1932

Abstract

Within the species-rich and trophically diverse phylum Nematoda, at least four independent major lineages of plant parasites have evolved, and in at least one of these major lineages plant parasitism arose independently multiple times. Ribosomal DNA data, sequence information from nematode-produced, plant cell wall–modifying enzymes, and the morphology and origin of the style(t), a protrusible piercing device used to penetrate the plant cell wall, all suggest that facultative and obligate plant parasites originate from fungivorous ancestors. Data on the nature and diversification of plant cell wall–modifying enzymes point at multiple horizontal gene transfer events from soil bacteria to bacterivorous nematodes resulting in several distinct lineages of fungal or oomycete-feeding nematodes. Ribosomal DNA frameworks with sequence data from more than 2,700 nematode taxa combined with detailed morphological information allow for explicit hypotheses on the origin of agronomically important plant parasites, such as root-knot, cyst, and lesion nematodes.

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2015-08-04
2024-04-21
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Literature Cited

  1. Aleshin VV, Kedrova OS, Milyutina IA, Vladychenskaya NS, Petrov NB. 1.  1998. Relationships among nematodes based on the analysis of 18S rRNA gene sequences: molecular evidence for monophyly of chromadorian and secernentian nematodes. Russ. J. Nematol. 6:175–84 [Google Scholar]
  2. Araki M. 2.  1992. Description of Meloidogyne ichinohei n. sp. (Nematoda: Meloigynidae) from Iris laevigata in Japan. Jpn. J. Nematol. 22:11–19 [Google Scholar]
  3. Baldwin JG, Nadler SA, Adams BJ. 3.  2004. Evolution of plant parasitism among nematodes. Annu. Rev. Phytopathol. 42:83–105 [Google Scholar]
  4. Barker KR, Darling HM. 4.  1965. Reproduction of Aphelenchus avenae on plant tissue in culture. Nematologica 11:162–66 [Google Scholar]
  5. Baujard P. 5.  1989. Remarques sur les genres des sous-familles Bursaphelenchina Paramonov, 1964 et Rhadinaphelenchinae, Paramonov, 1964 (Nematoda: Aphelenchoididae). Rev. Nématol. 12:323–24 [Google Scholar]
  6. Bert W, Claeys M, Borgonie G. 6.  2006. The comparative cellular architecture of the female gonoduct among Tylenchoidea (Nematoda: Tylenchina). J. Nematol. 38:362–75 [Google Scholar]
  7. Bert W, Karssen G, Helder J. 7.  2011. Phylogeny and evolution of nematodes. Genomics and Molecular Genetics of Plant Nematode Interactions J Jones, G Gheysen, C Fenoll 45–59 Dordrecht, the Neth.: Springer [Google Scholar]
  8. Bert W, Leliaert F, Vierstraete AR, Vanfleteren JR, Borgonie G. 8.  2008. Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda: Rhabditida). Mol. Phylogenet. Evol. 48:728–44 [Google Scholar]
  9. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P. 9.  et al. 1998. A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75 [Google Scholar]
  10. Blome D. 10.  2002. Five new genera of free-living marine nematodes from sandy beaches of eastern Australia. Mem. Qld. Mus. 48:29–43 [Google Scholar]
  11. Braasch H, Burgermeister W, Gu J. 11.  2009. Revised intra-generic grouping of Bursaphelenchus Fuchs, 1937 (Nematoda: Aphelenchoididae). J. Nematode Morphol. Syst. 12:65–88 [Google Scholar]
  12. Cheng HR, Lin MS, Li WQ. 12.  1983. The occurrence of a pine wilting disease caused by a nematode found in Nanjing. For. Pest Dis. 4:1–5 [Google Scholar]
  13. Chin DA, Estey RH. 13.  1966. Studies on the pathogenicity of Aphelenchus avenae Bastian, 1865. Phytoprotection 47:66–72 [Google Scholar]
  14. Clark WC. 14.  1961. A revised classification of the order Enoplida. N. Z. J. Sci. 4:123–50 [Google Scholar]
  15. Corbett DCM. 15.  1983. Three new species of Pratylenchus with a redescription of P. andinus Lordello, Zamith & Boock, 1961 (Nematoda: Pratylenchidae). Nematologica 29:390–403 [Google Scholar]
  16. Danchin EGJ, Rosso MN, Vieira P, De Almeida-Engler J, Coutinho PM. 16.  et al. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. USA 107:17651–56 [Google Scholar]
