Skip to main content Accessibility help
×
Home

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)...

Summary

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.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Signatures of adaptation to plant parasitism in nematode genomes
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Signatures of adaptation to plant parasitism in nematode genomes
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Signatures of adaptation to plant parasitism in nematode genomes
      Available formats
      ×

Copyright

The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution licence http://creativecommons.org/licenses/by/3.0/

Corresponding author

* Corresponding author: INRA, 400 route des Chappes, BP167, F-06903, Sophia-Antipolis, France. E-mail: etienne.danchin@gmail.com

References

Hide All
Abad, P., Gouzy, J., Aury, J.-M., Castagnone-Sereno, P., Danchin, E. G. J., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V. C., Caillaud, M.-C., Coutinho, P. M., Dasilva, C., Luca, F. D., Deau, F., Esquibet, M., Flutre, T., Goldstone, J. V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T. R., Markov, G. V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., Sallet, E., Ségurens, B., Steinbach, D., Tytgat, T., Ugarte, E., van Ghelder, C., Veronico, P., Baum, T. J., Blaxter, M., Bleve-Zacheo, T., Davis, E. L., Ewbank, J. J., Favery, B., Grenier, E., Henrissat, B., Jones, J. T., Laudet, V., Maule, A. G., Quesneville, H., Rosso, M.-N., Schiex, T., Smant, G., Weissenbach, J. and Wincker, P. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita . Nature Biotechnology 26, 909915. doi: 10.1038/nbt.1482.
Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. Cellular and Molecular Life Sciences 62, 11821197.
Baldwin, J. G., Nadler, S. A. and Adams, B. J. (2004). Evolution of plant parasitism among nematodes. Annual Review of Phytopathology 42, 83105.
Bird, D. M. (1996). Manipulation of host gene expression by root-knot nematodes. Journal of Parasitology 82, 881888.
Bird, D. M. (2004). Signaling between nematodes and plants. Current Opinion in Plant Biology 7, 372376. doi: 10.1016/j.pbi.2004.05.005.
Blaxter, M. (2011). Nematodes: the worm and its relatives. PLoS Biology 9, e1001050. doi: 10.1371/journal.pbio.1001050.
Blaxter, M. L., Ley, P. D., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175. doi: 10.1038/32160.
Blok, V. C., Jones, J. T., Phillips, M. S. and Trudgill, D. L. (2008). Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. Bioessays 30, 249259.
Bobay, B., DiGennaro, P., Scholl, E., Imin, N., Djordjevic, M. and Bird, D. M. (2013). Solution NMR studies of the plant peptide hormone CEP inform function. FEBS Letters 587, 39793985. doi: 10.1016/j.febslet.2013.10.033.
Boucher, Y., Douady, C. J., Papke, R. T., Walsh, D. A., Boudreau, M. E., Nesbo, C. L., Case, R. J. and Doolittle, W. F. (2003). Lateral gene transfer and the origins of prokaryotic groups. Annual Review of Genetics 37, 283328.
Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V. and Henrissat, B. (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 37, D233D238.
Castagnone-Sereno, P., Danchin, E. G., Perfus-Barbeoch, L. and Abad, P. (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.
Chronis, D., Chen, S., Lu, S., Hewezi, T., Carpenter, S. C. D., Loria, R., Baum, T. J. and Wang, X. (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.
Danchin, E. G., Rosso, M. N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B. and Abad, P. (2010). Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proceedings of the National Academy of Sciences USA 107, 1765117656.
Danchin, É. G. J. (2011). What nematode genomes tell us about the importance of horizontal gene transfers in the evolutionary history of animals. Mobile Genetic Elements 1, 269273.
Danchin, E. G. J. and Rosso, M.-N. (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.
Davis, E. L., Hussey, R. S., Mitchum, M. G. and Baum, T. J. (2008). Parasitism proteins in nematode–plant interactions. Current Opinion in Plant Biology 11, 360366. doi: 10.1016/j.pbi.2008.04.003.
De Ley, P. (2006). A quick tour of nematode diversity and the backbone of nematode phylogeny. WormBook: the Online Review of C. elegans Biology 18. doi: 10.1895/wormbook.1.41.1.
