Repeat-containing protein effectors of plant-associated organisms

Frontiers in Plant Science

Volumn 6, Issue OCTOBER, 2015, Pages

  Mesarich, Carl H ^a,b   Bowen, Joanna K ^b   Hamiaux, Cyril ^b   Templeton, Matthew D ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

Insects; Microbes; Nematodes; Plant associated organisms; Repeat containing protein effectors

Indexed keywords

EID: 84947445892     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00872     Document Type: Review

References (156)

1. Abramovitch, R. B., Janjusevic, R., Stebbins, C. E., and Martin, G. B. (2006). Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc. Natl. Acad. Sci. U.S.A. 103, 2851-2856. doi: 10.1073/pnas.0507892103
2. Abramovitch, R. B., Kim, Y.-J., Chen, S., Dickman, M. B., and Martin, G. B. (2003).Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69. doi: 10.1093/emboj/cdg006
3. Aggarwal, R., Subramanyam, S., Zhao, C., Chen, M. S., Harris, M. O., and Stuart, J. J. (2014). Avirulence effector discovery in a plant galling and plant parasitic arthropod, the Hessian fly (Mayetiola destructor). PLoS ONE 9:e100958. doi: 10.1371/journal.pone.0100958
4. Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., et al. (2004). Host-parasite coevolutionary conflict between Arabidopsisand downy mildew. Science 306, 1957-1960. doi: 10.1126/science.1104022
5. Allen, R. L., Meitz, J. C., Baumber, R. E., Hall, S. A., Lee, S. C., Rose, L. E., et al. (2008). Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol. Plant Pathol. 9, 511-523. doi: 10.1111/j.1364-3703.2008.00481.x
6. Angot, A., Peeters, N., Lechner, E., Vailleau, F., Baud, C., Gentzbittel, L., et al. (2006).Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc. Natl. Acad. Sci. U.S.A. 103, 14620-14625. doi: 10.1073/pnas.0509393103
7. Bailey, T. L., Johnson, J., Grant, C. E., and Noble, W. S. (2015). The MEME suite.Nucleic Acids Res. 43, W39-W49. doi: 10.1093/nar/gkv416
8. Block, A., and Alfano, J. R. (2011). Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Microbiol. 14, 39-46. doi: 10.1016/j.mib.2010.12.011
9. Boch, J., and Bonas, U. (2010). Xanthomonas AvrBs3 family-type III effectors: discovery and function. Ann. Rev. Phytopathol. 48, 419-436. doi: 10.1146/annurev-phyto-080508-081936
10. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., et al. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512. doi: 10.1126/science.1178811
11. Böhm, H., Albert, I., Fan, L., Reinhard, A., and Nürnberger, T. (2014). Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol. 20, 47-54. doi: 10.1016/j.pbi.2014.04.007
12. Bolton, M. D., van Esse, H. P., Vossen, J. H., de Jonge, R., Stergiopoulos, I., Stulemeijer, I. J., et al. (2008). The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69, 119-136. doi: 10.1111/j.1365-2958.2008.06270.x
13. Bos, J. I., Prince, D., Pitino, M., Maffei, M. E., Win, J., and Hogenhout, S. A. (2010). A functional genomics approach identifies candidate effectors from the aphid speciesMyzus persicae (green peach aphid). PLoS Genet. 6:e1001216. doi: 10.1371/journal.pgen.1001216
14. Boutemy, L. S., King, S. R. F., Win, J., Hughes, R. K., Clarke, T. A., Blumenschein, T. M. A., et al. (2011). Structures of Phytophthora RXLR effector proteins. J. Biol. Chem.286, 35834-35842. doi: 10.1074/jbc.M111.262303
15. Bozkurt, T. O., Schornack, S., Banfield, M. J., and Kamoun, S. (2012). Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15, 483-492. doi: 10.1016/j.pbi.2012.03.008
16. Brown, C. J., Johnson, A. K., Dunker, A. K., and Daughdrill, G. W. (2011). Evolution and disorder. Curr. Opin. Struct. Biol. 21, 441-446. doi: 10.1016/j.sbi.2011.02.005
17. Castagnone-Sereno, P., Semblat, J.-P., and Castagnone, C. (2009). Modular architecture and evolution of the map-1 gene family in the root-knot nematodeMeloidogyne incognita. Mol. Genet. Genomics 282, 547-554. doi: 10.1007/s00438-009-0487-x
18. Catanzariti, A.-M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., and Ellis, J. G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18, 243-256. doi: 10.1105/tpc.105.035980
19. Catanzariti, A.-M., Dodds, P. N., Ve, T., Kobe, B., Ellis, J. G., and Staskawicz, B. J. (2010). The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol. Plant Microbe Interact. 23, 49-57. doi: 10.1094/MPMI-23-1-0049
