Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2022-05-11

Morphological and molecular characteristics of Geocenamus longus and the first report of G. brevidens from a karst cave (Nematoda: Merliniidae Siddiqi, 1971)

Museum and Institute of Zoology PAS, Wilcza 64, 00-679 Warsaw, Poland
Museum and Institute of Zoology PAS, Wilcza 64, 00-679 Warsaw, Poland
Museum and Institute of Zoology PAS, Wilcza 64, 00-679 Warsaw, Poland
Nematoda Merliniinae mtCOI phylogeny Piekło pod Skibami Cave rDNA stunt nematodes taxonomy

Abstract

The taxonomic status of stunt nematodes remains under investigation. Many nematode species belonging to the subfamily Merliniinae still await for more detailed studies, especially for the analyzes on the molecular level. In the presented work, two nematode species belonging to this subfamily were investigated. Characteristics of Geocenamus longus were expanded on the morphological and the rDNA- and mtCOI-derived molecular data. The mitochondrial sequences are for the first time presented for Merliniinae. Additionally, a bisexual population of G. brevidens was reported and characterized from a new, unique underground environment.

 

References

  1. Andrássy, I. (2007) Free-living nematodes of Hungary (Nematoda errantia). Vol. II. Pedozoologica Hungarica No. 4. Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest, 496 pp.
    Allen, M. W. (1955) A review of the genus Tylenchorhynchus. University of California Publications in Zoology, 61, 129–66.
    Alvani, S., Mahdikhani-Moghadam, E., Rouhani, H. & Mohammadi, A. (2017) Morphological and molecular characterization and phylogenetic position of a new record, Tylenchorhynchus zeae, and some known species of Telotylenchidae Siddiqi, 1960 and Merliniidae Siddiqi, 1971 from Iran. Turkish Journal of Zoology, 41, 227–36. https://doi.org/10.3906/zoo-1506-47
    Azimi, S., Mahdikhani Moghadam, E. & Rouhani, H. (2016) Morphological, morphometric and molecular characterization of Merlinius microdorus (Geraert, 1966) Siddiqi, 1970, Scutylenchus rugosus (Siddiqi, 1963) Siddiqi, 1979 (Merliniidae), and Psilenchus curcumerus Rahaman, Ahmad and Jairajpuri, 1994 (Psilenchidae) and approaches to phylogenetic relationships. Journal of Zoology, 99 (1), 9–18. https://doi.org/10.19263/Redia-99.16.03
    Azizi, K., Eskandari, A., Karegar, A., Ghaderi, R., Van den Elsen, S., Holterman, M. & Helder, H. (2016) Morphological and molecular characterization of Pratylenchoides persicus n. sp. (Nematoda: Merliniidae) and additional data on two other species of the genus from Iran. Zootaxa, 4205 (5), 459–474. https://doi.org/10.11646/zootaxa.4205.5.4
    Bharti, L., Bhat, A.H., Chaubey, A.K. & Abolafia, J. (2020) Morphological and molecular characterisation of Merlinius brevidens (Allen, 1955) Siddiqi, 1970 (Nematoda: Rhabditida: Merlinidae) from India. Journal of Natural History, 54 (23–24), 1477–1498. https://doi.org/10.1080/00222933.2020.1810352
    Bongers, T. (1994) De Nematoden van Nederland. KNNV-bibliotheekuitgave 46. Schoorl., Pirola, 408 pp.
    Brzeski, M.W. (1977) Nicienie pasożyty roślin. Podrząd Tylenchina. Państwowe Wydawnictwo Naukowe, Warsaw, 87 pp.
    Brzeski, M.W. (1991) Taxonomy of Geocenamus Thorne and Malek, 1968 (Nematoda: Belonolaimidae). Nematologica, 37, 125–173. https://doi.org/10.1163/187529291X00169
    Brzeski, M.W. (1998) Nematodes od Tylenchina in Poland and temperate Europe. Muzeum i Instytut Zoologii Polska Akademia Nauk, Warszawa, 397 pp.
