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Description of Rotylenchus zhongshanensis sp. nov. (Tylenchomorpha: Hoplolaimidae) and discovery of its endosymbiont Cardinium

Published online by Cambridge University Press:  20 July 2022

F. Guo
Affiliation:
Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, People's Republic of China Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing Agricultural University, Nanjing 210095, People's Republic of China
P. Castillo
Affiliation:
Spanish National Research Council (CSIC), Institute for Sustainable Agriculture (IAS), Campus de Excelencia Internacional Agrolimentario, ceiA3, Avenida Menendez Pidal s/n, 14004 Cordoba, Spain
C. Li
Affiliation:
Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, People's Republic of China
X. Qing*
Affiliation:
Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, People's Republic of China Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing Agricultural University, Nanjing 210095, People's Republic of China
H. Li
Affiliation:
Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, People's Republic of China Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing Agricultural University, Nanjing 210095, People's Republic of China
*
Author for correspondence: Xue Qing, E-mail: [email protected]

Abstract

A new bisexual species of Rotylenchus is described and illustrated based on morphological, morphometric and molecular characterizations. Rotylenchus zhongshanensis sp. nov. is characterized by having a conoid lip region complying with the basic pattern for Hoplolaimidae, but with pharyngeal glands slightly overlapping intestine dorsally and cuticle thickened abnormally in female tail terminus. Females have robust stylet (30.1–33.8 μm). The pharyngeal gland has short dorsal (11.2–16.8 μm) overlap on the intestine. The vulva is located at 48.0–56.5% of body length, and phasmids are pore-like, 4–6 annuli posterior to the anus. For males, phasmids are pore-like, 11–17 annuli posterior to cloaca. The spicules are ventrally arcuate (21.0–28.5 μm) with gubernaculum in 5–8 μm length. The rRNA and mitochondrial COI genes were successfully sequenced from the assembled whole-genome sequences of the new species, and were used for reconstructing the phylogenetic relationships of the new species. A new strain of cyto-endosymbiont Cardinium was also discovered from the genome sequences of R. zhongshanensis sp. nov. The 16S rRNA phylogeny analyses revealed that this new bacterial strain is closed to that from cyst and root-lesion nematodes.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abascal, F, Zardoya, R and Telford, MJ (2010) Translator X: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38(Web Server issue), W7W13.CrossRefGoogle Scholar
Aliramaji, F, Pourjam, E, Álvarez-Ortega, S, Pedram, M and Atighi, MR (2015) Rotylenchus dalikhaniensis n. sp. (Nematoda: Hoplolaimidae), a monosexual species recovered from the rhizosphere of Ruscus hyrcanus Woronow in Mazandaran province, northern Iran. Nematology 17(1), 6777.CrossRefGoogle Scholar
Atighi, MR, Pourjam, E, Pedram, M, Cantalapiedra-Navarrete, C, Palomares-Rius, JE and Castillo, P (2011) Molecular and morphological characterisations of two new species of Rotylenchus (Nematoda: Hoplolaimidae) from Iran. Nematology 13(8), 951964.Google Scholar
Atighi, MR, Pourjam, E, Ghaemi, R, Pedram, M, Liébanas, G, Cantalapiedra-Navarrete, C, Castillo, P and Palomares-Rius, JE (2014) Description of Rotylenchus arasbaranensis n. sp. from Iran with discussion on the taxonomic status of Plesiorotylenchus Vovlas, Castillo and Lamberti, 1993 (Nematoda: Hoplolaimidae). Nematology 16(9), 10191045.CrossRefGoogle Scholar
Baldwin, JG and Bell, AH (1981) Pararotylenchus n. gen. (Pararotylenchinae n. subfam., Hoplolaimidae) with six new species and two new combinations. Journal of Nematology 13(2), 111128.Google ScholarPubMed
Blaxter, ML, De Ley, P, Garey, JR, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392(6671), 7175.CrossRefGoogle ScholarPubMed
