Functional analysis of chimeric lysin motif domain receptors mediating Nod factor-induced defense signaling in Arabidopsis thaliana and chitin-induced nodulation signaling in Lotus japonicus

Plant Journal

Volumn 78, Issue 1, 2014, Pages 56-69

  Wang, Wei ^a,b   Xie, Zhi Ping ^a   Staehelin, Christian ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arabidopsis thaliana; chimeric receptor; chitin; defense signaling; Lotus japonicus; LysM domain receptor; Nod factors; nodulation signaling

Indexed keywords

CHITIN; ENZYMES; GENES; PLANTS (BOTANY);

ARABIDOPSIS THALIANA; CHIMERIC RECEPTORS; DEFENSE SIGNALING; LOTUS JAPONICUS; LYSM DOMAIN RECEPTOR; NOD FACTOR; NODULATION;

SIGNALING;

ARABIDOPSIS PROTEIN; CERK1 PROTEIN, ARABIDOPSIS; CHITIN; LYSIN; MUCOPROTEIN; OLIGOSACCHARIDE; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

ARABIDOPSIS; FUSARIUM; GENETICS; IMMUNOLOGY; LOTUS; METABOLISM; MUTATION; NODULATION; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; RICE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHITIN; FUSARIUM; GENES, REPORTER; LOTUS; MUCOPROTEINS; MUTATION; OLIGOSACCHARIDES; ORYZA SATIVA; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOT NODULATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84897035674     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12450     Document Type: Article

References (65)

1. Akamatsu, A., Wong, H.L., Fujiwara, M., et al. (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe, 13, 465-476.
2. Albert, M., Jehle, A.K., Mueller, K., Eisele, C., Lipschis, M., and, Felix, G., (2010) Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors. J. Biol. Chem. 285, 19035-19042.
3. Arrighi, J.F., Barre, A., Ben Amor, B., et al. (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265-279.
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., et al. (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl Acad. Sci. USA, 109, 13859-13864.
6. Broughton, W.J., and, Dilworth, M.J., (1971) Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125, 1075-1080.
7. Brutus, A., Sicilia, F., Macone, A., Cervone, F., and, De Lorenzo, G., (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl Acad. Sci. USA, 107, 9452-9457.
8. Chabaud, M., Boisson-Dernier, A., Zhang, J., Taylor, C.G., Yu, O., and, Barker, D.G., (2006) Agrobacterium rhizogenes-Mediated Root Transformation. The Samuel Roberts Noble Foundation, Ardmore, OK, USA: The Medicago truncatula Handbook.
9. Constantinescu, S.N., Keren, T., Socolovsky, M., Nam, H.S., Henis, Y.I., and, Lodish, H.F., (2001) Ligand-independent oligomerization of cell-surface erythropoietin receptor is mediated by the transmembrane domain. Proc. Natl Acad. Sci. USA, 98, 4379-4384.
10. Davis, T.L., Walker, J.R., Loppnau, P., Butler-Cole, C., Allali-Hassani, A., and, Dhe-Paganon, S., (2008) Autoregulation by the juxtamembrane region of the human ephrin receptor tyrosine kinase A3 (EphA3). Structure, 16, 873-884.
11. 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.
12. Felix, G., Regenass, M., and, Boller, T., (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J. 4, 307-316.
13. Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.H., Lin, Y.H., Reid, D.E., and, Gresshoff, P.M., (2010) Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61-76.
14. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198, 190-202.
15. 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.
16. Gust, A.A., Willmann, R., Desaki, Y., Grabherr, H.M., and, Nürnberger, T., (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci. 17, 495-502.
17. Hamel, L.P., and, Beaudoin, N., (2010) Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta, 232, 787-806.
18. He, Z., Wang, Z.Y., Li, J., Zhu, Q., Lamb, C., Ronald, P., and, Chory, J., (2000) Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science, 288, 2360-2363.
19. Heckmann, A.B., Lombardo, F., Miwa, H., Perry, J.A., Bunnewell, S., Parniske, M., Wang, T.L., and, Downie, J.A., (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol. 142, 1739-1750.
20. Hussain, A.A., Jiang, Q., Broughton, W.J., and, Gresshoff, P.M., (1999) Lotus japonicus nodulates and fixes nitrogen with the broad host range Rhizobium sp. NGR234. Plant Cell Physiol. 40, 894-899.
21. Iizasa, E.I., Mitsutomi, M., and, Nagano, Y., (2010) Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 285, 2996-3004.
22. Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C.D., Men, A., Carroll, B.J., and, Gresshoff, P.M., (2010) Inactivation of duplicated Nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. 51, 201-214.
23. Indrasumunar, A., Searle, I., Lin, M.H., Kereszt, A., Men, A., Carroll, B.J., and, Gresshoff, P.M., (2011) Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr). Plant J. 65, 39-50.
24. 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.
25. Ke, D., Fang, Q., Chen, C., Zhu, H., Chen, T., Chang, X., Yuan, S., Kang, H., Hong, Z., and, Zhang, Z., (2012) The small GTPase ROP6 interacts with NFR5 and is involved in nodule formation in Lotus japonicus. Plant Physiol. 159, 131-143.
26. Kishi-Kaboshi, M., Okada, K., Kurimoto, L., et al. (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J. 63, 599-612.
27. Kishimoto, K., Kouzai, Y., Kaku, H., Shibuya, N., Minami, E., and, Nishizawa, Y., (2010) Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 64, 343-354.
28. Kouzai, Y., Kaku, H., Shibuya, N., Minami, E., and, Nishizawa, Y., (2013) Expression of the chimeric receptor between the chitin elicitor receptor CEBiP and the receptor-like protein kinase Pi-d2 leads to enhanced responses to the chitin elicitor and disease resistance against Magnaporthe oryzae in rice. Plant Mol. Biol. 81, 287-295.
29. Liang, Y., Cao, Y., Tanaka, K., Thibivilliers, S., Wan, J., Choi, J., Kang, C., Qiu, J., and, Stacey, G., (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science, 341, 1384-1387.
30. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., and, Geurts, R., (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science, 302, 630-633.
31. 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.
32. Liu, T., Liu, Z., Song, C., et al,. (2012b) Chitin-induced dimerization activates a plant immune receptor. Science, 336, 1160-1164.
33. Lohmann, G.V., Shimoda, Y., Nielsen, M.W., et al. (2010) Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant Microbe Interact. 23, 510-521.
34. Lopez-Gomez, M., Sandal, N., Stougaard, J., and, Boller, T., (2012) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J. Exp. Bot. 63, 393-401.
35. Madsen, E.B., Madsen, L.H., Radutoiu, S., et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature, 425, 637-640.
36. Madsen, E.B., Antolin-Llovera, M., Grossmann, C., 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.
37. Maillet, F., Poinsot, V., André, O., et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 469, 58-63.
38. 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.
39. Mueller, K., Bittel, P., Chinchilla, D., Jehle, A.K., Albert, M., Boller, T., and, Felix, G., (2012) Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato. Plant Cell, 24, 2213-2224.
40. Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takanashi, K., Yazaki, K., Aoki, T., Shibuya, N., and, Kouchi, H., (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.
41. Oláh, B., Brière, C., Bécard, G., Dénarié, J., and, Gough, C., (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44, 195-207.
42. Oldroyd, G.E., (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252-263.
43. Perret, X., Staehelin, C., and, Broughton, W.J., (2000) Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180-201.
44. 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.
45. 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.
46. Price, N.P.J., Relic, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S.G., Maillet, F., Dénarié, J., Promé, J.C., and, Broughton, W.J., (1992) Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6, 3575-3584.
47. Radutoiu, S., Madsen, L.H., Madsen, E.B., et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 425, 585-592.
48. Schauser, L., Roussis, A., Stiller, J., and, Stougaard, J., (1999) A plant regulator controlling development of symbiotic root nodules. Nature, 402, 191-195.
49. 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.
50. 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.
51. Soyano, T., Kouchi, H., Hirota, A., and, Hayashi, M., (2013) Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet. 9, e1003352.
52. Spaink, H.P., Okker, R.J., Wijffelman, C.A., Tak, T., Goosen-de Roo, L., Pees, E., van Brussel, A.A., and, Lugtenberg, B.J., (1989) Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J. Bacteriol. 171, 4045-4053.
53. Staehelin, C., Granado, J., Müller, J., Wiemken, A., Mellor, R.B., Felix, G., Regenass, M., Broughton, W.J., and, Boller, T., (1994) Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc. Natl Acad. Sci. USA, 91, 2196-2200.
54. Staehelin, C., Xie, Z.P., Illana, A., and, Vierheilig, H., (2011) Long-distance transport of signals during symbiosis: are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal. Behav. 6, 372-377.
55. Töpfer, R., Matzeit, V., Gronenborn, B., Schell, J., and, Steinbiss, H.H., (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res. 15, 5890.
56. Wan, J., Zhang, S., and, Stacey, G., (2004) Activation of a mitogen-activated protein kinase pathway in Arabidopsis by chitin. Mol. Plant Pathol. 5, 125-135.
57. 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.
58. 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.
59. 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.
60. Xie, Z.P., Staehelin, C., Vierheilig, H., Wiemken, A., Jabbouri, S., Broughton, W.J., Vögeli-Lange, R., and, Boller, T., (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol. 108, 1519-1525.
61. Xie, Z.P., Müller, J., Wiemken, A., Broughton, W.J., and, Boller, T., (1997) Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureus. New Phytol. 139, 361-366.
62. Yamaguchi, K., Yamada, K., Ishikawa, K., et al. (2013) 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.
63. Yang, K.Y., Liu, Y., and, Zhang, S., (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl Acad. Sci. USA, 98, 741-746.
64. Zhang, S., and, Liu, Y., (2001) Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell, 13, 1877-1889.
65. Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., and, Chua, N.H., (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646.