    Carta, L.K., Skantar, A.M. & Handoo, Z.A. (2010) Molecular rDNA phylogeny of Telotylenchidae Siddiqi, 1960 and evaluation of tail termini. Journal of nematology, 42 (4), 359–369.
    Chitambar, J.J. & Ferris, H. (2005) Geocenamus angelescresti n. sp., a Diagnostic Key and Compendium to the Species of the Genus Geocenamus Thorne & Malek, 1968 (Nematoda: Belonolaimidae). Journal of Nematology, 37 (4), 429–437.
    Derycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J., Vincx, M. & Moens, T. (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Marine Ecology Progress Series, 300, 91–103. https://doi.org/10.3354/meps300091
    Dobosz, R., Winiszewska, G., Malewski, T., Rybarczyk-Mydłowska, K., Tereba, A., Kowalewska, K., Gawlak, M. & Bogdanowicz, W. (2013) Morphological and molecular features of Punctodera stonei Brzeski, 1998 (Nematoda: Heteroderidae)—species associated with roots of grasses. Annales Zoologici, 63, 157–162. https://doi.org/10.3161/000345413X669487
    Dobies, T. (2004) Nicienie—pasożyty roślin (Nematoda, Tylenchida, Dorylaimida) szkółek leśnych. Acta Scientiarum Polonorum Silvarum Colendarum Ratio et Industria Lignaria, 3 (2), 33–48.
    Du Preez, G., Majdi, N., Swart, A., Traunspurger, W. & Fourie, H. (2017) Nematodes in caves: a historical perspective on their occurrence, distribution and ecological relevance, Nematology, 19 (6), 627–644. https://doi.org/10.1163/15685411-00003068
    Eroshenko, A.S. & Volkova, T.V. (1987) Nematodes Geocenamus patteruns n. sp. and Pathotylenchus nurserus n. gen. et n. sp. from rhisosphere of Coniferales of the Far East of the USSR. Parasitologiya, 21, 595–598.
    Fortuner, R. & Luc, M. (1987) A reappraisal of Tylenchina (Nemata). VI: The family Belonolaimidae Whitehead, 1960. Revue de Nématologie, 10 (2), 183–202.
    Geraert, E. (2006) Functional and Detailed Morphology of the Tylenchida (Nematoda). Nematology Monographs and Perspectives. Vol. 4. Brill, Leiden, 224 pp. https://doi.org/10.1163/9789047418320
    Geraert, E. (2011) The Dolichodoridae of the World. Identification of the family Dolichodoridae. Academia Press, Gent, pp. 107–130.
    Ghaderi, R., Karegar, A., Niknam, G. & Subbotin, S.A. (2014) Phylogenetic relationships of Telotylenchidae Siddiqi, 1960 and Merliniidae Siddiqi, 1971 (Nematoda: Tylenchida) from Iran, as inferred from the analysis of the D2D3 expansion fragments of 28S rRNA gene sequences. Nematology, 16 (7), 863–877. https://doi.org/10.1163/15685411-00002815
    Ghaderi, R. & Karegar, A. (2016) One new and three known species of Geocenamus Thorne & Malek, 1968 (Nematoda: Merliniidae) from Iran. Zootaxa, 4079 (2), 151–178. https://doi.org/10.11646/zootaxa.4079.2.1
    Ghaderi, R., Hamzehzarghani, H. & Karegar, A. (2017a) Numerical Taxonomy Helps Identification of Merliniidae and Telotylenchidae (Nematoda: Tylenchoidea) from Iran. Journal of nematology, 49 (2), 207–222. https://doi.org/10.21307/jofnem-2017-065