20. Chen, L. Q., Hou, B. H., Lalonde, S., Takanaga, H., Hartung, M. L., Qu, X. Q., et al. (2010). Sugar transporters for intercellular exchange and nutrition of pathogens.Nature 468, 527-532. doi: 10.1038/nature09606
21. Chen, S., Lang, P., Chronis, D., Zhang, S., De Jong, W. S., Mitchum, M. G., et al. (2015). In planta processing and glycosylation of a nematode CLAVATA3/ENDOSPERM SURROUNDING REGION-like effector and its interaction with a host CLAVATA2-like receptor to promote parasitism. Plant Physiol. 167, 262-272. doi: 10.1104/pp.114.251637
22. Cheng, W., Munkvold, K. R., Gao, H., Mathieu, J., Schwizer, S., Wang, S., et al. (2011). Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10, 616-626. doi: 10.1016/j.chom.2011.10.013
23. Chosed, R., Tomchick, D. R., Brautigam, C. A., Mukherjee, S., Negi, V. S., Machius, M., et al. (2007). Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitin-like protein proteases. J. Biol. Chem. 282, 6773-6782. doi: 10.1074/jbc.M608730200
24. Chou, S., Krasileva, K. V., Holton, J. M., Steinbrenner, A. D., Alber, T., and Staskawicz, B. J. (2011). Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc. Natl. Acad. Sci. U.S.A. 108, 13323-13328. doi: 10.1073/pnas.1109791108
25. Chu, Z., Yuan, M., Yao, J., Ge, X., Yuan, B., Xu, C., et al. (2006). Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 20, 1250-1255. doi: 10.1101/gad.1416306
26. Cui, H., Tsuda, K., and Parker, J. E. (2015). Effector-triggered immunity: from pathogen perception to robust defense. Ann. Rev. Plant Biol. 66, 487-511. doi: 10.1146/annurev-arplant-050213-040012
27. Cunnac, S., Occhialini, A., Barberis, P., Boucher, C., and Genin, S. (2004). Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol. Microbiol. 53, 115-128. doi: 10.1111/j.1365-2958.2004.04118.x
28. de Jonge, R., van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., et al. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953-955. doi: 10.1126/science.1190859
29. de Lange, O., Schreiber, T., Schandry, N., Radeck, J., Braun, K. H., Koszinowski, J., et al. (2013). Breaking the DNA-binding code of Ralstonia solanacearum TAL effectors provides new possibilities to generate plant resistance genes against bacterial wilt disease. New Phytol. 199, 773-786. doi: 10.1111/nph.12324
30. Deng, D., Yan, C., Pan, X., Mahfouz, M., Wang, J., Zhu, J. K., et al. (2012). Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335, 720-723. doi: 10.1126/science.1215670
31. Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644-655. doi: 10.1016/j.tplants.2012.06.011
32. de Torres, M., Mansfield, J. W., Grabov, N., Brown, I. R., Ammouneh, H., Tsiamis, G., et al. (2006). Pseudomonas syringae effector AvrPtoB suppresses basal defence inArabidopsis. Plant J. 47, 368-382. doi: 10.1111/j.1365-313X.2006.02798.x
33. Dong, J., Xiao, F., Fan, F., Gu, L., Cang, H., Martin, G. B., et al. (2009). Crystal structure of the complex between Pseudomonas effector AvrPtoB and the tomato Pto kinase reveals both a shared and a unique interface compared with AvrPto-Pto. Plant Cell 21, 1846-1859. doi: 10.1105/tpc.109.066878
34. Dong, S., Stam, R., Cano, L. M., Song, J., Sklenar, J., Yoshida, K., et al. (2014). Effector specialization in a lineage of the Irish potato famine pathogen. Science 343, 552-555. doi: 10.1126/science.1246300
35. Dou, D., and Zhou, J.-M. (2012). Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484-495. doi: 10.1016/j.chom.2012.09.003
36. Dyson, H. J., and Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208. doi: 10.1038/nrm1589
37. Elzinga, D. A., De Vos, M., and Jander, G. (2014). Suppression of plant defenses by aMyzus persicae (green peach aphid) salivary effector protein. Mol. Plant Microbe Interact. 27, 747-756. doi: 10.1094/MPMI-01-14-0018-R
38. Eves-van den Akker, S., Lilley, C. J., Jones, J. T., and Urwin, P. E. (2014). Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes. PLoS Pathog. 10:e1004391. doi: 10.1371/journal.ppat.1004391
39. Feng, F., Yang, F., Rong, W., Wu, X., Zhang, J., Chen, S., et al. (2012). A Xanthomonasuridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485, 114-118. doi: 10.1038/nature10962
