Description of a new needle nematode, Paralongidorus koreana n. sp., and two known Xiphinema spp. cobb, 1913, from turfgrass in Korea

  • Abraham Okki Mwamula
  • Wilfrida Decraemer
  • Yeong Ho Kim
  • Hyoung-Rai Ko
  • Heebeen Na
  • Young Ho Kim
  • Dong Woon LeeEmail author


A new needle nematode, Paralongidorus koreana n. sp., recovered from rhizosphere of Poa pratensis and Zoysia japonica from Korea, is described and illustrated based on inferences from morphological and molecular data. Additionally, the existence and taxonomic status of X. diffusum and X. insigne in Korea is also duly confirmed. Phylogenetic inferences were based on an integrative approach considering the analyses of the 28S rRNA, ITS1 rRNA, SSU rRNA and the partial COI gene sequences. The new species is characterized by medium body length (4.2–5.5 mm); lip region rounded, slightly set off from the body by a shallow indentation, 15.0–18.3 μm wide; amphidial fovea stirrup shaped; guiding ring anteriorly positioned (28.6–33.6 μm from anterior end); odontostyle moderately long (99.4–109.7 μm); tail short (34.0–43.5 μm), hemispherical to bluntly rounded. Males rare in population. Spicules moderate, 70 μm long; 13 irregular spaced ventromedian precloacal supplements anterior to the adanal pair; four juvenile developmental stages clearly distinguishable. The new species is morphologically similar to P. bikanerensis, P. inagreinus, P. hanliae, P. spasskii, P. nudus, P. indicus and P. sali but differs from all, either by lip region shape and width, amphidial fovea shape, body and odontostyle length, female tail length and shape or spicule length. Sequence data analyses from amplified regions suggest that it’s a sister species to P. bikanerensis and P. sali, and the three species are consistently placed in a clade outside the main clade for Paralongidorus. Xiphinema insigne and X. diffusum DNA sequences were similar to the respective species sequences available in GenBank.


18S D2-D3 ITS1 COMorphology Xiphinema insigne Xiphinema diffusum 



The authors thank golf course superintendents; D. H. Choi, D. C. Kang, J. G. Kim and J. Kim from Seo Kyung Tani Country Club, Yangsan Country Club, Dongrae Benest Golf Club and Sky72 Golf and Resorts, respectively for their cooperation during the survey. We also acknowledge Youngjoon Kim, Hyeon Jeong Ahn, Mungi Jeong, Faisal Md. Kabir, and Hyeon Guk Kim for the necessary laboratory technical support.

Compliance with ethical standards

Conflict of interest

All authors affirm that 1) there exist no actual or potential conflict of interests to disclose, 2) the manuscript is original and has not been published previously (partly or in full), and is not under review for publication elsewhere, 3) all the necessary local, national and international standards, regulations and conventions, including normal scientific ethical practices, have been duly followed and respected. Additionally, all authors have endorsed the final version of the manuscript before submission.

Research involving human participants and/or animals

The authors certify that no special permits were required for the fieldwork investigations. Permission for sampling the golf course was always granted by the respective Golf course superintendent, and investigations did not involve any species endangered or protected in South Korea.

Informed consent

All the authors declare that the principles of ethical and professional conduct were duly followed during the execution of this research. The research was locally funded by Forest Biomaterials Research Center, National Institute of Forest Science; and The Rural Development Administration, Republic of Korea under project “Research Program for Agriculture, Science and Technology Development, project no. PJ01342804”.


