1932

Abstract

Plant parasitism has evolved independently on at least four separate occasions in the phylum Nematoda. The application of next-generation sequencing (NGS) to plant-parasitic nematodes has allowed a wide range of genome- or transcriptome-level comparisons, and these have identified genome adaptations that enable parasitism of plants. Current genome data suggest that horizontal gene transfer, gene family expansions, evolution of new genes that mediate interactions with the host, and parasitism-specific gene regulation are important adaptations that allow nematodes to parasitize plants. Sequencing of a larger number of nematode genomes, including plant parasites that show different modes of parasitism or that have evolved in currently unsampled clades, and using free-living taxa as comparators would allow more detailed analysis and a better understanding of the organization of key genes within the genomes. This would facilitate a more complete understanding of the way in which parasitism has shaped the genomes of plant-parasitic nematodes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080516-035434
2017-08-04
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/phyto/55/1/annurev-phyto-080516-035434.html?itemId=/content/journals/10.1146/annurev-phyto-080516-035434&mimeType=html&fmt=ahah

Literature Cited

  1. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG. 1.  et al. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. . Nat. Biotechnol. 26:909–15 [Google Scholar]
  2. Ahmadinejad N, Dagan T, Gruenheit N, Martin W, Gabaldon T. 2.  2010. Evolution of spliceosomal introns following endosymbiotic gene transfer. BMC Evol. Biol. 10:57 [Google Scholar]
  3. Bauters L, Haegeman A, Kyndt T, Gheysen G. 3.  2014. Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival strategies and host-nematode interactions. Mol. Plant Pathol. 15:352–63 [Google Scholar]
  4. Betz R, Walter S, Requena N. 4.  2016. Alternative splicing—an elegant way to diversify the function of repeat‐containing effector proteins?. New Phytol 212:306–9 [Google Scholar]
  5. Bird DM, Jones JT, Opperman CH, Kikuchi T, Danchin EG. 5.  2014. Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 142:Suppl. 1S71–84 [Google Scholar]
  6. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P. 6.  et al. 1998. A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75 [Google Scholar]
  7. Boothby TC, Tenlen JR, Smith FW, Wang JR, Patanella KA. 7.  et al. 2015. Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. PNAS 112:15976–81 [Google Scholar]
  8. Burke M, Scholl EH, Bird DM, Schaff JE, Colman SD. 8.  et al. 2015. The plant parasite Pratylenchus coffeae carries a minimal nematode genome. Nematology 17:621–37 [Google Scholar]
  9. Castagnone-Sereno P. 9.  2006. Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–89 [Google Scholar]
  10. Castagnone-Sereno P, Danchin EG, Perfus-Barbeoch L, Abad P. 10.  2013. Diversity and evolution of root-knot nematodes, genus Meloidogyne: new insights from the genomic era. Annu. Rev. Phytopathol. 51:203–20 [Google Scholar]
  11. Castagnone-Sereno P, Semblat J-P, Castagnone C. 11.  2009. Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. . Mol. Genet. Genom. 282:547–54 [Google Scholar]
  12. 12. C. elegans Seq. Consort. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–18 [Google Scholar]
  13. Chen S, Chronis D, Wang X. 13.  2013. The novel GrCEP12 peptide from the plant-parasitic nematode Globodera rostochiensis suppresses flg22-mediated PTI. Plant Signal. Behav. 8:e25359 [Google Scholar]
  14. Chronis D, Chen S, Lu S, Hewezi T, Carpenter SC. 14.  et al. 2013. A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant J 74:185–96 [Google Scholar]
  15. Coghlan A. 15.  2005. Nematode genome evolution. WormBook https://doi.org/10.1895/wormbook.1.15.1 [Crossref]
