A novel Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor processing

New Phytologist

Volumn 204, Issue 4, 2014, Pages 955-967

  Petutschnig, Elena K ^a,b   Stolze, Marnie ^a   Lipka, Ulrike ^b,c   Kopischke, Michaela ^a,b   Horlacher, Juliane ^a   Valerius, Oliver ^d   Rozhon, Wilfried ^e   Gust, Andrea A ^c   Kemmerling, Birgit ^c   Poppenberger, Brigitte ^e   Braus, Gerhard H ^d   Nürnberger, Thorsten ^c   Lipka, Volker ^a,b,c  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b NORWICH RESEARCH PARK   (United Kingdom)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1); Arabidopsis; Cell death; Ectodomain shedding; Lysin motif receptor like kinase (LysM RLK); Pattern recognition receptor (PRR); Powdery mildew; Receptor processing

Indexed keywords

ARABIDOPSIS; ERYSIPHALES;

ARABIDOPSIS PROTEIN; CERK1 PROTEIN, ARABIDOPSIS; CHITIN; PROTEIN SERINE THREONINE KINASE; SALICYLIC ACID;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; ASCOMYCETES; CELL DEATH; CYTOLOGY; DRUG EFFECTS; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL DEATH; CHITIN; HOST-PATHOGEN INTERACTIONS; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SALICYLIC ACID; SIGNAL TRANSDUCTION;

EID: 84911992453     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12920     Document Type: Article

