Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity

Jeong B-ryool, Lin Y, Joe A, Guo M, Korneli C, Yang H, Wang P, Yu M, Cerny RL, Staiger D, Alfano JR, et al. (2011)
Journal of Biological Chemistry 286(50): 43272-43281.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ; ; ; ; ; ; ;
Alle
Abstract / Bemerkung
The Pseudomonas syringae type III effector HopU1 is a mono-ADP-ribosyltransferase (mADP-RT) that is injected into plant cells by the type III protein secretion system. Inside the plant cell it suppresses immunity by modifying RNA-binding proteins including the glycine-rich RNA-binding protein GRP7. The crystal structure of HopU1 at 2.7 angstrom resolution reveals two unique protruding loops, L1 and L4 not found in other mADP-RTs. Site-directed mutagenesis demonstrates these loops are essential for substrate recognition and enzymatic activity. HopU1 ADP-ribosylates the conserved arginine 49 (R49) of GRP7 and this reduces GRP7's ability to bind RNA in vitro. In vivo, expression of GRP7 with R49 replaced with lysine does not complement the reduced immune responses of the Arabidopsis thaliana grp7-1 mutant demonstrating the importance of this residue for GRP7 function. These data provide mechanistic details how HopU1 recognizes this novel type of substrate and highlights the role of GRP7 in plant immunity.
Erscheinungsjahr
Zeitschriftentitel
Journal of Biological Chemistry
Band
286
Ausgabe
50
Seite(n)
43272-43281
ISSN
eISSN
PUB-ID

Zitieren

Jeong B-ryool, Lin Y, Joe A, et al. Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Journal of Biological Chemistry. 2011;286(50):43272-43281.
Jeong, B. -ryool, Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., et al. (2011). Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Journal of Biological Chemistry, 286(50), 43272-43281. doi:10.1074/jbc.M111.290122
Jeong, B. -ryool, Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., Yu, M., Cerny, R. L., Staiger, D., et al. (2011). Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Journal of Biological Chemistry 286, 43272-43281.
Jeong, B.-ryool, et al., 2011. Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Journal of Biological Chemistry, 286(50), p 43272-43281.
B.-ryool Jeong, et al., “Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity”, Journal of Biological Chemistry, vol. 286, 2011, pp. 43272-43281.
Jeong, B.-ryool, Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., Yu, M., Cerny, R.L., Staiger, D., Alfano, J.R., Xu, Y.: Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Journal of Biological Chemistry. 286, 43272-43281 (2011).
Jeong, Byeong-ryool, Lin, Yan, Joe, Anna, Guo, Ming, Korneli, Christin, Yang, Huirong, Wang, Ping, Yu, Min, Cerny, Ronald L., Staiger, Dorothee, Alfano, James R., and Xu, Yanhui. “Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity”. Journal of Biological Chemistry 286.50 (2011): 43272-43281.
Link(s) zu Volltext(en)
Access Level
Restricted Closed Access

