Chitin-mediated plant-fungal interactions: Catching, hiding and handshaking

Current Opinion in Plant Biology

Volumn 26, Issue , 2015, Pages 64-71

  Shinya, Tomonori ^a   Nakagawa, Tomomi ^b   Kaku, Hanae ^b   Shibuya, Naoto ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b MEIJI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI;

CHITIN; VEGETABLE PROTEIN;

FUNGUS; GENE EXPRESSION REGULATION; METABOLISM; MYCORRHIZA; PATHOGENICITY; PHYSIOLOGY; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

CHITIN; FUNGI; GENE EXPRESSION REGULATION, PLANT; MYCORRHIZAE; PLANT PROTEINS; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84934960820     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2015.05.032     Document Type: Review

References (59)

1. Schwessinger B., Ronald P.C. Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 2012, 63:451-482.
2. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 2011, 11:539-548.
3. Dangl J.L., Horvath D.M., Staskawicz B.J. Pivoting the plant immune system from dissection to deployment. Science 2013, 341:746-751.
4. Kombrink A., Sanchez-Vallet A., Thomma B.P. The role of chitin detection in plant-pathogen interactions. Microbes Infect 2011, 13:1168-1176.
5. Silipo A., Erbs G., Shinya T., Dow J.M., Parrilli M., Lanzetta R., Shibuya N., Newman M.A., Molinaro A. Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 2010, 20:406-419.
6. Rovenich H., Boshoven J.C., Thomma B.P. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr Opin Plant Biol 2014, 20:96-103.
7. Schmitz A.M., Harrison M.J. Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 2014, 56:250-261.
8. Free S.J. Fungal cell wall organization and biosynthesis. Adv Genet 2013, 81:33-82.
9. Lenardon M.D., Munro C.A., Gow N.A. Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 2010, 13:416-423.
10. Shibuya N., Minami E. Oligosaccharide signalling for defense responses in plant. Physiol Mol Plant Pathol 2001, 59:223-233.
11. Collinge D.B., Kragh K.M., Mikkelsen J.D., Nielsen K.K., Rasmussen U., Vad K. Plant chitinases. Plant J 1993, 3:31-40.
12. Fujikawa T., Kuga Y., Yano S., Yoshimi A., Tachiki T., Abe K., Nishimura M. Dynamics of cell wall components of Magnaporthe grisea during infectious structure development. Mol Microbiol 2009, 73:553-570.
13. Gruber S., Seidl-Seiboth V. Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 2012, 158:26-34.
14. Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., Minami E., Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 2006, 103:11086-11091.
15. Buist G., Steen A., Kok J., Kuipers O.P. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 2008, 68:838-847.
16. Shimizu T., Nakano T., Takamizawa D., Desaki Y., Ishii-Minami N., Nishizawa Y., Minami E., Okada K., Yamane H., Kaku H., et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 2010, 64:204-214.
17. Shinya T., Motoyama N., Ikeda A., Wada M., Kamiya K., Hayafune M., Kaku H., Shibuya N. Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol 2012, 53:1696-1706.
18. Kouzai Y., Nakajima K., Hayafune M., Ozawa K., Kaku H., Shibuya N., Minami E., Nishizawa Y. CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol Biol 2014, 84:519-528.
19. Hayafune M., Berisio R., Marchetti R., Silipo A., Kayama M., Desaki Y., Arima S., Squeglia F., Ruggiero A., Tokuyasu K., et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA 2014, 111:E404-E413.
20. Liu B., Li J.F., Ao Y., Qu J., Li Z., Su J., Zhang Y., Liu J., Feng D., Qi K., et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012, 24:3406-3419.
21. Kouzai Y., Mochizuki S., Nakajima K., Desaki Y., Hayafune M., Miyazaki H., Yokotani N., Ozawa K., Minami E., Kaku H., et al. 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 2014, 27:975-982.
22. Ao Y., Li Z., Feng D., Xiong F., Liu J., Li J.F., Wang M., Wang J., Liu B., Wang H.B. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J 2014, 80:1072-1084.
23. Miya A., Albert P., Shinya T., Desaki Y., Ichimura K., Shirasu K., Narusaka Y., Kawakami N., Kaku H., Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 2007, 104:19613-19618.
24. Wan J., Zhang X.C., Neece D., Ramonell K.M., Clough S., Kim S.Y., Stacey M.G., Stacey G. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008, 20:471-481.
25. Iizasa E., Mitsutomi M., Nagano Y. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 2010, 285:2996-3004.
26. Petutschnig E.K., Jones A.M., Serazetdinova L., Lipka U., Lipka V. 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 2010, 285:28902-28911.
27. Liu T., Liu Z., Song C., Hu Y., Han Z., She J., Fan F., Wang J., Jin C., Chang J., et al. Chitin-induced dimerization activates a plant immune receptor. Science 2012, 336:1160-1164.
28. Cao Y., Liang Y., Tanaka K., Nguyen C.T., Jedrzejczak R.P., Joachimiak A., Stacey G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 2014, 3.
29. Faulkner C., Petutschnig E., Benitez-Alfonso Y., Beck M., Robatzek S., Lipka V., Maule A.J. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci USA 2013, 110:9166-9170.
30. Narusaka Y., Shinya T., Narusaka M., Motoyama N., Shimada H., Murakami K., Shibuya N. Presence of LYM2 dependent but CERK1 independent disease resistance in Arabidopsis. Plant Signal Behav 2013, 8:e25345.
