Morphological and molecular analyses of a Meloidogyne mali population with high intragenomic rRNA polymorphism

Ahmed, M., van de Vossenberg, B., Cornelisse, C. and Karssen, G. 2013. On the species status of the root–knot nematode Meloidogyne ulmi Palmisano and Ambrogioni, 2000 (Nematoda, Meloidogynidae). ZooKeys 362:1–27, doi: 10.3897/zookeys.362.6352. Ahmed M. van de Vossenberg B. Cornelisse C. and Karssen G. 2013 . On the species status of the root–knot nematode Meloidogyne ulmi Palmisano and Ambrogioni, 2000 (Nematoda, Meloidogynidae) . ZooKeys 362 : 1 – 27 , doi: 10.3897/zookeys.362.6352 . 386710424363598 Open DOISearch in Google Scholar

Álvarez-Ortega, S., Brito, J. A. and Subbotin, S. A. 2019. Multigene phylogeny of root-knot nematodes and molecular characterization of Meloidogyne nataliei Golden, Rose & Bird, 1981 (Nematoda: Tylenchida). Scientific Reports 9:11788, doi: 10.1038/s41598-019-48195-0. Álvarez-Ortega S. Brito J. A. and Subbotin S. A. 2019 . Multigene phylogeny of root-knot nematodes and molecular characterization of Meloidogyne nataliei Golden, Rose & Bird, 1981 (Nematoda: Tylenchida) . Scientific Reports 9 : 11788 , doi: 10.1038/s41598-019-48195-0 . 10.1038/s41598-019-48195-0669236431409860 Search in Google Scholar

Bert, W., Leliaert, F., Vierstraete, A. R., Vanfleteren, J. R. and Borgonie, G. 2008. Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda: Rhabditida). Molecular Phylogenetics and Evolution 48:728–744, doi: 10.1016/j.ympev.2008.04.011. Bert W. Leliaert F. Vierstraete A. R. Vanfleteren J. R. and Borgonie G. 2008 . Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda: Rhabditida) . Molecular Phylogenetics and Evolution 48 : 728 – 744 , doi: 10.1016/j.ympev.2008.04.011 . 18502668 Open DOISearch in Google Scholar

Cherry, T., Szalanski, A. L., Todd, T. C. and Powers, T. O. 1997. The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae). Journal of Nematology 29:23–29. Cherry T. Szalanski A. L. Todd T. C. and Powers T. O. 1997 . The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae) . Journal of Nematology 29 : 23 – 29 . Search in Google Scholar

Darriba, D., Taboada, G. L., Doallo, R. and Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772, doi: 10.1038/nmeth.2109. Darriba D. Taboada G. L. Doallo R. and Posada D. 2012 . jModelTest 2: more models, new heuristics and parallel computing . Nature Methods 9 : 772 , doi: 10.1038/nmeth.2109 . 459475622847109 Open DOISearch in Google Scholar

De Ley, P., Félix, M. A., Frisse, L. M., Nadler, S. A., Sternberg, P. W. and Thomas, W. K. 1999. Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology 1:591–612, doi: 10.1163/156854199508559. De Ley P. Félix M. A. Frisse L. M. Nadler S. A. Sternberg P. W. and Thomas W. K. 1999 . Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae) . Nematology 1 : 591 – 612 , doi: 10.1163/156854199508559 . Open DOISearch in Google Scholar

DeRycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J. Vincx, M. and Moens, T. 2005. Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Marine Ecology Progress Series 300:91–103, doi: 10.3354/meps300091. DeRycke S. Remerie T. Vierstraete A. Backeljau T. Vanfleteren J. Vincx M. and Moens T. 2005 . Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina . Marine Ecology Progress Series 300 : 91 – 103 , doi: 10.3354/meps300091 . Open DOISearch in Google Scholar

Eisenback, J. D., Graney, L. S. and Vieira, P. 2016. First report of the apple root-knot nematode (Meloidogyne mali) in North America, found parasitizing euonymus in New York. Plant Disease 101:510, doi: 10.1094/PDIS-06-16-0894-PDN. Eisenback J. D. Graney L. S. and Vieira P. 2016 . First report of the apple root-knot nematode (Meloidogyne mali) in North America, found parasitizing euonymus in New York . Plant Disease 101 : 510 , doi: 10.1094/PDIS-06-16-0894-PDN . Open DOISearch in Google Scholar

Georgi, L. L. and Abbott, G. A. 1998. Variation in ribosomal genes in Meloidogyne arenaria. Fundamental and Applied Nematology 21:685–694, doi: 10.1159/000021665. Georgi L. L. and Abbott G. A. 1998 . Variation in ribosomal genes in Meloidogyne arenaria . Fundamental and Applied Nematology 21 : 685 – 694 , doi: 10.1159/000021665 . 9885350 Open DOISearch in Google Scholar

