The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Oomycetes RXLR Effectors Function as Both Activator and Suppressor of Plant Immunity

  • Oh, Sang-Keun (Department of Plant Sciences and Plant Genomics & Breeding Institute, Seoul National University) ;
  • Kamoun, Sophien (The Sainsbury Laboratory) ;
  • Choi, Doil (Department of Plant Sciences and Plant Genomics & Breeding Institute, Seoul National University)
  • Received : 2010.04.26
  • Accepted : 2010.05.28
  • Published : 2010.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Plant pathogenic oomycetes, such as Phytophthora spp., are the causal agent of the most devastating plant diseases. During infection, these pathogens accomplish parasitic colonization of plants by modulating host defenses through an array of disease effector proteins. These effectors are classified in two classes based on their target sites in the host plant. Apoplastic effectors are secreted into the plant extracellular space, and cytoplasmic effectors are translocated inside the plant cell, through the haustoria that enter inside living host cell. Recent characterization of some oomycete Avr genes showed that they encode effector protein with general modular structure including N-terminal conserved RXLR-DEER motif. More detailed evidences suggest that these AVR effectors are secreted by the pathogenic oomycetes and then translocated into the host plant cell during infection. Recent findings indicated that one of the P. infestans effector, Avrblb2, specifically induces hypersensitive response (HR) in the presence of Solanum bulbocastanum late blight resistance genes Rpi-blb2. On the other hand, another secreted RXLR protein PexRD8 originated from P. infestans suppressed the HCD triggered by the elicitin INF1. In this review, we described recent progress in characterized RXLR effectors in Phytophthora spp. and their dual functions as modulators of host plant immunity.

Keywords

References

  1. 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 programmend cell death. EMBO J. 22:60-69. https://doi.org/10.1093/emboj/cdg006
  2. Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E. and Beynon, L. L. (2004). Host-parasite co-evolutionary conflict between Arabidopsis and downy mildew. Science 306:1957-1960. https://doi.org/10.1126/science.1104022
  3. Armstrong, M. R., Whisson, S. C., Pritchar, L., Bos, J. I. B., Venter, E., Avrova, A. O., Rehmany, A. P., Böhme, U., Brooks, K., Cherevach, I., Hamlin, N., White, B., Fraser, A., Lord, A., Quail, M. A., Churcher, C., Hall, N., Berriman, M., Huang, S., Kamoun, S., Beynon, J. L. and Birch, P. R. J. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences USA 102:7766-7771. https://doi.org/10.1073/pnas.0500113102
  4. Ballvora, A., Ercolano, M. R., Weiss, J., Meksem, K., Bormann, C. A., Oberhagemann, P., Salamini, F. and Gebhardt, C. (2002). The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 30:361-371. https://doi.org/10.1046/j.1365-313X.2001.01292.x
  5. Bhattacharjee, S., Hiller, N. L., Liolios, K., Win, J., Kanneganti, T. D., Young, C., Kamoun, S. and Haldar, K. (2006). The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2:e50 https://doi.org/10.1371/journal.ppat.0020050
  6. Birch, P. R., Armstrong, M., Bos, J., Boevink, P., Gilroy, E. M., Taylor, R. M., Wawra. S., Pritchard, L., Conti, L., Ewan, R., Whisson, S. C., van West, P., Sadanandom, A. and Kamoun, S. (2009). Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J. Exp. Bot. 60:1133-1140. https://doi.org/10.1093/jxb/ern353
  7. Birch, P. R., Boevink, P. C., Gilroy, E. M., Hein, I., Pritchard, L., and Whisson, S. C. (2008). Oomycete RXLR effectors: Delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11:373-379. https://doi.org/10.1016/j.pbi.2008.04.005
  8. Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S. and Beynon, J. L. (2006). Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol. 14:8-11. https://doi.org/10.1016/j.tim.2005.11.007
  9. Boner, C. (2003). The Bcl-2 pretein family: sensors and checkpoints for life-or-death decisions. Mol. Immunol. 30:615-647.