  16. Cotton J, Lilley C, Jones L, Kikuchi T, Reid A. 16.  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 [Google Scholar]
  17. Craig JP, Bekal S, Hudson M, Domier L, Niblack T, Lambert KN. 17.  2008. Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines. . Mol. Biol. Evol. 25:2085–98 [Google Scholar]
  18. Danchin EG, Arguel M-J, Campan-Fournier A, Perfus-Barbeoch L, Magliano M. 18.  et al. 2013. Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLOS Pathog 9:e1003745 [Google Scholar]
  19. Danchin EG, Guzeeva EA, Mantelin S, Berepiki A, Jones JT. 19.  2016. Horizontal gene transfer from bacteria has enabled the plant-parasitic nematode Globodera pallida to feed on host-derived sucrose. Mol. Biol. Evol. 33:1571–79 [Google Scholar]
  20. Danchin EG, Rosso M-N. 20.  2012. Lateral gene transfers have polished animal genomes: lessons from nematodes. Front. Cell. Infect. Microbiol. 2:27 [Google Scholar]
  21. Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM. 21.  et al. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. PNAS 107:17651–56 [Google Scholar]
  22. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V. 22.  et al. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–98 [Google Scholar]
  23. Erwin DC, Ribeiro OK. 23.  1996. Phytophthora Diseases Worldwide St. Paul, MN: APS Press
  24. Espada M, Silva AC, Eves van den Akker S, Cock PJ, Mota M, Jones JT. 24.  2016. Identification and characterization of parasitism genes from the pinewood nematode Bursaphelenchus xylophilus reveals a multilayered detoxification strategy. Mol. Plant Pathol. 17:286–95 [Google Scholar]
  25. Eves-van den Akker S, Birch PR. 25.  2016. Opening the effector protein toolbox for plant-parasitic cyst nematode interactions. Mol. Plant 9:1451–53 [Google Scholar]
  26. Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EG. 26.  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 [Google Scholar]
  27. Eves-van den Akker S, Lilley C, Danchin E, Rancurel C, Cock P. 27.  et al. 2014. The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biol. Evol. 6:2181–94 [Google Scholar]
  28. Eves-van den Akker S, Lilley CJ, Jones JT, Urwin PE. 28.  2014. Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes. PLOS Pathog 10:e1004391 [Google Scholar]
  29. Eves-Van Den Akker S, Lilley CJ, Yusup HB, Jones JT, Urwin PE. 29.  2016. Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis. . Mol. Plant Pathol. 17:1265–75 [Google Scholar]
  30. Faino L, Seidl MF, Shi-Kunne X, Pauper M, van den Berg GC. 30.  et al. 2016. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res 26:1091–100 [Google Scholar]
  31. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 31.  2003. The parasitome of the phytonematode Heterodera glycines. . Mol. Plant-Microbe Interact. 16:720–26 [Google Scholar]
  32. Haegeman A, Bauters L, Kyndt T, Rahman MM, Gheysen G. 32.  2013. Identification of candidate effector genes in the transcriptome of the rice root knot nematode Meloidogyne graminicola. . Mol. Plant Pathol. 14:379–90 [Google Scholar]
  33. Haegeman A, Jones JT, Danchin EG. 33.  2011. Horizontal gene transfer in nematodes: a catalyst for plant parasitism?. Mol. Plant-Microbe Interact. 24:879–87 [Google Scholar]
  34. Haegeman A, Vanholme B, Jacob J, Vandekerckhove T, Claeys M. 34.  et al. 2009. An endosymbiotic bacterium in a plant-parasitic nematode: member of a new Wolbachia supergroup. Int. J. Parasitol. 39:1045–54 [Google Scholar]
  35. Hamamouch N, Li C, Seo PJ, Park CM, Davis EL. 35.  2011. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol. Plant Pathol. 12:355–64 [Google Scholar]
  36. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG. 36.  et al. 2008. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell Online 20:3080 [Google Scholar]
