Abstract
During nematode surveys in France and in South Italy, several Pratylenchus populations were collected which were morphologically related to P. penetrans. The root-lesion nematode P. penetrans is widely distributed across the world and is considered one of the most economically damaging species in the genus. Correct identification of this species is needed. Unfortunately, most of the species belonging to the penetrans group are very difficult to identify morphologically. Thus DNA-based identification can be used as a rapid diagnostic tool. Therefore the ITS, the D2-D3 expansion domains of the 28S rRNA gene and the hsp90 gene of P. penetrans and of other Pratylenchus species were amplified. Sequence analyses of all molecular markers confirmed the high variability of P. penetrans genome. The phylogenetic reconstruction based on the sequences of the ITS and D2-D3 expansion domains confirmed the high sequence variability among the different populations of P. penetrans and the close relationships with the penetrans group. Furthermore, the isolation of two variants of the hsp90 gene in P. penetrans may be related to adaptation to environmental changes and different host plants.
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Results Paragraph: Ribosomal sequence characterization. Fig. 1: This figure is missing and the legend of Fig. 1 is erroneously labeled as Fig. 2, and associated to the phylogenetic tree which corresponds to Fig. 2.
References
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402.
Birnby, D. A., Link, E. M., Vowels, J. J., Thian, H., Colacurcio, P. L., & Thomas, J. H. (2000). A transmembrane guanylyl cyclase (DAF-11) and HSP90 (DAF-21) regulate a common set of chemosensory behavior in Caenorhabditis elegans. Genetics, 155, 85–104.
Boucher, A. C., Mimee, B., Montarry, J., Bardou-Valette, S., Belair, G., Moffett, P., & Grenier, E. (2013). Genetic diversity of the golden potato cyst nematode Globodera rostochiensis and determination of the origin of populations in Quebec, Canada. Molecular Phylogenetics and Evolution, 69, 75–82.
Castillo, P., & Vovlas, N. (2007). Pratylenchus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management. Nematology Monographs and Perspectives, 6. (Series editors: Hunt, D. J. & Perry, R. N.) Leiden, The Netherlands, Brill, 529 pp.
Chen, B., Piel, W. H., Gui, L., Bruford, E., & Monteiro, A. (2005). The HSP90 family of genes in the human genome: Insights into their divergence and evolution. Genomics, 86, 627–637.
De Luca, F., Fanelli, E., Di Vito, M., Reyes, A., & De Giorgi, C. (2004). Comparison of the sequences of the D3 expansion of the 26S ribosomal genes reveals different degrees of heterogeneity in different populations and species of Pratylenchus from the Mediterranean region. European Journal of Plant Pathology, 110, 949–957.
De Luca, F., Di Vito, M., Fanelli, E., Reyes, A., Greco, N., & De Giorgi, C. (2009). Characterization of the heat shock protein 90 gene in the plant parasitic nematode Meloidogyne artiellia and its expression as related to different developmental stages and temperature. Gene, 440, 16–22.
De Luca, F., Troccoli, A., Duncan, L. W., Subbotin, S. A., Waeyenberge, L., Moens, M., & Inserra, R. N. (2010). Characterisation of a population of Pratylenchus hippeastri from bromeliads and description of two related new species, P. floridensis n. sp and P. parafloridensis n. sp., from grasses in Florida. Nematology, 12, 847–868.
De Luca, F., Reyes, A., Troccoli, A., & Castillo, P. (2011). Molecular variability and phylogenetic relationships among different species and populations of Pratylenchus (Nematoda: Pratylenchidae) as inferred from the analysis of the ITS rDNA. European Journal of Plant Pathology, 130, 415–426.
De Luca, F., Troccoli, A., Duncan, L. W., Subbotin, S. A., Waeyenberge, L., Coyne, D. L., Brentu, F. C., & Inserra, R. N. (2012). Pratylenchus speijeri n. Sp. (Nematoda: Pratylenchidae), a new root-lesion nematode pest of plantain in West Africa. Nematology, 14, 1–18.
Esteves, I., Maleita, C., & Abrantes, I. (2015). Root-lesion and root-knot nematodes parasitizing potato. European Journal of Plant Pathology, 141, 397–406.
Geraert, E. (2013). The Pratylenchidae of the world - identification of the family Pratylenchidae (Nematoda: Tylenchida). Gent: Academia Press.
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 rDNAreveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution, 23, 1792–1800.
Handoo, Z. A., Carta, L. K., & SKantar, A. M. (2001). Morphological and molecular characterisation of Pratylenchus arlingtoni n. sp., P . convallariae and P. fallax (Nematoda: Pratylenchidae). Journal of Nematology, 3, 607-618.
Janssen, T., Karssen, G., Orlando, V., Subbotin, S. A., & Bert, W. (2016). Molecular characterization and species delimiting of plant-parasitic nematodes of the genus Pratylenchus from the penetrans group (Nematoda: Pratylenchidae). Molecular Phylogenetics and Evolution, 117, 30–48. https://doi.org/10.1016/j.ympev.2017.07.027.