Brown, AMV (2018) Endosymbionts of plant-parasitic nematodes. Annual Review of Phytopathology 56, 225242.Google ScholarPubMed
Brown, AMV, Wasala, SK, Howe, DK, Peetz, AB, Zasada, IA and Denver, DR (2018) Comparative genomics of WolbachiaCardinium dual endosymbiosis in a plant-parasitic nematode. Frontiers in Microbiology 9, 2482.CrossRefGoogle Scholar
Brzeski, MW, Choi, YE (1998) Synonymisation of Rotylenchus Filipjev, 1936 and Pararotylenchus Baldwin & Bell, 1981 (Nematoda: Hoplolaimidae). Nematologica 44(1), 4548.CrossRefGoogle Scholar
Cantalapiedra-Navarrete, C, Liébanas, G, Archidona-Yuste, A, Palomares-Rius, JE and Castillo, P (2012) Molecular and morphological characterization of Rotylenchus vitis n. sp. (Nematoda: Hoplolaimidae) infecting grapevine in southern Spain. Nematology 14(2), 235247.CrossRefGoogle Scholar
Cantalapiedra-Navarrete, C, Navas-Cortés, JA, Liébanas, G, Vovlas, N, Subbotin, SA, Palomares-Rius, JE and Castillo, P (2013) Comparative molecular and morphological characterisations in the nematode genus Rotylenchus: Rotylenchus paravitis n. sp., an example of cryptic speciation. Zoologischer Anzeiger – A Journal of Comparative Zoology 252(2), 246268.CrossRefGoogle Scholar
Castillo, P and Vovlas, N (2005) Bionomics and identification of the genus Rotylenchus (Nematoda: Hoplolaimidae). nematology monographs and perspectives 3. (Series editors: Hunt, D.J. and Perry, R.N.). Leiden, The Netherlands, Brill.CrossRefGoogle Scholar
Cobb, NA (1917) A new parasitic nema found infesting cotton and potatoes. Journal of Agricultural Research 11, 2733.Google Scholar
Coomans, A (1962) Morphological observations on Rotylenchus goodeyi Loof and Oostenbrink, 1958. Nematologica 7(3), 203215.CrossRefGoogle Scholar
Denver, DR, Brown, AMV, Howe, DK, Peetz, AB and Zasada, IA (2016) Genome skimming: a rapid approach to gaining diverse biological insights into multicellular pathogens. PLoS Pathogens 12(8), e1005713.CrossRefGoogle ScholarPubMed
Dierckxsens, N, Mardulyn, P and Smits, G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research 45(4), e18.Google ScholarPubMed
Endo, BY (1979) The ultrastructure and distribution of an intracellular bacterium-like microorganism in tissue of larvae of the soybean cyst nematode. Heterodera glycines. Journal of Ultrastructure Research 67(1), 114.CrossRefGoogle ScholarPubMed
Filipjev, IN (1934) The classification of free-living nematodes and their relations to parasitic nematodes. Smithsonian Miscellaneous Collections 89(6), 163.Google Scholar
Filipjev, IN (1936) On the classification of the Tylenchinae. Proceedings of the Helminthological Society of Washington 3(2), 8082.Google Scholar
Germani, G, Baldwin, JG, Bell, AH and Wu, XY (1985) Revision of the genus Scutellonema Andrássy 1958 (Nematoda: Tylenchida). Revue de Nématologie 8, 289320.Google Scholar
Golhasan, B, Heydari, R, Álvarez-Ortega, S, Meckes, O, Pedram, M and Atighi, MR (2016) Rotylenchus sardashtensis n. sp., a monosexual species from Iran, with molecular identification and detailed morphological observations on an Iranian population of Rotylenchus cypriensis Antoniou, 1980 (Nematoda: Rhabditida: Hoplolaimidae). Systematic Parasitology 93(4), 395411.CrossRefGoogle Scholar
Gotoh, T, Noda, H and Ito, S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98(1), 1320.CrossRefGoogle ScholarPubMed
Haegeman, A, Vanholme, B, Jacob, J, Vandekerckhove, TT, Claeys, M, Borgonie, G and Gheysen, G (2009) An endosymbiotic bacterium in a plant-parasitic nematode: member of a new Wolbachia supergroup. International Journal for Parasitology 39(9), 10451054.CrossRefGoogle Scholar
Hegedusova, E, Brejova, B, Tomaska, L, Sipiczki, M and Nosek, J (2014) Mitochondrial genome of the basidiomycetous yeast Jaminaea angkorensis. Current Genetics 60(1), 4959.CrossRefGoogle ScholarPubMed
Hunter, MS, Perlman, SJ and Kelly, SE (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proceedings of the Royal Society B: Biological Sciences 270(1529), 21852190.CrossRefGoogle ScholarPubMed
