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Signatures of adaptation to plant parasitism in nematode genomes

  • DAVID McK. BIRD (a1) (a2), JOHN T. JONES (a3), CHARLES H. OPPERMAN (a2), TAISEI KIKUCHI (a4) (a5) and ETIENNE G. J. DANCHIN (a6) (a7) (a8)...

Plant-parasitic nematodes cause considerable damage to global agriculture. The ability to parasitize plants is a derived character that appears to have independently emerged several times in the phylum Nematoda. Morphological convergence to feeding style has been observed, but whether this is emergent from molecular convergence is less obvious. To address this, we assess whether genomic signatures can be associated with plant parasitism by nematodes. In this review, we report genomic features and characteristics that appear to be common in plant-parasitic nematodes while absent or rare in animal parasites, predators or free-living species. Candidate horizontal acquisitions of parasitism genes have systematically been found in all plant-parasitic species investigated at the sequence level. Presence of peptides that mimic plant hormones also appears to be a trait of plant-parasitic species. Annotations of the few genomes of plant-parasitic nematodes available to date have revealed a set of apparently species-specific genes on every occasion. Effector genes, important for parasitism are frequently found among those species-specific genes, indicating poor overlap. Overall, nematodes appear to have developed convergent genomic solutions to adapt to plant parasitism.

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P. Abad , J. Gouzy , J.-M. Aury , P. Castagnone-Sereno , E. G. J. Danchin , E. Deleury , L. Perfus-Barbeoch , V. Anthouard , F. Artiguenave , V. C. Blok , M.-C. Caillaud , P. M. Coutinho , C. Dasilva , F. D. Luca , F. Deau , M. Esquibet , T. Flutre , J. V. Goldstone , N. Hamamouch , T. Hewezi , O. Jaillon , C. Jubin , P. Leonetti , M. Magliano , T. R. Maier , G. V. Markov , P. McVeigh , G. Pesole , J. Poulain , M. Robinson-Rechavi , E. Sallet , B. Ségurens , D. Steinbach , T. Tytgat , E. Ugarte , C. van Ghelder , P. Veronico , T. J. Baum , M. Blaxter , T. Bleve-Zacheo , E. L. Davis , J. J. Ewbank , B. Favery , E. Grenier , B. Henrissat , J. T. Jones , V. Laudet , A. G. Maule , H. Quesneville , M.-N. Rosso , T. Schiex , G. Smant , J. Weissenbach and P. Wincker (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909915. doi: 10.1038/nbt.1482.

J. O. Andersson (2005). Lateral gene transfer in eukaryotes. Cellular and Molecular Life Sciences 62, 11821197.

J. G. Baldwin , S. A. Nadler and B. J. Adams (2004). Evolution of plant parasitism among nematodes. Annual Review of Phytopathology 42, 83105.

D. M. Bird (1996). Manipulation of host gene expression by root-knot nematodes. Journal of Parasitology 82, 881888.

D. M. Bird (2004). Signaling between nematodes and plants. Current Opinion in Plant Biology 7, 372376. doi: 10.1016/j.pbi.2004.05.005.

M. Blaxter (2011). Nematodes: the worm and its relatives. PLoS Biology 9, e1001050. doi: 10.1371/journal.pbio.1001050.

M. L. Blaxter , P. D. Ley , J. R. Garey , L. X. Liu , P. Scheldeman , A. Vierstraete , J. R. Vanfleteren , L. Y. Mackey , M. Dorris , L. M. Frisse , J. T. Vida and W. K. Thomas (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175. doi: 10.1038/32160.

V. C. Blok , J. T. Jones , M. S. Phillips and D. L. Trudgill (2008). Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. Bioessays 30, 249259.

B. Bobay , P. DiGennaro , E. Scholl , N. Imin , M. Djordjevic and D. M. Bird (2013). Solution NMR studies of the plant peptide hormone CEP inform function. FEBS Letters 587, 39793985. doi: 10.1016/j.febslet.2013.10.033.

