1932

Abstract

Nematoda is a diverse phylum that is estimated to contain more than a million species. More than 4,100 of these species have the ability to parasitize plants and cause agricultural losses estimated at US $173 billion annually. This has led to considerable research into their biology to minimize crop losses via control methods. At the infancy of plant-parasitic nematode molecular biology, researchers compared nematode genomes, genes, and biological processes to the model nematode species , which is a free-living bacterial feeder This well-annotated and researched model nematode assisted the molecular biology research, e.g., with genome assemblies, of plant-parasitic nematodes. However, as research into these plant parasites progressed, the necessity of relying on the free-living relative as a reference has reduced. This is partly driven by revealing the considerable divergence between the two types of nematodes both genomically and anatomically, forcing comparisons to be redundant as well as the increased quality of molecular plant nematology proposing more suitable model organisms for this clade of nematode. The major irregularity between the two types of nematodes is the unique anatomical structure and effector repertoire that plant nematodes utilize to establish parasitism, which lacks, therefore reducing its value as a heterologous system to investigate parasitic processes. Despite this, remains useful for investigating conserved genes via its utility as an expression system because of the current inability to transform plant-parasitic nematodes. Unfortunately, owing to the expertise that this requires, it is not a common and/or accessible tool. Furthermore, we believe that the application of as an expression system for plant nematodes will be redundant once tools are established for stable reverse-genetics in these plant parasites. This will remove the restraints on molecular plant nematology and allow it to excel on par with the capabilities of research.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021622-113539
2024-09-09
2025-02-13
Loading full text...

Full text loading...

/deliver/fulltext/phyto/62/1/annurev-phyto-021622-113539.html?itemId=/content/journals/10.1146/annurev-phyto-021622-113539&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, et al. 2008.. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. . Nat. Biotechnol. 26::90915
    [Crossref] [Google Scholar]
  2. 2.
    Abad P, McCarter JP. 2011.. Genome analysis of plant parasitic nematodes. . In Genomics and Molecular Genetics of Plant-Nematode Interactions, ed. J Jones, G Gheysen, C Fenoll , pp. 10317. Dordrecht, Neth:.: Springer
    [Google Scholar]
  3. 3.
    Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, et al. 1997.. Evidence for a clade of nematodes, arthropods and other moulting animals. . Nature 387::48993
    [Crossref] [Google Scholar]
  4. 4.
    Ahmed M, Roberts NG, Adediran F, Smythe AB, Kocot KM, Holovachov O. 2022.. Phylogenomic analysis of the phylum Nematoda: conflicts and congruences with morphology, 18S rRNA, and mitogenomes. . Front. Ecol. Evol. 9::769565
    [Crossref] [Google Scholar]
  5. 5.
    Atkinson LE, Stevenson M, McCoy CJ, Marks NJ, Fleming C, et al. 2013.. flp-32 ligand/receptor silencing phenocopy faster plant pathogenic nematodes. . PLOS Pathog. 9::e1003169
    [Crossref] [Google Scholar]
  6. 6.
    Avery L, You YJ. 2012.. C. elegans feeding. . WormBook 2012::123
    [Google Scholar]
  7. 7.
    Barnes SN, Masonbrink RE, Maier TR, Seetharam A, Sindhu AS, et al. 2019.. Heterodera glycines utilizes promiscuous spliced leaders and demonstrates a unique preference for a species-specific spliced leader over C. elegans SL1. . Sci. Rep. 9::1356
    [Crossref] [Google Scholar]
  8. 8.
    Bell CA, Lilley CJ, McCarthy J, Atkinson HJ, Urwin PE. 2019.. Plant-parasitic nematodes respond to root exudate signals with host-specific gene expression patterns. . PLOS Pathog. 15::e1007503
    [Crossref] [Google Scholar]
  9. 9.
    Bird DM, Jones JT, Opperman CH, Kikuchi T, Danchin EG. 2015.. Signatures of adaptation to plant parasitism in nematode genomes. . Parasitology 142::S7184
    [Crossref] [Google Scholar]
  10. 10.
    Bird DM, Opperman CH. 1998.. Caenorhabditis elegans: a genetic guide to parasitic nematode biology. . J. Nematol. 30::299308
    [Google Scholar]
  11. 11.
    Bitar M, Boroni M, Macedo A, Machado CR, Franco G. 2013.. The spliced leader trans-splicing mechanism in different organisms: molecular details and possible biological roles. . Front. Genet. 4::199
    [Crossref] [Google Scholar]
  12. 12.