Jones, JT, Haegeman, A, Danchin, EG, et al. (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14(9), 946961.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4), 772780.CrossRefGoogle ScholarPubMed
Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G and Durbin, R (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25(16), 20782079.CrossRefGoogle ScholarPubMed
Loof, PAA and Oostenbrink, M (1958) Die identität Von Tylenchus Robustus De Man [The identity of Tylenchus robustus De Man]. Nematologica 3(1), 3443. [In German.]CrossRefGoogle Scholar
Maqbool, MA and Shahina, F (1986) Four new species of the family Hoplolaimidae: (Nematoda) with notes on Rotylenchus cypriensis Antoniou from Pakistan. Nematologia Mediterranea 14(1), 117128.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE) LA, New Orleans, LA, USA, 14 November 2010. Piscataway, NJ, Institute of Electrical and Electronics Engineers, pp. 18.CrossRefGoogle Scholar
Nadler, S, Felix, MA, Frisse, L, Sternberg, PW, De Ley, P and Thomas, WK (1999) Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology 1, 591612.Google Scholar
Nakamura, Y, Yukuhiro, F, Matsumura, M and Noda, H (2012) Cytoplasmic incompatibility involving Cardinium and Wolbachia in the white-backed planthopper Sogatella furcifera (Hemiptera: Delphacidae). Applied Entomology and Zoology 47(3), 273283.CrossRefGoogle Scholar
Nguyen, HT, Trinh, QP, Couvreur, M, Singh, PR, Decraemer, W and Bert, W (2019) Description of Rotylenchus rhomboides n. sp. and a Belgian population of Rotylenchus buxophilus (Tylenchomorpha: Hoplolaimidae). Journal of Nematology 51, e2019e2023.CrossRefGoogle Scholar
Noel, GR and Atibalentja, N (2006) Candidatus Paenicardinium endonii’, an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. International Journal of Systematic and Evolutionary Microbiology 56(7), 16971702.CrossRefGoogle Scholar
Noruzi, E, Asghari, R, Atighi, MR, Eskandari, A, Cantalapiedra-Navarrete, C, Archidona-Yuste, A, Liébanas, G, Castillo, P and Palomares-Rius, JE (2015) Description of Rotylenchus urmiaensis n. sp. (Nematoda: Hoplolaimidae) from North-western Iran with a molecular phylogeny of the genus. Nematology 17(5), 607619CrossRefGoogle Scholar
Palomares-Rius, JE, Cantalapiedra-Navarrete, C and Castillo, P (2014) Cryptic species in plant-parasitic nematodes. Nematology 16(10), 11051118.CrossRefGoogle Scholar
Palomares-Rius, JE, Archidona-Yuste, A, Cantalapiedra-Navarrete, C, Prieto, P and Castillo, P (2016) Molecular diversity of bacterial endosymbionts associated with dagger nematodes of the genus Xiphinema (Nematoda: Longidoridae) reveals a high degree of phylogenetic congruence with their host. Molecular Ecology 25(24), 62256247.CrossRefGoogle ScholarPubMed
Palomares-Rius, JE, Gutiérrez-Gutiérrez, C, Mota, M, et al. (2021) Candidatus Xiphinematincola pachtaicus’ gen. nov., sp. nov., an endosymbiotic bacterium associated with nematode species of the genus Xiphinema (Nematoda, Longidoridae). International Journal of Systematic and Evolutionary Microbiology 71(7), 004888.CrossRefGoogle Scholar
Phillips, SP (1971) Studies of plant and soil nematodes. 16. Eight new species of spiral nematodes (Nematoda: Tylenchoidea) from Queensland. Queensland Journal of Agricultural and Animal Sciences 28(4), 227242.Google Scholar
Robbins, RT (1983) Description of Pararotylenchus belli n. sp. (Nematoda: Hoplolaimidae). Journal of Nematology 15(3), 353356.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3), 539542.CrossRefGoogle ScholarPubMed
Sedlazeck, FJ, Rescheneder, P and von Haeseler, A (2013) NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics 29(21), 27902791.CrossRefGoogle ScholarPubMed
Shepherd, AM, Clark, SA and Kempton, A (1973) An intracellular micro-organism associated with tissues of Heterodera spp. Nematologica 19(1), 3134.Google Scholar
Sher, SA (1963) Revision of the Hoplolaiminae (Nematoda) III. Scutellonema Andrassy, 1958. Nematologica 9(3), 421443.CrossRefGoogle Scholar
