Suppression of plant defences by plant-parasitic nematodes

Advances in Botanical Research

Volumn 73, Issue , 2015, Pages 325-337

  Mantelin, Sophie ^a   Thorpe, Peter ^a   Jones, John T ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Cell biology; Effectors; SPRYSEC; Suppression of plant cell death

Indexed keywords

EID: 84925938536     PISSN: 00652296     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.abr.2014.12.011     Document Type: Article

References (54)

1. Abad P., Gouzy J., Aury J.-M., Castagnone-Sereno P., Danchin E.G.J., Deleury E., et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 2008, 26:909-915.
2. Albert M. Peptides as triggers of plant defence. Journal of Experimental Botany 2013, 64:5269-5279.
3. Aslam S., Newman M., Erbs G., Morrissey K., Chinchilla D., Boller T., et al. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Current Biology 2008, 18:1078-1083.
4. Bauters L., Haegeman A., Kyndt T., Gheysen G. Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival strategies and host-nematode interactions. Molecular Plant Pathology 2014, 15:352-363.
5. Bellafiore S., Shen Z.X., Rosso M.N., Abad P., Shih P., Briggs S.P. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathogens 2008, 4:e1000192.
6. Boatwright J.L., Pajerowska-Mukhtar K. Salicylic acid: an old hormone up to new tricks. Molecular Plant Pathology 2013, 14:623-634.
7. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 2009, 60:379-406.
8. Bos J.I., Armstrong M.R., Gilroy E.M., Boevink P.C., Hein I., Taylor R.M., et al. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:9909-9914.
9. Chen S., Chronis D., Wang X. The novel GrCEP12 peptide from the plant-parasitic nematode Globodera rostochiensis suppresses flg22-mediated PTI. Plant Signaling and Behavior 2013, 8:e25359.
10. Chronis D., Chen S., Lu S., Hewezi T., Carpenter S.C.D., Loria R., et al. Aubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. The Plant Journal 2013, 74:185-196.
11. Cook D.E., Lee T.G., Guo X.L., Melito S., Wang K., Bayless A.M., et al. Copy number variation of multiple genes in Rhg1 mediates nematode resistance in soybean. Science 2012, 338:1206-1209.
12. Cotton J.A., Lilley C.J., Jones L.M., Kikuchi T., Reid A.J., Thorpe P., et al. The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 2014, 15:R43.
13. Dempsey D.A., Vlot A.C., Wildermuth M.C., Klessig D.F. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 2011, 9:e0156.
14. Doyle E.A., Lambert K.N. Meloidogyne javanica chorismate mutase 1 alters plant cell development. Molecular Plant-Microbe Interactions 2003, 16:123-131.
15. Dubreuil G., Magliano M., Dubrana M., Lozano J., Lecomte P., Favery B., et al. Tobacco rattle virus mediates gene silencing in a plant parasitic root-knot nematode. Journal of Experimental Botany 2009, 60:4041-4050.
16. Elmore J.M., Lin Z.-J.D., Coaker G. Plant NB-LRR signaling: upstreams and downstreams. Current Opinion in Plant Biology 2011, 14:365-371.
17. Eves-van den Akker S., Lilley C.J., Jones J.T., Urwin P.E. Identification and characterisation of a hyper variable apoplastic effector gene family of G. pallida. PLoS Pathogens 2014, 10(9):e1004391.
18. Fu Z.Q., Dong X. Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 2013, 64:839-863.
19. Gao B., Allen R., Maier T., Davis E.L., Baum T.J., Hussey R.S. The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 2003, 16:720-726.
20. Gheysen G., Jones J.T. Molecular aspects of plant-nematode interactions. Plant nematology 2013, CAN International, Wallingford, UK. 2nd ed. R.N. Perry, M. Moens (Eds.).
21. Gimenez-Ibanez S., Hann D.R., Ntoukakis V., Petutschnig E., Lipka V., Rathjen J.P. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Current Biology 2009, 19:423-429.
22. Goehre V., Spallek T., Haeweker H., Mersmann S., Mentzel T., Boller T., et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Current Biology 2008, 18:1824-1832.
23. Haegeman A., Jones J.T., Danchin E. Horizontal gene transfer in nematodes: a catalyst for plant parasitism?. Molecular Plant-Microbe Interactions 2011, 24:879-887.
24. Haegeman A., Mantelin S., Jones J.T., Gheysen G. Secretions of plant parasitic nematodes. Gene 2012, 492:19-31.
25. Hamamouch N., Li C., Hewezi T., Baum T.J., Mitchum M.G., Hussey R.S., et al. The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1,3-endoglucanase may suppress host defence to promote parasitism. Journal of Experimental Botany 2012, 63:3683-3695.
26. Hewezi T., Howe P.J., Maier T.R., Hussey R.S., Mitchum M.G., Davis E.L., et al. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiology 2010, 152:968-984.
27. Iberkleid I., Vieira P., de Almeida Engeler J., Firester K., Spiegel Y., Brown Horowitz S. Fatty acid- and retinol- binding protein MjFAR-1 induced tomato host susceptibility to root-knot nematodes. PLoS One 2013, 8(5):e64586.