40. Gao, H., Wu, X., Chai, J., and Han, Z. (2012). Crystal structure of a TALE protein reveals an extended N-terminal DNA binding region. Cell Res. 22, 1716-1720. doi: 10.1038/cr.2012.156
41. Gaulin, E., Dramé, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline-Torregrosa, C., et al. (2006). Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18, 1766-1777. doi: 10.1105/tpc.105.038687
42. Gaulin, E., Jauneau, A., Villalba, F., Rickauer, M., Esquerré-Tugayé, M. T., and Bottin, A. (2002). The CBEL glycoprotein of Phytophthora parasitica var-nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. J. Cell Sci. 115, 4565-4575. doi: 10.1242/jcs.00138
43. Gemayel, R., Vinces, M. D., Legendre, M., and Verstrepen, K. J. (2010). Variable tandem repeats accelerate evolution of coding and regulatory sequences. Ann. Rev. Genet. 44, 445-477. doi: 10.1146/annurev-genet-072610-155046
44. Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., et al. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824-1832. doi: 10.1016/j.cub.2008.10.063
45. Gimenez-Ibanez, S., Hann, D. R., Ntoukakis, V., Petutschnig, E., Lipka, V., and Rathjen, J. P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423-429. doi: 10.1016/j.cub.2009.01.054
46. Goss, E. M., Press, C. M., and Grünwald, N. J. (2013). Evolution of RXLR-class effectors in the oomycete plant pathogen Phytophthora ramorum. PLoS ONE8:e79347. doi: 10.1371/journal.pone.0079347
47. Görnhardt, B., Rouhara, I., and Schmelzer, E. (2000). Cyst germination proteins of the potato pathogen Phytophthora infestans share homology with human mucins. Mol. Plant Microbe Interact. 13, 32-42. doi: 10.1094/MPMI.2000.13.1.32
48. Grove, T. Z., Cortajarena, A. L., and Regan, L. (2008). Ligand binding by repeat proteins: natural and designed. Curr. Opin. Struct. Biol. 18, 507-515. doi: 10.1016/j.sbi.2008.05.008
49. Guo, Y., Ni, J., Denver, R., Wang, X., and Clark, S. E. (2011). Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis. Plant Phys. 157, 476-484. doi: 10.1104/pp.111.180554
50. Gust, A. A., Willmann, R., Desaki, Y., Grabherr, H. M., and Nürnberger, T. (2012). Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci.17, 495-502. doi: 10.1016/j.tplants.2012.04.003
51. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., and Greenberg, J. T. (2002). A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295, 1722-1726. doi: 10.1126/science.295.5560.1722
52. Guy, E., Lautier, M., Chabannes, M., Roux, B., Lauber, E., Arlat, M., et al. (2013).xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLoS ONE 8:e73469. doi: 10.1371/journal.pone.0073469
53. He, P., Shan, L., Lin, N. C., Martin, G. B., Kemmerling, B., Nürnberger, T., et al. (2006). Specific bacterial suppressors of MAMP signaling upstream of MAPKKK inArabidopsis innate immunity. Cell 125, 563-575. doi: 10.1016/j.cell.2006.02.047
54. Herbers, K., Conrads-Strauch, J., and Bonas, U. (1992). Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356, 172-174. doi: 10.1038/356172a0
55. Heuer, H., Yin, Y. N., Xue, Q. Y., Smalla, K., and Guo, J. H. (2007). Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Appl. Environ. Microbiol. 73, 4379-4384. doi: 10.1128/AEM.00367-07
56. Hogenhout, S. A., van der Hoorn, R. A. L., Terauchi, R., and Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22, 115-122. doi: 10.1094/MPMI-22-2-0115
57. Hotson, A., Chosed, R., Shu, H., Orth, K., and Mudgett, M. B. (2003). Xanthomonastype III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol.50, 377-389. doi: 10.1046/j.1365-2958.2003.03730.x
58. Janjusevic, R., Abramovitch, R. B., Martin, G. B., and Stebbins, C. E. (2006). A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase.Science 311, 222-226. doi: 10.1126/science.1120131
59. Jaouannet, M., Rodriguez, P. A., Thorpe, P., Lenoir, C. J., MacLeod, R., Escudero-Martinez, C., et al. (2014). Plant immunity in plant-aphid interactions. Front. Plant Sci. 5:663. doi: 10.3389/fpls.2014.00663
60. Jelenska, J., van Hal, J. A., and Greenberg, J. T. (2010). Pseudomonas syringaehijacks plant stress chaperone machinery for virulence. Proc. Natl. Acad. Sci. U.S.A.107, 13177-13182. doi: 10.1073/pnas.0910943107
61. Jelenska, J., Yao, N., Vinatzer, B. A., Wright, C. M., Brodsky, J. L., and Greenberg, J. T. (2007). A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17, 499-508. doi: 10.1016/j.cub.2007.02.028