Y. Boucher , C. J. Douady , R. T. Papke , D. A. Walsh , M. E. Boudreau , C. L. Nesbo , R. J. Case and W. F. Doolittle (2003). Lateral gene transfer and the origins of prokaryotic groups. Annual Review of Genetics 37, 283328.

B. L. Cantarel , P. M. Coutinho , C. Rancurel , T. Bernard , V. Lombard and B. Henrissat (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 37, D233D238.

P. Castagnone-Sereno , E. G. Danchin , L. Perfus-Barbeoch and P. Abad (2013). Diversity and evolution of root-knot nematodes, genus Meloidogyne: new insights from the genomic era. Annual Review of Phytopathology 51, 203220. doi: 10.1146/annurev-phyto-082712-102300.

D. Chronis , S. Chen , S. Lu , T. Hewezi , S. C. D. Carpenter , R. Loria , T. J. Baum and X. Wang (2013). A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant Journal: for Cell and Molecular Biology 74, 185196. doi: 10.1111/tpj.12125.

E. G. Danchin , M. N. Rosso , P. Vieira , J. de Almeida-Engler , P. M. Coutinho , B. Henrissat and P. Abad (2010). Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proceedings of the National Academy of Sciences USA 107, 1765117656.

É. G. J. Danchin (2011). What nematode genomes tell us about the importance of horizontal gene transfers in the evolutionary history of animals. Mobile Genetic Elements 1, 269273.

E. G. J. Danchin and M.-N. Rosso (2012). Lateral gene transfers have polished animal genomes: lessons from nematodes. Frontiers in Cellular and Infection Microbiology 2, art. 27. doi: 10.3389/fcimb.2012.00027.

E. L. Davis , R. S. Hussey , M. G. Mitchum and T. J. Baum (2008). Parasitism proteins in nematode–plant interactions. Current Opinion in Plant Biology 11, 360366. doi: 10.1016/j.pbi.2008.04.003.

C. A. Desjardins , G. C. Cerqueira , J. M. Goldberg , J. C. D. Hotopp , B. J. Haas , J. Zucker , J. M. C. Ribeiro , S. Saif , J. Z. Levin , L. Fan , Q. Zeng , C. Russ , J. R. Wortman , D. L. Fink , B. W. Birren and T. B. Nutman (2013). Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature Genetics 45, 495500. doi: 10.1038/ng.2585.

C. Dieterich , S. W. Clifton , L. N. Schuster , A. Chinwalla , K. Delehaunty , I. Dinkelacker , L. Fulton , R. Fulton , J. Godfrey , P. Minx , M. Mitreva , W. Roeseler , H. Tian , H. Witte , S. P. Yang , R. K. Wilson and R. J. Sommer (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 11931198.

E. A. Doyle and K. N. Lambert (2002). Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Molecular Plant Microbe Interactions 15, 549556.

J. C. Dunning Hotopp (2011). Horizontal gene transfer between bacteria and animals. Trends in Genetics 27, 157163. doi: 10.1016/j.tig.2011.01.005.

C. Ejima , T. Uwatoko , B. T. Ngan , H. Honda , N. Shimizu , S. Kiyohara , R. Hamasaki and S. Sawa (2011). SNPs of CLAVATA receptors in tomato, in the context of root-knot nematode infection. Nematological Research 41, 3540.

B. Elsworth , J. Wasmuth and M. Blaxter (2011). NEMBASE4: the nematode transcriptome resource. International Journal for Parasitology 41, 881894. doi: 10.1016/j.ijpara.2011.03.009.

B. Gao , R. Allen , T. Maier , E. L. Davis , T. J. Baum and R. S. Hussey (2003). The parasitome of the phytonematode Heterodera glycines. Molecular Plant Microbe Interactions 16, 720726.

D. M. Gardiner , M. C. McDonald , L. Covarelli , P. S. Solomon , A. G. Rusu , M. Marshall , K. Kazan , S. Chakraborty , B. A. McDonald and J. M. Manners (2012). Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathogens 8, e1002952. doi: 10.1371/journal.ppat.1002952.

