https://doi.org/10.7235/hort.2014.12203
  22. Kim, J., Mwamula, A. O., Kabir, F., Shin, J. H., Choi, Y. H., Lee, J. K. and Lee, D. 2016. Effcacy of different nematicidal compounds on hatching and mortality of Heterodera schachtii infective juveniles. Korean J. Pestic. Sci. 20:293-299. https://doi.org/10.7585/kjps.2016.20.4.293
  23. Kimpinski, J., Plumas, G. and MacDonald, M. C. 1993. Occurrence of the clover cyst nematode, Heterodera trifolii, in Prince Edward Island soils. J. Nematol. 25:876-879.
  24. Kwon, O. G., Shin, J. H., Kabir, F. M., Lee, J. K. and Lee, D. W. 2016. Dispersal of sugar beet cyst nematode (Heterodera schachtii) by water and soil in highland Chinese cabbage fields. Korean J. Hortic. Sci. Technol. 34:195-205 (in Korean).
  25. Lafi, H. A., Al-Banna, L., Sadder, M. T. and Migdadi, H. M. 2015. Morphological and morphometrical analysis of Heterodera spp. populations in Jordan. Saudi J. Biol. Sci. 23:108-114.
  26. Lee, J. K., Park, B. Y. and Cho, M. R. 2013. Sugar beet cyst nematode occurrence and prevention of diffusion. In: 2013 Annual meeting on the Korean Society of Pesticide Science. p. 60 (Abstract).
  27. Madani, M., Kyndt, T., Colpaert, N., Subbotin, S. A., Gheysen, G. and Moens, M. 2007. Polymorphism among sugar beet cyst nematode Heterodera schachtii populations as inferred from AFLP and ITS-rDNA gene analyses. Russ. J. Nematol. 15:117-128.
  28. Mercer, C. F. and Woodfeld, D. R. 1986. A survey of root knot and clover cyst nematodes in dry hill country. New Zeal. J. Agr. Res. 29:129-135. https://doi.org/10.1080/00288233.1986.10417985
  29. Mulvey, R. H. 1957. Taxonomic value of the cone top and the underbridge in the cyst-forming nematodes Heterodera schachtii, H. schachtii var. trifolii, and H. avenae (Nematoda: Heteroderidae). Can. J. Zool. 35:421-423. https://doi.org/10.1139/z57-032
  30. Mulvey, R. H. and Golden, A. M. 1983. An illustrated key to the cyst-forming genera and species of Heteroderidae in the west- ern hemisphere with species morphometrics and distribution. J. Nematol. 15:1-59.
  31. Schlang, J. 1990. Erstnachweis des Gelben Rubenzystennematoden (Heterodera trifolii) für die Bundesrepublik Deutschland. Nachrichtenblatt des Deutschen Pfanzenschutzdienstes (Braunschweig) 42:58-59.
  32. Seinhorst, J. W. 1959. A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4:67-69. https://doi.org/10.1163/187529259X00381
  33. Sekimoto, S., Uehara, T. and Mizukubo, T. 2017. Characterization of populations of Heterodera trifolii Goffart, 1932 (Nematoda: Heteroderidae) in Japan and their phylogenetic relationships with closely related species. Nematology 19:543-558. https://doi.org/10.1163/15685411-00003067
  34. Sekimoto, S., Uehara, T. and Mizukubo, T. 2016. Geographical distribution of Heterodera trifolii in eastern Japan. Jpn. J. Nematol. 46:1-8. https://doi.org/10.3725/jjn.46.1
  35. Steele, A. E. 1965. The host range of the sugar-beet nematode, Heterodera schachtii Schmidt. J. Am. Soc. Sugar Beet Technol. 13:573-603. https://doi.org/10.5274/jsbr.13.7.573
  36. Steele, A. E. and Whitehand, L. 1984. Comparative morphometrics of eggs and second-stage juveniles of Heterodera schachtii and a race of H. trifolii parasitic on sugar-beet in The Netherlands. J. Nematol. 16:171-177.
  37. Subbotin, S. A., Vierstraete, A., De Ley, P., Rower, J., Waeyenberge, L., Moens, M. and Vanfeteren, J. R. 2001. Phylogenetic relationships within the cyst-forming nematodes (Namatoda, Heteroderidae) based on analysis of sequences from the ITS regions of ribosomal DNA. Mol. Phylogenet. Evol. 21:1-6. https://doi.org/10.1006/mpev.2001.0998
  38. Subbotin, S. A., Waeyenberge, L. and Moens, M. 2000. Identification of cyst forming nematode of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA-RFLPs. Nematology 2:153-164. https://doi.org/10.1163/156854100509042
  39. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  40. Tarte, R. and Mai, W. F. 1976. Morphological variation in Pratylenchus penetrans. J. Nematol. 8:185-195.
  41. Turner, J. S. and Subbotin, S. A. 2013. Cyst nematodes. In: Plant Nematology, eds. R. N. Perry and M. Moens, pp. 109-143. CABI, Nosworthy Way Wallingford, UK.
  42. Van Bezooijen, J. 2006. Methods and techniques for nematology. Wageningen: Wageningen University. 20 pp.
  43. Vovlas, N., Vovlas, A., Leonetti, P., Leibanas, G., Castillo, P., Subbotin, S. A. and Rius, J. E. P. 2015. Parasitism effects on white clover by root-knot and cyst nematodes and molecular separation of Heterodera daverti from H. trifolii. Eur. J. Plant Pathol. 143:833-845. https://doi.org/10.1007/s10658-015-0735-3
  44. Waeyenberge, L., Viaene, N., Subbotin, S. A. and Moens, M. 2009. Molecular identifcation of Heterodera spp., an overview of ffteen years of research. In: Proceedings of the frst workshop of the international cereal cyst nematode initiative, pp. 21-23.
  45. Wouts, W. M. and Baldwin, J. G. 1998. Taxonomy and identifcation. In: The cyst nematodes, ed. S. B. Sharma, pp. 83-122. Kluwer Academic Publishers, London, UK.