    Ghaderi, R., Karegar, A., Miraeiz, E. & Hashemi, K. (2017b) Comparative morphology of the anterior end of selected taxa of Merliniidae Siddiqi, 1971 (Nematoda: Tylenchoidea), with morphological characterisation of two species and taxonomic keys to several genera. Zootaxa, 4300 (4), 571–588. https://doi.org/10.11646/zootaxa.4300.4.6
    Grodzicki, J., Urban, J. & Kasza, A. (2013) Piekło pod Skibami. Jaskinie Polski. PIG-PIB, Available from: http://jaskiniepolski.pgi.gov.pl/Details/Information/831 (accessed 8 February 2022)
    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
    Handoo, Z., Khan, A. & Islam, S. (2007) A key and diagnostic compendium to the species of the genus Merlinius Siddiqi, 1970 (Nematoda: Tylenchida) with description of Merlinius khuzdarensis n. sp. associated with date palm. Nematology, 9 (2), 251–260. https://doi.org/10.1163/156854107780739045
    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. Molecular Biology and Evolution, 23 (9), 1792–1800. https://doi.org/10.1093/molbev/msl044
    Holterman, M., Rybarczyk, K., Van den Elsen, S., Van Megen, H., Mooyman, P., Santiago, R.P., Bongers, T., Bakker, J. & Helder, J. (2008) A ribosomal DNA-based framework for the detection and quantification of stress—sensitive nematode families in terrestrial habitats. Molecular Ecology Resources, 8 (1), 23–34. https://doi.org/10.1111/j.1471-8286.2007.01963.x
    Holterman, M., Karssen, G., Van Den Elsen, S., Van Megen, H., Bakker, J. & Helder, J. (2009) 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 (3), 227–235. https://doi.org/10.1094/PHYTO-99-3-0227
    Hu, M., Chilton, N.B., Zhu, X. & Gasser, R.B. (2002) Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis, 23 (1), 27–34. https://doi.org/10.1002/1522-2683(200201)23:1%3C27::AID-ELPS27%3E3.0.CO;2-7
    Jordaan, E.M., Vandenberg, E. & De Waele, D. (1992) Plant-parasitic nematodes on field crops in South Africa. 5. Wheat. Fundamental Applied Nematology, 15 (6), 531–537.
    Knobloch, N.A. (1971) Emendation of the description of Tylenchorhynchus longus Wu, 1969. Nematologica, 17 (4), 602–603. https://doi.org/10.1163/187529271X00341
    Kasapoğlu, E.BU., Yýldýz, Þ., Ýmren, M., Öcal, A. & Elekcioğlu, Ý.H. (2018) Occurrence of plant parasitic nematode species in important crops in the Southeast Anatolia Region of Turkey. Türkiye Entomoloji Dergisi-Turkish Journal Of Entomology, 42 (1), 63–74. https://doi.org/10.16970/entoted.359616
    Lišková, M. & Renčo, M. (2007) Communities of free living and plant parasitic nematodes in hop gardens in Slovakia. Helminthologia, 44 (2), 80–86. https://doi.org/10.2478/s11687-007-0008-6
    Maggenti, A.R., Luc, M., Rasici, D.J., Fortuner, R. & Geraert, E. (1988) A reappraisal of Tylenchina (Nemata): 11. List of generic and supra-generic taxa, with their junior synonyms. Revue de Nématologie, 11 (2), 177–188.
    Malek, R.B. (1980) Population Response to Temperature in the Subfamily Tylenchorhynchinae. Journal of Nematology, 12 (1), 1–3.
