Cytokinin-induced structural adaptability of a Lupinus luteus PR-10 protein

FEBS Journal

Volumn 276, Issue 6, 2009, Pages 1596-1609

  Fernandes, Humberto ^b   Bujacz, Anna ^c   Bujacz, Grzegorz ^b,c   Jelen, Filip ^d   Jasinski, Michal ^b   Kachlicki, Piotr ^e   Otlewski, Jacek ^d   Sikorski, Michal M ^b   Jaskolski, Mariusz ^a,b  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^c LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

^d UNIVERSITY OF WROC AW   (Poland)

^e INSTITUTE OF PLANT GENETICS   (Poland)

Author keywords

Cytokinin; N,N diphenylurea; Plant hormones; PR 10 proteins; Yellow lupine

Indexed keywords

ANTIFUNGAL AGENT; BACTERIAL PROTEIN; CARBANILIDE; CYTOKININ; LIPR 10.2B PROTEIN; PR 10 PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; UNCLASSIFIED DRUG; UREA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROPHOBICITY; LIGAND BINDING; LIPID TRANSPORT; LUPIN; LUPINUS LUTEUS; NONHUMAN; OPTICAL RESOLUTION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FOLDING; QUALITY CONTROL; STOICHIOMETRY; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; CYTOKININS; LUPINUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

LUPINUS LUTEUS;

EID: 61349091683     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.06892.x     Document Type: Article

References (55)