  1. Archidona-Yuste, A., Cantalapiedra-Navarrete, C., Castillo, P., & Palomares-Rius, J. E. (2019). Molecular phylogenetic analysis and comparative morphology reveals the diversity and distribution of needle nematodes of the genus Longidorus (Dorylaimida: Longidoridae) from Spain. Contributions to Zoology, 1(88), 1–41.CrossRefGoogle Scholar
  2. Bajaj, H. K., & Jairajpuri, M. S. (1977). Variability within Xiphinema insigne populations from India. Nematologica, 23(1), 33–46.CrossRefGoogle Scholar
  3. Barker, K. R., Nusbaum, C. J., & Nelson, L. A. (1969). Effects of storage temperature and extraction procedure on recovery of plant-parasitic nematodes from field soils. Journal of Nematology, 1(3), 240–247.PubMedPubMedCentralGoogle Scholar
  4. Barsi, L., & De Luca, F. D. (2017). Morphological and molecular characterisation of Paralongidorus francolambertii sp. n. (Nematoda: Longidoridae) from Serbia. Nematology, 19(6), 681–695.Google Scholar
  5. Cai, R., Maria, M., Qu, N., Castillo, P., & Zheng, J. (2018). Morphological and molecular characterization of Paralongidorus sali Siddiqi, Hooper, and Khan, 1963 with a description of the first-stage juvenile and male of Longidorus jonesi Siddiqi, 1962 from China. Journal of Nematology, 50(3), 419–436.PubMedCrossRefGoogle Scholar
  6. Chawla, M. L., & Samathanam, G. J. (1981). Two new species of the superfamily Longidoroidea (Dorylaimida: Nematoda) from lndia. Indian Journal of Nematology., 10(1980), 205–210.Google Scholar
  7. Chen, Q., Hooper, D. J., Loof, P. A. A., & Xu, J. (1997). A revised polytomous key for the identification of species of the genus Longidorus Micoletzky, 1922 (Nematoda: Dorylaimoidea). Fundamental and Applied Nematology, 20(1), 15–28.Google Scholar
  8. Chen, D. Y., Ni, H. F., Yen, J. H., Cheng, Y. H., & Tsay, T. T. (2005). Differentiation of the Xiphinema americanum-group nematodes X. brevicollum, X. incognitum, X. diffusum and X. oxycaudatum in Taiwan by morphometrics and nuclear ribosomal DNA sequences. Nematology, 7(5), 713–726.CrossRefGoogle Scholar
  9. Cherry, T., Szalanski, A. L., Todd, T. C., & Powers, T. O. (1997). The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae). Journal of Nematology, 29(1), 23–29.PubMedPubMedCentralGoogle Scholar
  10. Choi, Y. E. (1999). Systematic study of Dorylaimida from Korea 5. List of recorded species and redescription of seven species of Dorylaimida from Korea. Korean Journal of Applied Entomology, 38(3), 177–185.Google Scholar
  11. Choi, Y. E., Choi, Y. S., & Cho, M. R. (1992). Nematodes associated with forest trees in Korea III. A new species of Xiphinemella Loos, 1950, and four unrecorded species of Xiphinema cobb, 1913. Korean Journal of Applied Entomology, 31(4), 416–426.Google Scholar
  12. Coomans, A., Huys, R., Heyns, J., & Luc, M. (2001). Character analysis, phylogeny, and biogeography of the genus Xiphinema cobb, 1913 (Nematoda: Longidoridae). Annales du Musée royal de l’Afrique Centrale (Zoologie), Tervuren, Belgique 287, 239 pp.Google Scholar
  13. Coomans, A., De Ley, I. T., Jimenez, L. A., & De Ley, P. (2012). Morphological, molecular characterisation and phylogenetic position of Longidorus mindanaoensis n. sp. (Nematoda: Longidoridae) from a Philippine Avicennia mangrove habitat. Nematology, 14(3), 285–307.CrossRefGoogle Scholar
  14. De Luca, F., Lamberti, F., & Barsi, L. (2007). Morphological and molecular characterisation of Longidorus danuvii sp. n. and L. silvae Roca, 1993 (Nematoda: Dorylaimida) from Serbia. Nematology, 9(4), 585–598.CrossRefGoogle Scholar