    Maria, M., Miao, W., Castillo, P. & Zheng, J. (2020) A new stunt nematode, Geocenamus chengi n. sp. (Nematoda: Merliniinae) in the rhizosphere of tea (Camellia sinensis) from Zhejiang Province, China. Journal of nematology, 52, 1–13. https://doi.org/10.21307/jofnem-2020-042
    Meldal, B.H.M., Debenham, N.J., De Ley, P., De Ley, I.T., Vanfleteren, J.R., Vierstraete, A.R., Bert, W., Borgonie, G., Moens, T., Tyler, P.A., Austen, M.C., Blaxter, M.L., Rogers, A.D. & Lambshead, P.J.D. (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Molecular Phylogenetics and Evolution, 42, 622–636. https://doi.org/10.1016/j.ympev.2006.08.025
    Munawar, M., Yevtushenko, D.P. & Castillo, P. (2021) Integrative taxonomy, distribution, and host associations of Geocenamus brevidens and Quinisulcius capitatus from southern Alberta, Canada. Journal of nematology, 53, e2021-15. https://doi.org/10.21307/jofnem-2021-015
    Nguyen, H.T., Le, T.M.L., Nguyen, T.D., Liebanas, G., Nguyen, T.A.D. & Trinh, Q.P. (2019) Description of Geocenamus vietnamensis sp. n. (Nematoda: Merliniidae) from Vietnam. Journal of nematology, 51, 1–12. https://doi.org/10.21307/jofnem-2019-025
    Nunn, G.B. (1992) Nematode molecular evolution: An investigation of evolutionary patterns among nematodes based upon DNA sequences. Ph.D. Thesis, University of Nottingham, Nottingham, 228 pp.
    Ortiz, V., Phelan, S. & Mullins, E. (2016) A temporal assessment of nematode community structure and diversity in the rhizosphere of cisgenic Phytophthora infestans-resistant potatoes. Bmc Ecology, 16 (1), 1–23. https://doi.org/10.1186/s12898-016-0109-5
    Palomares-Rius, J.E., Castillo, P., Montes-Borrego, M., Navas-Cortes, J.A. & Landa, B.B. (2015) Soil properties and olive cultivar determine the structure and diversity of plant-parasitic nematode communities infesting olive orchards soils in southern Spain. PLoS One, 10 (1), e0116890. https://doi.org/10.1371/journal.pone.0116890
    Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 6 April 2022)
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
    Ryss, A.Y. (1993) Phylogeny of the order Tylenchida (Nematoda). Russian Journal of Nematology, 1 (2), 74–95.
    Shokoohi, E., Iqbal, E., Mashela, P.W. & Kazi, N. (2022) Observations of Merlinius brevidens associated with the cultivated cherry in Balochistan, Pakistan. Biologia, 77 (1), 167–180. https://doi.org/10.1007/s11756-021-00929-0
    Siddiqi, M.R. (1961) Studies on Tylenchorhynchus spp. (Nematoda: Tylenchida) from India. Z. Parasitenk, 21, 46–64. https://doi.org/10.1007/BF00260176
    Siddiqi, M.R. (1970) On the plant-parasitic nematode genera Merlinius gen. n. and Tylenchorhynchus Cobb and the Classification of the Families Dolichodoridae and Belonolaimidae n. rank. Proceedings of the Helminthological Society of Washington, 37 (1), 68–77.
    Siddiqi, M.R. (1979) Taxonomy of the plant nematode subfamily Merliniinae Siddiqi, 1970, with descriptions of Merlinius processus n. sp., M. loofi n. sp., and Amplimerlinius globigerus n. sp. from Europe. Systematic Parasitology, 1 (1), 43–59. https://doi.org/10.1007/BF00009773
    Siddiqi, M.R. (2000) Tylenchida parasites of plants and insects. 2nd Edition. CABI Publishing, Oxon, 833 pp. https://doi.org/10.1079/9780851992020.0000
    Sikora, G., Kubicz, M. & Kocot-Zalewska, J. (2018) Nicienie z wybranych jaskiń Polski. In: Czyżewski, Ł. & Sudoł-Procyk, M. (Eds.), Materiały 52. Sympozjum Speleologicznego. Sekcja Speleologiczna Polskiego Towarzystwa Przyrodników im. Kopernika, Kraków, pp. 73–74.
    Skwiercz A.T. (1984) Two new species of the genus Scutylenchus Jajrajpuri, 1971 (Tylenchoidea: Nematoda) from Poland with a key to the species. Revue de Nematologie, 7, 87–93.