Desjardins, C. A., Cerqueira, G. C., Goldberg, J. M., Hotopp, J. C. D., Haas, B. J., Zucker, J., Ribeiro, J. M. C., Saif, S., Levin, J. Z., Fan, L., Zeng, Q., Russ, C., Wortman, J. R., Fink, D. L., Birren, B. W. and Nutman, T. B. (2013). Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature Genetics 45, 495500. doi: 10.1038/ng.2585.
Dieterich, C., Clifton, S. W., Schuster, L. N., Chinwalla, A., Delehaunty, K., Dinkelacker, I., Fulton, L., Fulton, R., Godfrey, J., Minx, P., Mitreva, M., Roeseler, W., Tian, H., Witte, H., Yang, S. P., Wilson, R. K. and Sommer, R. J. (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 11931198.
Doyle, E. A. and Lambert, K. N. (2002). Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica . Molecular Plant Microbe Interactions 15, 549556.
Dunning Hotopp, J. C. (2011). Horizontal gene transfer between bacteria and animals. Trends in Genetics 27, 157163. doi: 10.1016/j.tig.2011.01.005.
Ejima, C., Uwatoko, T., Ngan, B. T., Honda, H., Shimizu, N., Kiyohara, S., Hamasaki, R. and Sawa, S. (2011). SNPs of CLAVATA receptors in tomato, in the context of root-knot nematode infection. Nematological Research 41, 3540.
Elsworth, B., Wasmuth, J. and Blaxter, M. (2011). NEMBASE4: the nematode transcriptome resource. International Journal for Parasitology 41, 881894. doi: 10.1016/j.ijpara.2011.03.009.
Gao, B., Allen, R., Maier, T., Davis, E. L., Baum, T. J. and Hussey, R. S. (2003). The parasitome of the phytonematode Heterodera glycines . Molecular Plant Microbe Interactions 16, 720726.
Gardiner, D. M., McDonald, M. C., Covarelli, L., Solomon, P. S., Rusu, A. G., Marshall, M., Kazan, K., Chakraborty, S., McDonald, B. A. and Manners, J. M. (2012). Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathogens 8, e1002952. doi: 10.1371/journal.ppat.1002952.
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi . Science 317, 17561760.
Gogarten, J. P. and Townsend, J. P. (2005). Horizontal gene transfer, genome innovation and evolution. Nature Reviews Microbiology 3, 679687. doi: 10.1038/nrmicro1204.
Haegeman, A., Joseph, S. and Gheysen, G. (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.
Haegeman, A., Jones, J. T. and Danchin, E. G. (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.
Haegeman, A., Bauters, L., Kyndt, T., Rahman, M. M. and Gheysen, G. (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.
Hirakawa, Y., Shinohara, H., Kondo, Y., Inoue, A., Nakanomyo, I., Ogawa, M., Sawa, S., Ohashi-Ito, K., Matsubayashi, Y. and Fukuda, H. (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.
Hirsch, S., Kim, J., Muñoz, A., Heckmann, A. B., Downie, J. A. and Oldroyd, G. E. D. (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.
Huang, G., Gao, B., Maier, T., Allen, R., Davis, E. L., Baum, T. J. and Hussey, R. S. (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.
Huang, G., Dong, R., Allen, R., Davis, E. L., Baum, T. J. and Hussey, R. S. (2006). A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Molecular Plant Microbe Interactions 19, 463470.
Jaouannet, M., Magliano, M., Arguel, M. J., Gourgues, M., Evangelisti, E., Abad, P. and Rosso, M. N. (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.
Jaubert, S., Laffaire, J. B., Abad, P. and Rosso, M. N. (2002). A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita . FEBS Letters 522, 109112.
Jex, A. R., Liu, S., Li, B., Young, N. D., Hall, R. S., Li, Y., Yang, L., Zeng, N., Xu, X., Xiong, Z., Chen, F., Wu, X., Zhang, G., Fang, X., Kang, Y., Anderson, G. A., Harris, T. W., Campbell, B. E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E. M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P. W., Yang, H., Wang, J., Wang, J. and Gasser, R. B. (2011). Ascaris suum draft genome. Nature 479, 529533. doi: 10.1038/nature10553.
Jones, J. T., Furlanetto, C. and Kikuchi, T. (2005). Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7, 641646.
Jones, J. T., Moens, M., Mota, M., Li, H. and Kikuchi, T. (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.
Judelson, H. S. (2012). Dynamics and innovations within oomycete genomes: insights into biology, pathology, and evolution. Eukaryotic Cell 11, 13041312. doi: 10.1128/EC.00155-12.
Kikuchi, T., Jones, J. T., Aikawa, T., Kosaka, H. and Ogura, N. (2004). A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus . FEBS Letters 572, 201205.