62. Jiang, R. H., Tripathy, S., Govers, F., and Tyler, B. M. (2008). RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc. Natl. Acad. Sci. U.S.A. 105, 4874-4879. doi: 10.1073/pnas.0709303105
63. Kajava, A. V. (2012). Tandem repeats in proteins: from sequence to structure. J. Struct. Biol. 179, 279-288. doi: 10.1016/j.jsb.2011.08.009
64. Kappel, C., Zachariae, U., Dölker, N., and Grubmüller, H. (2010). An unusual hydrophobic core confers extreme flexibility to HEAT repeat proteins. Biophys. J. 99, 1596-1603. doi: 10.1016/j.bpj.2010.06.032
65. Kay, S., Hahn, S., Marois, E., Hause, G., and Bonas, U. (2007). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318, 648-651. doi: 10.1126/science.1144956
66. Khatib, M., Lafitte, C., Esquerré-Tugayé, M.-T., Bottin, A., and Rickauer, M. (2004). The CBEL elicitor of Phytophthora parasitica var. nicotianae activates defence inArabidopsis thaliana via three different signalling pathways. New Phytol. 162, 501-510. doi: 10.1111/j.1469-8137.2004.01043.x
67. Kim, J. G., Li, X., Roden, J. A., Taylor, K. W., Aakre, C. D., Su, B., et al. (2009).Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21, 1305-1323. doi: 10.1105/tpc.108.063123
68. Kim, J.-G., Stork, W., and Mudgett, M. B. (2013). Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13, 143-154. doi: 10.1016/j.chom.2013.01.006
69. Kim, J.-G., Taylor, K. W., Hotson, A., Keegan, M., Schmelz, E. A., and Mudgett, M. B. (2008). XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell20, 1915-1929. doi: 10.1105/tpc.108.058529
70. Kim, Y. J., Lin, N.-C., and Martin, G. B. (2002). Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109, 589-598. doi: 10.1016/S0092-8674(02)00743-2
71. Kloppholz, S., Kuhn, H., and Requena, N. (2011). A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204-1209. doi: 10.1016/j.cub.2011.06.044
72. Krasileva, K. V., Dahlbeck, D., and Staskawicz, B. J. (2010). Activation of anArabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22, 2444-2458. doi: 10.1105/tpc.110.075358
73. Kucheryava, N., Bowen, J. K., Sutherland, P. W., Conolly, J. J., Mesarich, C. H., Rikkerink, E. H., et al. (2008). Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane.Fungal Genet. Biol. 45, 1329-1339. doi: 10.1016/j.fgb.2008.07.010
74. Kucukoglu, M., and Nilsson, O. (2015). CLE peptide signaling in plants - the power of moving around. Physiol. Plant. 155, 74-87. doi: 10.1111/ppl.12358
75. Laluk, K., Abuqamar, S., and Mengiste, T. (2011). The Arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Phys. 156, 2053-2068. doi: 10.1104/pp.111.177501
76. Lanver, D., Berndt, P., Tollot, M., Naik, V., Vranes, M., Warmann, T., et al. (2014). Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog.10:e1004272. doi: 10.1371/journal.ppat.1004272
77. Lanver, D., Mendoza-Mendoza, A., Brachmann, A., and Kahmann, R. (2010). Sho1 and Msb2-related proteins regulate appressorium development in the smut fungusUstilago maydis. Plant Cell 22, 2085-2101. doi: 10.1105/tpc.109.073734
78. Leonelli, L., Pelton, J., Schoeffler, A., Dahlbeck, D., Berger, J., Wemmer, D. E., et al. (2011). Structural elucidation and functional characterization of theHyaloperonospora arabidopsidis effector protein ATR13. PLoS Pathog. 7:e1002428. doi: 10.1371/journal.ppat.1002428
79. Li, L., Atef, A., Piatek, A., Ali, Z., Piatek, M., Aouida, M., et al. (2013). Characterization and DNA-binding specificities of Ralstonia TAL-like effectors. Mol. Plant 6, 1318-1330. doi: 10.1093/mp/sst006
80. Lo Presti, L., Lanver, D., Schweizer, G., Tanaka, S., Liang, L., Tollot, M., et al. (2015). Fungal effectors and plant susceptibility. Ann. Rev. Plant Biol. 66, 513-545. doi: 10.1146/annurev-arplant-043014-114623
81. Lu, S. W., Chen, S., Wang, J., Yu, H., Chronis, D., Mitchum, M. G., et al. (2009). Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol. Plant Microbe Interact. 22, 1128-1142. doi: 10.1094/MPMI-22-9-1128
82. Luo, H., and Nijveen, H. (2014). Understanding and identifying amino acid repeats.Brief. Bioinformatics. 15, 582-591. doi: 10.1093/bib/bbt003
