Tomato SOBIR1/EVR homologs are involved in elicitin perception and plant defense against the oomycete pathogen Phytophthora parasitica

Molecular Plant-Microbe Interactions

Volumn 28, Issue 8, 2015, Pages 913-926

  Peng, Ke Chun ^a   Wang, Chao Wen ^b   Wu, Chih Hang ^a   Huang, Chun Tzu ^a   Liou, Ruey Fen ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; PHYTOPHTHORA; PHYTOPHTHORA PARASITICA;

ARABIDOPSIS PROTEIN; CARBOXYLESTERASE; ELICITIN, PHYTOPHTHORA; PATTERN RECOGNITION RECEPTOR; PROTEIN; SOBER1 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

CELL DEATH; CYTOLOGY; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PATHOGENICITY; PHYTOPHTHORA; PLANT DISEASE; SEQUENCE HOMOLOGY; TOBACCO; TOMATO;

ARABIDOPSIS PROTEINS; CARBOXYLIC ESTER HYDROLASES; CELL DEATH; CLONING, MOLECULAR; ENDOCYTOSIS; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYTOPHTHORA; PLANT DISEASES; PLANT PROTEINS; PROTEINS; RECEPTORS, PATTERN RECOGNITION; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO;

EID: 84939153142     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-12-14-0405-R     Document Type: Article

References (64)