42 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Systematic prediction of genes functionally linked to CRISPR-Cas systems by gene neighborhood analysis.
Shmakov SA, Makarova KS, Wolf YI, Severinov KV, Koonin EV., Proc Natl Acad Sci U S A 115(23), 2018
PMID: 29784811
Structural basis of ubiquitin modification by the Legionella effector SdeA.
Dong Y, Mu Y, Xie Y, Zhang Y, Han Y, Zhou Y, Wang W, Liu Z, Wu M, Wang H, Pan M, Xu N, Xu CQ, Yang M, Fan S, Deng H, Tan T, Liu X, Liu L, Li J, Wang J, Fang X, Feng Y., Nature 557(7707), 2018
PMID: 29795342
Mechanism of phosphoribosyl-ubiquitination mediated by a single Legionella effector.
Akturk A, Wasilko DJ, Wu X, Liu Y, Zhang Y, Qiu J, Luo ZQ, Reiter KH, Brzovic PS, Klevit RE, Mao Y., Nature 557(7707), 2018
PMID: 29795346
RING-H2-type E3 gene VpRH2 from Vitis pseudoreticulata improves resistance to powdery mildew by interacting with VpGRP2A.
Wang L, Xie X, Yao W, Wang J, Ma F, Wang C, Yang Y, Tong W, Zhang J, Xu Y, Wang X, Zhang C, Wang Y., J Exp Bot 68(7), 2017
PMID: 28369599
Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity.
Franceschetti M, Maqbool A, Jiménez-Dalmaroni MJ, Pennington HG, Kamoun S, Banfield MJ., Microbiol Mol Biol Rev 81(2), 2017
PMID: 28356329
Genome-Wide Analysis of Alternative Splicing during Development and Drought Stress in Maize.
Thatcher SR, Danilevskaya ON, Meng X, Beatty M, Zastrow-Hayes G, Harris C, Van Allen B, Habben J, Li B., Plant Physiol 170(1), 2016
PMID: 26582726
Protein ADP-Ribosylation Takes Control in Plant-Bacterium Interactions.
Feng B, Liu C, Shan L, He P., PLoS Pathog 12(12), 2016
PMID: 27907213
A Host KH RNA-Binding Protein Is a Susceptibility Factor Targeted by an RXLR Effector to Promote Late Blight Disease.
Wang X, Boevink P, McLellan H, Armstrong M, Bukharova T, Qin Z, Birch PR., Mol Plant 8(9), 2015
PMID: 25936676
Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity.
Hackmann C, Korneli C, Kutyniok M, Köster T, Wiedenlübbert M, Müller C, Staiger D., Plant Cell Environ 37(3), 2014
PMID: 23961939
A glycine-rich RNA-binding protein affects gibberellin biosynthesis in Arabidopsis.
Löhr B, Streitner C, Steffen A, Lange T, Staiger D., Mol Biol Rep 41(1), 2014
PMID: 24281950
Distinct Pseudomonas type-III effectors use a cleavable transit peptide to target chloroplasts.
Li G, Froehlich JE, Elowsky C, Msanne J, Ostosh AC, Zhang C, Awada T, Alfano JR., Plant J 77(2), 2014
PMID: 24299018
Transcriptional control of plant defence responses.
Buscaill P, Rivas S., Curr Opin Plant Biol 20(), 2014
PMID: 24840291
The ABCs and 123s of bacterial secretion systems in plant pathogenesis.
Chang JH, Desveaux D, Creason AL., Annu Rev Phytopathol 52(), 2014
PMID: 24906130
The hnRNP-Q protein LIF2 participates in the plant immune response.
Le Roux C, Del Prete S, Boutet-Mercey S, Perreau F, Balagué C, Roby D, Fagard M, Gaudin V., PLoS One 9(6), 2014
PMID: 24914891
Structural basis of nucleic acid binding by Nicotiana tabacum glycine-rich RNA-binding protein: implications for its RNA chaperone function.
Khan F, Daniëls MA, Folkers GE, Boelens R, Saqlan Naqvi SM, van Ingen H., Nucleic Acids Res 42(13), 2014
PMID: 24957607
Novel bacterial ADP-ribosylating toxins: structure and function.
Simon NC, Aktories K, Barbieri JT., Nat Rev Microbiol 12(9), 2014
PMID: 25023120
Regulation of pri-miRNA processing by the hnRNP-like protein AtGRP7 in Arabidopsis.
Köster T, Meyer K, Weinholdt C, Smith LM, Lummer M, Speth C, Grosse I, Weigel D, Staiger D., Nucleic Acids Res 42(15), 2014
PMID: 25104024
Mutational definition of binding requirements of an hnRNP-like protein in Arabidopsis using fluorescence correlation spectroscopy.
Leder V, Lummer M, Tegeler K, Humpert F, Lewinski M, Schüttpelz M, Staiger D., Biochem Biophys Res Commun 453(1), 2014
PMID: 25251471
Emerging role for RNA-based regulation in plant immunity.
Staiger D, Korneli C, Lummer M, Navarro L., New Phytol 197(2), 2013
PMID: 23163405
Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7.
Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F, Westedt I, Staiger D, Alfano JR, Zipfel C., EMBO J 32(5), 2013
PMID: 23395902
Phytopathogen type III effectors as probes of biological systems.
Lee AH, Middleton MA, Guttman DS, Desveaux D., Microb Biotechnol 6(3), 2013
PMID: 23433088
An antifungal peptide from Coffea canephora seeds with sequence homology to glycine-rich proteins exerts membrane permeabilization and nuclear localization in fungi.
Zottich U, Da Cunha M, Carvalho AO, Dias GB, Casarin N, Vasconcelos IM, Gomes VM., Biochim Biophys Acta 1830(6), 2013
PMID: 23500079
Plant innate immunity: an updated insight into defense mechanism.
Muthamilarasan M, Prasad M., J Biosci 38(2), 2013
PMID: 23660678
On the front line: structural insights into plant-pathogen interactions.
Wirthmueller L, Maqbool A, Banfield MJ., Nat Rev Microbiol 11(11), 2013
PMID: 24100360
The RNA-binding protein FPA regulates flg22-triggered defense responses and transcription factor activity by alternative polyadenylation.
Lyons R, Iwase A, Gänsewig T, Sherstnev A, Duc C, Barton GJ, Hanada K, Higuchi-Takeuchi M, Matsui M, Sugimoto K, Kazan K, Simpson GG, Shirasu K., Sci Rep 3(), 2013
PMID: 24104185
mADP-RTs: versatile virulence factors from bacterial pathogens of plants and mammals.
Wirthmueller L, Banfield MJ., Front Plant Sci 3(), 2012
PMID: 22754560
Catch me if you can: bacterial effectors and plant targets.
Deslandes L, Rivas S., Trends Plant Sci 17(11), 2012
PMID: 22796464
AvrRpm1 missense mutations weakly activate RPS2-mediated immune response in Arabidopsis thaliana.
Cherkis KA, Temple BR, Chung EH, Sondek J, Dangl JL., PLoS One 7(8), 2012
PMID: 22880057
An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana.
Streitner C, Köster T, Simpson CG, Shaw P, Danisman S, Brown JW, Staiger D., Nucleic Acids Res 40(22), 2012
PMID: 23042250

