The Arabidopsis LecRK-VI.2 associates with the pattern-recognition receptor FLS2 and primes Nicotiana benthamiana pattern-triggered immunity

Plant Journal

Volumn 79, Issue 2, 2014, Pages 243-255

  Huang, Pin Yao ^a   Yeh, Yu Hung ^a   Liu, An Chi ^a   Cheng, Chiu Ping ^a   Zimmerli, Laurent ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Arabidopsis thaliana; bacteria; innate immunity; lectin receptor kinase; Nicotiana benthamiana; pattern recognition receptor; pattern triggered immunity; priming

Indexed keywords

BACTERIA; ENZYMES; GENE EXPRESSION; PROTEINS;

ARABIDOPSIS THALIANA; INNATE IMMUNITY; LECTIN RECEPTORS; NICOTIANA BENTHAMIANA; PATTERN-RECOGNITION RECEPTOR; PATTERN-TRIGGERED IMMUNITY; PRIMING;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; LOBELIA; NICOTIANA BENTHAMIANA; NICOTIANA OBTUSIFOLIA; NICOTIANA RUSTICA;

ARABIDOPSIS PROTEIN;

ARABIDOPSIS; GENETICS; INNATE IMMUNITY; METABOLISM; PHYSIOLOGY; PLANT IMMUNITY; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; IMMUNITY, INNATE; PLANT IMMUNITY; TOBACCO;

EID: 84904050452     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12557     Document Type: Article

References (84)