1. Altenbach, D., and Robatzek, S. 2007. Pattern recognition receptors: From the cell surface to intracellular dynamics. Mol. Plant-Microbe Interact. 20:1031-1039.
2. Baldauf, S. L., Roger, A. J., Wenk-Siefert, I., and Doolittle, W. F. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972-977.
3. Bar, M., and Avni, A. 2009. EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J. 59:600-611.
4. Bar, M., and Avni, A. 2014. Endosomal trafficking and signaling in plant defense responses. Curr. Opin. Plant Biol. 22:86-92.
5. Beck, M., Zhou, J., Faulkner, C., MacLean, D., and Robatzek, S. 2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24: 4205-4219.
6. Bindschedler, L. V., Dewdney, J., Blee, K. A., Stone, J. M., Asai, T., Plotnikov, J., Denoux, C., Hayes, T., Gerrish, C., Davies, D. R., Ausubel, F. M., and Bolwell, G. P. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47:851-863.
7. Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu. Rev. Plant Biol. 60:379-406.
8. Bolte, S., Talbot, C., Boutte, Y., Catrice, O., Read, N. D., and Satiat- Jeunemaitre, B. 2004. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214:159-173.
9. Brunner, F., Rosahl, S., Lee, J., Rudd, J. J., Geiler, C., Kauppinen, S., Rasmussen, G., Scheel, D., and Nürnberger, T. 2002. Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO (Eur. Mol. Biol. Organ.) J. 21:6681-6688.
10. Chaparro-Garcia, A., Wilkinson, R. C., Gimenez-Ibanez, S., Findlay, K., Coffey, M. D., Zipfel, C., Rathjen, J. P., Kamoun, S., and Schornack, S. 2011. The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen phytophthora infestans in Nicotiana benthamiana. PLoS ONE 6:e16608.
11. Chen, P. Y., Wang, C. K., Soong, S. C., and To, K. Y. 2003. Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol. Breed. 11:287-293.
12. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nürnberger, T., Jones, J. D., Felix, G., and Boller, T. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
13. Chinchilla, D., Shan, L., He, P., de Vries, S., and Kemmerling, B. 2009. One for all: The receptor-associated kinase BAK1. Trends Plant Sci. 14: 535-541.
14. Dodds, P. N., and Rathjen, J. P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11: 539-548.
15. Ebine, K., Fujimoto, M., Okatani, Y., Nishiyama, T., Goh, T., Ito, E., Dainobu, T., Nishitani, A., Uemura, T., Sato, M. H., Thordal- Christensen, H., Tsutsumi, N., Nakano, A., and Ueda, T. 2011. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13:853-859.
16. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora diseases worldwide. American Phytopathological Society, St. Paul, MN, U.S.A.
17. Gao, M., Wang, X., Wang, D., Xu, F., Ding, X., Zhang, Z., Bi, D., Cheng, Y. T., Chen, S., Li, X., and Zhang, Y. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6:34-44.
18. Gaulin, E., Dramé, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline- Torregrosa, C., Khatib, M., Mazarguil, H., Villalba-Mateos, F., Kamoun, S., Mazars, C., Dumas, B., Bottin, A., Esquerré-Tugayé, M. T., and Rickauer, M. 2006. Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18:1766-1777.
19. Geldner, N., and Robatzek, S. 2008. Plant receptors go endosomal: A moving view on signal transduction. Plant Physiol. 147:1565-1574.
20. Geldner, N., Hyman, D. L., Wang, X., Schumacher, K., and Chory, J. 2007. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21:1598-1602.
21. Gibbon, B. C., Kovar, D. R., and Staiger, C. J. 1999. Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11: 2349-2363.
22. Gómez-Gómez, L., and Boller, T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-1011.
23. He, K., Gou, X., Yuan, T., Lin, H., Asami, T., Yoshida, S., Russell, S. D., and Li, J. 2007. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17:1109-1115.
24. Heese, A., Hann, D. R., Gimenez-Ibanez, S., Jones, A. M., He, K., Li, J., Schroeder, J. I., Peck, S. C., and Rathjen, J. P. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. U.S.A. 104:12217-12222.
25. Hofzumahaus, S., and Schallmey, A. 2013. Escherichia coli-based expression system for the heterologous expression and purification of the elicitin b-cinnamomin from Phytophthora cinnamomi. Protein Expr. Purif. 90:117-123.
26. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444: 323-329.
27. Kamoun, S., Klucher, K. M., Coffey, M. D., and Tyler, B. M. 1993a. A gene encoding a host-specific elicitor protein of Phytophthora parasitica. Mol. Plant-Microbe Interact. 6:573-581.
28. Kamoun, S., Young, M., Glascock, C. B., and Tyler, B. M. 1993b. Extracellular protein elicitors from Phytophthora: Host-specificity and induction of resistance to bacterial and fungal phytopathogens. Mol. Plant-Microbe Interact. 6:15-25.
29. Kamoun, S., van West, P., de Jong, A. J., de Groot, K. E., Vleeshouwers, V. G., and Govers, F. 1997. A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant-Microbe Interact. 10:13-20.
30. Kamoun, S., Furzer, O., Jones, J. D., Judelson, H. S., Ali, G. S., Dalio, R. J., Roy, S. G., Schena, L., Zambounis, A., Panabières, F., Cahill, D., Ruocco, M., Figueiredo, A., Chen, X. R., Hulvey, J., Stam, R., Lamour, K., Gijzen, M., Tyler, B. M., Grünwald, N. J., Mukhtar, M. S., Tomé, D. F., Tör, M., Van Den Ackerveken, G., McDowell, J., Daayf, F., Fry, W. E., Lindqvist- Kreuze, H., Meijer, H. J., Petre, B., Ristaino, J., Yoshida, K., Birch, P. R., and Govers, F. 2015. The top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16:413-434.
31. Kanzaki, H., Saitoh, H., Takahashi, Y., Berberich, T., Ito, A., Kamoun, S., and Terauchi, R. 2008. NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta 228:977-987.