  10. Bos, J. I., Kanneganti, T. D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M. R., Birch, P. R. and Kamoun, S. (2006). The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J. 48:165-176. https://doi.org/10.1111/j.1365-313X.2006.02866.x
  11. Bos, J. I. B., Chaparro-Garcia, A., Quesada-Ocampo, L. M., McSpadden- Gardener, B. B. and Kamoun, S. (2009). Distinct amino acids of the Phytophthora infestans effector AVR3a condition activation of R3a hypersensitivity and suppression of cell death. Mol. Plant Microbe Interact. 22:269-281. https://doi.org/10.1094/MPMI-22-3-0269
  12. Dangl, J. L. and Jones, J. D. (2001). Plant pathogens and integrated defence responses to infection. Nature. 411:826-833. https://doi.org/10.1038/35081161
  13. Dou, D., Kale, S. D., Wang, X., Chen, Y., Wang, Q., Jiang, R. H., Arredondo, F. D., Anderson, R. G., Thakur, P. B., McDowell, J. M., Wang, Y. and Tyler, B. M. (2008a). Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20:1118-1133. https://doi.org/10.1105/tpc.107.057067
  14. Dou, D., Kale, S. D., Wang, X., Jiang, R. H., Bruce, N. A., Arredondo, F. D., Zhang, X. and Tyler, B. M. (2008b). RXLRmediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20:1930-1947. https://doi.org/10.1105/tpc.107.056093
  15. Erwin, D. C. and Ribeiro, O. K. (1996). Phytophthora Diseases Worldwide, The American Phytopathological Society, St Paul, MN.
  16. Fry, W. E. (2008). Phytophthora infestans: The plant (and R gene) destroyer. Mol. Plant Pathol. 9:385-402. https://doi.org/10.1111/j.1364-3703.2007.00465.x
  17. Govers, F. and Bouwmeester, K. (2008). Effector trafficking: RXLR-dEER as extra gear for delivery into plant cell. Plant Cell 20:1728-1730. https://doi.org/10.1105/tpc.108.062075
  18. Grouffaud, S., van West, P., Avrova, A. O., Birch, P. R. and Whisson, S. C. (2008). Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154:3743-3751. https://doi.org/10.1099/mic.0.2008/021964-0
  19. Haas, B. and Kamoun, S. et al. (2009). Genome sequence and comparative analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398. https://doi.org/10.1038/nature08358
  20. Hausbeck, M. K. and Lamour, K. H. (2004). Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Dis. 88:1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
  21. Hewitt, W. B. and Pearson, R. C. (1988). Downy mildew. In Compendium of Grape Diseases, ed, RC Pearson, AC Goheen, pp. 11-13. St. Paul, MN: APS Press.
  22. Huang, S., van der Vossen, E., Kuang, H., Vleeshouwers, V., Zhang, N., Borm, T., van Eck, H., Baker, B., Jacobsen, E. and Visser, R. (2005). Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 42: 251-261. https://doi.org/10.1111/j.1365-313X.2005.02365.x
  23. Jamir, Y., Guo, M., Oh, H. S., Petnicki-Ocwieja, T., Chen, S., Tang, X. et al. (2004). Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37:554-565. https://doi.org/10.1046/j.1365-313X.2003.01982.x
  24. 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. Pro. Nat. Sci. USA 105:4874-4879. https://doi.org/10.1073/pnas.0709303105
  25. Jones, J. D. and Dangl, J. L. (2006). The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  26. Judelson, H. S. and Blanco, F. A. (2005). The spores of Phytophthora: weapons of the plant destroyer. Nat. Rev. Microbiol. 3:47-58. https://doi.org/10.1038/nrmicro1064
  27. Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44:41-60. https://doi.org/10.1146/annurev.phyto.44.070505.143436
  28. Kamoun, S. (2007). Groovy times: Filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10:358-365. https://doi.org/10.1016/j.pbi.2007.04.017
  29. Kamoun, S. and Smart, C. D. (2005). Late blight of potato and tomato in the genomics era. Plant Dis. 89:692-699. https://doi.org/10.1094/PD-89-0692
  30. Kamoun, S., van West, P., Vleeshouwers, V. G. A. A., de Groot, K. E. and Goers, F. (1998). Resistance of Nicotiana benthamiana to Phytophthora infestans in mediated by the recognition of the elicitor protein INF1. Plant Cell 10:1413-1426. https://doi.org/10.1105/tpc.10.9.1413
  31. Kamoun, S., Young, M., Glascock, C. and Tyler, B. M. (1993). Extracellular protein elicitors from Phytophthora: Host-specificity and induction of resistance to fungal and bacterial phytopathogens. Mol. Plant Microbe Interact. 6:15-25. https://doi.org/10.1094/MPMI-6-015
  32. Lamour, K. H. and Kamoun, S. (2009). Oomycete Genetics and Genomics: Diversity, Intreractions and Research Tools. Hoboken, NJ: Wiley-Blackwell.