83. Macho, A. P., Guidot, A., Barberis, P., Beuzón, C. R., and Genin, S. (2010). A competitive index assay identifies several Ralstonia solanacearum type III effector mutant strains with reduced fitness in host plants. Mol. Plant Microbe Interact. 23, 1197-1205. doi: 10.1094/MPMI-23-9-1197
84. Madoff, L. C., Michel, J. L., Gong, E. W., Kling, D. E., and Kasper, D. L. (1996). Group B streptococci escape host immunity by deletion of tandem repeat elements of the alpha C protein. Proc. Natl. Acad. Sci. U.S.A. 93, 4131-4136. doi: 10.1073/pnas.93.9.4131
85. Mak, A. N., Bradley, P., Cernadas, R. A., Bogdanove, A. J., and Stoddard, B. L. (2012). The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335, 716-719. doi: 10.1126/science.1216211
86. Marín, M., and Ott, T. (2014). Intrinsic disorder in plant proteins and phytopathogenic bacterial effectors. Chem. Rev. 114, 6912-6932. doi: 10.1021/cr400488d
87. Marín, M., Uversky, V. N., and Ott, T. (2013). Intrinsic disorder in pathogen effectors: protein flexibility as an evolutionary hallmark in a molecular arms race. Plant Cell 25, 3153-3157. doi: 10.1105/tpc.113.116319
88. Marois, E., Van den Ackerveken, G., and Bonas, U. (2002). The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol. Plant Microbe Interact. 15, 637-646. doi: 10.1094/MPMI.2002.15.7.637
89. Mathieu, J., Schwizer, S., and Martin, G. B. (2014). Pto kinase binds two domains of AvrPtoB and its proximity to the effector E3 ligase determines if it evades degradation and activates plant immunity. PLoS Pathog. 10:e1004227. doi: 10.1371/journal.ppat.1004227
90. Mendes, T. A., Lobo, F. P., Rodrigues, T. S., Rodrigues-Luiz, G. F., daRocha, W. D., Fujiwara, R. T., et al. (2013). Repeat-enriched proteins are related to host cell invasion and immune evasion in parasitic protozoa. Mol. Biol. Evol. 30, 951-963. doi: 10.1093/molbev/mst001
91. Mesarich, C. H., Schmitz, M., Tremouilhac, P., McGillivray, D. J., Templeton, M. D., and Dingley, A. J. (2012). Structure, dynamics and domain organization of the repeat protein Cin1 from the apple scab fungus. BBA Proteins Proteom. 1824, 1118-1128. doi: 10.1016/j.bbapap.2012.06.015
92. Mitchum, M. G., Hussey, R. S., Baum, T. J., Wang, X., Elling, A. A., Wubben, M., et al. (2013). Nematode effector proteins: an emerging paradigm of parasitism. New Phytol.199, 879-894. doi: 10.1111/nph.12323
93. Moscou, M. J., and Bogdanove, A. J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501. doi: 10.1126/science.1178817
94. Mucyn, T. S., Clemente, A., Andriotis, V. M., Balmuth, A. L., Oldroyd, G. E., Staskawicz, B. J., et al. (2006). The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18, 2792-2806. doi: 10.1105/tpc.106.044016
95. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., and de Vries, R. P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol.45(Suppl. 1), S63-S70. doi: 10.1016/j.fgb.2008.03.012
96. Mukaihara, T., and Tamura, N. (2009). Identification of novel Ralstonia solanacearum type III effector proteins through translocation analysis of hrpB-regulated gene products. Microbiology 155, 2235-2244. doi: 10.1099/mic.0.027763-0
97. Müller, O., Schreier, P. H., and Uhrig, J. F. (2008). Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol. Genet. Genomics 279, 27-39. doi: 10.1007/s00438-007-0291-4
98. Nilsson, J., Grahn, M., and Wright, A. P. H. (2011). Proteome-wide evidence for enhanced positive Darwinian selection within intrinsically disordered regions in proteins. Genome Biol. 12:R65. doi: 10.1186/gb-2011-12-7-r65
99. Nissan, G., Manulis-Sasson, S., Chalupowicz, L., Teper, D., Yeheskel, A., Pasmanik-Chor, M., et al. (2012). The type III effector HsvG of the gall-forming Pantoea agglomerans mediates expression of the host gene HSVGT. Mol. Plant Microbe Interact. 25, 231-240. doi: 10.1094/MPMI-06-11-0173
100. Nissan, G., Manulis-Sasson, S., Weinthal, D., Mor, H., Sessa, G., and Barash, I. (2006). The type III effectors HsvG and HsvB of gall-forming Pantoea agglomeransdetermine host specificity and function as transcriptional activators. Mol. Microbiol.61, 1118-1131. doi: 10.1111/j.1365-2958.2006.05301.x
101. Palma, K., Zhang, Y., and Li, X. (2005). An importin α homolog, MOS6, plays an important role in plant innate immunity. Curr. Biol. 15, 1129-1135. doi: 10.1016/j.cub.2005.05.022