1. Hammond-Kosack KE Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8, 1773 1791.
2. Van Loon LC, Pierpoint WS, Boller T Conejero V (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12, 245 264.
3. Van Loon LC, Rep M Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44, 135 162.
4. Breiteneder H (2004) Thaumatin-like proteins - a new family of pollen and fruit allergens. Allergy 59, 479 481.
5. Chadha P Das RH (2006) A pathogenesis related protein, AhPR10 from peanut: an insight of its mode of antifungal activity. Planta 225, 213 222.
6. Somssich IE, Schmelzer E, Kawalleck P Hahlbrock K (1988) Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol Gen Genet 213, 93 98.
7. Handschuh L, Femiak I, Kasperska M, Figlerowicz M Sikorski MM (2007) Structural and functional characteristics of two novel members of pathogenesis-related multigene family of class 10 from yellow lupine. Acta Biochim Pol 54, 783 796.
8. Crowell DN, John ME, Russel D Amasino RM (1992) Characterisation of stress-induced, developmentally regulated gene family from soybean. Plant Mol Biol 18, 459 466.
9. Breda C, Sallaud C, El-Turk J, Buffard D, de Kozak I, Esnault R Kondorosi A (1996) Defence reaction in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles. Mol Plant Microbe Interact 9, 713 719.
10. Sikorski MM, Biesiadka J, Kasperska AE, Kopcinska J, Lotocka B, Golinowski W Legocki AB (1999) Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci 149, 125 137.
11. Moiseyev GP, Beintema JJ, Fedoreyeva LI Yakovlev GI (1994) High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intracellular pathogenesis-related proteins are ribonucleases. Planta 193, 470 472.
12. Samanani N Facchini PJ (2002) Purification and characterization of norcoclaurine synthase. The first committed enzyme in benzylisoquinoline alkaloid biosynthesis in plants. J Mol Chem 277, 33878 33883.
13. Bais HP, Vepachedu R, Lawrence CB, Stermitz FR Vivanco JM (2003) Molecular and biochemical characterization of an enzyme responsible for the formation of hypericin in St. John's wort (Hypericum perforatum L.). J Biol Chem 278, 32413 32422.
14. Flores T, Alape-Giron A, Flores-Diaz M Flores HE (2002) Ocatin. A novel tuber storage protein from the Andean tuber crop oca with antibacterial and antifungal activities. Plant Physiol 128, 1291 1302.
15. Park CJ, Kim KJ, Shin R, Park JM, Shin YC Paek KH (2004) Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37, 186 198.
16. Liu X, Huang B, Lin J, Fei J, Chen Z, Pang Y, Sun X Tang K (2006) A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress- and pathogen-inducible. J Plant Physiol 163, 546 556.
17. Gajhede M, Osmark P, Poulsen FM, Ipsen H, Larsen JN, Joost van Neerven RJ, Schou C, Lowenstein H Spangfort MD (1996) X-ray and NMR structure of Bet v1, the origin of birch pollen allergy. Nat Struct Biol 3, 1040 1045.
18. Mirza O, Henriksen A, Ipsen H, Larsen JN, Wissenbach M, Spangfort MD Gajhede M (2000) Dominant epitopes and allergic cross-reactivity: complex formation between a Fab fragment of a monoclonal murine IgG antibody and the major allergen from birch pollen Bet v 1. J Immunol 165, 331 338.
19. Neudecker P, Schweimer K, Nerkamp J, Scheurer S, Vieths S, Sticht H Rosch P (2001) Allergic cross-reactivity made visible: solution structure of the major cherry allergen Pru av 1. J Biol Chem 276, 22756 22763.
20. Biesiadka J, Bujacz G, Sikorski MM Jaskolski M (2002) Crystal structures of two homologous pathogenesis-related proteins from yellow lupine. J Mol Biol 319, 1223 1234.
21. Markovic-Housley Z, Degano M, Lamba D, von Roepenack-Lahaye E, Clemens S, Susani M, Ferreira F, Scheiner O Breiteneder H (2003) Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. J Mol Biol 325, 123 133.
22. Pasternak O, Biesiadka J, Dolot R, Handschuh L, Bujacz G, Sikorski MM Jaskolski M (2005) Structure of a yellow lupin pathogenesis-related PR-10 protein belonging to a novel subclass. Acta Crystallogr D: Biol Crystallogr 61, 99 107.
23. Schirmer T, Hoffimann-Sommergrube K, Susani M, Breiteneder H Markovic-Housley Z (2005) Crystal structure of the major celery allergen Api g 1: molecular analysis of cross-reactivity. J Mol Biol 351, 1101 1109.
24. Pasternak O, Bujacz GD, Fujimoto Y, Hashimoto Y, Jelen F, Otlewski J, Sikorski MM Jaskolski M (2006) Crystal structure of Vigna radiata cytokinin-specific binding protein in complex with zeatin. Plant Cell 18, 2622 2634.
25. Fernandes H, Pasternak O, Bujacz G, Bujacz A, Sikorski MM Jaskolski M (2008) L. luteus pathogenesis-related protein as a reservoir for cytokinin. J Mol Biol 378, 1040 1051.
26. Tsujishita Y Hurley JH (2000) Structure and lipid transport mechanism of a StAR-related domain. Nat Struct Biol 7, 408 414.
27. Shantz EM Steward FC (1955) The identification of compound A from coconut milk as 1,3-diphenylurea. J Am Chem Soc 77, 6351 6353.
28. Mok DW Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52, 89 118.
29. Muller P, Kopke S Sheldrick GM (2003) Is the bond-valence method able to identify metal atoms in protein structures? Acta Crystallogr D: Biol Crystallogr 59, 32 37.
30. Hirel PH, Schmitter MJ, Dessesn P, Fayat G Blanquet S (1989) Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc Natl Acad Sci USA 86, 8247 8251.
31. Laskowski RA (1995) surfnet: a program for visualizing molecular surfaces, cavities and intermolecular interactions. J Mol Graph 13, 323 330.
32. Heigaard J, Jacobsen S, Bjorn SE Kragh KM (1992) Antifungal activity of chitin-binding PR-4 type proteins from barley grain and stressed leaf. FEBS Lett 307, 389 392.
33. Yun DJ, D'Urzo MP, Abad L, Takeda S, Salzman R, Chen Z, Lee H, Hasegawa PM Bressan RA (1996) Novel osmotically induced antifungal chitinases and bacterial expression of an active recombinant isoform. Plant Physiol 111, 1219 1225.
34. Van Loon LC Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55, 85 97.
35. Mogensen JE, Wimmer R, Larsen JN, Spangfort MD Otzen DE (2002) The major birch allergen, Bet v 1, shows affinity for a broad spectrum of physiological ligands. J Biol Chem 277, 23684 23692.
36. Koistinen KM, Soininen P, Venalainen TA, Hayrinen J, Laatikainen R, Perakyla M, Tervahauta AI Karenlampi SO (2005) Birch PR-10c interacts with several biologically important ligands. Phytochemistry 66, 2524 2533.
37. Ilari A, Franceschini S, Bonamore A, Arenghi F, Botta B, Macone A, Pasquo A, Bellucci L Boffi A (2009) Structural basis of enzymatic S-norcoclaurine biosynthesis. J Biol Chem 284, 897 904.
38. Fernandes H, Konieczna M, Kolodziejczyk R, Bujacz G, Sikorski MM Jaskolski M (2008) Crystallization and preliminary crystallographic studies of Hyp-1, a St John's wort protein implicated in the biosynthesis of hypericin. Acta Crystallogr F: Struct Biol Cryst Commun 64, 405 408.
39. Mok MC (1994) Cytokinins and plant development - an overview. In Cytokinins: Chemistry, Activity and Function (Mok DWS Mok MC, eds pp. 155 166. CRC Press, Boca Raton, FL.
40. Shudo K (1994) Chemistry of phenylurea cytokinins. In Cytokinins: Chemistry, Activity and Function (Mok DWS Mok MC, eds pp. 35 42. CRC Press, Boca Raton, FL.
41. Mok MC, Kim SG, Armstrong DJ Mok DW (1979) Induction of cytokinin autonomy by N,N'-diphenylurea in tissue cultures of Phaseolus lunatus L. Proc Natl Acad Sci USA 76, 3880 3884.
42. Kabsch W (1976) A solution for the best rotation to relate two sets of vectors. Acta Crystallogr A 32, 922 923.
43. Moiseyev GP, Fedoreyeva LI, Zhuravlev YN, Yasnetskaya E, Jekel PA Beintema JJ (1997) Primary structures of two ribonucleases from ginseng calluses. New members of the PR-10 family of intracellular pathogenesis-related plant proteins. FEBS Lett 407, 207 210.
44. Sikorski MM (1997) Expression of Lupinus luteus cDNA coding for PR10 protein in Escherichia coli: purification of the recombinant protein for structural and functional studies. Acta Biochim Polon 44, 565 578.
45. Teng T-Y (1990) Mounting of crystals for macromolecular crystallography in a free-standing thin film. J Appl Crystallogr 23, 387 391.
46. Otwinowski Z Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 276, 307 326.
47. Vagin A Teplyakov A (1997) molrep: an automated program for molecular replacement. J Appl Crystallogr 30, 1022 1025.
48. McRee DE (1999) XtalView/Xfit - a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125, 156 165.
49. Emsley P Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D: Biol Crystallogr 60, 2126 2132.
50. Murshudov GN, Vagin AA Dodson EJ (1997) Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallogr D: Biol Crystallogr 53, 240 255.
51. Sclumbaum A, Mauch F, Vogeli U Boller T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324, 365 367.
52. Kleywegt GJ Jones TA (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D: Biol Crystallogr 50, 178 185.
53. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
54. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31, 3497 3500.
55. Wallace AC, Laskowski RA Thornton JM (1995) ligplot: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8, 127 134.