  15. Decraemer, W., & Chaves, E. (2012). Longidoridae and trichodoridae. In R. Manzanilla-Lopez & N. Marban Mendoza (Eds.), Practical plant nematology (pp. 579–617). Mexico: Fundacion Colegio de Posgraduados and Mundi Prensa.Google Scholar
  16. EScuer, M., & Arias, M. (1997). Paralongidorus iberis sp. n. and P. monegrensis sp. n. from Spain with a polytomous key to the species of the genus Paralongidorus Siddiqi, Hooper & Khan, 1963 (Nematoda: Longidoridae). Fundamental and Applied Nematology, 20(2), 135–148.Google Scholar
  17. Gutiérrez-Gutiérrez, C., Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Landa, B. B., Esmenjaud, D., & Castillo, P. (2010). Molecular analysis and comparative morphology to resolve a complex of cryptic Xiphinema species. Zoologica Scripta, 39(5), 483–498.CrossRefGoogle Scholar
  18. Gutiérrez-Gutiérrez, C., Mota, M., Castillo, P., Santos, M. T., & Palomares-Rius, J. E. (2018). Description and molecular phylogeny of one new and one known needle nematode of the genus Paralongidorus (Nematoda: Longidoridae) from grapevine in Portugal using integrative approach. European Journal of Plant Pathology, 151(1), 155–172.Google Scholar
  19. Handoo, Z. A., Carta, L. K., Skantar, A. M., Subbotin, S. A., & Fraedrich, S. W. (2016). Molecular and morphological characterization of Xiphinema chambersi population from live oak in Jekyll Island, Georgia, with comments on morphometric variations. Journal of Nematology, 48(1), 20–27.PubMedPubMedCentralCrossRefGoogle Scholar
  20. He, Y., Jones, J., Armstrong, M., Lamberti, F., & Moens, M. (2005). The mitochondrial genome of Xiphinema americanum sensu stricto (Nematoda: Enoplea): Considerable economization in the length and structural features of encoded genes. Journal of Molecular Evolution, 61(6), 819–833.PubMedCrossRefGoogle Scholar
  21. Heyns, J. (1966). Further studies on south African Longidoridae (Nematoda). South African Journal of Agricultural Science, 9(4), 927–944.Google Scholar
  22. Heyns, J. (1972). Observations on south African Paralongidorus species (Nematoda: Longidoridae) with descriptions of two new species. Phytophylactica, 4(4), 127–132.Google Scholar
  23. Heyns, J. (1991). The genus Xiphinema in southern Africa. XXII. X. miekeae spec. Nov., with notes on X. clavatum Heyns, 1965, X. setariae Luc, 1958, and X. insigne Loos, 1949 (Nematoda: Longidoridae). Phytophylactica, 23(3), 207–211.Google Scholar
  24. Hunt, D. J. (1993). Aphelenchida, Longidoridae and Trichodoridae: Their systematics and bionomics (352 p). Wallingford: CAB International.Google Scholar
  25. Iwahori, H., Kanzaki, N., & Futai, K. (2000). A simple, polymerase chain reaction-restriction fragment length polymorphism-aided diagnosis method for pine wilt disease. Forest Pathology, 30(3), 157–164.CrossRefGoogle Scholar
  26. Jenkins, W. R. (1964). A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Report, 48(9), 692.Google Scholar
  27. Khan, E., Chawla, M. L., & Saha, M. (1978). Comments on the classification of the Longidoroidea (Nematoda) with description of three new species. Indian Journal of Nemalology, 6(1976), 47–62.Google Scholar
  28. Kirjanova, E. S. (1951). Nematody pochvy khlipkovogo polya i tseling v Golodnoi Stepi (Uzbekistan). Trav. Inst. Zool. Acad. Sci. U.E.S.S, 9, 625–657.Google Scholar
  29. Kumari, S., Decraemer, W., & De Luca, F. (2010). Molecular characterization of Xiphinema brevicollum (Nematoda: Longidoridae) from the Czech Republic. European Journal of Plant Pathology, 128(2), 243–250.CrossRefGoogle Scholar
  30. Lal, A., & Mathur, V. K. (1987). Nematodes in the rhizosphere of date palm with description of Longidoroides bikanerensis sp. n. (Nematoda: Dorylaimoidea). Date Palm Journal, 5(2), 208–214.Google Scholar