  17. DeBoy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H. 17.  et al. 2008. Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J. Bacteriol. 190:5455–63 [Google Scholar]
  18. Decraemer W, Hunt DJ. 18.  2006. Structure and classification. Plant Nematology RN Perry, M Moens 3–32 Wallingford, UK: CABI [Google Scholar]
  19. De Ley IT, De Ley P, Vierstraete A, Karssen G, Moens M, Vanfleteren J. 19.  2002. Phylogenetic analyses of Meloidogyne small subunit rDNA. J. Nematol. 34:319–27 [Google Scholar]
  20. Doolittle WF. 20.  1998. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14:307–11 [Google Scholar]
  21. Duarte IM, De Almeida MTM, Brown DJF, Marques I, Neilson R, Decraemer W. 21.  2010. Phylogenetic relationships, based on SSU rDNA sequences, among the didelphic genera of the family Trichodoridae from Portugal. Nematology 12:171–80 [Google Scholar]
  22. Eisenback JD, Dodge DJ. 22.  2012. Description of a unique, complex feeding socket caused by the putative primitive root-knot nematode, Meloidogyne kikuyensis. J. Nematol. 44:148–52 [Google Scholar]
  23. Eisenback JD, Hirschmann-Triantaphyllou H. 23.  1991. Root-knot nematodes: Meloidogyne species and races. Manual of Agricultural Nematology WR Nickle 191–274 New York: Marcel Dekker [Google Scholar]
  24. Fu Z, Agudelo P, Wells CE. 24.  2012. Differential expression of a β-1,4-endoglucanase induced by diet change in the foliar nematode Aphelenchoides fragariae. Phytopathology 102:804–11 [Google Scholar]
  25. Fukushige H. 25.  1991. Propagation of Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) on fungi growing in pine-shoot segments. Appl. Entomol. Zool. 26:371–76 [Google Scholar]
  26. Geraert E. 26.  1997. Comparison of the head patterns in the Tylenchoidea (Nematoda). Nematologica 43:283–94 [Google Scholar]
  27. Giblin-Davis RM, Gerber K, Griffith R. 27.  1989. In vivo and in vitro culture of the red ring nematode, Rhadinaphelenchus cocophilus. Nematropica 19:135–42 [Google Scholar]
  28. Giblin-Davis RM, Kanzaki N, Ye W, Mundo-Ocampo M, Baldwin JG, Thomas WK. 28.  2006. Morphology and description of Bursaphelenchus platzeri n. sp. (Nematoda: Parasitaphelenchidae), an associate of nitidulid beetles. J. Nematol. 38:150–57 [Google Scholar]
  29. Grootaert P, Coomans A. 29.  1980. The formation of the anterior feeding apparatus in dorylaims. Nematologica 26:406–31 [Google Scholar]
  30. Haegeman A, Jacob J, Vanholme B, Kyndt T, Gheysen G. 30.  2008. A family of GHF5 endo-1,4-beta-glucanases in the migratory plant-parasitic nematode Radopholus similis. Plant Pathol. 57:581–90 [Google Scholar]
  31. Haegeman A, Mantelin S, Jones JT, Gheysen G. 31.  2012. Functional roles of effectors of plant-parasitic nematodes. Gene 492:19–31 [Google Scholar]
  32. Holterman M, Karssen G, van den Elsen S, Van Megen H, Bakker J, Helder J. 32.  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 99:227–35 [Google Scholar]
  33. Holterman M, Rybarczyk K, van den Elsen S, Van Megen H, Mooyman P. 33.  et al. 2008. A ribosomal DNA-based framework for the detection and quantification of stress-sensitive nematode families in terrestrial habitats. Mol. Ecol. Resour. 8:23–34 [Google Scholar]
  34. Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T. 34.  et al. 2006. Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol. Biol. Evol. 23:1792–800 [Google Scholar]
  35. Hope WD, Tchesunov AV. 35.  1999. Smithsoninema inaequale n.g. and n.sp. (Nematoda, Leptolaimidae) inhabiting the test of a foraminiferan. Invert. Biol. 118:95–108 [Google Scholar]
  36. Hugall A, Stanton J, Moritz C. 36.  1999. Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Mol. Biol. Evol. 16:157–64 [Google Scholar]
  37. Hunt DJ. 37.  1993. Aphelenchida, Longidoridae and Trichodoridae: Their Systematics and Bionomics Wallingford, UK: CABI352
  38. Jaubert S, Laffaire JB, Abad P, Rosso MN. 38.  2002. A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 522:109–12 [Google Scholar]