66 References

Daten bereitgestellt von Europe PubMed Central.

Type III protein secretion in plant pathogenic bacteria.
Buttner D, He SY., Plant Physiol. 150(4), 2009
PMID: 19458111
Bacterial virulence effectors and their activities.
Hann DR, Gimenez-Ibanez S, Rathjen JP., Curr. Opin. Plant Biol. 13(4), 2010
PMID: 20466583
The plant immune system.
Jones JD, Dangl JL., Nature 444(7117), 2006
PMID: 17108957
Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity.
Tsuda K, Katagiri F., Curr. Opin. Plant Biol. 13(4), 2010
PMID: 20471306
Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains.
Lindeberg M, Cartinhour S, Myers CR, Schechter LM, Schneider DJ, Collmer A., Mol. Plant Microbe Interact. 19(11), 2006
PMID: 17073298
The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity.
Guo M, Tian F, Wamboldt Y, Alfano JR., Mol. Plant Microbe Interact. 22(9), 2009
PMID: 19656042
A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity.
Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB., Nature 448(7151), 2007
PMID: 17637671
Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases.
Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou JM., Curr. Biol. 18(1), 2007
PMID: 18158241
Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity.
Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, Sheen J., Cell Host Microbe 4(1), 2008
PMID: 18621007
Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB.
Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S., Curr. Biol. 18(23), 2008
PMID: 19062288
AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants.
Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP., Curr. Biol. 19(5), 2009
PMID: 19249211
A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases.
Wang Y, Li J, Hou S, Wang X, Li Y, Ren D, Chen S, Tang X, Zhou JM., Plant Cell 22(6), 2010
PMID: 20571112
A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.
Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM., Cell Host Microbe 1(3), 2007
PMID: 18005697
A bacterial virulence protein suppresses host innate immunity to cause plant disease.
Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY., Science 313(5784), 2006
PMID: 16840699
A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity.
Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR., Nature 447(7142), 2007
PMID: 17450127
The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity.
Block A, Guo M, Li G, Elowsky C, Clemente TE, Alfano JR., Cell. Microbiol. 12(3), 2009
PMID: 19863557
Pseudomonas syringae hijacks plant stress chaperone machinery for virulence.
Jelenska J, van Hal JA, Greenberg JT., Proc. Natl. Acad. Sci. U.S.A. 107(29), 2010
PMID: 20615948
Needle in the haystack: structure-based toxin discovery.
Fieldhouse RJ, Merrill AR., Trends Biochem. Sci. 33(11), 2008
PMID: 18815047
Molecular mechanisms of the cytotoxicity of ADP-ribosylating toxins.
Deng Q, Barbieri JT., Annu. Rev. Microbiol. 62(), 2008
PMID: 18785839
Rho-modifying C3-like ADP-ribosyltransferases.
Aktories K, Wilde C, Vogelsgesang M., Rev. Physiol. Biochem. Pharmacol. 152(), 2004
PMID: 15372308
A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins.
Holbourn KP, Shone CC, Acharya KR., FEBS J. 273(20), 2006
PMID: 16956368