  31. Lamberti, F. (1975). Taxonomy of Longidorus (Micoletzky) Filipjev and Paralongidorus Siddiqi, Hooper and Khan. In nematode vectors of plant viruses (pp. 71–90). Springer, Boston.CrossRefGoogle Scholar
  32. Lamberti, F., & Bleve-Zacheo, T. (1979). Studies on Xiphinema americanum sensu lato with descriptions of fifteen new species (Nematoda, Longidoridae). Nematologia Mediterranea, 7(1), 51–106.Google Scholar
  33. Lamberti, F., Ciancio, A., Agostinelli, A., & Coiro, M. I. (1991). Relationship between Xiphinema brevicolle and X. diffusum with a redescription of X. brevicolle and descriptions of three new species of Xiphinema (Nematoda: Dorylaimida). Nematologia Mediterranea, 19(2), 311–326.Google Scholar
  34. Lamberti, F., Molinari, S., Moens, M., & Brown, D. J. F. (2000). The Xiphinema americanum group. I. Putative species, their geographical occurrence and distribution, and regional polytomous identification keys for the group. Russian Journal of Nematology, 8(1), 65–84.Google Scholar
  35. Lamberti, F., Molinari, S., Moens, M., & Brown, D. J. F. (2002). The Xiphinema americanum-group. II. Morphometric relationships. Russian Journal of Nematology, 10(2), 99–112.Google Scholar
  36. Lamberti, F., Hockland, S., Agostinelli, A., Moens, M., & Brown, D. J. F. (2004). The Xiphinema americanum group. III. Keys to species identification. Nematologia Mediterranea, 32(1), 53–56.Google Scholar
  37. Lazarova, S., Malloch, G., Oliveira, C. M. G., Hübschen, J., & Neilson, R. (2006). Ribosomal and mitochondrial DNA analyses of Xiphinema americanum-group populations. Journal of Nematology, 38(4), 404–410.PubMedPubMedCentralGoogle Scholar
  38. Lazarova, S., Peneva, V., & Kumari, S. (2016). Morphological and molecular characterization, and phylogenetic position of X. browni sp. n., X. penevi sp. n. and two known species of Xiphinema americanum-group (Nematoda, Longidoridae). ZooKeys, (574), 1-42.Google Scholar
  39. Lazarova, S., Oliveira, C. M. G., Prior, T., Peneva, V., & Kumari, S. (2019). An integrative approach to the study of Xiphinema brevicolle Lordello and Da Costa 1961, supports its limited distribution worldwide (Nematoda: Longidoridae). European Journal of Plant Pathology, 153(2), 441–464.CrossRefGoogle Scholar
  40. Liebenberg, A., & Swart, A. (1993). Studies on Paralongidorus species from southern Africa. I. Introduction and description of P. capensis Heyns, 1967 and P. hanliae spec. Nov. (Nematoda: Longidoridae). Phytophylactica, 25(2), 91–100.Google Scholar
  41. Loof, P. A. A., Luc, M., & Baujard, P. (1996). A revised polytomous key for the identification of species of the genus Xiphinema cobb, 1913 (Nematoda: Longidoridae) with exclusion of the X. americanum-group: Supplement 2. Systematic Parasitology, 33(1), 23–29.Google Scholar
  42. Loos, C. A. (1949). Notes on free-living and plant-parasitic nematodes of Ceylon. No: 5. Journal of Zoological Society of India, 1(1), 23–29.Google Scholar
  43. Lordello, L. G. E. (1953). Contribuic¸a˜o ao conhecimentodos nemato’deos do solo de algumas regio˜es do Estado de Sa˜o Paulo. Thesis. Escola Superior Agric. “Luiz de Queiroz” Univ. Sa˜o Paulo, 80 pp.Google Scholar
  44. Luc, M., & Baujard, P. (2001). On specific determination within the Xiphinema americanum group (Nematoda: Longidoridae). Nematology, 3(7), 727–728.CrossRefGoogle Scholar
  45. Luc, M., & Doucet, M. E. (1984). Description of Xiphidorus achalae n. sp. and proposal for a classification of longidorids (Nematoda: Dorylaimoidea). Revue de Nématologie, 7(2), 103–112.Google Scholar