1. Arnaud, D., Desclos-Theveniau, M., and, Zimmerli, L., (2012) Disease resistance to Pectobacterium carotovorum is negatively modulated by the Arabidopsis lectin receptor kinase LecRK-V.5. Plant Signal. Behav. 7, 1070-1072.
2. Beckers, G.J., Jaskiewicz, M., Liu, Y., Underwood, W.R., He, S.Y., Zhang, S., and, Conrath, U., (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell, 21, 944-953.
3. Bogre, L., Calderini, O., Binarova, P., et al. (1999) A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell, 11, 101-113.
4. Boller, T., and, Felix, G., (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406.
5. Bouwmeester, K., and, Govers, F., (2009) Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J. Exp. Bot. 60, 4383-4396.
6. Bouwmeester, K., de Sain, M., Weide, R., Gouget, A., Klamer, S., Canut, H., and, Govers, F., (2011) The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog. 7, e1001327.
7. Bouwmeester, K., Han, M., Blanco-Portales, R., Song, W., Weide, R., Guo, L.-Y., van der Vossen, E.A.G., and, Govers, F., (2014) The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnol. J. 12, 10-16.
8. Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and, Felix, G., (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell, 18, 465-476.
9. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, 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.
10. Conrath, U., Beckers, G.J.M., Flors, V., et al. (2006) Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062-1071.
11. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S., and, Somerville, C.R., (2000) Random GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl Acad. Sci. USA, 97, 3718-3723.
12. Davidsson, P.R., Kariola, T., Niemi, O., and, Palva, E.T., (2013) Pathogenicity of and plant immunity to soft rot pectobacteria. Front. Plant Sci. 4, 191.
13. Desclos-Theveniau, M., Arnaud, D., Huang, T.-Y., Lin, G.J.-C., Chen, W.-Y., Lin, Y.-C., and, Zimmerli, L., (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog. 8, e1002513.
14. Deslandes, L., and, Rivas, S., (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644-655.
15. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and, Pikaard, C.S., (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
16. Felix, G., Duran, J.D., Volko, S., and, Boller, T., (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
17. Feng, F., and, Zhou, J.-M., (2012) Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15, 469-476.
18. Feng, F., Yang, F., Rong, W., Wu, X., Zhang, J., Chen, S., He, C., and, Zhou, J.M., (2012) A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature, 485, 114-118.
19. Fradin, E.F., Abd-El-Haliem, A., Masini, L., van den Berg, G.C., Joosten, M.H., and, Thomma, B.P., (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156, 2255-2265.
20. Gassmann, W., and, Bhattacharjee, S., (2012) Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol. Plant Microbe Interact. 25, 862-868.
21. Gasson, M.J., (1980) Indicator technique for antimetabolic toxin production by phytopathogenic species of Pseudomonas. Appl. Environ. Microbiol. 39, 25-29.
22. Gõmez-Gõmez, 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. Gomez-Gomez, L., Felix, G., and, Boller, T., (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277-284.
24. Gurr, S.J., and, Rushton, P.J., (2005) Engineering plants with increased disease resistance: what are we going to express? Trends Biotechnol. 23, 275-282.
25. Halter, T., Imkampe, J., Mazzotta, S., et al. (2014) The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24, 134-143.
26. Hammond-Kosack, K.E., and, Parker, J.E., (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Plant Biol. 14, 177-193.
27. Heese, A., Hann, D.R., Gimenez-Ibanez, S., Jones, A.M.E., 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. USA, 104, 12217-12222.
28. Jaskiewicz, M., Conrath, U., and, Peterhansel, C., (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50-55.
29. Jehle, A.K., Lipschis, M., Albert, M., Fallahzadeh-Mamaghani, V., Furst, U., Mueller, K., and, Felix, G., (2013) The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell, 25, 2330-2340.
30. Jones, J.D.G., and, Dangl, J.L., (2006) The plant immune system. Nature, 444, 323-329.
31. de Jonge, R., van Esse, H.P., Maruthachalam, K., et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl Acad. Sci. USA, 109, 5110-5115.
32. Kadota, Y., Sklenar, J., Derbyshire, P., et al. (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell, 54, 1-13.
33. Kariola, T., Brader, G., Li, J., and, Palva, E.T., (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell, 17, 282-294.
34. Keppler, L.D., Baker, C.J., and, Atkinson, M.M., (1989) Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells. Phytopathology, 79, 974-978.
35. Kim, H.S., Thammarat, P., Lommel, S.A., Hogan, C.S., and, Charkowski, A.O., (2011) Pectobacterium carotovorum elicits plant cell death with DspE/F but the P. carotovorum DspE does not suppress callose or induce expression of plant genes early in plant-microbe interactions. Mol. Plant Microbe Interact. 24, 773-786.
36. Korasick, D.A., McMichael, C., Walker, K.A., Anderson, J.C., Bednarek, S.Y., and, Heese, A., (2010) Novel functions of Stomatal Cytokinesis-Defective 1 (SCD1) in innate immune responses against bacteria. J. Biol. Chem. 285, 23340-23348.
37. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and, Felix, G., (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell, 16, 3496-3507.
38. Kwon, S.J., Jin, H.C., Lee, S., Nam, M.H., Chung, J.H., Kwon, S.I., Ryu, C.M., and, Park, O.K., (2009) GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J. 58, 235-245.
39. Lacombe, S., Rougon-Cardoso, A., Sherwood, E., et al. (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28, 365-369.
40. Leach, J.E., Vera Cruz, C.M., Bai, J., and, Leung, H., (2001) Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39, 187-224.
41. Li, L., Li, M., Yu, L., et al. (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RBOHD to control plant immunity. Cell Host Microbe, 15, 329-338.