Barbieri J., Burns D.., 2003
Toward a unified nomenclature for mammalian ADP-ribosyltransferases.
Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F., Trends Biochem. Sci. 35(4), 2010
PMID: 20106667
Structure of the ecto-ADP-ribosyl transferase ART2.2 from rat.
Mueller-Dieckmann C, Ritter H, Haag F, Koch-Nolte F, Schulz GE., J. Mol. Biol. 322(4), 2002
PMID: 12270706
Structure and function of eukaryotic mono-ADP-ribosyltransferases.
Okazaki IJ, Moss J., Rev. Physiol. Biochem. Pharmacol. 129(), 1996
PMID: 8898563
Structural basis for the NAD-hydrolysis mechanism and the ARTT-loop plasticity of C3 exoenzymes.
Menetrey J, Flatau G, Boquet P, Menez A, Stura EA., Protein Sci. 17(5), 2008
PMID: 18369192
A proteomic analysis of oligo(dT)-bound mRNP containing oxidative stress-induced Arabidopsis thaliana RNA-binding proteins ATGRP7 and ATGRP8.
Schmidt F, Marnef A, Cheung MK, Wilson I, Hancock J, Staiger D, Ladomery M., Mol. Biol. Rep. 37(2), 2009
PMID: 19672695
Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana.
Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH, Woo Y, Oh SH, Han YS, Kang H., Plant J. 55(3), 2008
PMID: 18410480
The small glycine-rich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana.
Streitner C, Danisman S, Wehrle F, Schoning JC, Alfano JR, Staiger D., Plant J. 56(2), 2008
PMID: 18573194

Sambrook J., Russell D.., 2001
Two simple media for the demonstration of pyocyanin and fluorescin.
KING EO, WARD MK, RANEY DE., J. Lab. Clin. Med. 44(2), 1954
PMID: 13184240

