Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1

Cell Research

Volumn 25, Issue 1, 2015, Pages 110-120

  Tang, Jiao ^a   Han, Zhifu ^a   Sun, Yadong ^a   Zhang, Heqiao ^a   Gong, Xinqi ^a   Chai, Jijie ^a  

^a Tsinghua University   (China)

Author keywords

AtPeps; BAK1; Crystal structure; LRR; PEPR1; Repeat receptor kinase

Indexed keywords

ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; PEPR1 PROTEIN, ARABIDOPSIS; PEPTIDE;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT;

EID: 84920282062     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.161     Document Type: Article

References (46)

1. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004; 16:1220-1234.
2. Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 2009; 60:379-406.
3. Ryan CA, Huffaker A, Yamaguchi Y. New insights into innate immunity in Arabidopsis. Cell Microbiol 2007; 9:1902-1908.
4. Macho AP, Zipfel C. Plant PRRs and the activation of innate immune signaling. Mol Cell 2014; 54:263-272.
5. Gomez-Gomez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 2000; 5:1003-1011.
6. Zipfel C, Kunze G, Chinchilla D, et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 2006; 125:749-760.
7. Miya A, Albert P, Shinya T, et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 2007; 104:19613-19618.
8. Wan J, Zhang XC, Neece D, et al. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008; 20:471-481.
9. Chinchilla D, Zipfel C, Robatzek S, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007; 448:497-500.
10. Chinchilla D, Shan L, He P, de Vries S, Kemmerling B. One for all: the receptor-associated kinase BAK1. Trends Plant Sci 2009; 14:535-541.
11. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 2002; 110:213-222.
12. Nam KH, Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 2002; 110:203-212.
13. Liu T, Liu Z, Song C, et al. Chitin-induced dimerization activates a plant immune receptor. Science 2012; 336:1160-1164.
14. Huffaker A, Pearce G, Ryan CA. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 2006; 103:10098-10103.
15. Pearce G, Yamaguchi Y, Munske G, Ryan CA. Structure-activity studies of AtPep1, a plant peptide signal involved in the innate immune response. Peptides 2008; 29:2083-2089.
16. Bartels S, Lori M, Mbengue M, et al. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J Exp Bot 2013; 64:5309-5321.
17. Ryan CA, Pearce G. Systemins: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci USA 2003; 100 Suppl 2:14577-14580.
18. Yamaguchi Y, Pearce G, Ryan CA. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA 2006; 103:10104-10109.
19. Krol E, Mentzel T, Chinchilla D, et al. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 2010; 285:13471-13479.
20. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 2010; 22:508-522.
21. Qi Z, Verma R, Gehring C, et al. Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proc Natl Acad Sci USA 2010; 107:21193-21198.
22. Ma Y, Walker RK, Zhao Y, Berkowitz GA. Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc Natl Acad Sci USA 2012; 109:19852-19857.
23. Postel S, Kufner I, Beuter C, et al. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol 2010; 89:169-174.
24. Schulze B, Mentzel T, Jehle AK, et al. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 2010; 285:9444-9451.
25. Huffaker A, Ryan CA. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 2007; 104:10732-10736.
26. Liu Z, Wu Y, Yang F, et al. BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci USA 2013; 110:6205-6210.
27. Tintor N, Ross A, Kanehara K, et al. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc Natl Acad Sci USA 2013; 110:6211-6216.
28. Flury P, Klauser D, Schulze B, Boller T, Bartels S. The anticipation of danger: microbe-associated molecular pattern perception enhances AtPep-triggered oxidative burst. Plant Physiol 2013; 161:2023-2035.
29. Ross A, Yamada K, Hiruma K, et al. The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J 2014; 33:62-75.
30. Sun Y, Li L, Macho AP, et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 2013; 342:624-628.
31. Sun Y, Han Z, Tang J, et al. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 2013; 23:1326-1329.
32. Santiago J, Henzler C, Hothorn M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 2013; 341:889-892.
33. Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 2012; 46:701-724.
34. Hothorn M, Belkhadir Y, Dreux M, et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 2011; 474:467-471.
35. She J, Han Z, Kim TW, et al. Structural insight into brassinosteroid perception by BRI1. Nature 2011, 474:472-476.
36. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004; 16:3496-3507.
37. Felix G, Duran JD, Volko S, Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 1999; 18:265-276.
38. Kondo T, Sawa S, Kinoshita A, et al. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 2006; 313:845-848.
39. Song DH, Lee JO. Sensing of microbial molecular patterns by toll-like receptors. Immunol Rev 2012; 250:216-229.
40. Han Z, Sun Y, Chai J. Structural insight into the activation of plant receptor kinases. Curr Opin Plant Biol 2014; 20C:55-63.
41. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol 1997; 276:307-326.
42. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007; 40:658-674.
43. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004; 60:2126-2132.
44. Adams PD, Grosse-Kunstleve RW, Hung LW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 2002; 58:1948-1954.
45. Gong X, Wang P, Yang F, et al. Protein-protein docking with binding site patch prediction and network-based terms enhanced combinatorial scoring. Proteins 2010; 78:3150-3155.
46. Pronk S, Pall S, Schulz R, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013; 29:845-854.