    Blanc-Mathieu R, Perfus-Barbeoch L, Aury JM, Da Rocha M, Gouzy J, et al. 2017.. Hybridization and polyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes. . PLOS Genet. 13::e1006777
    [Crossref] [Google Scholar]
  13. 13.
    Blaxter M, Koutsovoulos G. 2015.. The evolution of parasitism in Nematoda. . Parasitology 142:(Suppl. 1):S2639
    [Crossref] [Google Scholar]
  14. 14.
    Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. 1998.. A molecular evolutionary framework for the phylum Nematoda. . Nature 392::7175
    [Crossref] [Google Scholar]
  15. 15.
    Bürglin TR, Lobos E, Blaxter ML. 1998.. Caenorhabditis elegans as a model for parasitic nematodes. . Int. J. Parasitol. 28::395411
    [Crossref] [Google Scholar]
  16. 16.
    Burke M, Scholl EH, Bird DM, Schaff JE, Colman SD, et al. 2015.. The plant parasite Pratylenchus coffeae carries a minimal nematode genome. . Nematology 17::62137
    [Crossref] [Google Scholar]
  17. 17.
    Burns AR, Luciani GM, Musso G, Bagg R, Yeo M, et al. 2015.. Caenorhabditis elegans is a useful model for anthelmintic discovery. . Nat. Commun. 6::7485
    [Crossref] [Google Scholar]
  18. 18.
    C. elegans Seq. Consort. 1998.. Genome sequence of the nematode C. elegans: a platform for investigating biology. . Science 282::201218
    [Crossref] [Google Scholar]
  19. 19.
    Calahorro F, Chapman M, Dudkiewicz K, Holden-Dye L, O'Connor V. 2022.. PharmacoGenetic targeting of a C. elegans essential neuron provides an in vivo screening for novel modulators of nematode ion channel function. Pestic. . Biochem. Physiol. 186::105152
    [Google Scholar]
  20. 20.
    Costa JC, Lilley CJ, Atkinson HJ, Urwin PE. 2009.. Functional characterisation of a cyst nematode acetylcholinesterase gene using Caenorhabditis elegans as a heterologous system. . Int. J. Parasitol. 39::84958
    [Crossref] [Google Scholar]
  21. 21.
    Costa JC, Lilley CJ, Urwin PE. 2007.. Caenorhabditis elegans as a model for plant-parasitic nematodes. . Nematology 9::316
    [Crossref] [Google Scholar]
  22. 22.
    Cotton JA, Lilley CJ, Jones LM, Kikuchi T, Reid AJ, et al. 2014.. The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. . Genome Biol. 15::R43
    [Crossref] [Google Scholar]
  23. 23.
    Crisford A, Calahorro F, Ludlow E, Marvin JMC, Hibbard JK, et al. 2020.. Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection. . PLOS Pathog. 16::e1008884
    [Crossref] [Google Scholar]
  24. 24.
    Crook M. 2014.. The dauer hypothesis and the evolution of parasitism: 20 years on and still going strong. . Int. J. Parasitol. 44::18
    [Crossref] [Google Scholar]
  25. 25.
    Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM, et al. 2010.. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. . PNAS 107::1765156
    [Crossref] [Google Scholar]
  26. 26.
    Dayi M, Sun S, Maeda Y, Tanaka R, Yoshida A, et al. 2020.. Nearly complete genome assembly of the pinewood nematode Bursaphelenchus xylophilus strain Ka4C1. . Microbiol. Resour. Announc. 9::e01002-20
    [Crossref] [Google Scholar]
  27. 27.
    Decraemer W, Hunt DJ. 2006.. Structure and classification. . In Plant Nematology, ed. RN Perry, M Moens , pp. 332. Cambridge, MA:: CABI
    [Google Scholar]
  28. 28.
    Diaz-Granados A, Petrescu AJ, Goverse A, Smant G. 2016.. SPRYSEC effectors: a versatile protein-binding platform to disrupt plant innate immunity. . Front. Plant Sci. 7::1575
    [Crossref] [Google Scholar]
  29. 29.
    Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, et al. 2008.. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. . Nat. Genet. 40::119398
    [Crossref] [Google Scholar]
  30. 30.
    Dieterich C, Sommer RJ. 2009.. How to become a parasite: lessons from the genomes of nematodes. . Trends Genet. 25::2039
    [Crossref] [Google Scholar]
  31. 31.
