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 (2014)
Plant, Cell & Environment 37(3): 696-706.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
Plants overexpressing the RNA-binding protein AtGRP7 (AtGRP7-ox plants) constitutively express the PR-1 (PATHOGENESIS-RELATED-1), PR-2 and PR-5 transcripts associated with salicylic acid (SA)-mediated immunity and show enhanced resistance against Pseudomonas syringae pv. tomato (Pto) DC3000. Here, we investigated whether the function of AtGRP7 in plant immunity depends on SA. Endogenous SA was elevated fivefold in AtGRP7-ox plants. The elevated PR-1, PR-2 and PR-5 levels were eliminated upon expression of the salicylate hydroxylase nahG in AtGRP7-ox plants and elevated PR-1 levels were suppressed by sid (salicylic acid deficient) 2-1 that is impaired in SA biosynthesis. RNA immunoprecipitation showed that AtGRP7 does not bind the PR-1 transcript in vivo, whereas it binds PDF1.2. Constitutive or inducible AtGRP7 overexpression increases PR-1 promoter activity, indicating that AtGRP7 affects PR-1 transcription. In line with this, the effect of AtGRP7 on PR-1 is suppressed by npr (non-expressor of PR genes) 1. Whereas AtGRP7-ox plants restricted growth of Pto DC3000 compared with wild type (wt), sid2-1 AtGRP7-ox plants allowed more growth than AtGRP7-ox plants. Furthermore, we show an enhanced hypersensitive response triggered by avirulent Pto DC3000 (AvrRpt2) in AtGRP7-ox compared with wt. In sid2-1 AtGRP7-ox, an intermediate phenotype was observed. Thus, AtGRP7 has both SA-dependent and SA-independent effects on plant immunity. (2013 John Wiley & Sons Ltd.)
Erscheinungsjahr
Zeitschriftentitel
Plant, Cell & Environment
Band
37
Ausgabe
3
Seite(n)
696-706
ISSN
PUB-ID

Zitieren

Hackmann C, Korneli C, Kutyniok M, et al. Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity. Plant, Cell & Environment. 2014;37(3):696-706.
Hackmann, C., Korneli, C., Kutyniok, M., Köster, T., Wiedenlübbert, M., Müller, C., & Staiger, D. (2014). Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity. Plant, Cell & Environment, 37(3), 696-706. doi:10.1111/pce.12188
Hackmann, C., Korneli, C., Kutyniok, M., Köster, T., Wiedenlübbert, M., Müller, C., and Staiger, D. (2014). Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity. Plant, Cell & Environment 37, 696-706.
Hackmann, C., et al., 2014. Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity. Plant, Cell & Environment, 37(3), p 696-706.
C. Hackmann, et al., “Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity”, Plant, Cell & Environment, vol. 37, 2014, pp. 696-706.
Hackmann, C., Korneli, C., Kutyniok, M., Köster, T., Wiedenlübbert, M., Müller, C., Staiger, D.: Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity. Plant, Cell & Environment. 37, 696-706 (2014).
Hackmann, Christian, Korneli, Christin, Kutyniok, Magdalene, Köster, Tino, Wiedenlübbert, Matthias, Müller, Caroline, and Staiger, Dorothee. “Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity”. Plant, Cell & Environment 37.3 (2014): 696-706.

12 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

On the move through time - a historical review of plant clock research.
Johansson M, Köster T., Plant Biol (Stuttg) 21 Suppl 1(), 2019
PMID: 29607587
RNA-Binding Proteins Revisited - The Emerging Arabidopsis mRNA Interactome.
Köster T, Marondedze C, Meyer K, Staiger D., Trends Plant Sci 22(6), 2017
PMID: 28412036
Adaptation of iCLIP to plants determines the binding landscape of the clock-regulated RNA-binding protein AtGRP7.
Meyer K, Köster T, Nolte C, Weinholdt C, Lewinski M, Grosse I, Staiger D., Genome Biol 18(1), 2017
PMID: 29084609
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
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

63 References

Daten bereitgestellt von Europe PubMed Central.