  37. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG. 37.  et al. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. . Plant Physiol. 152:968–84 [Google Scholar]
  38. Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S. 38.  2009. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant-Microbe Interact. 22:115–22 [Google Scholar]
  39. Howe KL, Bolt BJ, Shafie M, Kersey P, Berriman M. 39.  2016. WormBase ParaSite—a comprehensive resource for helminth genomics. Mol. Biochem. Parasitol. http://dx.doi.org/10.1016/j.molbiopara.2016.11.005 [Crossref]
  40. Huang GZ, Gao BL, Maier T, Allen R, Davis EL. 40.  et al. 2003. A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. . Mol. Plant-Microbe Interact. 16:376–81 [Google Scholar]
  41. Huang J. 41.  2013. Horizontal gene transfer in eukaryotes: the weak-link model. BioEssays 35:868–75 [Google Scholar]
  42. Hunt VL, Tsai IJ, Coghlan A, Reid AJ, Holroyd N. 42.  et al. 2016. The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat. Genet. 48:299–307 [Google Scholar]
  43. Jasmer DP, Goverse A, Smant G. 43.  2003. Parasitic nematode interactions with mammals and plants. Annu. Rev. Phytopathol. 41:245–70 [Google Scholar]
  44. Jones J, Gheysen G, Fenoll C. 44.  2011. Genomics and Molecular Genetics of Plant-Nematode Interactions Dordrecht, Neth: Springer
  45. Jones J, Reavy B, Smant G, Prior A. 45.  2004. Glutathione peroxidases of the potato cyst nematode Globodera Rostochiensis. . Gene 324:47–54 [Google Scholar]
  46. Jones JD, Dangl JL. 46.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  47. Jones JT, Furlanetto C, Bakker E, Banks B, Blok V. 47.  et al. 2003. Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. . Mol. Plant Pathol. 4:43–50 [Google Scholar]
  48. Jones JT, Furlanetto C, Kikuchi T. 48.  2005. Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7:641–46 [Google Scholar]
  49. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J. 49.  et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14:946–61 [Google Scholar]
  50. Jones JT, Moens M, Mota M, Li H, Kikuchi T. 50.  2008. Bursaphelenchus xylophilus: opportunities in comparative genomics and molecular host-parasite interactions Mol. . Plant Pathol. 9:357–68 [Google Scholar]
  51. Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D. 51.  et al. 2011. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol 155:1960–75 [Google Scholar]
  52. Kanzaki N, Giblin-Davis RM. 52.  2016. Pine wilt and red ring, lethal plant diseases caused by insect-mediated Bursaphelenchus nematodes. Vector-Mediated Transmission of Plant Pathogens JK Brown 87–107 St. Paul, MN: APS Press [Google Scholar]
  53. Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N. 53.  et al. 2011. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. . PLOS Pathog. 7:e1002219 [Google Scholar]
  54. Kikuchi T, Jones JT, Aikawa T, Kosaka H, Ogura N. 54.  2004. A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. . FEBS Lett. 572:201–5 [Google Scholar]
  55. Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J. 55.  et al. 2016. No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. . PNAS 113:5053–58 [Google Scholar]
  56. Ku C, Martin WF. 56.  2016. A natural barrier to lateral gene transfer from prokaryotes to eukaryotes revealed from genomes: the 70% rule. BMC Biol 14:89 [Google Scholar]
  57. Kumar M, Gantasala NP, Roychowdhury T, Thakur PK, Banakar P. 57.  et al. 2014. De novo transcriptome sequencing and analysis of the cereal cyst nematode. Heterodera avenae. PLOS ONE 9:e96311 [Google Scholar]
  58. Lambert KN, Bekal S, Domier LL, Niblack TL, Noel GR, Smyth CA. 58.  2005. Selection of Heterodera glycines chorismate mutase-1 alleles on nematode-resistant soybean. Mol. Plant-Microbe Interact. 18:593–601 [Google Scholar]