  46. Luc, M., & Southey, J. F. (1980). Study of biometrical variability in Xiphinema insigne Loos, 1949, and X. elongatum Schuurmans Stekhoven & Teunissen, 1938; description of X. savanicola n. sp. (Nematoda: Longidoridae) and comments on thelytokous species. Revue de Ne’matologie, 3(2), 243–269.Google Scholar
  47. Luc, M., Coomans, A., Loof, P. A. A., & Baujard, P. (1998). The Xiphinema americanum-group (Nematoda: Longidoridae). 2. Observations of Xiphinema brevicollum Lordello & da Costa, 1961 and comments on the group. Fundamental and Applied Nematology, 21(5), 475–490.Google Scholar
  48. Nunn, G. B. (1992). Nematode molecular evolution. Ph.D. Thesis, University of Nottingham, Nottingham, UK.Google Scholar
  49. Oliveira, C. M. G., Fenton, B., Malloch, G., Brown, D. J. F., & Neilson, R. (2005). Development of species-specific primers for the ectoparasitic nematode species Xiphinema brevicolle, X. diffusum, X. elongatum, X. ifacolum and X. longicaudatum (Nematoda: Longidoridae) based on ribosomal DNA sequences. Annals of Applied Biology, 146(3), 281–288.CrossRefGoogle Scholar
  50. Orlando, V., Chitambar, J. J., Dong, K., Chizhov, V. N., Mollov, D., Bert, W., & Subbotin, S. A. (2016). Molecular and morphological characterisation of Xiphinema americanum group species (Nematoda: Dorylaimida) from California, USA, and other regions, and co-evolution of bacteria from the genus Candidatus Xiphinematobacter with nematodes. Nematology, 18(9), 1015–1043.CrossRefGoogle Scholar
  51. Oteifa, B. A., & Tarjan, A. C. (1965). Potentially important plant-parasitic nematodes present in established orchards of a newly reclaimed area of the united Arab Republic. Plant Disease Report, 49, 596–597.Google Scholar
  52. Palomares-Rius, J. E., Subbotin, S. A., Landa, B. B., Vovlas, N., & Castillo, P. (2008). Description and molecular characterisation of Paralongidorus litoralis sp. n. and P. paramaximus Heyns, 1965 (Nematoda: Longidoridae) from Spain. Nematology, 10(1), 87–102.CrossRefGoogle Scholar
  53. Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Gutiérrez-Gutiérrez, C., Liébanas, G., & Castillo, P. (2013). Morphological and molecular characterisation of Paralongidorus plesioepimikis n. sp. (Nematoda: Longidoridae) from southern Spain. Nematology, 15(3), 363–378.CrossRefGoogle Scholar
  54. Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Archidona-Yuste, A., Subbotin, S. A., & Castillo, P. (2017). The utility of mtDNA and rDNA for barcoding and phylogeny of plant-parasitic nematodes from Longidoridae (Nematoda, Enoplea). Scientific Reports, 7(1), 10905.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Pedram, M., Pourjam, E., Namjou, S., Atighi, M. R., Cantalapiedra-Navarrete, C., Liébanas, G., & Castillo, P. (2012). Molecular and morphological characterisation of Paralongidorus iranicus n. sp. and P. bikanerensis (Lal & Mathur, 1987) Siddiqi, Baujard & Mounport, 1993 (Nematoda: Longidoridae) from Iran. Nematology, 14(4), 427–443.CrossRefGoogle Scholar
  56. Phukan, P. N., and Sanwal, K. C, (1982) - Siddiqia indicus sp. n. (Nematoda: Longidoroidea) from Assam India. Indian Journal Nematology, 12(1), 188–191.Google Scholar
  57. Razak, A. R., & Loof, P. A. A. (1998). The genus Xiphinema cobb, 1913 (Nematoda: Longidoridae) in western Malaysia. Fundamental and Applied Nematology, 21(4), 413–428.Google Scholar
  58. Robbins, R. T. (1978). Descriptions of females (emended), a male, and juveniles of Paralongidorus microlaimus (Nematoda: Longidoridae). Journal of Nematology, 10(1), 28–34.PubMedPubMedCentralGoogle Scholar
