Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27

Plant Journal

Volumn 79, Issue 1, 2014, Pages 56-66

  Shinya, Tomonori ^a,b   Yamaguchi, Koji ^c   Desaki, Yoshitake ^a   Yamada, Kenta ^c   Narisawa, Tomoko ^a   Kobayashi, Yoshihiro ^a   Maeda, Kanako ^a   Suzuki, Maruya ^a   Tanimoto, Takumi ^a   Takeda, Jun ^a   Nakashima, Masato ^a   Funama, Ryota ^c   Narusaka, Mari ^d   Narusaka, Yoshihiro ^d   Kaku, Hanae ^a   Kawasaki, Tsutomu ^c   Shibuya, Naoto ^a  

^a MEIJI UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c KINKI UNIVERSITY   (Japan)

^d Research Institute for Biological Science OKAYAMA   (Japan)

Author keywords

Arabidopsis thaliana; CERK1; chitin; microbe associated molecular pattern; PBL27; plant immunity; receptor; receptor like cytoplasmic kinase

Indexed keywords

BACTERIA; ENZYMES; PATTERN RECOGNITION; PHOSPHORYLATION;

ARABIDOPSIS THALIANA; CERK1; MOLECULAR PATTERNS; PBL27; PLANT IMMUNITIES; RECEPTOR; RECEPTOR-LIKE CYTOPLASMIC KINASE;

CHITIN;

ARABIDOPSIS PROTEIN; BAK1 PROTEIN, ARABIDOPSIS; CALLOSE; CELL RECEPTOR; CERK1 PROTEIN, ARABIDOPSIS; CHITIN; GLUCAN; PATTERN RECOGNITION RECEPTOR; PBL27 PROTEIN, ARABIDOPSIS; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE;

ALTERNARIA; ARABIDOPSIS; BIOLOGICAL MODEL; CELL MEMBRANE; DISEASE RESISTANCE; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; SIGNAL TRANSDUCTION; TOBACCO; TRANSGENIC PLANT;

ALTERNARIA; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CHITIN; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; GLUCANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TOBACCO;

EID: 84903178917     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12535     Document Type: Article

References (43)