  33. Lokossou, A. A., Park, T. H., van Arkel, G., Arens, M., Ruyter- Spira, C., Morales, J., Whisson, S. C., Birch, P. R., Visser, R. G., Jacobsen, E. and van der Vossen, E. A. (2009). Exploiting Knowledge of R/Avr Genes to Rapidly Clone a New LZ-NBSLRR Family of Late Blight Resistance Genes from Potato Linkage Group IV. Mol. Plant Microbe Interact. 22:630-641. https://doi.org/10.1094/MPMI-22-6-0630
  34. Morgan, W. and Kamoun, S. (2007). RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol. 10:332-338. https://doi.org/10.1016/j.mib.2007.04.005
  35. Nurnberger, T., Brunner, F., Kemmerling, B. and Piater, L. (2004). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev. 198:249-66. https://doi.org/10.1111/j.0105-2896.2004.0119.x
  36. O'Connell, R. J. and Panstruga, R. (2006). Tete a tete inside a plant cell: establishing compatibility between plants and biotrophic fungi and Oomycetes. New Phytol. 171:699-718. https://doi.org/10.1111/j.1469-8137.2006.01829.x
  37. Oh, S.-K., Young, C., Lee, M., Oliva, R., Bozkurt, T. O., Cano, L. M., Win, J., Bos, J. I., Liu, H. Y., van Damme, M., Morgan, W., Choi, D., Van der Vossen, E. A., Vleeshouwers, V. G. and Kamoun, S. (2009). In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21:2928-2947. https://doi.org/10.1105/tpc.109.068247
  38. Panstruga, R. (2003). Establishing compatibility between plants and obligate biotrophic pathogens. Curr. Opin. Plant Biol. 6: 320-326. https://doi.org/10.1016/S1369-5266(03)00043-8
  39. Qutob, D., Tedman-Jones, J., Dong, S., Kuflu, K., Pham, H., Wang, Y., Dou, D., Kale, S. D., Arredondo, F. D., Tyler, B. M. and Gijzen, M. (2009). Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS One 4:e5056. https://doi.org/10.1371/journal.pone.0005056
  40. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., Kamoun, S., Tyler, B. M., Birch, P. R. and Beynon, J. L. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839-1850. https://doi.org/10.1105/tpc.105.031807
  41. Rizzo, D. M., Garbelootto, M. and Hansen, E. M. (2005). Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu. Rev. Phytopathol. 43:309-335. https://doi.org/10.1146/annurev.phyto.42.040803.140418
  42. Schmitthenner, A. F. (1985). Problems and progress toward control of Phytophthora root rot of soybean. Plant Dis. 69:362-368. https://doi.org/10.1094/PD-69-362
  43. Schornack, S., Huitema, E., Cano, L. M., Bozkurt T. O., Oliva, R., Van Damme, M., Schwizer, S., Raffaele, S., Chaparro-Garcia, A., Farrer, R., Segretin, M. E., Bos, J., Haas, B. J., Zody, M. C., Nusbaum, C., Win, J., Thines, M. and Kamoun, S. (2009). Ten things to know about oomycete effectors. New Phytol. 10:795-803.