102. Peeters, N., Carrère, S., Anisimova, M., Plener, L., Cazalé, A. C., and Genin, S. (2013). Repertoire, unified nomenclature and evolution of the Type III effector gene set in theRalstonia solanacearum species complex. BMC Genomics 14:859. doi: 10.1186/1471-2164-14-859
103. Petre, B., Lorrain, C., Saunders, D. G. O., Win, J., Sklenar, J., Duplessis, S., et al. (2015a). Rust fungal effectors mimic host transit peptides to translocate into chloroplasts. Cell. Microbiol. doi: 10.1111/cmi.12530. [Epub ahead of print].
104. Petre, B., Saunders, D. G., Sklenar, J., Lorrain, C., Win, J., Duplessis, S., et al. (2015b). Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. Mol. Plant Microbe Interact. 28, 689-700. doi: 10.1094/MPMI-01-15-0003-R
105. Pitino, M., Coleman, A. D., Maffei, M. E., Ridout, C. J., and Hogenhout, S. A. (2011). Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 6:e25709. doi: 10.1371/journal.pone.0025709
106. Pitino, M., and Hogenhout, S. A. (2013). Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol. Plant Microbe Interact. 26, 130-139. doi: 10.1094/MPMI-07-12-0172-FI
107. Pradhan, B. B., Ranjan, M., and Chatterjee, S. (2012). XadM, a novel adhesin ofXanthomonas oryzae pv. oryzae, exhibits similarity to Rhs family proteins and is required for optimum attachment, biofilm formation, and virulence. Mol. Plant Microbe Interact. 25, 1157-1170. doi: 10.1094/MPMI-02-12-0049-R
108. Raffaele, S., Win, J., Cano, L. M., and Kamoun, S. (2010). Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genomics 11:637. doi: 10.1186/1471-2164-11-637
109. Rafiqi, M., Gan, P. H. P., Ravensdale, M., Lawrence, G. J., Ellis, J. G., Jones, D. A., et al. (2010). Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22, 2017-2032. doi: 10.1105/tpc.109.072983
110. Rafiqi, M., Jelonek, L., Akum, N. F., Zhang, F., and Kogel, K.-H. (2013). Effector candidates in the secretome of Piriformospora indica, a ubiquitous plant-associated fungus. Front. Plant Sci. 4:228. doi: 10.3389/fpls.2013.00228
111. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., et al. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17, 1839-1850. doi: 10.1105/tpc.105.031807
112. Remigi, P., Anisimova, M., Guidot, A., Genin, S., and Peeters, N. (2011). Functional diversification of the GALA type III effector family contributes to Ralstonia solanacearum adaptation on different plant hosts. New Phytol. 192, 976-987. doi: 10.1111/j.1469-8137.2011.03854.x
113. Richard, G.-F., and Pâques, F. (2000). Mini- and microsatellite expansions: the recombination connection. EMBO Rep. 1, 122-126. doi: 10.1093/embo-reports/kvd031
114. Römer, P., Hahn, S., Jordan, T., Strauss, T., Bonas, U., and Lahaye, T. (2007). Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318, 645-648. doi: 10.1126/science.1144958
115. Römer, P., Strauss, T., Hahn, S., Scholze, H., Morbitzer, R., Grau, J., et al. (2009). Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol. 150, 1697-1712. doi: 10.1104/pp.109.139931
116. Robold, A. V., and Hardham, A. R. (2005). During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr. Genet. 47, 307-315. doi: 10.1007/s00294-004-0559-8
117. Roden, J. A., Belt, B., Ross, J. B., Tachibana, T., Vargas, J., and Mudgett, M. B. (2004). A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc. Natl. Acad. Sci. U.S.A. 101, 16624-16629. doi: 10.1073/pnas.0407383101
118. Rosebrock, T. R., Zeng, L., Brady, J. J., Abramovitch, R. B., Xiao, F., and Martin, G. B. (2007). A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448, 370-374. doi: 10.1038/nature05966
119. Rudd, J. J., Antoniw, J., Marshall, R., Motteram, J., Fraaije, B., and Hammond-Kosack, K. (2010). Identification and characterisation of Mycosphaerella graminicolasecreted or surface-associated proteins with variable intragenic coding repeats.Fungal Genet. Biol. 47, 19-32. doi: 10.1016/j.fgb.2009.10.009
120. Rutter, W. B., Hewezi, T., Maier, T. R., Mitchum, M. G., Davis, E. L., Hussey, R. S., et al. (2014). Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104, 879-885. doi: 10.1094/PHYTO-11-13-0326-R
121. Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D. J., Thomma, B. P., et al. (2013). Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2:e00790. doi: 10.7554/eLife.00790