E. Ghedin , S. Wang , D. Spiro , E. Caler , Q. Zhao , J. Crabtree , J. E. Allen , A. L. Delcher , D. B. Guiliano , D. Miranda-Saavedra , S. V. Angiuoli , T. Creasy , P. Amedeo , B. Haas , N. M. El-Sayed , J. R. Wortman , T. Feldblyum , L. Tallon , M. Schatz , M. Shumway , H. Koo , S. L. Salzberg , S. Schobel , M. Pertea , M. Pop , O. White , G. J. Barton , C. K. Carlow , M. J. Crawford , J. Daub , M. W. Dimmic , C. F. Estes , J. M. Foster , M. Ganatra , W. F. Gregory , N. M. Johnson , J. Jin , R. Komuniecki , I. Korf , S. Kumar , S. Laney , B. W. Li , W. Li , T. H. Lindblom , S. Lustigman , D. Ma , C. V. Maina , D. M. Martin , J. P. McCarter , L. McReynolds , M. Mitreva , T. B. Nutman , J. Parkinson , J. M. Peregrin-Alvarez , C. Poole , Q. Ren , L. Saunders , A. E. Sluder , K. Smith , M. Stanke , T. R. Unnasch , J. Ware , A. D. Wei , G. Weil , D. J. Williams , Y. Zhang , S. A. Williams , C. Fraser-Liggett , B. Slatko , M. L. Blaxter and A. L. Scott (2007). Draft genome of the filarial nematode parasite Brugia malayi . Science 317, 17561760.

J. P. Gogarten and J. P. Townsend (2005). Horizontal gene transfer, genome innovation and evolution. Nature Reviews Microbiology 3, 679687. doi: 10.1038/nrmicro1204.

A. Haegeman , S. Joseph and G. Gheysen (2011 a). Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Molecular and Biochemical Parasitology 178, 714. doi: 10.1016/j.molbiopara.2011.04.001.

A. Haegeman , J. T. Jones and E. G. Danchin (2011 b). Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant Microbe Interactions 24, 879887. doi: 10.1094/MPMI-03-11-0055.

A. Haegeman , L. Bauters , T. Kyndt , M. M. Rahman and G. Gheysen (2013). Identification of candidate effector genes in the transcriptome of the rice root knot nematode Meloidogyne graminicola. Molecular Plant Pathology 14, 379390. doi: 10.1111/mpp.12014.

Y. Hirakawa , H. Shinohara , Y. Kondo , A. Inoue , I. Nakanomyo , M. Ogawa , S. Sawa , K. Ohashi-Ito , Y. Matsubayashi and H. Fukuda (2008). Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proceedings of the National Academy of Sciences USA 105, 1520815213. doi: 10.1073/pnas. 0808444105.

S. Hirsch , J. Kim , A. Muñoz , A. B. Heckmann , J. A. Downie and G. E. D. Oldroyd (2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell Online 21, 545557. doi: 10.1105/tpc.108.064501.

G. Huang , B. Gao , T. Maier , R. Allen , E. L. Davis , T. J. Baum and R. S. Hussey (2003). A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita . Molecular Plant Microbe Interactions 16, 376381.

G. Huang , R. Dong , R. Allen , E. L. Davis , T. J. Baum and R. S. Hussey (2006). A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Molecular Plant Microbe Interactions 19, 463470.

M. Jaouannet , M. Magliano , M. J. Arguel , M. Gourgues , E. Evangelisti , P. Abad and M. N. Rosso (2013). The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant Microbe Interactions 26, 97105. doi: 10.1094/MPMI-05-12-0130-R.

S. Jaubert , J. B. Laffaire , P. Abad and M. N. Rosso (2002). A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Letters 522, 109112.