Kikuchi, T., Cotton, J. A., Dalzell, J. J., Hasegawa, K., Kanzaki, N., McVeigh, P., Takanashi, T., Tsai, I. J., Assefa, S. A., Cock, P. J., Otto, T. D., Hunt, M., Reid, A. J., Sanchez-Flores, A., Tsuchihara, K., Yokoi, T., Larsson, M. C., Miwa, J., Maule, A. G., Sahashi, N., Jones, J. T. and Berriman, M. (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.
Kikuchi, T., Cock, P. J., Helder, J. and Jones, J. T. (2013). Characterisation of the transcriptome of Aphelenchoides besseyi and identification of a GHF 45 cellulase. Nematology. In press. http://booksandjournals.brillonline.com/content/journals/10.1163/15685411-00002748.
Kumar, S., Schiffer, P. H. and Blaxter, M. (2012). 959 nematode genomes: a semantic wiki for coordinating sequencing projects. Nucleic Acids Research 40, D1295D1300. doi: 10.1093/nar/gkr826.
Laing, R., Kikuchi, T., Martinelli, A., Tsai, I. J., Beech, R. N., Redman, E., Holroyd, N., Bartley, D. J., Beasley, H., Britton, C., Curran, D., Devaney, E., Gilabert, A., Hunt, M., Jackson, F., Johnston, S. L., Kryukov, I., Li, K., Morrison, A. A., Reid, A. J., Sargison, N., Saunders, G. I., Wasmuth, J. D., Wolstenholme, A., Berriman, M., Gilleard, J. S. and Cotton, J. A. (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.
Lambshead, P. J. D. (1993). Recent developments in marine benthic biodiversity research. Oceanis 19, 524.
Lambshead, P. J. D. and Boucher, G. (2003). Marine nematode deep-sea biodiversity – hyperdiverse or hype? Journal of Biogeography 30, 475485. doi: 10.1046/j.1365-2699.2003.00843.x.
Ledger, T. N., Jaubert, S., Bosselut, N., Abad, P. and Rosso, M. N. (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.
Lee, C., Chronis, D., Kenning, C., Peret, B., Hewezi, T., Davis, E. L., Baum, T. J., Hussey, R., Bennett, M. and Mitchum, M. G. (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.
Leroy, S., Duperray, C. and Morand, S. (2003). Flow cytometry for parasite nematode genome size measurement. Molecular and Biochemical Parasitology 128, 9193.
Lohar, D. P. and Bird, D. M. (2003). Lotus japonicus: a new model to study root-parasitic nematodes. Plant and Cell Physiology 44, 11761184.
Lu, S. W., Chen, S., Wang, J., Yu, H., Chronis, D., Mitchum, M. G. and Wang, X. (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.
Martin, J., Abubucker, S., Heizer, E., Taylor, C. M. and Mitreva, M. (2011). Nematode.net update 2011: addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Research 40, D720D728. doi: 10.1093/nar/gkr1194.
McCarter, J. P. (2009). Molecular approaches toward resistance to plant-parasitic nematodes. In Cell Biology of Plant Nematode Parasitism (ed. Berg, R. H. and Taylor, C. G.), pp. 239267. Springer, Berlin, Germany.
McCarter, J. P., Mitreva, M. D., Martin, J., Dante, M., Wylie, T., Rao, U., Pape, D., Bowers, Y., Theising, B., Murphy, C. V., Kloek, A. P., Chiapelli, B. J., Clifton, S. W., Bird, D. M. and Waterston, R. H. (2003). Analysis and functional classification of transcripts from the nematode Meloidogyne incognita . Genome Biology 4, R26.
Mitchum, M. G., Wang, X. and Davis, E. L. (2008). Diverse and conserved roles of CLE peptides. Current Opinion in Plant Biology 11, 7581. doi: 10.1016/j.pbi.2007.10.010.
Mitreva, M., Jasmer, D. P., Zarlenga, D. S., Wang, Z., Abubucker, S., Martin, J., Taylor, C. M., Yin, Y., Fulton, L., Minx, P., Yang, S.-P., Warren, W. C., Fulton, R. S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S. W., McCarter, J. P., Appleton, J., Mardis, E. R. and Wilson, R. K. (2011). The draft genome of the parasitic nematode Trichinella spiralis . Nature Genetics 43, 228235. doi: 10.1038/ng.769.
Mitreva-Dautova, M., Roze, E., Overmars, H., de Graaff, L., Schots, A., Helder, J., Goverse, A., Bakker, J. and Smant, G. (2006). A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita . Molecular Plant Microbe Interactions 19, 521529.
Ni, J., Guo, Y., Jin, H., Hartsell, J. and Clark, S. E. (2011). Characterization of a CLE processing activity. Plant Molecular Biology 75, 6775. doi: 10.1007/s11103-010-9708-2.
Nicol, P., Gill, R., Fosu-Nyarko, J. and Jones, M. G. K. (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.
Ohyama, K., Ogawa, M. and Matsubayashi, Y. (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.