    Elling A. 2013.. Major emerging problems with minor Meloidogyne species. . Phytopathology 103:(11):1092102
    [Crossref] [Google Scholar]
  32. 32.
    Elling AA, Mitreva M, Recknor J, Gai X, Martin J, et al. 2007.. Divergent evolution of arrested development in the dauer stage of Caenorhabditis elegans and the infective stage of Heterodera glycines. . Genome Biol. 8::R211
    [Crossref] [Google Scholar]
  33. 33.
    Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EGJ, et al. 2016.. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. . Genome Biol. 17::124
    [Crossref] [Google Scholar]
  34. 34.
    Gendrel M, Atlas EG, Hobert O. 2016.. A cellular and regulatory map of the GABAergic nervous system of C. elegans. . eLife 5::e17686
    [Crossref] [Google Scholar]
  35. 35.
    Gilabert A, Curran DM, Harvey SC, Wasmuth JD. 2016.. Expanding the view on the evolution of the nematode dauer signalling pathways: refinement through gene gain and pathway co-option. . BMC Genom. 17::476
    [Crossref] [Google Scholar]
  36. 36.
    Gillet FX, Bournaud C, Antonino de Souza JD Jr., Grossi-de-Sa MF. 2017.. Plant-parasitic nematodes: towards understanding molecular players in stress responses. . Ann. Bot. 119::77589
    [Google Scholar]
  37. 37.
    Guiliano DB, Hall N, Jones SJ, Clark LN, Corton CH, et al. 2002.. Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes. . Genome Biol. 3::research0057.1
    [Crossref] [Google Scholar]
  38. 38.
    Haegeman A, Jones JT, Danchin EGJ. 2011.. Horizontal gene transfer in nematodes: a catalyst for plant parasitism?. Mol. Plant-Microbe Interact. 24::87987
    [Crossref] [Google Scholar]
  39. 39.
    Han Z, Boas S, Schroeder NE. 2016.. Unexpected variation in neuroanatomy among diverse nematode species. . Front. Neuroanat. 9::162
    [Crossref] [Google Scholar]
  40. 40.
    Han Z, Sieriebriennikov B, Susoy V, Lo WS, Igreja C, et al. 2022.. Horizontally acquired cellulases assist the expansion of dietary range in Pristionchus nematodes. . Mol. Biol. Evol. 39:(2):msab370
    [Crossref] [Google Scholar]
  41. 41.
    Han Z, Thapa S, Reuter-Carlson U, Reed H, Gates M, et al. 2018.. Immobility in the sedentary plant-parasitic nematode H. glycines is associated with remodeling of neuromuscular tissue. . PLOS Pathog. 14::e1007198
    [Crossref] [Google Scholar]
  42. 42.
    Holden-Dye L, Walker RJ. 2011.. Neurobiology of plant parasitic nematodes. . Invertebr. Neurosci. 11::919
    [Crossref] [Google Scholar]
  43. 43.
    Holden-Dye L, Walker RJ. 2014.. Anthelmintic drugs and nematicides: studies in Caenorhabditis elegans. . WormBook 2014::129
    [Crossref] [Google Scholar]
  44. 44.
    Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, 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::1792800
    [Crossref] [Google Scholar]
  45. 45.
    Hu L-J, Wu X-Q, Ding X-L, Ye J-R. 2021.. Comparative transcriptomic analysis of candidate effectors to explore the infection and survival strategy of Bursaphelenchus xylophilus during different interaction stages with pine trees. . BMC Plant Biol. 21::224
    [Crossref] [Google Scholar]
  46. 46.
    Johnston MJ, McVeigh P, McMaster S, Fleming CC, Maule AG. 2010.. FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology. . J. Helminthol. 84::25365
    [Crossref] [Google Scholar]
  47. 47.
    Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, et al. 2013.. Top 10 plant-parasitic nematodes in molecular plant pathology. . Mol. Plant Pathol. 14::94661
    [Crossref] [Google Scholar]
  48. 48.
    Jones L, Giorgi C, Urwin P. 2011.. C. elegans as a resource for studies on plant parasitic nematodes. . In Genomics and Molecular Genetics of Plant-Nematode Interactions, ed. J Jones, G Gheysen, C Fenoll , pp. 175220. Dordrecht, Neth:.: Springer
    [Google Scholar]
  49. 49.