A. R. Jex , S. Liu , B. Li , N. D. Young , R. S. Hall , Y. Li , L. Yang , N. Zeng , X. Xu , Z. Xiong , F. Chen , X. Wu , G. Zhang , X. Fang , Y. Kang , G. A. Anderson , T. W. Harris , B. E. Campbell , J. Vlaminck , T. Wang , C. Cantacessi , E. M. Schwarz , S. Ranganathan , P. Geldhof , P. Nejsum , P. W. Sternberg , H. Yang , J. Wang , J. Wang and R. B. Gasser (2011). Ascaris suum draft genome. Nature 479, 529533. doi: 10.1038/nature10553.

J. T. Jones , C. Furlanetto and T. Kikuchi (2005). Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7, 641646.

J. T. Jones , M. Moens , M. Mota , H. Li and T. Kikuchi (2008). Bursaphelenchus xylophilus: opportunities in comparative genomics and molecular host–parasite interactions. Molecular Plant Pathology 9, 357368. doi: 10.1111/j.1364-3703.2007.00461.x.

H. S. Judelson (2012). Dynamics and innovations within oomycete genomes: insights into biology, pathology, and evolution. Eukaryotic Cell 11, 13041312. doi: 10.1128/EC.00155-12.

T. Kikuchi , J. T. Jones , T. Aikawa , H. Kosaka and N. Ogura (2004). A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Letters 572, 201205.

T. Kikuchi , J. A. Cotton , J. J. Dalzell , K. Hasegawa , N. Kanzaki , P. McVeigh , T. Takanashi , I. J. Tsai , S. A. Assefa , P. J. Cock , T. D. Otto , M. Hunt , A. J. Reid , A. Sanchez-Flores , K. Tsuchihara , T. Yokoi , M. C. Larsson , J. Miwa , A. G. Maule , N. Sahashi , J. T. Jones and M. Berriman (2011). Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 7, e1002219. doi: 10.1371/journal.ppat.1002219.

S. Kumar , P. H. Schiffer and M. Blaxter (2012). 959 nematode genomes: a semantic wiki for coordinating sequencing projects. Nucleic Acids Research 40, D1295D1300. doi: 10.1093/nar/gkr826.

R. Laing , T. Kikuchi , A. Martinelli , I. J. Tsai , R. N. Beech , E. Redman , N. Holroyd , D. J. Bartley , H. Beasley , C. Britton , D. Curran , E. Devaney , A. Gilabert , M. Hunt , F. Jackson , S. L. Johnston , I. Kryukov , K. Li , A. A. Morrison , A. J. Reid , N. Sargison , G. I. Saunders , J. D. Wasmuth , A. Wolstenholme , M. Berriman , J. S. Gilleard and J. A. Cotton (2013). The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biology 14, R88. doi: 10.1186/gb-2013-14-8-r88.

P. J. D. Lambshead and G. Boucher (2003). Marine nematode deep-sea biodiversity – hyperdiverse or hype? Journal of Biogeography 30, 475485. doi: 10.1046/j.1365-2699.2003.00843.x.

T. N. Ledger , S. Jaubert , N. Bosselut , P. Abad and M. N. Rosso (2006). Characterization of a new beta-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 382, 121128.

C. Lee , D. Chronis , C. Kenning , B. Peret , T. Hewezi , E. L. Davis , T. J. Baum , R. Hussey , M. Bennett and M. G. Mitchum (2011). The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiology 155, 866880. doi: 10.1104/pp.110.167197.

S. Leroy , C. Duperray and S. Morand (2003). Flow cytometry for parasite nematode genome size measurement. Molecular and Biochemical Parasitology 128, 9193.

D. P. Lohar and D. M. Bird (2003). Lotus japonicus: a new model to study root-parasitic nematodes. Plant and Cell Physiology 44, 11761184.

S. W. Lu , S. Chen , J. Wang , H. Yu , D. Chronis , M. G. Mitchum and X. Wang (2009). Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Molecular Plant Microbe Interactions 22, 11281142. doi: 10.1094/MPMI-22-9-1128.

J. Martin , S. Abubucker , E. Heizer , C. M. Taylor and M. Mitreva (2011). update 2011: addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Research 40, D720D728. doi: 10.1093/nar/gkr1194.