Griffiths, B. S., Donn, S., Neilson, R. and Daniell, T. J. 2006. Molecular sequencing and morphological analysis of a nematode community. Applied Soil Ecology 32:325–337, doi: 10.1016/j.apsoil.2005.07.006. Griffiths B. S. Donn S. Neilson R. and Daniell T. J. 2006 . Molecular sequencing and morphological analysis of a nematode community . Applied Soil Ecology 32 : 325 – 337 , doi: 10.1016/j.apsoil.2005.07.006 . Open DOISearch in Google Scholar

Gu, J. and He, J. 2015. First report of the apple root-knot nematode, Meloidogyne mali, infecting crape myrtle from Japan. Plant Disease 99:893, doi: 10.1094/PDIS-11-14-1145-PDN. Gu J. and He J. 2015 . First report of the apple root-knot nematode, Meloidogyne mali, infecting crape myrtle from Japan . Plant Disease 99 : 893 , doi: 10.1094/PDIS-11-14-1145-PDN . Open DOISearch in Google Scholar

Gu, J., Wang, J., Shao, F., Gao, F. and Ge, J. 2013. Identification of Meloidogyne mali detected in Acer palmatum from japan. Plant Quarantine 27:43–49, doi: CNKI:SUN:ZWJY.0.2013-01-014. Gu J. Wang J. Shao F. Gao F. and Ge J. 2013 . Identification of Meloidogyne mali detected in Acer palmatum from japan . Plant Quarantine 27 : 43 – 49 , doi: CNKI:SUN:ZWJY.0.2013-01-014. Search in Google Scholar

Hartman, K. M. and Sasser, J. N. 1985. “Identification of Meloidogyne species on the basis of differential host test and perineal-pattern morphology”, In Barker, K. R., Carter, C. C. and Sasser, J. N. (Eds), An Advanced Treatise on Meloidogyne, Vol. II methodology North Carolina University Graphics, North Carolina. Hartman K. M. and Sasser J. N. 1985 . “ Identification of Meloidogyne species on the basis of differential host test and perineal-pattern morphology ”, In Barker K. R. Carter C. C. and Sasser J. N. (Eds), An Advanced Treatise on Meloidogyne, Vol. II methodology North Carolina University Graphics , North Carolina . Search in Google Scholar

Holterman, M., van der Wurff, A., van den Elsen, S., van Megen, H., Bongers, T., Holovachov, O., Bakker, J. and 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 23:1792–1800, doi: 10.1093/molbev/msl044Itoh. Holterman M. van der Wurff A. van den Elsen S. van Megen H. Bongers T. Holovachov O. Bakker J. and 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 : 1792 – 1800 , doi: 10.1093/molbev/msl044Itoh . Open DOISearch in Google Scholar

Janssen, T., Karssen, G., Topalović, O., Coyne, D. and Bert, W. 2017. Integrative taxonomy of root-knot nematodes reveals multiple independent origins of mitotic parthenogenesis. PLoS ONE 12:e0172190, doi: 10.1371/journal.pone.0172190. Janssen T. Karssen G. Topalović O. Coyne D. and Bert W. 2017 . Integrative taxonomy of root-knot nematodes reveals multiple independent origins of mitotic parthenogenesis . PLoS ONE 12 : e0172190 , doi: 10.1371/journal.pone.0172190 . Open DOISearch in Google Scholar

Karssen, G., van Keulen, I., van Hoenselaar, T. and van Heese, E. 2008. Meloidogyne ulmi: een nieuwe iepen parasiet in Nederland?. Boomzorg 1:62–63. Karssen G. van Keulen I. van Hoenselaar T. and van Heese E. 2008 . Meloidogyne ulmi: een nieuwe iepen parasiet in Nederland? . Boomzorg 1 : 62 – 63 . Search in Google Scholar

Katoh, K. and Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772–780, doi: 10.1093/molbev/mst010. Katoh K. and Standley D. M. 2013 . MAFFT multiple sequence alignment software version 7: improvements in performance and usability . Molecular Biology and Evolution 30 : 772 – 780 , doi: 10.1093/molbev/mst010 . Open DOISearch in Google Scholar

Li, S. and Yu, Z. 1991. Investigation on plant root-knot nematodes and pathogen identification of Henan. Journal of Henan Agricultural University 25:169–174, doi: 10.16445/j.cnki.1000-2340.1991.02.008. Li S. and Yu Z. 1991 . Investigation on plant root-knot nematodes and pathogen identification of Henan . Journal of Henan Agricultural University 25 : 169 – 174 , doi: 10.16445/j.cnki.1000-2340.1991.02.008 . Open DOISearch in Google Scholar