32. Leborgne-Castel, N., Lherminier, J., Der, C., Fromentin, J., Houot, V., and Simon-Plas, F. 2008. The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in bright yellow-2 tobacco cells. Plant Physiol. 146:1255-1266.
33. Leborgne-Castel, N., Adam, T., and Bouhidel, K. 2010. Endocytosis in plant-microbe interactions. Protoplasma 247:177-193.
34. Leslie, M. E., Lewis, M. W., Youn, J. Y., Daniels, M. J., and Liljegren, S. J. 2010. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137:467-476.
35. Liebrand, T. W. H., van den Berg, G. C. M., Zhang, Z., Smit, P., Cordewener, J. H. G., America, A. H. P., Sklenar, J., Jones, A. M. E., Tameling, W. I. L., Robatzek, S., Thomma, B. P. H.. J., and Joosten, M. H. A. J. 2013. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. U.S.A. 110:10010-10015.
36. Liebrand, T.W., van den Burg, H. A., and Joosten, M. H. 2014. Two for all: Receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 19: 123-132.
37. Liu, Y., Schiff, M., and Dinesh-Kumar, S. P. 2002. Virus-induced gene silencing in tomato. Plant J. 31:777-786.
38. Lu, Y. J., Schornack, S., Spallek, T., Geldner, N., Chory, J., Schellmann, S., Schumacher, K., Kamoun, S., and Robatzek, S. 2012. Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell. Microbiol. 14:682-697.
39. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B., and Ton, J. 2011. Callose deposition: A multifaceted plant defense response. Mol. Plant- Microbe Interact. 24:183-193.
40. Mateos, F. V., 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.
41. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and Shibuya, N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104:19613-19618.
42. Monaghan, J., and Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-357.
43. Mooren, O. L., Galletta, B. J., and Cooper, J. A. 2012. Roles for actin assembly in endocytosis. Annu. Rev. Biochem. 81:661-686.
44. Morillo, S. A., and Tax, F. E. 2006. Functional analysis of receptor-like kinases in monocots and dicots. Curr. Opin. Plant Biol. 9:460-469.
45. Nguyen, H. P., Chakravarthy, S., Velásquez, A. C., McLane, H. L., Zeng, L., Nakayashiki, H., Park, D. H., Collmer, A., and Martin, G. B. 2010. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant-Microbe Interact. 23:991-999.
46. Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W. R., Hahlbrock, K., and Scheel, D. 1994. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78: 449-460.
47. Ponchet, M., Panabières, Milat M-L., F., Mikes, V., Montillet, J. L., Suty, L., Triantaphylides, C., Tirilly, Y., and Blein, J. P. 1999. Are elicitins cryptograms in plant-oomycete communications? Cell. Mol. Life Sci. 56:1020-1047.
48. Ricci, P., Bonnet, P., Huet, J. C., Sallantin, M., Beauvais-Cante, F., Bruneteau, M., Billard, V., Michel, G., and Pernollet, J. C. 1989. Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 183:555-563.
49. Robatzek, S., Chinchilla, D., and Boller, T. 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20:537-542.
50. Roux, M., Schwessinger, B., Albrecht, C., Chinchilla, D., Jones, A., Holton, N., Malinovsky, F. G., Tör, M., de Vries, S., and Zipfel, C. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440-2455.
51. Schwessinger, B., Roux, M., Kadota, Y., Ntoukakis, V., Sklenar, J., Jones, A., and Zipfel, C. 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptorlike kinase BAK1. PLoS Genet. 7:e1002046.
52. Shan, L., He, P., Li, J., Heese, A., Peck, S. C., Nürnberger, T., Martin, G. B., and Sheen, J. 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.
53. Shiu, S. H., and Bleecker, A. B. 2003. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132:530-543.
54. Spector, I., Shochet, N. R., Blasberger, D., and Kashman, Y. 1989. Latrunculins-Novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil. Cytoskeleton 13:127-144.
55. Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A. 2001. Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO (Eur. Mol. Biol. Organ.) J. 20:4730-4741.
56. Wang, X., Kota, U., He, K., Blackburn, K., Li, J., Goshe, M. B., Huber, S. C., and Clouse, S. D. 2008. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15:220-235.
57. Wendehenne, D., Binet, M. N., Blein, J. P., Ricci, P., and Pugin, A. 1995. Evidence for specific, high-affinity binding sites for a proteinaceous elicitor in tobacco plasma membrane. FEBS (Fed. Eur. Biochem. Soc.) Lett. 374:203-207.
58. Wu, C. H., Lee, S. C., and Wang, C. W. 2011. Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. J. Cell Biol. 193:521-535.
59. Yan, H. Z., and Liou, R. F. 2006. Selection of internal control genes for realtime quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genet. Biol. 43:430-438.
60. Zhang, W., Fraiture, M., Kolb, D., Löffelhardt, B., Desaki, Y., Boutrot, F. F. G., Tör, M., Zipfel, C., Gust, A. A., and Brunner, F. 2013. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25:4227-4241.
61. Zhang, L., Kars, I., Essenstam, B., Liebrand, T.W., Wagemakers, L., Elberse, J., Tagkalaki, P., Tjoitang, D., van den Ackerveken, G., and van Kan, J. A. 2014. Fungal endopolygalacturonases are recognized as microbeassociated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol. 164:352-364.
62. Zipfel, C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-420.
63. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D., Felix, G., and Boller, T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764-767.
64. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D., Boller, T., and Felix, G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749-760.