J. P. McCarter (2009). Molecular approaches toward resistance to plant-parasitic nematodes. In Cell Biology of Plant Nematode Parasitism (ed. R. H. Berg and C. G. Taylor ), pp. 239267. Springer, Berlin, Germany.

J. P. McCarter , M. D. Mitreva , J. Martin , M. Dante , T. Wylie , U. Rao , D. Pape , Y. Bowers , B. Theising , C. V. Murphy , A. P. Kloek , B. J. Chiapelli , S. W. Clifton , D. M. Bird and R. H. Waterston (2003). Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biology 4, R26.

M. G. Mitchum , X. Wang and E. L. Davis (2008). Diverse and conserved roles of CLE peptides. Current Opinion in Plant Biology 11, 7581. doi: 10.1016/j.pbi.2007.10.010.

M. Mitreva , D. P. Jasmer , D. S. Zarlenga , Z. Wang , S. Abubucker , J. Martin , C. M. Taylor , Y. Yin , L. Fulton , P. Minx , S.-P. Yang , W. C. Warren , R. S. Fulton , V. Bhonagiri , X. Zhang , K. Hallsworth-Pepin , S. W. Clifton , J. P. McCarter , J. Appleton , E. R. Mardis and R. K. Wilson (2011). The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228235. doi: 10.1038/ng.769.

M. Mitreva-Dautova , E. Roze , H. Overmars , L. de Graaff , A. Schots , J. Helder , A. Goverse , J. Bakker and G. Smant (2006). A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita. Molecular Plant Microbe Interactions 19, 521529.

J. Ni , Y. Guo , H. Jin , J. Hartsell and S. E. Clark (2011). Characterization of a CLE processing activity. Plant Molecular Biology 75, 6775. doi: 10.1007/s11103-010-9708-2.

P. Nicol , R. Gill , J. Fosu-Nyarko and M. G. K. Jones (2012). De novo analysis and functional classification of the transcriptome of the root lesion nematode, Pratylenchus thornei, after 454 GS FLX sequencing. International Journal for Parasitology 42, 225237. doi: 10.1016/j.ijpara.2011.11.010.

K. Ohyama , M. Ogawa and Y. Matsubayashi (2008). Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant Journal: for Cell and Molecular Biology 55, 152160. doi: 10.1111/j.1365-313X.2008.03464.x.

R. Oliva , J. Win , S. Raffaele , L. Boutemy , T. O. Bozkurt , A. Chaparro-Garcia , M. E. Segretin , R. Stam , S. Schornack , L. M. Cano , M. Van Damme , E. Huitema , M. Thines , M. J. Banfield and S. Kamoun (2010). Recent developments in effector biology of filamentous plant pathogens: filamentous pathogen effectors. Cellular Microbiology 12, 705715. doi: 10.1111/j.1462-5822.2010.01471.x.

A. N. Olsen and K. Skriver (2003). Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends in Plant Science 8, 5557.

C. H. Opperman , D. M. Bird , V. M. Williamson , D. S. Rokhsar , M. Burke , J. Cohn , J. Cromer , S. Diener , J. Gajan , S. Graham , T. D. Houfek , Q. Liu , T. Mitros , J. Schaff , R. Schaffer , E. Scholl , B. R. Sosinski , V. P. Thomas and E. Windham (2008). Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences USA 105, 1480214807.

J. Paganini , A. Campan-Fournier , M. Da Rocha , P. Gouret , P. Pontarotti , E. Wajnberg , P. Abad and E. G. J. Danchin (2012). Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLoS ONE 7, e50875. doi: 10.1371/journal.pone.0050875.

J. Parkinson , C. Whitton , R. Schmid , M. Thomson and M. Blaxter (2004). NEMBASE: a resource for parasitic nematode ESTs. Nucleic Acids Research 32, D427D430.

G. Poinar , H. Kerp and H. Hass (2008). Palaeonema phyticum gen. n., sp. n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 10, 914.

W. J. Postma , E. J. Slootweg , S. Rehman , A. Finkers-Tomczak , T. O. G. Tytgat , K. van Gelderen , J. L. Lozano-Torres , J. Roosien , R. Pomp , C. van Schaik , J. Bakker , A. Goverse and G. Smant (2012). The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiology 160, 944954. doi: 10.1104/pp.112.200188.

L. Qin , U. Kudla , E. H. Roze , A. Goverse , H. Popeijus , J. Nieuwland , H. Overmars , J. T. Jones , A. Schots , G. Smant , J. Bakker and J. Helder (2004). Plant degradation: a nematode expansin acting on plants. Nature 427, 30.

L. Robertson , J. A. López-Pérez , A. Bello , M. A. Díez-Rojo , M. Escuer , A. Piedra-Buena , C. Ros and C. Martínez (2006). Characterization of Meloidogyne incognita, M. arenaria and M. hapla populations from Spain and Uruguay parasitizing pepper (Capsicum annuum L.). Crop Protection 25, 440445.

M. N. Rosso , B. Favery , C. Piotte , L. Arthaud , J. M. De Boer , R. S. Hussey , J. Bakker , T. J. Baum and P. Abad (1999). Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Molecular Plant Microbe Interactions 12, 585591.

K. Rybarczyk-Mydłowska , P. Mooyman , H. van Megen , S. van den Elsen , M. Vervoort , P. Veenhuizen , J. van Doorn , R. Dees , G. Karssen , J. Bakker and J. Helder (2012). Small subunit ribosomal DNA-based phylogenetic analysis of foliar nematodes (Aphelenchoides spp.) and their quantitative detection in complex DNA backgrounds. Phytopathology 102, 11531160. doi: 10.1094/PHYTO-05-12-0114-R.

M. A. Sacco , K. Koropacka , E. Grenier , M. J. Jaubert , A. Blanchard , A. Goverse , G. Smant and P. Moffett (2009). The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathogens 5, e1000564. doi: 10.1371/journal.ppat.1000564.

G. Schönknecht , A. P. M. Weber and M. J. Lercher (2014). Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 36, 920. doi: 10.1002/bies.201300095.

V. K. Sharma , J. Ramirez and J. C. Fletcher (2003). The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Molecular Biology 51, 415425. doi: 10.1023/A:1022038932376.

S. Sikora , A. Strongin and A. Godzik (2005). Convergent evolution as a mechanism for pathogenic adaptation. Trends in Microbiology 13, 522527. doi: 10.1016/j.tim.2005.08.010.

G. Smant , J. P. Stokkermans , Y. Yan , J. M. de Boer , T. J. Baum , X. Wang , R. S. Hussey , F. J. Gommers , B. Henrissat , E. L. Davis , J. Helder , A. Schots and J. Bakker (1998). Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proceedings of the National Academy of Sciences USA 95, 49064911.

P. W. Sternberg (2005). Vulval development. WormBook. doi: 10.1895/wormbook.1.6.1.

The C. elegans Genome Sequencing Consortium (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 20122018.

H. Van Megen , S. van den Elsen , M. Holterman , G. Karssen , P. Mooyman , T. Bongers , O. Holovachov , J. Bakker and J. Helder (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11, 927950.

J. Wang , C. Lee , A. Replogle , S. Joshi , D. Korkin , R. Hussey , T. J. Baum , E. L. Davis , X. Wang and M. G. Mitchum (2010). Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytologist 187, 10031017. doi: 10.1111/j.1469-8137.2010.03300.x.

X. Wang , M. G. Mitchum , B. Gao , C. Li , H. Diab , T. J. Baum , R. S. Hussey and E. L. Davis (2005). A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology 6, 187191. doi: 10.1111/j.1364-3703.2005.00270.x.

H. Watanabe and G. Tokuda (2010). Cellulolytic systems in insects. Annual Review of Entomology 55, 609632. doi: 10.1146/annurev-ento-112408-085319.

R. R. Weerasinghe , D. M. Bird and N. S. Allen (2005). Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proceedings of the National Academy of Sciences USA 102, 31473152. doi: 10.1073/pnas.0407926102.

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