  59. Robbins, R. T., Brown, D. J. F., Halbrendt, J. M., & Vrain, T. C. (1995). Compendium of Longidorus juvenile stages with observations on L. pisi, L. taniwha, and L. diadecturus (Nematoda: Longidoridae). Systematic Parasitology, 32(1), 33–52.CrossRefGoogle Scholar
  60. Robbins, R. T., Zheng, J. W., & Brown, D. J. F. (2000). Observations on a Xiphinema insigne population with several males from Hangzhou, China. Journal of Nematology, 32(3), 253–257.PubMedPubMedCentralGoogle Scholar
  61. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Seinhorst, J. W. (1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica, 4(1), 67–69.CrossRefGoogle Scholar
  63. Shah, F. A., Bell, N. L., & Bulman, S. R. (2009). Morphological and molecular confirmation of Xiphinema brevicollum, a nematode from the virus-vectoring X. americanum group, from New Zealand. Australasian Plant Pathology, 38(5), 500–504.CrossRefGoogle Scholar
  64. Siddiqi, M. R. (1962). Studies on the genus Longidorus Micoletzky, 1922 (Nematoda: Dorylaimoidea), with descriptions of three new species. Proceedings of the Helminthological Society of Washington, 29(2), 177–188.Google Scholar
  65. Siddiqi, M. R. (1965). Longidorus nirulai n. sp., a parasite of potato plants in Shillong, India, with a key to species of Longidorus (Nematoda: Dorylaimoidea). Proceedings of the Helminthological Society of Washington, 32(1), 95–99.Google Scholar
  66. Siddiqi, M. R., Hooper, D. J., & Khan, E. (1963). A new nematode genus Paralongidorus (Nematoda: Dory1aimoidea) with description of two new species and observations on Paralongidorus citri (Siddiqi, 1959) n. comb. Nematologica, 9(1), 7–14.CrossRefGoogle Scholar
  67. Siddiqi, M. R., Baujard, P., & Mounport, D. (1993). Description of Paratylenchus pernoxius sp. n. and Paralongidorus duncani sp. n. from Senegal, and synonymization of Longidoroides with Paralongidorus. Afro-Asian Journal of Nematology, 3(1), 81–89.Google Scholar
  68. Swofford, D. L. (2018). PAUP*: Phylogenetic analysis using parsimony and other methods. Version 4.0a164. Sunderland, MA, USA, Sinauer Associates.Google Scholar
  69. Tarjan, A. C., & Luc, M. (1963). Observations on Xiphinema Insigne Loos, 1949 and Xiphinema Elongatum Schuurmans Stekhoven & Teunissen, 1938 (Nematoda: Dorylaimidae). Nematologica, 9(2), 163–172.CrossRefGoogle Scholar
  70. Taylor, C. E., & Brown, D. J. F. (1997). Nematode vectors of plant viruses. Wallingford: CAB International.Google Scholar
  71. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24), 4876–4882.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Vrain, T. C., Wakarchuk, D. A., Levesque, A. C., & Hamilton, R. I. (1992). Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology, 15(6), 563–573.Google Scholar
  73. Xu, J., Fu, P., & Cheng, H. (1995). A taxonomic study on species of Xiphinema from seven provinces of China (Nematoda: Longidoridae). Journal of Nanjing Agricultural University, 18(1), 37–42.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2019

Authors and Affiliations

  1. 1.Department of Ecological ScienceKyungpook National UniversitySangjuSouth Korea
  2. 2.Department of Zoology, Entomology and Fisheries Sciences, College of Natural SciencesMakerere UniversityKampalaUganda
  3. 3.Department of BiologyGhent UniversityGhentBelgium
  4. 4.School of Ecological Environment and TourismKyungpook National UniversitySangjuSouth Korea
  5. 5.Crop Protection Division, National Institute of Agricultural ScienceRural Development AdministrationWanjuSouth Korea

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