Oliva, R., Win, J., Raffaele, S., Boutemy, L., Bozkurt, T. O., Chaparro-Garcia, A., Segretin, M. E., Stam, R., Schornack, S., Cano, L. M., Van Damme, M., Huitema, E., Thines, M., Banfield, M. J. and Kamoun, S. (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.
Olsen, A. N. and Skriver, K. (2003). Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends in Plant Science 8, 5557.
Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J., Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. (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.
Paganini, J., Campan-Fournier, A., Da Rocha, M., Gouret, P., Pontarotti, P., Wajnberg, E., Abad, P. and Danchin, E. G. J. (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.
Parkinson, J., Whitton, C., Schmid, R., Thomson, M. and Blaxter, M. (2004). NEMBASE: a resource for parasitic nematode ESTs. Nucleic Acids Research 32, D427D430.
Poinar, G., Kerp, H. and Hass, H. (2008). Palaeonema phyticum gen. n., sp. n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 10, 914.
Poinar, G. O. (2011). The Evolutionary History of Nematodes: As Revealed in Stone, Amber and Mummies. Brill, Leiden, the Netherlands.
Popeijus, H., Overmars, H., Jones, J., Blok, V., Goverse, A., Helder, J., Schots, A., Bakker, J. and Smant, G. (2000). Degradation of plant cell walls by a nematode. Nature 406, 3637.
Postma, W. J., Slootweg, E. J., Rehman, S., Finkers-Tomczak, A., Tytgat, T. O. G., van Gelderen, K., Lozano-Torres, J. L., Roosien, J., Pomp, R., van Schaik, C., Bakker, J., Goverse, A. and Smant, G. (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.
Qin, L., Kudla, U., Roze, E. H., Goverse, A., Popeijus, H., Nieuwland, J., Overmars, H., Jones, J. T., Schots, A., Smant, G., Bakker, J. and Helder, J. (2004). Plant degradation: a nematode expansin acting on plants. Nature 427, 30.
Robertson, L., López-Pérez, J. A., Bello, A., Díez-Rojo, M. A., Escuer, M., Piedra-Buena, A., Ros, C. and Martínez, C. (2006). Characterization of Meloidogyne incognita, M. arenaria and M. hapla populations from Spain and Uruguay parasitizing pepper (Capsicum annuum L.). Crop Protection 25, 440445.
Rosso, M. N., Favery, B., Piotte, C., Arthaud, L., De Boer, J. M., Hussey, R. S., Bakker, J., Baum, T. J. and Abad, P. (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.
Rybarczyk-Mydłowska, K., Mooyman, P., van Megen, H., van den Elsen, S., Vervoort, M., Veenhuizen, P., van Doorn, J., Dees, R., Karssen, G., Bakker, J. and Helder, J. (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.
Sacco, M. A., Koropacka, K., Grenier, E., Jaubert, M. J., Blanchard, A., Goverse, A., Smant, G. and Moffett, P. (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.
Schönknecht, G., Weber, A. P. M. and Lercher, M. J. (2014). Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 36, 920. doi: 10.1002/bies.201300095.
Sharma, V. K., Ramirez, J. and Fletcher, J. C. (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.
Sikora, S., Strongin, A. and Godzik, A. (2005). Convergent evolution as a mechanism for pathogenic adaptation. Trends in Microbiology 13, 522527. doi: 10.1016/j.tim.2005.08.010.
Smant, G., Stokkermans, J. P., Yan, Y., de Boer, J. M., Baum, T. J., Wang, X., Hussey, R. S., Gommers, F. J., Henrissat, B., Davis, E. L., Helder, J., Schots, A. and Bakker, J. (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.
Sternberg, P. W. (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.
Van Megen, H., van den Elsen, S., Holterman, M., Karssen, G., Mooyman, P., Bongers, T., Holovachov, O., Bakker, J. and Helder, J. (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11, 927950.
Wang, J., Lee, C., Replogle, A., Joshi, S., Korkin, D., Hussey, R., Baum, T. J., Davis, E. L., Wang, X. and Mitchum, M. G. (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.
Wang, X., Mitchum, M. G., Gao, B., Li, C., Diab, H., Baum, T. J., Hussey, R. S. and Davis, E. L. (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.
Watanabe, H. and Tokuda, G. (2010). Cellulolytic systems in insects. Annual Review of Entomology 55, 609632. doi: 10.1146/annurev-ento-112408-085319.
Weerasinghe, R. R., Bird, D. M. and Allen, N. S. (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.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed