The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice

Plant and Cell Physiology

Volumn 55, Issue 11, 2014, Pages 1864-1872

  Miyata, Kana ^a   Kozaki, Toshinori ^b   Kouzai, Yusuke ^c   Ozawa, Kenjirou ^c   Ishii, Kazuo ^b   Asamizu, Erika ^d   Okabe, Yoshihiro ^d   Umehara, Yosuke ^c   Miyamoto, Ayano ^a   Kobae, Yoshihiro ^e   Akiyama, Kohki ^f   Kaku, Hanae ^a   Nishizawa, Yoko ^c   Shibuya, Naoto ^a   Nakagawa, Tomomi ^a  

^a MEIJI UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f Osaka Prefecture University   (Japan)

Author keywords

Arbuscular mycorrhizal fungi; Defense; Lotus japonicus; Rhizobia; Rice; Symbiosis

Indexed keywords

FABACEAE; FUNGI; LOTUS CORNICULATUS VAR. JAPONICUS; RHIZOBIUM;

CHITIN; PROTEIN SERINE THREONINE KINASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; IMMUNOLOGY; LOTUS; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; MYCORRHIZA; PHYSIOLOGY; PROTEIN MOTIF; RHIZOBIUM; RICE; SIGNAL TRANSDUCTION; SYMBIOSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CHITIN; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; LOTUS; MOLECULAR SEQUENCE DATA; MUTATION; MYCORRHIZAE; ORYZA SATIVA; PLANT PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84911964533     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu129     Document Type: Article

References (47)

1. Ane, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E., Ayax, C. et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367.
2. Arrighi, J.F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L.C., Mirabella, R. et al. (2006) The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new noduleexpressed genes. Plant Physiol. 142: 265-279.
3. Becard, G. and Fortin, J.A. (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108: 211-218.
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. Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J.T., Maolanon, N. et al. (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl Acad. Sci. USA 109: 13859-13864.
6. Czaja, L.F., Hogekamp, C., Lamm, P., Maillet, F., Martinez, E.A., Samain, E. et al. (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP-and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol. 159: 1671-1685.
7. de Jonge, R., van Esse, H.P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R. et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitintriggered immunity in plants. Science 329: 953-955.
8. De Mita, S., Streng, A., Bisseling, T. and Geurts, R. (2014) Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism. New Phytol. 201: 961-972.
9. Delaux, P.M., Becard, G. and Combier, J.P. (2013) NSP1 is a component of the Myc signaling pathway. New Phytol. 199: 59-65.
10. Dodds, P.N. and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11: 539-548.
11. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kalo, P. and Kiss, G.B. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.
12. Genre, A., Chabaud, M., Balzergue, C., Puech-Pages, V., Novero, M., Rey, T. et al. (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198: 190-202.
13. 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.
14. Groth, M., Takeda, N., Perry, J., Uchida, H., Draxl, S., Brachmann, A. et al. (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22: 2509-2526.
15. Gutjahr, C., Banba, M., Croset, V., An, K., Miyao, A., An, G. et al. (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20: 2989-3005.
16. Ihaka, R. and Gentleman, R. (1996) R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5: 299-314.
17. Imaizumi-Anraku, H., Takeda, N., Charpentier, M., Perry, J., Miwa, H., Umehara, Y. et al. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433: 527-531.
18. John, M., Rohrig, H., Schmidt, J., Wieneke, U. and Schell, J. (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc. Natl Acad. Sci. USA 90: 625-629.
19. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K. et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl Acad. Sci. USA 103: 11086-11091.
20. Kanamori, N., Madsen, L.H., Radutoiu, S., Frantescu, M., Quistgaard, E.M., Miwa, H. et al. (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl Acad. Sci. USA 103: 359-364.
21. Kouchi, H., Imaizumi-Anraku, H., Hayashi, M., Hakoyama, T., Nakagawa, T., Umehara, Y. et al. (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51: 1381-1397.
22. Kouzai, Y., Mochizuki, S., Nakajima, K., Desaki, Y., Hayafune, M., Miyasaki, H. et al. (2014a) Targeted gene disruption of OsCERK1 reveals its indispensable role in chitin perception and involvement in the peptidoglycan response and immunity in rice. Mol. Plant Microbe Interact. 27: 975-982.
23. Kouzai, Y., Nakajima, K., Hayafune, M., Ozawa, K., Kaku, H., Shibuya, N. et al. (2014b) CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol. Biol. 84: 519-528.
24. Kunishima, M., Kawachi, C., Hioki, K., Terao, K. and Tani, S. (2001) Formation of carboxamides by direct condensation of carboxylic acids and amines in alcohols using a new alcohol-and water-soluble condensing agent: DMT-MM. Tetrahedron 57: 1551-1558.
25. Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods 9: 357-359.
26. Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G. et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
27. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T. and Geurts, R. (2003) LysM domain receptor kinases regulating rhizobial Nod factorinduced infection. Science 302: 630-633.
28. Liu, T., Liu, Z., Song, C., Hu, Y., Han, Z., She, J. et al. (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336: 1160-1164.
29. Madsen, E.B., Antolin-Llovera, M., Grossmann, C., Ye, J., Vieweg, S., Broghammer, A. et al. (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65: 404-417.
30. Madsen, E.B., Madsen, L.H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K. et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640.
31. Maillet, F., Poinsot, V., Andre, O., Puech-Pages, V., Haouy, A., Gueunier, M. et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
32. Messinese, E., Mun, J.H., Yeun, L.H., Jayaraman, D., Rouge, P., Barre, A. et al. (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium-and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant Microbe Interact. 20: 912-921.
33. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K. et al. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 104: 19613-19618.
34. Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takanashi, K. et al. (2011) From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J. 65: 169-180.
35. Op den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W. et al. (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331: 909-912.
36. Parniske, M. (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6: 763-775.
37. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M. et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592.
38. Redecker, D., Kodner, R. and Graham, L.E. (2000) Glomalean fungi from the Ordovician. Science 289: 1920-1921.
39. Saito, K., Yoshikawa, M., Yano, K., Miwa, H., Uchida, H., Asamizu, E. et al. (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19: 610-624.
40. Schultze, M., Staehelin, C., Rohrig, H., John, M., Schmidt, J., Kondorosi, E. et al. (1995) In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure. Proc. Natl Acad. Sci. USA 92: 2706-2709.
41. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y. et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64: 204-214.
42. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T. et al. (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962.
43. Takeda, N., Tsuzuki, S., Suzaki, T., Parniske, M. and Kawaguchi, M. (2013) CERBERUS and NSP1 of Lotus japonicus are common symbiosis genes that modulate arbuscular mycorrhiza development. Plant Cell Physiol. 54: 1711-1723.
44. Willmann, R., Lajunen, H.M., Erbs, G., Newman, M.A., Kolb, D., Tsuda, K. 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.
45. Yano, K., Yoshida, S., Muller, J., Singh, S., Banba, M., Vickers, K. et al. (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. USA 105: 20540-20545.
46. Zhang, X.C., Wu, X., Findley, S., Wan, J., Libault, M., Nguyen, H.T. et al. (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol. 144: 623-636.
47. Zhu, H., Riely, B.K., Burns, N.J. and Ane, J.M. (2006) Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 172: 2491-2499.