  59. Lambshead PJD, Boucher G. 59.  2003. Marine nematode deep-sea biodiversity: hyperdiverse or hype?. J. Biogeogr. 30:475–85 [Google Scholar]
  60. Lee C, Chronis D, Kenning C, Peret B, Hewezi T. 60.  et al. 2011. The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–80 [Google Scholar]
  61. Leroy S, Duperray C, Morand S. 61.  2003. Flow cytometry for parasite nematode genome size measurement. Mol. Biochem. Parasitol. 128:91–93 [Google Scholar]
  62. Lu S-W, Tian D, Borchardt-Wier HB, Wang X. 62.  2008. Alternative splicing: a novel mechanism of regulation identified in the chorismate mutase gene of the potato cyst nematode Globodera rostochiensis. . Mol. Biochem. Parasitol. 162:1–15 [Google Scholar]
  63. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. 63.  2014. The complex hybrid origins of the root knot nematodes revealed through comparative genomics. PeerJ 2:e356 [Google Scholar]
  64. Maier TR, Hewezi T, Peng J, Baum TJ. 64.  2013. Isolation of whole esophageal gland cells from plant-parasitic nematodes for transcriptome analyses and effector identification. Mol. Plant-Microbe Interact. 26:31–35 [Google Scholar]
  65. Mei Y, Thorpe P, Guzha A, Haegeman A, Blok VC. 65.  et al. 2015. Only a small subset of the SPRY domain gene family in Globodera pallida is likely to encode effectors, two of which suppress host defences induced by the potato resistance gene Gpa2. . Nematology 17:409–24 [Google Scholar]
  66. Nicol JM, Turner SJ, Coyne DL, Den Nijs L, Hockland S, Maafi ZT. 66.  2011. Current nematode threats to world agriculture. See Ref. 44 21–43
  67. Noon JB, Baum TJ. 67.  2016. Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients. BMC Evol. Biol. 16:1 [Google Scholar]
  68. Noon JB, Hewezi TAF, Maier TR, Simmons C, Wei J-Z. 68.  et al. 2015. Eighteen new candidate effectors of the phytonematode Heterodera glycines produced specifically in the secretory esophageal gland cells during parasitism. Phytopathology 105:1362–72 [Google Scholar]
  69. Noon JB, Qi M, Sill DN, Muppirala U, Eves-van den Akker S. 69.  et al. 2016. A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. New Phytol 212:444–60 [Google Scholar]
  70. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M. 70.  et al. 2008. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. PNAS 105:14802–7 [Google Scholar]
  71. Paganini J, Campan-Fournier A, Da Rocha M, Gouret P, Pontarotti P. 71.  et al. 2012. Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLOS ONE 7:e50875 [Google Scholar]
  72. Petitot AS, Dereeper A, Agbessi M, Da Silva C, Guy J. 72.  et al. 2016. Dual RNA‐seq reveals Meloidogyne graminicola transcriptome and candidate effectors during the interaction with rice plants. Mol. Plant Pathol. 17:860–74 [Google Scholar]
  73. Quist CW, Smant G, Helder J. 73.  2015. Evolution of plant parasitism in the phylum Nematoda. Annu. Rev. Phytopathol. 53:289–310 [Google Scholar]
  74. Raffaele S, Win J, Cano LM, Kamoun S. 74.  2010. Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. . BMC Genom. 11:637 [Google Scholar]
  75. Rehman S, Postma W, Tytgat T, Prins P, Qin L. 75.  et al. 2009. A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Mol. Plant-Microbe Int. 22:330–40 [Google Scholar]
  76. Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E. 76.  et al. 2000. Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. . Mol. Biochem. Parasitol. 111:41–49 [Google Scholar]
  77. Roman J, Triantaphyllou A. 77.  1969. Gametogenesis and reproduction of seven species of Pratylenchus. J. Nematol. 1:357 [Google Scholar]
  78. Rosso M-N, Vieira P, de Almeida-Engler J, Castagnone-Sereno P. 78.  2011. Proteins secreted by root-knot nematodes accumulate in the extracellular compartment during root infection. Plant Signal. Behav. 6:1232–34 [Google Scholar]