  39. Jochmann R, Schmidt-Rhaesa A. 39.  2007. New ultrastructural data from the larva of Paragordius varius (Nematomorpha). Acta Zool. 88:137–44 [Google Scholar]
  40. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J. 40.  et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14:946–61 [Google Scholar]
  41. Kanzaki N, Giblin-Davis RM, Herre EA, Scheffrahn RH, Center BJ. 41.  2010. Pseudaphelenchus vindai n. sp. (Tylenchomorpha: Aphelenchoididae) associated with termites (Termitidae) in Barro Colorado Island, Panama. Nematology 12:905–14 [Google Scholar]
  42. Karim N, Jones JT, Okada H, Kikuchi T. 42.  2009. Analysis of expressed sequence tags and identification of genes encoding cell-wall-degrading enzymes from the fungivorous nematode Aphelenchus avenae. BMC Genomics 10:525 [Google Scholar]
  43. Keen NT, Roberts PA. 43.  1998. Plant parasitic nematodes: digesting a page from the microbe book. Proc. Natl. Acad. Sci. USA 95:4789–90 [Google Scholar]
  44. Kiewnick S, Holterman M, van den Elsen S, van Megen H, Frey JE, Helder J. 44.  2014. Comparison of two short DNA barcoding loci (COI and COII) and two longer ribosomal DNA genes (SSU and LSU rRNA) for specimen identification among quarantine root-knot nematodes (Meloidogyne spp.) and their close relatives. Eur. J. Plant Pathol. 140:97–110 [Google Scholar]
  45. Kikuchi T, Cock PJA, Helder J, Jones JT. 45.  2014. Characterisation of the transcriptome of Aphelenchoides besseyi and identification of a GHF 45 cellulase. Nematology 16:99–107 [Google Scholar]
  46. Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N. 46.  et al. 2011. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLOS Pathog. 7:e1002219 [Google Scholar]
  47. Kyndt T, Haegeman A, Gheysen G. 47.  2008. Evolution of GHF5 endoglucanase gene structure in plant-parasitic nematodes: no evidence for an early domain shuffling event. BMC Evol. Biol. 8:305 [Google Scholar]
  48. Lamberti F, Molinari S, Moens M, Brown DJF. 48.  2000. The Xiphinema americanum group. I. Putative species, their geographical occurrence and distribution, and regional polytomous identification keys for the group. Russ. J. Nematol. 8:65–84 [Google Scholar]
  49. Luc M. 49.  1987. A reappraisal of Tylenchina (Nemata). 7. The family Pratylenchidae Thorne, 1949. Rev. Nematol. 10:203–18 [Google Scholar]
  50. Luc M, Fortuner R, Raski DJ, Geraert E. 50.  1987. A reappraisal of Tylenchina (Nemata). 1. For a new approach to the taxonomy of Tylenchina. Rev. Nematol. 10:127–34 [Google Scholar]
  51. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. 51.  2014. The complex hybrid origins of the root-knot nematodes revealed through comparative genomics. PeerJ 2:e356 [Google Scholar]
  52. Maggenti AR. 52.  1971. Nemic relationships and the origin of plant parasitic nematodes. Plant Parasitic Nematodes BM Zuckerman, WF Mai, RA Rohde 65–81 New York: Academic [Google Scholar]
  53. Meldal BHM, Debenham NJ, De Ley P, De Ley IT, Vanfleteren J. 53.  et al. 2007. An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol. Phylogenet. Evol. 42:622–36 [Google Scholar]
  54. Múnera GE, Bert W, Decraemer W. 54.  2009. Morphological and molecular characterisation of Pratylenchus araucensis n. sp. (Pratylenchidae), a root-lesion nematode associated with Musa plants in Colombia. Nematology 11:799–813 [Google Scholar]
  55. Othman AA, Baldwin JG, Mundo-Ocampo M. 55.  1988. Comparative morphology of Globodera, Cactodera and Punctodera spp. (Heteroderidae) with scanning electron microscopy. Rev. Nématol. 11:53–63 [Google Scholar]
  56. Plantard O, Valette S, Gross MF. 56.  2007. The root-knot nematode producing galls on Spartina alterniflora belongs to the genus Meloidogyne: rejection of Hypsoperine and Spartonema spp. J. Nematol. 39:127–32 [Google Scholar]
  57. Popeijus H, Overmars H, Jones J, Blok V, Goverse A. 57.  et al. 2000. Enzymology: degradation of plant cell walls by a nematode. Nature 406:36–37 [Google Scholar]
  58. Qin L, Kudla U, Roze EHA, Goverse A, Popeijust H. 58.  et al. 2004. A nematode expansin acting on plants. Nature 427:30 [Google Scholar]