Bechtold N., Ellis J., Pelletier G.., 1993
Crystallization and preliminary crystallographic analysis of the ADP-ribosyltransferase HopU1.
Lin Y, Wang P, Yang H, Xu Y., Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66(Pt 8), 2010
PMID: 20693672
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard.
Terwilliger TC, Adams PD, Read RJ, McCoy AJ, Moriarty NW, Grosse-Kunstleve RW, Afonine PV, Zwart PH, Hung LW., Acta Crystallogr. D Biol. Crystallogr. 65(Pt 6), 2009
PMID: 19465773
Coot: model-building tools for molecular graphics.
Emsley P, Cowtan K., Acta Crystallogr. D Biol. Crystallogr. 60(Pt 12 Pt 1), 2004
PMID: 15572765
Main-chain bond lengths and bond angles in protein structures.
Laskowski RA, Moss DS, Thornton JM., J. Mol. Biol. 231(4), 1993
PMID: 8515464
Searching protein structure databases with DaliLite v.3.
Holm L, Kaariainen S, Rosenstrom P, Schenkel A., Bioinformatics 24(23), 2008
PMID: 18818215
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling.
Arnold K, Bordoli L, Kopp J, Schwede T., Bioinformatics 22(2), 2005
PMID: 16301204
The Protein Model Portal.
Arnold K, Kiefer F, Kopp J, Battey JN, Podvinec M, Westbrook JD, Berman HM, Bordoli L, Schwede T., J. Struct. Funct. Genomics 10(1), 2008
PMID: 19037750
ZDOCK: an initial-stage protein-docking algorithm.
Chen R, Li L, Weng Z., Proteins 52(1), 2003
PMID: 12784371
Defining parameters for homology-tolerant database searching.
Kayser JP, Vallet JL, Cerny RL., J Biomol Tech 15(4), 2004
PMID: 15585825
Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation.
Schoning JC, Streitner C, Page DR, Hennig S, Uchida K, Wolf E, Furuya M, Staiger D., Plant J. 52(6), 2007
PMID: 17924945
Structural and functional analysis of the type III secretion system from Pseudomonas fluorescens Q8r1-96.
Mavrodi DV, Joe A, Mavrodi OV, Hassan KA, Weller DM, Paulsen IT, Loper JE, Alfano JR, Thomashow LS., J. Bacteriol. 193(1), 2010
PMID: 20971913

Abramoff M., Magelhaes P., Ram S.., 2004
The PredictProtein server.
Rost B, Yachdav G, Liu J., Nucleic Acids Res. 32(Web Server issue), 2004
PMID: 15215403
Comparison of super-secondary structures in proteins.
Rao ST, Rossmann MG., J. Mol. Biol. 76(2), 1973
PMID: 4737475
Structural basis of actin recognition and arginine ADP-ribosylation by Clostridium perfringens iota-toxin.
Tsuge H, Nagahama M, Oda M, Iwamoto S, Utsunomiya H, Marquez VE, Katunuma N, Nishizawa M, Sakurai J., Proc. Natl. Acad. Sci. U.S.A. 105(21), 2008
PMID: 18490658
The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence.
Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D., Proc. Natl. Acad. Sci. U.S.A. 107(5), 2010
PMID: 20133879
Crystal structures of the type III effector protein AvrPphF and its chaperone reveal residues required for plant pathogenesis.
Singer AU, Desveaux D, Betts L, Chang JH, Nimchuk Z, Grant SR, Dangl JL, Sondek J., Structure 12(9), 2004
PMID: 15341731
Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA.
Ding J, Hayashi MK, Zhang Y, Manche L, Krainer AR, Xu RM., Genes Dev. 13(9), 1999
PMID: 10323862
Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A.
Nagai K, Oubridge C, Jessen TH, Li J, Evans PR., Nature 348(6301), 1990
PMID: 2147232
Chemical shift mapping of the RNA-binding interface of the multiple-RBD protein sex-lethal.
Lee AL, Volkman BF, Robertson SA, Rudner DZ, Barbash DA, Cline TW, Kanaar R, Rio DC, Wemmer DE., Biochemistry 36(47), 1997
PMID: 9398148
Common themes in the design and function of bacterial effectors.
Galan JE., Cell Host Microbe 5(6), 2009
PMID: 19527884
RNA recognition motifs: boring? Not quite.
Clery A, Blatter M, Allain FH., Curr. Opin. Struct. Biol. 18(3), 2008
PMID: 18515081
Regulation of nitrogenase activity by reversible ADP ribosylation.
Ludden PW, Roberts GP., Curr. Top. Cell. Regul. 30(), 1989
PMID: 2575970
AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana.
Heintzen C, Nater M, Apel K, Staiger D., Proc. Natl. Acad. Sci. U.S.A. 94(16), 1997
PMID: 9238008
Global transcript profiling of transgenic plants constitutively overexpressing the RNA-binding protein AtGRP7.
Streitner C, Hennig L, Korneli C, Staiger D., BMC Plant Biol. 10(), 2010
PMID: 20946635

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 22013065
PubMed | Europe PMC

Suchen in

Google Scholar