  44. Shan, W., Cao, M., Leung, D. and Tyler, B. M. (2004). The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions 17:394-403. https://doi.org/10.1094/MPMI.2004.17.4.394
  45. Slusarenko, A. J. and Schlaich, N. L. (2003). Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol. Plant Pathol. 4:159-170. https://doi.org/10.1046/j.1364-3703.2003.00166.x
  46. Sohn, K. H., Lei, R., Nemri., and Jones, J. D. (2007). The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. The Plant Cell 19: 4077-4090. https://doi.org/10.1105/tpc.107.054262
  47. Song, J., Bradeen, J. M., Naess, S. K., Raasch, J. A., Wielgus, S. M., Haberlach, G. T., Liu, J., Kuang, H., Austin-Phillips, S., Buell, C. R., Helgeson, J. P. and Jiang, J. (2003). Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci. USA 100: 9128-9133. https://doi.org/10.1073/pnas.1533501100
  48. Tyler et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261-1266. https://doi.org/10.1126/science.1128796
  49. Tyler, B. M. (2009). Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbebiol. 11:13-20. https://doi.org/10.1111/j.1462-5822.2008.01240.x
  50. van der Vossen, E. A. G., Gros, J., Sikkema, A., Muskens, M., Wouters, D., Wolters, P., Pereira, A. and Allefs, S. (2005). The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homologh conferring broad-spectrum late blight resistance in potato. Plant J. 44:208-222. https://doi.org/10.1111/j.1365-313X.2005.02527.x
  51. van Poppel, P. M., Guo, J., van de Vondervoort, P. J., Jung, M. W., Birch, P. R., Whisson, S. C. and Govers, F. (2008). The Phytophthora infestans avirulence gene Avr4 encodes an RXLRdEER effector. Mol. Plant Microbe Interact. 21:1460-1470. https://doi.org/10.1094/MPMI-21-11-1460
  52. van Poppel, P. M., Jiang, R. H., Sliwka, J. and Govers, F. (2009). Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C-terminal domains comprising W motifs. Mol. Plant Pathol. 10:611-620. https://doi.org/10.1111/j.1364-3703.2009.00556.x
  53. Vleeshouwers, V. G., Rietman, H. and Krenek, P. et al. (2008). Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS One 3:e2875. https://doi.org/10.1371/journal.pone.0002875
  54. Vleeshouwers, V. G. A. A., Driesprong, J.-D., Kamphuis, L. G., Torto-Alalibo, T., van't Slot, K. A. E., Govers, F., Visser, R. G. F., Jacobsen, E. and Kamoun, S. (2006). Agroinfection-based high throughput screening reveals specific recognition of INF elicitins in Solanum. Mol. Plant Pathol. 7:499-510. https://doi.org/10.1111/j.1364-3703.2006.00355.x
  55. Whisson, S. C. et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115-118. https://doi.org/10.1038/nature06203
  56. Win, J., Kanneganti, T. D., Torto-Alalibo, T. and Kamoun, S. (2006). Computational and comparative analyses of 150 fulllength cDNA sequences from the oomycete plant pathogen Phytophthora infestans. Fungal Genet. Biol. 43:20-33. https://doi.org/10.1016/j.fgb.2005.10.003

Cited by

  1. The Secreted Proteins of Achlya hypogyna and Thraustotheca clavata Identify the Ancestral Oomycete Secretome and Reveal Gene Acquisitions by Horizontal Gene Transfer vol.7, pp.1, 2015, https://doi.org/10.1093/gbe/evu276
  2. Eicosapolyenoic acids vol.6, pp.4, 2011, https://doi.org/10.4161/psb.6.4.14782
  3. Identification and analysis of Phytophthora cactorum genes up-regulated during cyst germination and strawberry infection vol.57, pp.5, 2011, https://doi.org/10.1007/s00294-011-0348-0
  4. Arms race: diverse effector proteins with conserved motifs vol.14, pp.2, 2019, https://doi.org/10.1080/15592324.2018.1557008