  59. Ragsdale EJ, Ngo PT, Crum J, Ellisman MH, Baldwin JG. 59.  2009. Comparative, three-dimensional anterior sensory reconstruction of Aphelenchus avenae (Nematoda: Tylenchomorpha). J. Comp. Neurol. 517:616–32 [Google Scholar]
  60. Rota-Stabelli O, Daley AC, Pisani D. 60.  2013. Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr. Biol. 23:392–98 [Google Scholar]
  61. Rybarczyk-Mydłowska K, Mooyman P, Van Megen H, van den Elsen S, Vervoort MTW. 61.  et al. 2012. Small subunit ribosomal DNA-based phylogenetic analysis of foliar nematodes (Aphelenchoides spp.) and their quantitative detection in complex DNA backgrounds. Phytopathology 102:1153–60 [Google Scholar]
  62. Rybarczyk-Mydłowska K, Ruvimbo Maboreke H, Van Megen H, van den Elsen S, Mooyman P. 62.  et al. 2012. Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes. BMC Evol. Biol. 12:221 [Google Scholar]
  63. Schmidt-Rhaesa A. 63.  1996. The nervous system of Nectonema munidae and Gordius aquaticus, with implications for the ground pattern of the Nematomorpha. Zoomorphology 116:133–42 [Google Scholar]
  64. Siddiqi MR. 64.  1980. On the generic status of Atlantadorus Siddiqi, 1974 and Nanidorus Siddiqi, 1974 (Nematoda: Trichodoridae). Syst. Parasitol. 1:151–52 [Google Scholar]
  65. Siddiqi MR. 65.  1980. The origin and phylogeny of the nematode orders Tylenchida Thorne, 1949 and Aphelenchida N. Ord. Helminthol. Abstracts Ser. B 49:143–70 [Google Scholar]
  66. Siddiqi MR. 66.  1983. Evolution of plant parasitism in nematodes. Concepts in Nematode Systematics AR Stone, HM Platt, LF Khalil 22113–29 London: Academic [Google Scholar]
  67. Siddiqi MR. 67.  2000. Tylenchida: Parasites of Plants and Insects Wallingford, UK: CABI833
  68. Smant G, Stokkermans J, Yan YT, de Boer JM, Baum TJ. 68.  et al. 1998. Endogenous cellulases in animals: isolation of beta-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. USA 95:4906–11 [Google Scholar]
  69. Stamatakis A. 69.  2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–90 [Google Scholar]
  70. Sturhan D. 70.  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). J. Nematode Morphol. Syst. 15:127–47 [Google Scholar]
  71. Subbotin SA, Ragsdale EJ, Mullens T, Roberts PA, Mundo-Ocampo M, Baldwin JG. 71.  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. Mol. Phylogenet. Evol. 48:491–505 [Google Scholar]
  72. Subbotin SA, Sturhan D, Chizhov VN, Vovlas N, Baldwin JG. 72.  2006. Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology 8:455–74 [Google Scholar]
  73. Tzortzakakis EA, Archidona-Yuste A, Cantalapiedra-Navarrete C, Nasiou E, Lazanaki MS. 73.  et al. 2014. Integrative diagnosis and molecular phylogeny of dagger and needle nematodes of olives and grapevines in the island of Crete, Greece, with description of Xiphinema cretense n. sp. (Nematoda, Longidoridae). Eur. J. Plant Pathol. 140:563–90 [Google Scholar]
  74. Valadas V, Laranjo M, Mota M, Oliveira S. 74.  2013. Molecular characterization of Portuguese populations of the pinewood nematode Bursaphelenchus xylophilus using cytochrome b and cellulase genes. J. Helminthol. 87:457–66 [Google Scholar]
  75. Van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P. 75.  et al. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–50 [Google Scholar]
  76. Wang F, Li D, Wang Z, Dong A, Liu L. 76.  et al. 2014. Transcriptomic analysis of the rice white tip nematode, Aphelenchoides besseyi (Nematoda: Aphelenchoididae). PLOS ONE 9:e91591 [Google Scholar]
  77. Yan YT, Smant G, Stokkermans J, Qin L, Helder J. 77.  et al. 1998. Genomic organization of four beta-1,4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications. Gene 220:61–70 [Google Scholar]
  78. Zasada IA, Peetz A, Howe DK, Wilhelm LJ, Cheam D. 78.  et al. 2014. Using mitogenomic and nuclear ribosomal sequence data to investigate the phylogeny of the Xiphinema americanum species complex. PLOS ONE 9:e90035 [Google Scholar]
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