122. Saunders, D. G., Win, J., Cano, L. M., Szabo, L. J., Kamoun, S., and Raffaele, S. (2012). Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS ONE 7:e29847. doi: 10.1371/journal.pone.0029847
123. Séjalon-Delmas, N., Mateos, F. V., Bottin, A., Rickauer, M., Dargent, R., and Esquerre-Tugaye, M. T. (1997). Purification, elicitor activity, and cell wall localization of a glycoprotein from Phytophthora parasitica var. nicotianae, a fungal pathogen of tobacco. Phytopathology 87, 899-909. doi: 10.1094/PHYTO.1997.87.9.899
124. Semblat, J. P., Rosso, M. N., Hussey, R. S., Abad, P., and Castagnone-Sereno, P. (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. doi: 10.1094/MPMI.2001.14.1.72
125. Shan, L., He, P., Li, J., Heese, A., Peck, S. C., Nürnberger, T., et al. (2008). Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17-27. doi: 10.1016/j.chom.2008.05.017
126. Singer, A. U., Schulze, S., Skarina, T., Xu, X., Cui, H., Eschen-Lippold, L., et al. (2013). A pathogen type III effector with a novel E3 ubiquitin ligase architecture. PLoS Pathog. 9:e1003121. doi: 10.1371/journal.ppat.1003121
127. Sohn, K. H., Lei, R., Nemri, A., and Jones, J. D. (2007). The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana.Plant Cell 19, 4077-4090. doi: 10.1105/tpc.107.054262
128. Steinbrenner, A. D., Goritschnig, S., and Staskawicz, B. J. (2015). Recognition and activation domains contribute to allele-specific responses of an Arabidopsis NLR receptor to an oomycete effector protein. PLoS Pathog. 11:e1004665. doi: 10.1371/journal.ppat.1004665
129. Stergiopoulos, I., De Kock, M. J. D., Lindhout, P., and De Wit, P. J. (2007). Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol. Plant Microbe Interact. 20, 1271-1283. doi: 10.1094/MPMI-20-10-1271
130. Taylor, K. W., Kim, J.-G., Su, X. B., Aakre, C. D., Roden, J. A., Adams, C. M., et al. (2012). Tomato TFT1 is required for PAMP-triggered immunity and mutations that prevent T3S effector XopN from binding to TFT1 attenuate Xanthomonas virulence.PLoS Pathog. 8:e1002768. doi: 10.1371/journal.ppat.1002768
131. Teertstra, W. R., Deelstra, H. J., Vranes, M., Bohlmann, R., Kahmann, R., Kämper, J., et al. (2006). Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis. Microbiology 152, 3607-3612. doi: 10.1099/mic.0.29034-0
132. Teertstra, W. R., van der Velden, G. J., de Jong, J. F., Kruijtzer, J. A., Liskamp, R. M., Kroon-Batenburg, L. M., et al. (2009). The filament-specific Rep1-1 repellent of the phytopathogen Ustilago maydis forms functional surface-active amyloid-like fibrils.J. Biol. Chem. 284, 9153-9159. doi: 10.1074/jbc.M900095200
133. Thomma, B. P. H. J., Nürnberger, T., and Joosten, M. H. A. J. (2011). Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4-15. doi: 10.1105/tpc.110.082602
134. Valinsky, L., Manulis, S., Nizan, R., Ezra, D., and Barash, I. (1998). A pathogenicity gene isolated from the pPATH plasmid of Erwinia herbicola pv. gypsophilae determines host specificity. Mol. Plant Microbe Interact. 11, 753-762. doi: 10.1094/MPMI.1998.11.8.753
135. Ve, T., Williams, S. J., Catanzariti, A.-M., Rafiqi, M., Rahman, M., Ellis, J. G., et al. (2013). Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity. Proc. Natl. Acad. Sci. U.S.A.110, 17594-17599. doi: 10.1073/pnas.1307614110
136. Verstrepen, K. J., and Fink, G. R. (2009). Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Ann. Rev. Genet. 43, 1-24. doi: 10.1146/annurev-genet-102108-134156
137. Vieira, P., Danchin, E. G. J., Neveu, C., Crozat, C., Jaubert, S., Hussey, R. S., et al. (2011). The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 62, 1241-1253. doi: 10.1093/jxb/erq352
138. Villalba Mateos, F., Rickauer, M., and Esquerré-Tugayé, M. T. (1997). Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol. Plant Microbe Interact. 10, 1045-1053. doi: 10.1094/MPMI.1997.10.9.1045
139. Wang, G., Roux, B., Feng, F., Guy, E., Li, L., Li, N., et al. (2015b). The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18, 285-295. doi: 10.1016/j.chom.2015.08.004
140. Wang, K., Remigi, P., Anisimova, M., Lonjon, F., Kars, I., Kajava, A., et al. (2015a). Functional assignment to positively selected sites in the core type III effector RipG7 from Ralstonia solanacearum. Mol.Plant Pathol. doi: 10.1111/mpp.12302. [Epub ahead of print].