References (59)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, USA 95: 10306-10311.
2. Antolin-Llovera M, Ried MK, Parniske M. 2014. Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with Nod factor receptor 5. Current Biology: CB 24: 422-427.
3. Arribas J, Borroto A. 2002. Protein ectodomain shedding. Chemical Reviews 102: 4627-4638.
4. Bi D, Cheng YT, Li X, Zhang Y. 2010. Activation of plant immune responses by a gain-of-function mutation in an atypical receptor-like kinase. Plant Physiology 153: 1771-1779.
5. Borner GH, Lilley KS, Stevens TJ, Dupree P. 2003. Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiology 132: 568-577.
6. Carpenter G, Liao HJ. 2009. Trafficking of receptor tyrosine kinases to the nucleus. Experimental Cell Research 315: 1556-1566.
7. Castells E, Casacuberta JM. 2007. Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. Journal of Experimental Botany 58: 3503-3511.
8. Deslandes L, Rivas S. 2012. Catch me if you can: bacterial effectors and plant targets. Trends in Plant Science 17: 644-655.
9. Dou D, Zhou JM. 2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host & Microbe 12: 484-495.
10. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proceedings of the National Academy of Sciences, USA 110: 9166-9170.
11. Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng YT, Chen S, Li X et al. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host & Microbe 6: 34-44.
12. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP. 2009. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Current Biology: CB 19: 423-429.
13. Glazebrook J, Rogers EE, Ausubel FM. 1996. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973-982.
14. Gómez-Gómez L, Boller T. 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Molecular Cell 5: 1003-1011.
15. Halter T, Imkampe J, Mazzotta S, Wierzba M, Postel S, Bucherl C, Kiefer C, Stahl M, Chinchilla D, Wang X et al. 2014. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Current Biology: CB 24: 134-143.
16. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proceedings of the National Academy of Sciences, USA 111: E404-E413. doi: 10.1073/pnas.1312099111.
17. Hayashida K, Bartlett AH, Chen Y, Park PW. 2010. Molecular and cellular mechanisms of ectodomain shedding. Anatomical Record (Hoboken, NJ, USA: 2007) 293: 925-937.
18. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J. 2007. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Current Biology: CB 17: 1109-1115.
19. Higashiyama S, Nanba D, Nakayama H, Inoue H, Fukuda S. 2011. Ectodomain shedding and remnant peptide signalling of EGFRs and their ligands. Journal of Biochemistry 150: 15-22.
20. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL. 2002. Arabidopsis map-based cloning in the post-genome era. Plant Physiology 129: 440-450.
21. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Müssig C et al. 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Current Biology: CB 17: 1116-1122.
22. Kim BH, Kim SY, Nam KH. 2013. Assessing the diverse functions of BAK1 and its homologs in arabidopsis, beyond BR signaling and PTI responses. Molecules and Cells 35: 7-16.
23. Lal M, Caplan M. 2011. Regulated intramembrane proteolysis: signaling pathways and biological functions. Physiology 26: 34-44.
24. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M et al. 2012. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research 40(Database issue): 1202-1210.
25. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J. 1995. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant-Microbe Interactions 8: 863-870.
26. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC. 2009. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326: 850-853.
27. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC. 2013. Retraction. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 342: 191.
28. Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH, America AH, Sklenar J, Jones AM, Tameling WI, Robatzek S et al. 2013. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proceedings of the National Academy of Sciences, USA 110: 10010-10015.
29. Liebrand TW, van den Burg HA, Joosten MH. 2014. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends in Plant Science 19: 123-132.
30. Lipka U, Fuchs R, Lipka V. 2008. Arabidopsis non-host resistance to powdery mildews. Current Opinion in Plant Biology 11: 404-411.
31. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D et al. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
32. Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan F, Wang J, Jin C, Chang J et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336: 1160-1164.
33. Lu H, Rate DN, Song JT, Greenberg JT. 2003. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. The Plant Cell 15: 2408-2420.
34. Lukowitz W, Gillmor CS, Scheible WR. 2000. Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiology 123: 795-805.
35. Meinke DW. 2013. A survey of dominant mutations in Arabidopsis thaliana. Trends in Plant Science 18: 84-91.
36. Meyer Y, Grosset J, Chartier Y, Cleyet-Marel JC. 1988. Preparation by two-dimensional electrophoresis of proteins for antibody production: antibodies against proteins whose synthesis is reduced by auxin in tobacco mesophyll protoplasts. Electrophoresis 9: 704-712.
37. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proceedings of the National Academy of Sciences, USA 104: 19613-19618.
38. Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology 15: 349-357.
39. Newman MA, Sundelin T, Nielsen JT, Erbs G. 2013. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers in Plant Science 4: 139.
40. Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC. 2003. Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969-972.
41. Park CJ, Ronald PC. 2012. Cleavage and nuclear localization of the rice XA21 immune receptor. Nature Communications 3: 920.
42. Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, 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. Journal of Biological Chemistry 285: 28902-28911.
43. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries S, 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. The Plant Cell 23: 2440-2455.
44. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C. 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genetics 7: e1002046.
45. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analytical Chemistry 68: 850-858.
46. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H et al. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant Journal: For Cell and Molecular Biology 64: 204-214.
47. Shirano Y, Kachroo P, Shah J, Klessig DF. 2002. A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. The Plant Cell 14: 3149-3162.
48. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, Epple P, Kuhns C, Sureshkumar S, Schwartz C, Lanz C et al. 2010. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465: 632-636.
49. Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Nguyen TH, Stacey G. 2012. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiology 160: 396-406.
50. Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S, Kim S-Y, Stacey MG, Stacey G. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. The Plant Cell 20: 471-481.
51. Weber S, Saftig P. 2012. Ectodomain shedding and ADAMs in development. Development 139: 3693-3709.
52. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565.
53. Willmann R, Lajunen HM, Erbs G, Newman M-A, Kolb D, Tsuda K, Katagiri F, Fliegmann J, Bono J-J, Cullimore JV et al. 2011. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proceedings of the National Academy of Sciences, USA 108: 19824-19829.
54. Zeng L, Velasquez AC, Munkvold KR, Zhang J, Martin GB. 2012. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant Journal: For Cell and Molecular Biology 69: 92-103.
55. Zhang L, Kars I, Essenstam B, Liebrand TW, Wagemakers L, Elberse J, Tagkalaki P, Tjoitang D, van den Ackerveken G, van Kan JA. 2014. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiology 164: 352-364.
56. Zhang W, Fraiture M, Kolb D, Loffelhardt B, Desaki Y, Boutrot FF, Tor M, Zipfel C, Gust AA, Brunner F. 2013. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. The Plant Cell 25: 4227-4241.
57. Zhang Y, Goritschnig S, Dong X, Li X. 2003. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. The Plant Cell 15: 2636-2646.
58. Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X. 2010. Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. The Plant Cell 22: 3153-3163.
59. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.