1. Albert, P., Miya, A., Hiratsuka, K., Kawakami, N., and, Shibuya, N., (2006) A high-throughput evaluation system for Arabidopsis mutants for defense signaling. Plant Biotechnol. 23, 459-466.
2. Antolin-Llovera, M., Ried, M.K., Binder, A., and, Parniske, M., (2012) Receptor kinase signaling pathways in plant-microbe interactions. Annu. Rev. Phytopathol. 50, 451-473.
3. 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.
4. 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.
5. Faulkner, C., Petutschnig, E., Benitez-Alfonso, Y., Beck, M., Robatzek, S., Lipka, V., and, Maule, A.J., (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl Acad. Sci. USA, 110, 9166-9170.
6. 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.
7. Gehl, C., Waadt, R., Kudla, J., Mendel, R.R., and, Hansch, R., (2009) New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol. Plant, 2, 1051-1058.
8. Gomez-Gomez, 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.
9. Gust, A.A., Biswas, R., Lenz, H.D., et al. (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 282, 32338-32348.
10. Hayafune, M., Berisio, R., Marchetti, R., et al. (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl Acad. Sci. USA, 111, E404-E413.
11. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., and, Shibuya, N., (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl Acad. Sci. USA, 103, 11086-11091.
12. Liu, B., Li, J.F., Ao, Y., et al. (2012a) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell, 24, 3406-3419.
13. Liu, T., Liu, Z., Song, C., et al. (2012b) Chitin-induced dimerization activates a plant immune receptor. Science, 336, 1160-1164.
14. Liu, Z., Wu, Y., Yang, F., Zhang, Y., Chen, S., Xie, Q., Tian, X., and, Zhou, J.M., (2013) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc. Natl Acad. Sci. USA, 110, 6205-6210.
15. Lu, D., Wu, S., Gao, X., Zhang, Y., Shan, L., and, He, P., (2010) 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.
16. Millet, Y.A., Danna, C.H., Clay, N.K., Songnuan, W., Simon, M.D., Werck-Reichhart, D., and, Ausubel, F.M., (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell, 22, 973-990.
17. 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.
18. Monaghan, J., and, Zipfel, C., (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349-357.
19. 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.
20. Narusaka, Y., Narusaka, M., Seki, M., Ishida, J., Shinozaki, K., Nan, Y., Park, P., Shiraishi, T., and, Kobayashi, M., (2005) Cytological and molecular analyses of non-host resistance of Arabidopsis thaliana to Alternaria alternata. Mol. Plant Pathol. 6, 615-627.
21. Narusaka, Y., Shinya, T., Narusaka, M., Motoyama, N., Shimada, H., Murakami, K., and, Shibuya, N., (2013) Presence of LYM2 dependent but CERK1 independent disease resistance in Arabidopsis. Plant Signal. Behav. 8, e25345.
22. Petutschnig, E.K., Jones, A.M., Serazetdinova, L., Lipka, U., and, Lipka, V., (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285, 28902-28911.
23. Pietraszewska-Bogiel, A., Lefebvre, B., Koini, M.A., Klaus-Heisen, D., Takken, F.L., Geurts, R., Cullimore, J.V., and, Gadella, T.W., (2013) Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses. PLoS ONE, 8, e65055.
24. 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.
25. Sainsbury, F., Thuenemann, E.C., and, Lomonossoff, G.P., (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol. J. 7, 682-693.
26. Schulze, B., Mentzel, T., Jehle, A.K., Mueller, K., Beeler, S., Boller, T., Felix, G., and, Chinchilla, D., (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451.
27. 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.
28. 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.
29. Shimizu, T., Nakano, T., Takamizawa, D., et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204-214.
30. Shinya, T., Motoyama, N., Ikeda, A., Wada, M., Kamiya, K., Hayafune, M., Kaku, H., and, Shibuya, N., (2012) Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. 53, 1696-1706.
31. Shiu, S.H., Karlowski, W.M., Pan, R., Tzeng, Y.H., Mayer, K.F., and, Li, W.H., (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell, 16, 1220-1234.
32. Silipo, A., Erbs, G., Shinya, T., Dow, J.M., Parrilli, M., Lanzetta, R., Shibuya, N., Newman, M.A., and, Molinaro, A., (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology, 20, 406-419.
33. Sun, W., Cao, Y., Jansen Labby, K., Bittel, P., Boller, T., and, Bent, A.F., (2012) Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell, 24, 1096-1113.
34. Sun, Y., Li, L., Macho, A.P., Han, Z., Hu, Z., Zipfel, C., Zhou, J.M., and, Chai, J., (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science, 342, 624-628.
35. Wan, J., Patel, A., Mathieu, M., Kim, S.Y., Xu, D., and, Stacey, G., (2008a) A lectin receptor-like kinase is required for pollen development in Arabidopsis. Plant Mol. Biol. 67, 469-482.
36. Wan, J., Zhang, X.C., Neece, D., Ramonell, K.M., Clough, S., Kim, S.Y., Stacey, M.G., and, Stacey, G., (2008b) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 20, 471-481.
37. Wan, J., Tanaka, K., Zhang, X.C., Son, G.H., Brechenmacher, L., Nguyen, T.H., and, Stacey, G., (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 160, 396-406.
38. 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.
39. Yamaguchi, K., Imai, K., Akamatsu, A., Mihashi, M., Hayashi, N., Shimamoto, K., and, Kawasaki, T., (2012) SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J. 70, 389-397.
40. Yamaguchi, K., Yamada, K., Ishikawa, K., et al. (2013a) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe, 13, 347-357.
41. Yamaguchi, K., Yamada, K., and, Kawasaki, T., (2013b) Receptor-like cytoplasmic kinases are pivotal components in pattern recognition receptor-mediated signaling in plant immunity. Plant Signal. Behav. 8, e25662.
42. Zhang, J., Li, W., Xiang, 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.
43. 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.