Li, H., Trinh, P. Q., Waeyenberge, L. and Moens, M. 2008. Bursaphelenchus chengi sp. n. (Nematoda: Parasitaphelenchidae) isolated at Nanjing, China, in packaging wood from Taiwan. Nematology 10:335–346, doi: 10.1163/156854108783900294. Li H. Trinh P. Q. Waeyenberge L. and Moens M. 2008 . Bursaphelenchus chengi sp. n. (Nematoda: Parasitaphelenchidae) isolated at Nanjing, China, in packaging wood from Taiwan . Nematology 10 : 335 – 346 , doi: 10.1163/156854108783900294 . Open DOISearch in Google Scholar

Lunt, D. H. 2008. Genetic tests of ancient asexuality in root knot nematodes reveal recent hybrid origins. BMC Evolutionary Biology 8:194–, doi: 10.1186/1471-2148-8-194. Lunt D. H. 2008 . Genetic tests of ancient asexuality in root knot nematodes reveal recent hybrid origins . BMC Evolutionary Biology 8 : 194 –, doi: 10.1186/1471-2148-8-194 . Open DOISearch in Google Scholar

Miller, M., Pfeiffer, W. and Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE), doi: 10.1109/GCE.2010.5676129. Miller M. Pfeiffer W. and Schwartz T. 2010 . Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE) , doi: 10.1109/GCE.2010.5676129 . Open DOISearch in Google Scholar

Nadler, S. A., Carreno, R. A., Adams, B. J., Kinde, H., Baldwin, J. G. and Mundo-Ocampo, M. 2003. Molecular phylogenetics and diagnosis of soil and clinical isolates of Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea), an opportunistic pathogen of horses. International Journal for Parasitology 33:1115–1125, doi: 10.1016/S0020-7519(03)00134-6. Nadler S. A. Carreno R. A. Adams B. J. Kinde H. Baldwin J. G. and Mundo-Ocampo M. 2003 . Molecular phylogenetics and diagnosis of soil and clinical isolates of Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea), an opportunistic pathogen of horses . International Journal for Parasitology 33 : 1115 – 1125 , doi: 10.1016/S0020-7519(03)00134-6 . Open DOISearch in Google Scholar

Ohshima, Y. and Ichinohe, M. 1969. A root-knot nematode, Meloidogyne mali n. sp. on apple-tree from Japan (Tylenchida: Heteroderidae). Applied Entomology and Zoology 4:194–202, doi: 10.1303/aez.4.194. Ohshima Y. and Ichinohe M. 1969 . A root-knot nematode, Meloidogyne mali n. sp. on apple-tree from Japan (Tylenchida: Heteroderidae) . Applied Entomology and Zoology 4 : 194 – 202 , doi: 10.1303/aez.4.194 . Open DOISearch in Google Scholar

Palmisano, A. and Ambrogioni, L. 2000. Meloidogyne ulmi sp. n., a root-knot nematode from elm. Nematologia Mediterranea 28:279–293. Palmisano A. and Ambrogioni L. 2000 . Meloidogyne ulmi sp. n., a root-knot nematode from elm . Nematologia Mediterranea 28 : 279 – 293 . Search in Google Scholar

Pereira, T. J. and Baldwin, J. G. 2016. Contrasting evolutionary patterns of 28S and ITS rRNA genes reveal high intragenomic variation in Cephalenchus (Nematoda): implications for species delimitation. Molecular Phylogenetics Evolution 98:244–260, doi: 10.1016/j.ympev.2016.02.016. Pereira T. J. and Baldwin J. G. 2016 . Contrasting evolutionary patterns of 28S and ITS rRNA genes reveal high intragenomic variation in Cephalenchus (Nematoda): implications for species delimitation . Molecular Phylogenetics Evolution 98 : 244 – 260 , doi: 10.1016/j.ympev.2016.02.016 . 26926945 Open DOISearch in Google Scholar

Prior, T., Tozer, H., Yale, R., Jones, E., Lawson, R., Jutson, L., Correia, M., Stubbs, J., Hockland, S. and Karssen, G. 2019. First report of Meloidogyne mali causing root galling to elm trees in the UK. New Disease Reports 39:10, doi: 10.5197/j.2044-0588.2019.039.010. Prior T. Tozer H. Yale R. Jones E. Lawson R. Jutson L. Correia M. Stubbs J. Hockland S. and Karssen G. 2019 . First report of Meloidogyne mali causing root galling to elm trees in the UK . New Disease Reports 39 : 10 , doi: 10.5197/j.2044-0588.2019.039.010 . Open DOISearch in Google Scholar