Janssen, T., Karssen, G., Verhaeven, M., Coyne, D., & Bert, W. (2017). Mitochondrial coding genome analysis of tropical root-knot nematodes (Meloidogyne) supports haplotype based diagnostics and reveals evidence of recent reticulate evolution. Scientific Reports 6.
Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., Jones, M. G. K., Kikuchi, T., Manzanilla-Lopez, R., Palomares-Rius, J. E., Wesemael, W. M. L., & Perry, R. N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14, 946–961.
Kandel, S. L., Smiley, R. W., Garland-Campbell, K., Elling, A. A., Abatzoglou, J., Huggins, D., Rupp, R., & Paulitz, T. C. (2013). Relationship between climatic factors and distribution of Pratylenchus spp. in the dryland wheat-production areas of eastern Washington. Plant Disease, 97, 1448–1456.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.
Madani, M., Ward, L. J., & De Boer, S. H. (2011). Hsp90 gene, an additional target for discrimination between the potato cyst nematodes, Globodera rostochiensis and G. pallida, and the related species, G. tabacum tabacum. European Journal of Plant Pathology, 130, 271–285.
Mokrini, F., Waeyenberge, L., Viaene, N., Andaloussi, F. A., & Moens, M. (2013). Quantitative detection of the root-lesion nematode, Pratylenchus penetrans, using qPCR. European Journal of Plant Pathology, 137, 403–413.
Mokrini, F., Waeyenberge, L., Viaene, N., Andaloussi, F. A., & Moens, M. (2016). Diversity of root-lesion nematodes (Pratylenchus spp.) associated with wheat (Triticum aestivum and T. durum) in Morocco. Nematology, 18, 781–801.
Nunn, G. B. (1992). Nematode molecular evolution. Ph.D. thesis. In University of Nottingham. UK: Nottingham.
Palomares-Rius, J. E., Guesmi, I., Horrigue-Raouani, N., Cantalapiedra-Navarrete, C., Liébanas, G., & Castillo, P. (2014). Morphological and molecular characterisation of Pratylenchus oleae n. sp. (Nematoda: Pratylenchidae) parasitizing wild and cultivated olives in Spain and Tunisia. European Journal of Plant Pathology, 140, 53–67.
Skantar, A. M., & Carta, L. K. (2004). Molecular characterization and phylogenetic evaluation of the hsp90 gene from selected nematodes. Journal of Nematology, 36, 466–480.
Subbotin, S. A., Vierstraete, A., De Ley, P., Rowe, J., Waeyenberge, L., Moens, M., & Vanfleteren, J. R. (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.
Subbotin, S. A., Ragsdale, E. J., Mullens, T., Roberts, P. A., Mundo-Ocampo, M., & Baldwin, J. G. (2008). A phylogenetic framework for root-lesion nematodes of the genus Pratylenchus (Nematoda): Evidence from 18S and D2–D3 expansion segments of 28S ribosomal RNA genes and morphological characters. Molecular Phylogenetics and Evolution, 48, 491–505.
Tirchi, N., Troccoli, A., Fanelli, E., Mokabli, A., Mouhouche, F., & De Luca, F. (2016). Morphological and molecular identification of potato and cereal cyst nematode isolates from Algeria and their phylogenetic relationships with other populations from distant geographical areas. European Journal of Plant Pathology, 146, 861–880.
Troccoli, A., Lamberti, F., & Greco, N. (1992). Pratylenchus species occurring in Algeria (Nematoda, Pratylenchidae). Nematologia Mediterranea, 20, 97–103.
Troccoli, A., Subbotin, S. A., Chitambar, J. J., Janssen, T., Waeyenberge, L., Stanley, J. D., Duncan, L. W., Agudelo, P., Uribe, G. E. M., Franco, J., & Inserra, R. N. (2016). Characterisation of amphimictic and parthenogenetic populations of Pratylenchus bolivianus Corbett, 1983 (Nematoda: Pratylenchidae) and their phylogenetic relationships with closely related species. Nematology, 18, 651–678.
Zasada, I., Peetz, A., & Forge, T. (2017). Pratylenchus species associated with blueberry (Vacciniums spp.) and weed species in the North-west of North America. Canadian Journal of Plant Pathology, 39, 497–502.
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This research was partially supported by a grant 219262 ArimNET-ERANET FP7 2012-2016 Project PESTOLIVE “ Contribution of olive history for the management of soilborne parasites in the Mediterranean basin”.
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Fanelli, E., Troccoli, A., Capriglia, F. et al. Sequence variation in ribosomal DNA and in the nuclear hsp90 gene of Pratylenchus penetrans (Nematoda: Pratylenchidae) populations and phylogenetic analysis. Eur J Plant Pathol 152, 355–365 (2018). https://doi.org/10.1007/s10658-018-1480-1
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DOI: https://doi.org/10.1007/s10658-018-1480-1