Showmaker, KC, Walden, KKO, Fields, CJ, Lambert, KN and Hudson, ME (2018) Genome sequence of the soybean cyst nematode (Heterodera glycines) endosymbiont ‘Candidatus Cardinium hertigii’ strain cHgTN10. Genome Announcements 6(26), e00624–18.CrossRefGoogle Scholar
Singh, PR, Nyiragatare, A, Janssen, T, Couvreur, M, Decraemer, W and Bert, W (2018) Morphological and molecular characterisation of Pratylenchus rwandae n. sp. (tylenchida: Pratylenchidae) associated with maize in Rwanda. Nematology 20(8), 781794.CrossRefGoogle Scholar
Singh, PR, van de Vossenberg, B, Rybarczyk-Mydłowska, K, Kowalewska-Groszkowska, M, Bert, W and Karssen, G (2021) An integrated approach for synonymization of Rotylenchus rhomboides with R. goodeyi (Nematoda: Hoplolaimidae) reveals high intraspecific mitogenomic variation. Phytopathology 112(5), 11521164.CrossRefGoogle Scholar
Sohlenius, B and Sandor, A (1987) Vertical distribution of nematodes in arable soil under grass (Festuca pratensis) and barley (Hordeum distichum). Biology and Fertility of Soils 3(1–2), 1925.Google Scholar
Stamatakis, A, Hoover, P and Rougemont, J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57(5), 758771.CrossRefGoogle ScholarPubMed
Talezari, A, Pourjam, E, Kheiri, A, Liebanas, G, Aliramaji, F, Pedram, M, Rezaee, S and Atighi, MR (2015) Rotylenchus castilloi n. sp. (Nematoda: Hoplolaimidae), a new species with long stylet from northern Iran. Zootaxa 3931(1), 88100.CrossRefGoogle Scholar
Tzortzakakis, EA, Archidona-Yuste, A, Liébanas, G, Birmpilis, IG, Cantalapiedra-Navarrete, C, Navas-Cortés, JA, Castillo, P and Palomares-Rius, JE (2016) Rotylenchus cretensis n. sp. and R. cypriensis Antoniou 1980 (Nematoda: Hoplolaimidae) recovered from the rhizosphere of olive at Crete (Greece) with a molecular phylogeny of the genus. European Journal of Plant Pathology 144(1), 167184.CrossRefGoogle Scholar
Vandekerckhove, TT, Willems, A, Gillis, M and Coomans, A (2000) Occurrence of novel verrucomicrobial species, endosymbiotic and associated with parthenogenesis in Xiphinema americanum-group species (Nematoda, Longidoridae). International Journal of Systematic and Evolutionary Microbiology 50(6), 21972205.CrossRefGoogle Scholar
Van den Berg, E and Heyns, J (1974) South African Hoplolaiminae. 3. The genus Rotylenchus Filipjev, 1936. Phytophylactica 6, 165184.Google Scholar
Vovlas, N, Subbotin, SA, Troccoli, A, Liébanas, G and Castillo, P (2008) Molecular phylogeny of the genus Rotylenchus (Nematoda, Tylenchida) and description of a new species. Zoologica Scripta 37(5), 521537CrossRefGoogle Scholar
Walsh, JA, Lee, DL and Shepherd, AM (1983a) The distribution and effect of intracellular rickettsia-like microorganisms infecting adult males of the potato cyst-nematode Globodera rostochiensis. Nematologica 29(2), 227239.Google Scholar
Walsh, JA, Shepherd, AM and Lee, DL (1983b) The distribution and effect of intracellular rickettsia-like microorganisms infecting second-stage juveniles of the potato cyst-nematode Globodera rostochiensis. Journal of Zoology 199(3), 395419.CrossRefGoogle Scholar
Weeks, AR, Velten, R and Stouthamer, R (2003) Prevalence of a new sex ratio distorting endosymbiotic bacterium among arthropods. Proceedings of the Royal Society B: Biological Sciences 270(1526), 18571865.CrossRefGoogle Scholar
White, JA, Kelly, SE, Cockburn, SN, Perlman, SJ and Hunter, MS (2011) Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium. Heredity 106(4), 585591.CrossRefGoogle Scholar
Whitehead, AG and Hemming, JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Annals of Applied Biology 55(1), 2538.CrossRefGoogle Scholar
Yang, D, Chen, C, Liu, Q and Jian, H (2017) Comparative analysis of pre- and post-parasitic transcriptomes and mining pioneer effectors of Heterodera avenae. Cell and Bioscience 7, 11.CrossRefGoogle ScholarPubMed
Zchori-Fein, E, Perlman, SJ, Kelly, SE, Katzir, N and Hunter, MS (2004) Characterization of a ‘Bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’. International Journal of Systematic and Evolutionary Microbiology 54(3), 961968.Google ScholarPubMed