28. Jaouannet M., Maglianao M., Arguel M.J., Gourges M., Evangelisti E., Abad P., et al. The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions 2012, 26:97-105.
29. Jaubert S., Milac A.L., Petrescu A.J., de Almeida-Engler J., Abad P., Rosso M.N. In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Molecular Plant-Microbe Interactions 2005, 18:1277-1284.
30. Jones J.D.G., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
31. Jones J.T., Reavy B., Smant G., Prior A.E. Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 2004, 324:47-54.
32. Kikuchi T., Cotton J.A., Dalzell J.J., Hasegawa K., Kanzaki N., McVeigh P., et al. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 2011, 7:e1002219.
33. Liu S., Kandoth P.K., Warren S.D., Yeckel G., Heinz R., Alden J., et al. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 2012, 492:256-260.
34. Lozano-Torres J.L., Wilbers R.H.P., Gawronski P., Boshoven J.C., Finkers-Tomczak A., Cordewener J.H.G., et al. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:10119-10124.
35. Mei Y., Thorpe P., Guzha A., Haegeman A., Blok V.C., MacKenzie K., et al. 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 -in press 2015.
36. Milligan S.B., Bodeau J., Yaghoobi J., Kaloshian I., Zabel P., Williamson V.M. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine- rich repeat family of plant genes. Plant Cell 1998, 10:1307-1319.
37. Mukhtar M.S., Carvunis A.-R., Dreze M., Epple P., Steinbrenner J., Moore J., et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 2011, 333:596-601.
38. Opperman C.H., Bird D.M., Williamson V.M., Rokhsar D.S., Burke M., Cohn J., et al. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:14802-14807.
39. Postma W.J., Slootweg E.J., Rehman S., Finkers-Tomczak A., Tytgat T.O.G., van Gelderen K., et al. The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR mediated disease resistance in plants. Plant Physiology 2012, 160:944-954.
40. Prior A.E., Jones J.T., Blok V.C., Beauchamp J., McDermott L., Cooper A., et al. A surface-associated retinol- and fatty acid-binding protein (GpLBP20) from the potato cyst nematode Globodera pallida - lipid binding activities, structural analysis and expression pattern. Biochemical Journal 2001, 356:387-394.
41. Robertson L., Robertson W.M., Sobczak M., Bakker J., Tetaud E., Arinagayayam M.R., et al. Cloning, expression and functional characterisation of a thioredoxin peroxidase from the potato cyst nematode Globodera rostochiensis. Molecular and Biochemical Parasitology 2000, 111:41-49.
42. Rosebrock T.R., Zeng L., Brady J.J., Abramovitch R.B., Xiao F., Martin G.B. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 2007, 448:370-374.
43. Rossi M., Goggin F.L., Milligan S.B., Kaloshian I., Ullman D.E., Williamson V.M. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:9750-9754.
44. Sacco M.A., Koropacka K., Grenier E., Jaubert M.J., Blanchard A., Goverse A., et al. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2-and RanGAP2-dependent plant cell death. PLoS Pathogens 2009, 5:e1000564.
45. Semblat J.P., Rosso M.N., Hussey R.S., Abad P., Castagnone-Sereno P. Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 2001, 14:72-79.
46. Smant G., Jones J.T. Suppression of plant defences by nematodes. Genomics and molecular genetics of plant-nematode interactions 2011, 273-286. Springer Academic Publishers. J.T. Jones, G. Gheysen, C. Fenoll (Eds.).
47. Sobczak M., Avrova A., Jupowicz J., Phillips M.S., Ernst K., Kumar A. Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Molecular Plant-Microbe Interactions 2005, 18:158-168.
48. Thorpe P., Mantelin S., Cock P.J.A., Blok V.C., Coke M.C., Cotton J.A., et al. Characterisation of the full effector complement of the potato cyst nematode Globodera pallida. BMC Genomics 2014, 15:923.
49. Trujillo M., Shirasu K. Ubiquitination in plant immunity. Current Opinion in Plant Biology 2010, 13:402-408.
50. Tytgat T., Vanholme B., De Meutter J., Claeys M., Couvreur M., Vanhoutte I., et al. A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Molecular Plant-Microbe Interactions 2004, 17:846-852.
51. Uehara T., Sugiyama S., Matsuura H., Arie T., Masuta C. Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant and Cell Physiology 2010, 51:1524-1536.
52. Vieira P., Danchin E.G.J., Neveu C., Crozat C., Jaubert S., Hussey R.S., et al. The plant apoplasm is an important recipient compartment for nematode secreted proteins. Journal of Experimental Botany 2011, 62:1241-1253.
53. Vierstra R.D. The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews Molecular Cell Biology 2009, 10:385-397.
54. Zipfel C. Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology 2009, 12:414-420.