31. Fliegmann J., Uhlenbroich S., Shinya T., Martinez Y., Lefebvre B., Shibuya N., Bono J.J. Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Physiol Biochem 2011, 49:709-720.
32. Gimenez-Ibanez S., Hann D.R., Ntoukakls V., Petutschnig E., Lipka V., Rathjen J.P. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 2009, 19:423-429.
33. Tanaka S., Ichikawa A., Yamada K., Tsuji G., Nishiuchi T., Mori M., Koga H., Nishizawa Y., O'Connell R., Kubo Y. HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol 2010, 10:288.
34. Lee W.S., Rudd J.J., Hammond-Kosack K.E., Kanyuka K. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol Plant Microbe Interact 2014, 27:236-243.
35. Yamaguchi K., Yamada K., Ishikawa K., Yoshimura S., Hayashi N., Uchihashi K., Ishihama N., Kishi-Kaboshi M., Takahashi A., Tsuge S., et al. 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 2013, 13:347-357.
36. Shinya T., Yamaguchi K., Desaki Y., Yamada K., Narisawa T., Kobayashi Y., Maeda K., Suzuki M., Tanimoto T., Takeda J., et al. Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J 2014, 79:56-66.
37. Akamatsu A., Wong H.L., Fujiwara M., Okuda J., Nishide K., Uno K., Imai K., Umemura K., Kawasaki T., Kawano Y., et al. An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 2013, 13:465-476.
38. Petutschnig E.K., Stolze M., Lipka U., Kopischke M., Horlacher J., Valerius O., Rozhon W., Gust A.A., Kemmerling B., Poppenberger B., et al. A novel Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor processing. New Phytol 2014, 204:955-967.
39. Bolton M.D., van Esse H.P., Vossen J.H., de Jonge R., Stergiopoulos I., Stulemeijer I.J., van den Berg G.C., Borras-Hidalgo O., Dekker H.L., de Koster C.G., et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 2008, 69:119-136.
40. de Jonge R., van Esse H.P., Kombrink A., Shinya T., Desaki Y., Bours R., van der Krol S., Shibuya N., Joosten M.H.A.J., Thomma B.P.H.J. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329:953-955.
41. Marshall R., Kombrink A., Motteram J., Loza-Reyes E., Lucas J., Hammond-Kosack K.E., Thomma B.P., Rudd J.J. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 2011, 156:756-769.
42. Mentlak T.A., Kombrink A., Shinya T., Ryder L.S., Otomo I., Saitoh H., Terauchi R., Nishizawa Y., Shibuya N., Thomma B.P., et al. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012, 24:322-335.
43. Sanchez-Vallet A., Saleem-Batcha R., Kombrink A., Hansen G., Valkenburg D.J., Thomma B.P., Mesters J.R. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2013, 2:e00790.
44. Chen X.L., Shi T., Yang J., Shi W., Gao X., Chen D., Xu X., Xu J.R., Talbot N.J., Peng Y.L. N-Glycosylation of effector proteins by an α-1,3-mannosyltransferase is required for the rice blast fungus to evade host innate immunity. Plant Cell 2014, 26:1360-1376.
45. van Esse H.P., Bolton M.D., Stergiopoulos L., de Wit P.J.G.M., Thomma B.P.H.J. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 2007, 20:1092-1101.
46. Fujikawa T., Sakaguchi A., Nishizawa Y., Kouzai Y., Minami E., Yano S., Koga H., Meshi T., Nishimura M. Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 2012, 8:e1002882.
47. El Gueddari N.E., Rauchhaus U., Moerschbacher B.M., Deising H.B. Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 2002, 156:103-112.
48. Antolin-Llovera M., Petutsching E.K., Ried M.K., Lipka V., Nurnberger T., Robatzek S., Parniske M. Knowing your friends and foes-plant receptor-like kinases as initiators of symbiosis or defence. New Phytol 2014, 204:791-802.
49. Oldroyd G.E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 2013, 11:252-263.
50. De Mita S., Streng A., Bisseling T., Geurts R. Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism. New Phytol 2014, 201:961-972.
51. Nakagawa T., Kaku H., Shimoda Y., Sugiyama A., Shimamura M., Takanashi K., Yazaki K., Aoki T., Shibuya N., Kouchi H. 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 2011, 65:169-180.
52. Madsen E.B., Antolin-Llovera M., Grossmann C., Ye J., Vieweg S., Broghammer A., Krusell L., Radutoiu S., Jensen O.N., Stougaard J., et al. 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 2011, 65:404-417.
53. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008, 6:763-775.
54. Maillet F., Poinsot V., Andre O., Puech-Pages V., Haouy A., Gueunier M., Cromer L., Giraudet D., Formey D., Niebel A., et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-63.
55. Czaja L.F., Hogekamp C., Lamm P., Maillet F., Martinez E.A., Samain E., Denarie J., Kuster H., Hohnjec N. 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 2012, 159:1671-1685.
56. Op den Camp R., Streng A., De Mita S., Cao Q., Polone E., Liu W., Ammiraju J.S., Kudrna D., Wing R., Untergasser A., et al. LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 2011, 331:909-912.
57. Genre A., Chabaud M., Balzergue C., Puech-Pages V., Novero M., Rey T., Fournier J., Rochange S., Becard G., Bonfante P., et al. 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 2013, 198:190-202.
58. Miyata K., Kozaki T., Kouzai Y., Ozawa K., Ishii K., Asamizu E., Okabe Y., Umehara Y., Miyamoto A., Kobae Y., et al. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol 2014, 55:1864-1872.
59. Zhang X., Dong W., Sun J., Feng F., Deng Y., He Z., Oldroyd G.E., Wang E. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J 2015, 81:258-267.