42. Lin, Y.M., Shih, S.L., Lin, W.C., Wu, J.W., Chen, Y.T., Hsieh, C.Y., Guan, L.C., Lin, L., and, Cheng, C.P., (2014) Phytoalexin biosynthesis genes are regulated and involved in plant response to Ralstonia solanacearum infection. Plant Science, 224, 86-94.
43. Lu, D., Wu, S., Gao, X., Zhang, Y., Shan, L., and, He, P., (2010a) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl Acad. Sci. USA, 107, 496-501.
44. Lu, D., Wu, S., He, P., and, Shan, L., (2010b) Phosphorylation of receptor-like cytoplasmic kinases by bacterial flagellin. Plant Signal. Behav. 5, 598-600.
45. Lu, Q., Tang, X., Tian, G., et al. (2010c) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J. 61, 259-270.
46. Luna, E., Bruce, T.J.A., Roberts, M.R., Flors, V., and, Ton, J., (2012) Next-generation systemic acquired resistance. Plant Physiol. 158, 844-853.
47. Maekawa, T., Kufer, T.A., and, Schulze-Lefert, P., (2011) NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817-826.
48. Maekawa, T., Kracher, B., Vernaldi, S., Loren, V., van Themaat, E., and, Schulze-Lefert, P., (2012) Conservation of NLR-triggered immunity across plant lineages. Proc. Natl Acad. Sci. USA, 109, 20119-20123.
49. McDonald, B.A., and, Linde, C., (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349-379.
50. Medina, J., Ballesteros, M.L., and, Salinas, J., (2007) Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J. Exp. Bot. 58, 4333-4346.
51. 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. USA, 104, 19613-19618.
52. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and, Kimura, T., (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41.
53. Newman, M.A., Sundelin, T., Nielsen, J.T., and, Erbs, G., (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 4, 139.
54. 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.
55. Nuhse, T.S., Peck, S.C., Hirt, H., and, Boller, T., (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J. Biol. Chem. 275, 7521-7526.
56. Oerke, E.C., (2007) Crop losses to animal pests, plant pathogens, and weeds. In Encyclopedia of Pest Management, Volume II (, Pimentel, D., ed.). UK: CRC Press, pp. 116-120.
57. Po-Wen, C., Singh, P., and, Zimmerli, L., (2013) Priming of the Arabidopsis pattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol. Plant Pathol. 14, 58-70.
58. Rasmann, S., De Vos, M., Casteel, C.L., Tian, D., Halitschke, R., Sun, J.Y., Agrawal, A.A., Felton, G.W., and, Jander, G., (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158, 854-863.
59. Ribeiro, R.D.L.D., Hagedorn, D.J., Durbin, R.D., and, Uchytil, T.F., (1979) Characterization of the bacterium inciting bean wildfire in Brazil. Phytopathology, 69, 208-212.
60. Ron, M., and, Avni, A., (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell, 16, 1604-1615.
61. Roux, M., Schwessinger, B., Albrecht, C., Chinchilla, D., Jones, A., Holton, N., Malinovsky, F.G., Tor, 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.
62. 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 receptor-like kinase BAK1. PLoS Genet. 7, e1002046.
63. Segonzac, C., Feike, D., Gimenez-Ibanez, S., Hann, D.R., Zipfel, C., and, Rathjen, J.P., (2011) Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol. 156, 687-699.
64. Shi, H., Shen, Q., Qi, Y., Yan, H., Nie, H., Chen, Y., Zhao, T., Katagiri, F., and, Tang, D., (2013) BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell, 25, 1143-1157.
65. Singh, P., and, Zimmerli, L., (2013) Lectin receptor kinases in plant innate immunity. Front. Plant Sci. 4, 124.
66. Singh, P., Kuo, Y.C., Mishra, S., et al. (2012a) The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell, 24, 1256-1270.
67. Singh, P., Chien, C.-C., Mishra, S., Tsai, C.-H., and, Zimmerli, L., (2012b) The Arabidopsis LECTIN RECEPTOR KINASE-VI.2 is a functional protein kinase and is dispensable for basal resistance to Botrytis cinerea. Plant Signal. Behav. 8, e22611.
68. Sticher, L., Mauch-Mani, B., and, Metraux, J.P., (1997) Systemic acquired resistance. Annu. Rev. Phytopathol. 35, 235-270.
69. Sun, Y.D., Li, L., Macho, A.P., Han, Z.F., Hu, Z.H., Zipfel, C., Zhou, J.M., and, Chai, J.J., (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science, 342, 624-628.
70. Tena, G., Boudsocq, M., and, Sheen, J., (2011) Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 14, 519-529.
71. Tsuda, K., and, Katagiri, F., (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459-465.
72. Van Wees, S.C., Van der Ent, S., and, Pieterse, C.M., (2008) Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11, 443-448.
73. Veronese, P., Nakagami, H., Bluhm, B., Abuqamar, S., Chen, X., Salmeron, J., Dietrich, R.A., Hirt, H., and, Mengiste, T., (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell, 18, 257-273.
74. Vinatzer, B.A., Teitzel, G.M., Lee, M.-W., Jelenska, J., Hotton, S., Fairfax, K., Jenrette, J., and, Greenberg, J.T., (2006) The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol. Microbiol. 62, 26-44.
75. Walter, M., Chaban, C., Schütze, K., et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438.
76. Wan, J., Zhang, X.C., Neece, D., Ramonell, K.M., Clough, S., Kim, S.Y., Stacey, M.G., and, Stacey, G., (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 20, 471-481.
77. Willmann, R., Lajunen, H.M., Erbs, G., et al. (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl Acad. Sci. USA, 108, 19824-19829.
78. Wulff, B.B.H., Horvath, D.M., and, Ward, E.R., (2011) Improving immunity in crops: new tactics in an old game. Curr. Opin. Plant Biol. 14, 468-476.
79. Yoo, S.D., Cho, Y.H., and, Sheen, J., (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
80. Zhang, J., Li, W., Xiang, T.T., et al. (2010) Receptor-like Cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe, 7, 290-301.
81. Zimmerli, L., Metraux, J.P., and, Mauch-Mani, B., (2001) beta-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 126, 517-523.
82. Zipfel, C., and, Robatzek, S., (2010) Pathogen-associated molecular pattern-triggered immunity: Veni, Vidi. ? Plant Physiol. 154, 551-554.
83. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D.G., Felix, G., and, Boller, T., (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428, 764-767.
84. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D.G., 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.