Qing, X., Wang, M., Karssen, G., Bucki, P., Bert, W. and Braun-Miyara, S. 2020a. PPNID: a reference database and molecular identification pipeline for plant-parasitic nematodes. Bioinformatics 36:1052–1056, doi: 10.1093/bioinformatics/btz707. Qing X. Wang M. Karssen G. Bucki P. Bert W. and Braun-Miyara S. 2020a . PPNID: a reference database and molecular identification pipeline for plant-parasitic nematodes . Bioinformatics 36 : 1052 – 1056 , doi: 10.1093/bioinformatics/btz707 . 31529041 Open DOISearch in Google Scholar

Qing, X., Bik, H., Yergaliyev, T. M., Gu, J., Fonderie, P., Brown-Miyara, S., Szitenberg, A. and Bert, W. 2020b. Widespread prevalence but contrasting patterns of intragenomic rRNA polymorphisms in nematodes: Implications for phylogeny, species delimitation and life history inference. Molecular Ecology Resources 20:318–332, doi: 10.1111/1755-0998.13118. Qing X. Bik H. Yergaliyev T. M. Gu J. Fonderie P. Brown-Miyara S. Szitenberg A. and Bert W. 2020b . Widespread prevalence but contrasting patterns of intragenomic rRNA polymorphisms in nematodes: Implications for phylogeny, species delimitation and life history inference . Molecular Ecology Resources 20 : 318 – 332 , doi: 10.1111/1755-0998.13118 . 31721426 Open DOISearch in Google Scholar

Ronquist, F. and Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574, doi: 10.1093/bioinformatics/btg180. Ronquist F. and Huelsenbeck J. P. 2003 . MrBayes 3: Bayesian phylogenetic inference under mixed models . Bioinformatics 19 : 1572 – 1574 , doi: 10.1093/bioinformatics/btg180 . 12912839 Open DOISearch in Google Scholar

Seinhorst, J. W. 1959. A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4:67–69, doi: 10.1163/187529259X00381. Seinhorst J. W. 1959 . A rapid method for the transfer of nematodes from fixative to anhydrous glycerin . Nematologica 4 : 67 – 69 , doi: 10.1163/187529259X00381 . Open DOISearch in Google Scholar

Stamatakis, A., Hoover, P. and Rougemont, J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57:758–771, doi: 10.1080/10635150802429642. Stamatakis A. Hoover P. and Rougemont J. 2008 . A rapid bootstrap algorithm for the RAxML web servers . Systematic Biology 57 : 758 – 771 , doi: 10.1080/10635150802429642 . 18853362 Open DOISearch in Google Scholar

Van Den Berg, E., Palomares-Rius, J. E., Vovlas, N., Tiedt, L. R., Castillo, P. and Subbotin, S. A. 2016. Morphological and molecular characterisation of one new and several known species of the reniform nematode, Rotylenchulus Linford & Oliveira, 1940 (Hoplolaimidae: Rotylenchulinae), and a phylogeny of the genus. Nematology 18:67–107, doi: 10.1163/15685411-00002945. Van Den Berg E. Palomares-Rius J. E. Vovlas N. Tiedt L. R. Castillo P. and Subbotin S. A. 2016 . Morphological and molecular characterisation of one new and several known species of the reniform nematode, Rotylenchulus Linford & Oliveira, 1940 (Hoplolaimidae: Rotylenchulinae), and a phylogeny of the genus . Nematology 18 : 67 – 107 , doi: 10.1163/15685411-00002945 . Open DOISearch in Google Scholar

Vrain, T. C. 1993. Restriction fragment length polymorphism separates species of the Xiphinema americanum group. Journal of Nematology 25:361–364, doi: 10.1006/jipa.1993.1100. Vrain T. C. 1993 . Restriction fragment length polymorphism separates species of the Xiphinema americanum group . Journal of Nematology 25 : 361 – 364 , doi: 10.1006/jipa.1993.1100 . Open DOISearch in Google Scholar

Ye, W., Giblin-Davis, R. M., Braasch, H., Morris, K. and Thomas, W. K. 2007. Phylogenetic relationships among Bursaphelenchus species (Nematoda: Parasitaphelenchidae) inferred from nuclear ribosomal and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 43:1185–1197, doi: 10.1016/j.ympev.2007.02.006. Ye W. Giblin-Davis R. M. Braasch H. Morris K. and Thomas W. K. 2007 . Phylogenetic relationships among Bursaphelenchus species (Nematoda: Parasitaphelenchidae) inferred from nuclear ribosomal and mitochondrial DNA sequence data . Molecular Phylogenetics and Evolution 43 : 1185 – 1197 , doi: 10.1016/j.ympev.2007.02.006 . 17433722 Open DOISearch in Google Scholar

Zhang, S. and Weng, Z. 1991. Identification of root-knot nematode species in Fujian. Journal of Fujian Agricultural University 20:159–164. Zhang S. and Weng Z. 1991 . Identification of root-knot nematode species in Fujian . Journal of Fujian Agricultural University 20 : 159 – 164 . Search in Google Scholar