    Kearn J, Ludlow E, Dillon J, O'Connor V, Holden-Dye L. 2014.. Fluensulfone is a nematicide with a mode of action distinct from anticholinesterases and macrocyclic lactones. . Pestic. Biochem. Physiol. 109::4457
    [Crossref] [Google Scholar]
  50. 50.
    Khan M, Khan AU. 2021.. Plant parasitic nematodes effectors and their crosstalk with defense response of host plants: a battle underground. . Rhizosphere 17::100288
    [Crossref] [Google Scholar]
  51. 51.
    Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, et al. 2011.. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. . PLOS Pathog. 7::e1002219
    [Crossref] [Google Scholar]
  52. 52.
    Kikuchi T, Eves-van den Akker S, Jones JT. 2017.. Genome evolution of plant-parasitic nematodes. . Annu. Rev. Phytopathol. 55::33354
    [Crossref] [Google Scholar]
  53. 53.
    Kimber MJ, Fleming CC. 2005.. Neuromuscular function in plant parasitic nematodes: a target for novel control strategies?. Parasitology 131::S12942
    [Crossref] [Google Scholar]
  54. 54.
    Kimber MJ, Fleming CC, Prior A, Jones JT, Halton DW, Maule AG. 2002.. Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. . Int. J. Parasitol. 32::1095105
    [Crossref] [Google Scholar]
  55. 55.
    Kiontke K, Fitch DHA. 2005.. The phylogenetic relationships of Caenorhabditis and other rhabditids. . WormBook 2005::111
    [Google Scholar]
  56. 56.
    Kranse O, Beasley H, Adams S, Pires-daSilva A, Bell C, et al. 2021.. Toward genetic modification of plant-parasitic nematodes: delivery of macromolecules to adults and expression of exogenous mRNA in second stage juveniles. . G3 11:(2):jkaa058
    [Crossref] [Google Scholar]
  57. 57.
    Lambert K, Bekal S. 2002.. Introduction to plant-parasitic nematodes. . Plant Health Instr. https://doi.org/10.1094/PHI-I-2002-1218-01
    [Crossref] [Google Scholar]
  58. 58.
    Leroy S, Bouamer S, Morand S, Fargette M. 2007.. Genome size of plant-parasitic nematodes. . Nematology 9::44950
    [Crossref] [Google Scholar]
  59. 59.
    Lilley CJ, Atkinson HJ, Urwin PE. 2005.. Molecular aspects of cyst nematodes. . Mol. Plant Pathol. 6::57788
    [Crossref] [Google Scholar]
  60. 60.
    Lilley CJ, Maqbool A, Wu D, Yusup HB, Jones LM, et al. 2018.. Effector gene birth in plant parasitic nematodes: neofunctionalization of a housekeeping glutathione synthetase gene. . PLOS Genet. 14::e1007310
    [Crossref] [Google Scholar]
  61. 61.
    McCarter JP, Mitreva MD, Martin J, Dante M, Wylie T, et al. 2003.. Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. . Genome Biol. 4::R26
    [Crossref] [Google Scholar]
  62. 62.
    McCoy CJ, Atkinson LE, Zamanian M, McVeigh P, Day TA, et al. 2014.. New insights into the FLPergic complements of parasitic nematodes: informing deorphanisation approaches. . EuPA Open Proteom. 3::26272
    [Crossref] [Google Scholar]
  63. 63.
    McVeigh P, Atkinson L, Marks NJ, Mousley A, Dalzell JJ, et al. 2012.. Parasite neuropeptide biology: seeding rational drug target selection?. Int. J. Parasitol. Drugs Drug Resist. 2::7691
    [Crossref] [Google Scholar]
  64. 64.
    Mejias J, Bazin J, Truong N-M, Chen Y, Marteu N, et al. 2021.. The root-knot nematode effector MiEFF18 interacts with the plant core spliceosomal protein SmD1 required for giant cell formation. . New Phytol. 229::340823
    [Crossref] [Google Scholar]
  65. 65.
    Mitreva M, Smant G, Helder J. 2009.. Role of horizontal gene transfer in the evolution of plant parasitism among nematodes. . Methods Mol. Biol. 532::51735
    [Crossref] [Google Scholar]
  66. 66.
    Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, et al. 2008.. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. . PNAS 105::148027
    [Crossref] [Google Scholar]
  67. 67.