  79. Rutter WB, Hewezi T, Maier TR, Mitchum MG, Davis EL. 79.  et al. 2014. Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104:879–85 [Google Scholar]
  80. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A. 80.  et al. 2009. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLOS Pathog 5:e1000564 [Google Scholar]
  81. Schoch CL, Sung GH, Lopez-Giraldez F, Townsend JP, Miadlikowska J. 81.  et al. 2009. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst. Biol. 58:224–39 [Google Scholar]
  82. Scholl EH, Thorne JL, McCarter JP, Bird DM. 82.  2003. Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39 [Google Scholar]
  83. Schulze-Lefert P, Panstruga R. 83.  2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–25 [Google Scholar]
  84. Semblat J-P, Rosso M-N, Hussey RS, Abad P, Castagnone-Sereno P. 84.  2001. Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. . Mol. Plant-Microbe Interact. 14:72–79 [Google Scholar]
  85. Smant G, Jones J. 85.  2011. Suppression of plant defences by nematodes. See Ref. 44 273–86
  86. Smant G, Stokkermans JP, Yan Y, de Boer JM, Baum TJ. 86.  et al. 1998. Endogenous cellulases in animals: isolation of β-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. PNAS 95:4906–11 [Google Scholar]
  87. Sobczak M, Golinowski W. 87.  2011. Cyst nematodes and syncytia. See Ref. 44 61–82
  88. Soucy SM, Huang J, Gogarten JP. 88.  2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:472–82 [Google Scholar]
  89. Sperschneider J, Gardiner DM, Dodds PN, Tini F, Covarelli L. 89.  et al. 2015. EffectorP: predicting fungal effector proteins from secretomes using machine learning. New Phytol 210:743–61 [Google Scholar]
  90. Thorpe P, Mantelin S, Cock PJ, Blok VC, Coke MC. 90.  et al. 2014. Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida. . BMC Genom. 15:923 [Google Scholar]
  91. Tsai IJ, Tanaka R, Kanzaki N, Akiba M, Yokoi T. 91.  et al. 2016. Transcriptional and morphological changes in the transition from mycetophagous to phytophagous phase in the plant-parasitic nematode Bursaphelenchus xylophilus. . Mol. Plant Pathol. 17:77–83 [Google Scholar]
  92. Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M. 92.  et al. 2004. A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Mol. Plant-Microbe Interact. 17:846–52 [Google Scholar]
  93. van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P. 93.  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]
  94. Vieira P, Danchin EGJ, Neveu C, Crozat C, Jaubert S. 94.  et al. 2011. The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 62:1241–53 [Google Scholar]
  95. Vieira P, Eves-van den Akker S, Verma R, Wantoch S, Eisenback JD, Kamo K. 95.  2015. The Pratylenchus penetrans transcriptome as a source for the development of alternative control strategies: mining for putative genes involved in parasitism and evaluation of in planta RNAi. PLOS ONE 10:e0144674 [Google Scholar]
  96. Walton AC. 96.  1959. Some parasites and their chromosomes. J. Parasitol. 45:1–20 [Google Scholar]
  97. Weerasinghe RR, Bird DM, Allen NS. 97.  2005. Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. PNAS 102:3147–52 [Google Scholar]
  98. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 98.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  99. Woo JS, Imm JH, Min CK, Kim KJ, Cha SS, Oh BH. 99.  2006. Structural and functional insights into the B30.2/SPRY domain. EMBO J 25:1353–63 [Google Scholar]
  100. Zhang R, Calixto CPG, Marquez Y, Venhuizen P, Tzioutziou NA. 100.  et al. 2017. A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing. Nucleic Acids Res. 45:5061–73 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080516-035434
Loading
/content/journals/10.1146/annurev-phyto-080516-035434
Loading

Data & Media 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