141. Wang, Y.-S., Pi, L.-Y., Chen, X., Chakrabarty, P. K., Jiang, J., De Leon, A. L., et al. (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18, 3635-3646. doi: 10.1105/tpc.106.046730
142. White, F. F., Potnis, N., Jones, J. B., and Koebnik, R. (2009). The type III effectors ofXanthomonas. Mol. Plant Pathol. 10, 749-766. doi: 10.1111/j.1364-3703.2009.00590.x
143. Win, J., Chaparro-Garcia, A., Belhaj, K., Saunders, D. G., Yoshida, K., Dong, S., et al. (2012a). Effector biology of plant-associated organisms: concepts and perspectives.Cold Spring Harb. Symp. Quant. Biol. 77, 235-247. doi: 10.1101/sqb.2012.77.015933
144. Win, J., Krasileva, K. V., Kamoun, S., Shirasu, K., Staskawicz, B. J., and Banfield, M. J. (2012b). Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog. 8:e1002400. doi: 10.1371/journal.ppat.1002400
145. Win, J., Morgan, W., Bos, J., Krasileva, K. V., Cano, L. M., Chaparro-Garcia, A., et al. (2007). Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19, 2349-2369. doi: 10.1105/tpc.107.051037
146. Wösten, H. A., Bohlmann, R., Eckerskorn, C., Lottspeich, F., Bolker, M., and Kahmann, R. (1996). A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO J. 15, 4274-4281.
147. Xiao, F., He, P., Abramovitch, R. B., Dawson, J. E., Nicholson, L. K., Sheen, J., et al. (2007). The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant J. 52, 595-614. doi: 10.1111/j.1365-313X.2007.03259.x
148. Xcc8004, a type III effector with a leucine-rich repeat domain fromXanthomonas campestris pathovar campestris confers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. J. Bacteriol. 190, 343-355. doi: 10.1128/JB.00978-07
149. Yang, B., Sugio, A., and White, F. F. (2005). Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector ofXanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 18, 142-149. doi: 10.1094/MPMI-18-0142
150. Yang, B., Sugio, A., and White, F. F. (2006). Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc. Natl. Acad. Sci. U.S.A. 103, 10503-10508. doi: 10.1073/pnas.0604088103
151. Yang, B., and White, F. F. (2004). Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice.Mol. Plant Microbe Interact. 17, 1192-1200. doi: 10.1094/MPMI.2004.17.11.1192
152. Yang, Y., and Gabriel, D. W. (1995). Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities. J. Bacteriol. 177, 4963-4968.
153. Ye, W., Wang, Y., and Wang, Y. (2015). Bioinformatics analysis reveals abundant short alpha-helices as a common structural feature of oomycete RxLR effector proteins. PLoS ONE 10:e0135240. doi: 10.1371/journal.pone.0135240
154. Yuan, M., Chu, Z., Li, X., Xu, C., and Wang, S. (2009). Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant Cell Phys. 50, 947-955. doi: 10.1093/pcp/pcp046
155. Zeng, L., Velásquez, A. C., Munkvold, K. R., Zhang, J., and Martin, G. B. (2012). A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 69, 92-103. doi: 10.1111/j.1365-313X.2011.04773.x
156. Zhao, C., Escalante, L. N., Chen, H., Benatti, T. R., Qu, J., Chellapilla, S., et al. (2015). A massive expansion of effector genes underlies gall-formation in the wheat pestMayetiola destructor. Curr. Biol. 25, 613-620. doi: 10.1016/j.cub.2014.12.057