    Perry R, Moens M. 2011.. Introduction to plant-parasitic nematodes; modes of parasitism. . In Genomics and Molecular Genetics of Plant-Nematode Interactions, ed. J Jones, G Gheysen, C Fenoll , pp. 320. Dordrecht, Neth:.: Springer
    [Google Scholar]
  68. 68.
    Politz SM, Philipp M. 1992.. Caenorhabditis elegans as a model for parasitic nematodes: a focus on the cuticle. . Parasitol. Today 8::612
    [Crossref] [Google Scholar]
  69. 69.
    Quist CW, Smant G, Helder J. 2015.. Evolution of plant parasitism in the phylum Nematoda. . Annu. Rev. Phytopathol. 53::289310
    [Crossref] [Google Scholar]
  70. 70.
    Salinas G, Risi G. 2018.. Caenorhabditis elegans: nature and nurture gift to nematode parasitologists. . Parasitology 145::97987
    [Crossref] [Google Scholar]
  71. 71.
    Schafer W. 2016.. Nematode nervous systems. . Curr. Biol. 26::R95559
    [Crossref] [Google Scholar]
  72. 72.
    Schleker ASS, Rist M, Matera C, Damijonaitis A, Collienne U, et al. 2022.. Mode of action of fluopyram in plant-parasitic nematodes. . Sci. Rep. 12::11954
    [Crossref] [Google Scholar]
  73. 73.
    Scholl EH, Thorne JL, McCarter JP, Bird DM. 2003.. Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. . Genome Biol. 4::R39
    [Crossref] [Google Scholar]
  74. 74.
    Sommer RJ, Bumbarger DJ. 2012.. Nematode model systems in evolution and development. . Wiley Interdiscip. Rev. Dev. Biol. 1::389400
    [Crossref] [Google Scholar]
  75. 75.
    Stevens L, Félix MA, Beltran T, Braendle C, Caurcel C, et al. 2019.. Comparative genomics of 10 new Caenorhabditis species. . Evol. Lett. 3::21736
    [Crossref] [Google Scholar]
  76. 76.
    Susič N, Koutsovoulos GD, Riccio C, Danchin EGJ, Blaxter ML, et al. 2020.. Genome sequence of the root-knot nematode Meloidogyne luci. . J. Nematol. 52::e2020-25
    [Crossref] [Google Scholar]
  77. 77.
    Thapa S, Gates MK, Reuter-Carlson U, Androwski RJ, Schroeder NE. 2019.. Convergent evolution of saccate body shapes in nematodes through distinct developmental mechanisms. . EvoDevo 10::5
    [Crossref] [Google Scholar]
  78. 78.
    Tytgat T, Meutter J, Gheysen L, Coomans A. 2000.. Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes. . Nematology 2::11321
    [Crossref] [Google Scholar]
  79. 79.
    Urwin PE, Lilley CJ, Atkinson HJ. 2002.. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. . Mol. Plant-Microbe Interact. 15::74752
    [Crossref] [Google Scholar]
  80. 80.
    van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, et al. 2009.. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. . Nematology 11::92750
    [Crossref] [Google Scholar]
  81. 81.
    Viney M. 2018.. The genomic basis of nematode parasitism. . Brief. Funct. Genom. 17::814
    [Crossref] [Google Scholar]
  82. 82.
    Vlaar LE, Bertran A, Rahimi M, Dong L, Kammenga JE, et al. 2021.. On the role of dauer in the adaptation of nematodes to a parasitic lifestyle. . Parasites Vectors 14::554
    [Crossref] [Google Scholar]
  83. 83.
    Warnock ND, Wilson L, Patten C, Fleming CC, Maule AG, Dalzell JJ. 2017.. Nematode neuropeptides as transgenic nematicides. . PLOS Pathog. 13::e1006237
    [Crossref] [Google Scholar]
  84. 84.
    Winter MD, McPherson MJ, Atkinson HJ. 2002.. Neuronal uptake of pesticides disrupts chemosensory cells of nematodes. . Parasitology 125::56165
    [Crossref] [Google Scholar]
  85. 85.
    Woods DJ, Lauret C, Geary T. 2007.. Anthelmintic discovery and development in the animal health industry. . Expert Opin. Drug Discov. 2::S2533
    [Crossref] [Google Scholar]
  86. 86.
    Zheng J, Peng D, Chen L, Liu H, Chen F, et al. 2016.. The Ditylenchus destructor genome provides new insights into the evolution of plant parasitic nematodes. . Proc. R. Soc. B 283:(1835):20160942
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-phyto-021622-113539
Loading
  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error