    Smiley, R.W., Whittaker, R.G., Gourlie, J.A. & Easley, S.A. (2006) Geocenamus brevidens associated with Reduced Yield of No-Till Annual Spring Wheat in Oregon. Plant disease, 90 (7), 885–890. https://doi.org/10.1094/PD-90-0885
    Sturhan, D. (1981) Studies on Geocenamus species from Germany (Nematoda: Dolichodoridae). Nematologica, 27 (3), 306–314. https://doi.org/10.1163/187529281X00539
    Sturhan, D. (2011) On lateral fields and deirids in Merliniinae (Tylenchida, Telotylenchidae) and the genus Pratylenchoides (Pratylenchidae). Journal of Nematode Morphology and Systematics, 14 (2), 179–182.
    Sturhan, D. (2012) Contribution to a revision of the family Merliniidae Ryss, 1998, with proposal of Pratylenchoidinae subfam. n., Paramerlinius gen. n., Macrotylenchus gen. n. and description of M. hylophilus sp. n. (Tylenchida). Journal of Nematode Morphology and Systematics, 15 (2), 127–147.
    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 (3), 455–474. https://doi.org/10.1163/156854106778493420
    Tarjan, A.C. (1973) A synopsis of the genera and species in the Tylenchorhynchinae (Tylenchoidea, Nematoda). Proceedings of The Helminthological Society of Washington, 40 (1), 123–144.
    Thorne, G. & Malek, R.B. (1968) Nematodes of the Northern Great Plains: Part 1 Tylenchida (Nemata Secernentra). Technical Bulletin South Dakota Agricultural Experiment Station, 31, 1–111.
    Tzortzakakis, E.A., Cantalapiedra-Navarrete, C., Kormpi, M., Lazanaki, M.S., Castillo, P. & Archidona-Yuste, A. (2018) First Report of Bitylenchus hispaniensis, Pratylenchoides alkani, and Helicotylenchus vulgaris in association with cultivated and wild olives in Crete, Greece and molecular identification of Helicotylenchus microlobus and Merlinius brevidens. Journal of Nematology, 50, 413–418. https://doi.org/10.21307/jofnem-2018-020
    van Benzooijen, J. (2006) Methods and techniques for nematology. The Nematology Department Manual, Wageningen University, Wageningen, 112 pp.
    van Megen, H., van den Elsen, S., Holterman, M., Karssen, G., Mooyman, P., Bongers, A.M.T., Holovachov, O., Bakker, J. & Helder, J. (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences, Nematology, 11 (6), 927–950. https://doi.org/10.1163/156854109X456862
    Volkova, T.V. (1995) Geocenamus khashanicus sp. n. (Tylenchida: Merliniinae) from the Russian Far East. Russian Journal of Nematology, 3, 31–33.
    Wołoszyn, B.W. (1977) s.n. Rocznik Świętokrzyski, KTN 5, 128–142.
    Wu, L.Y. (1969) Three new species of the genus Tylenchorhynchus Cobb, 1913 (Tylenchidae: Nematoda) from Canada. Canadian Journal of Zoology, 47, 563–567.
    Yoder, M., De Ley, I.T., King, I.W., Mundo-Ocampo, M., Mann, J., Blaxter, M. & De Ley, P. (2006) DESS: a versatile solution for preserving morphology and extractable DNA of nematodes. Nematology, 8 (3), 367–376. https://doi.org/10.1163/156854106778493448
    Zapałowska, A. & Skwiercz, A.T. (2018) Populations of parasitic nematodes colonizing Jerusalem artichoke (Helianthus tuberosus L.). Acta Societatis Botanicorum Poloniae, 87 (2), 1–10. https://doi.org/10.5586/asbp.3578
    Zepp, A.L. (1974) Abnormal male of Merlinius brevidens (Allen, 1955) Siddiqi, 1970. Nematologia mediterranea, 2 (1), 81–82.

  2.