Early genomic responses to salicylic acid in Arabidopsis.
Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L., Plant Mol. Biol. 70(1-2), 2009
PMID: 19199050
The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel.
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF., Proc. Natl. Acad. Sci. U.S.A. 97(16), 2000
PMID: 10900264
A central role of salicylic Acid in plant disease resistance.
Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J., Science 266(5188), 1994
PMID: 17810266
Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.
Delaney TP, Friedrich L, Ryals JA., Proc. Natl. Acad. Sci. U.S.A. 92(14), 1995
PMID: 11607555
NPR1, all things considered.
Dong X., Curr. Opin. Plant Biol. 7(5), 2004
PMID: 15337097
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
NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.
Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X., Nature 486(7402), 2012
PMID: 22699612
Requirement of salicylic Acid for the induction of systemic acquired resistance.
Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J., Science 261(5122), 1993
PMID: 17757215
Signaling pathways that regulate the enhanced disease resistance of Arabidopsis "defense, no death" mutants.
Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF., Mol. Plant Microbe Interact. 21(10), 2008
PMID: 18785824
Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
Glazebrook J, Rogers EE, Ausubel FM., Genetics 143(2), 1996
PMID: 8725243
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
Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity.
Jeong BR, Lin Y, Joe A, Guo M, Korneli C, Yang H, Wang P, Yu M, Cerny RL, Staiger D, Alfano JR, Xu Y., J. Biol. Chem. 286(50), 2011
PMID: 22013065
Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense
Jeong, Plant, Cell & Physiology 52(), 2012
The plant immune system.
Jones JD, Dangl JL., Nature 444(7117), 2006
PMID: 17108957
Nuclear localization of NPR1 is required for activation of PR gene expression.
Kinkema M, Fan W, Dong X., Plant Cell 12(12), 2000
PMID: 11148282
The salicylic acid signal in plants
Klessig, Plant Molecular Biology Reporter 26(), 1994
Towards a reporter system to identify regulators of cross-talk between salicylate and jasmonate signaling pathways in Arabidopsis
Koornneef, Plant Signaling & Behaviour 3(), 2008
Different roles of glycine-rich RNA-binding protein7 in plant defense against Pectobacterium carotovorum, Botrytis cinerea, and tobacco mosaic viruses.
Lee HJ, Kim JS, Yoo SJ, Kang EY, Han SH, Yang KY, Kim YC, McSpadden Gardener B, Kang H., Plant Physiol. Biochem. 60(), 2012
PMID: 22902796
Salicylic acid in plant defence--the players and protagonists.
Loake G, Grant M., Curr. Opin. Plant Biol. 10(5), 2007
PMID: 17904410
Reversible photoswitchable DRONPA-s monitors nucleocytoplasmic transport of an RNA-binding protein in transgenic plants.
Lummer M, Humpert F, Steuwe C, Caesar K, Schuttpelz M, Sauer M, Staiger D., Traffic 12(6), 2011
PMID: 21453442
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
Networking by small-molecule hormones in plant immunity.
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC., Nat. Chem. Biol. 5(5), 2009
PMID: 19377457
NPR1: the spider in the web of induced resistance signaling pathways.
Pieterse CM, Van Loon LC., Curr. Opin. Plant Biol. 7(4), 2004
PMID: 15231270
A putative RNA-binding protein positively regulates salicylic acid-mediated immunity in Arabidopsis.
Qi Y, Tsuda K, Joe A, Sato M, Nguyen le V, Glazebrook J, Alfano JR, Cohen JD, Katagiri F., Mol. Plant Microbe Interact. 23(12), 2010
PMID: 20636102
A role for nonsense-mediated mRNA decay in plants: pathogen responses are induced in Arabidopsis thaliana NMD mutants.
Rayson S, Arciga-Reyes L, Wootton L, De Torres Zabala M, Truman W, Graham N, Grant M, Davies B., PLoS ONE 7(2), 2012
PMID: 22384098
Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response.
Riehs-Kearnan N, Gloggnitzer J, Dekrout B, Jonak C, Riha K., Nucleic Acids Res. 40(12), 2012
PMID: 22379136
Systemic Acquired Resistance.
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD., Plant Cell 8(10), 1996
PMID: 12239363
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
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
Changes in conformational dynamics of mRNA upon AtGRP7 binding studied by fluorescence correlation spectroscopy.
Schuttpelz M, Schoning JC, Doose S, Neuweiler H, Peters E, Staiger D, Sauer M., J. Am. Chem. Soc. 130(29), 2008
PMID: 18576621
Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis.
Scott IM, Clarke SM, Wood JE, Mur LA., Plant Physiol. 135(2), 2004
PMID: 15173571
Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene
Shah, Molecular Plant Microbe Interaction 10(), 1997
Regulators of cell death in disease resistance.
Shirasu K, Schulze-Lefert P., Plant Mol. Biol. 44(3), 2000
PMID: 11199395
The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of the night
Staiger, Plant Molecular Biology Reporter 40(), 1999
Emerging role for RNA-based regulation in plant immunity.
Staiger D, Korneli C, Lummer M, Navarro L., New Phytol. 197(2), 2012
PMID: 23163405
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
An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana.
Streitner C, Koster T, Simpson CG, Shaw P, Danisman S, Brown JW, Staiger D., Nucleic Acids Res. 40(22), 2012
PMID: 23042250
Small changes in ambient temperature affect alternative splicing in Arabidopsis thaliana
Streitner, Plant Signaling & Behaviour 8(), 2013
Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins.
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X., Science 321(5891), 2008
PMID: 18635760
Salicylic Acid, a multifaceted hormone to combat disease.
Vlot AC, Dempsey DA, Klessig DF., Annu Rev Phytopathol 47(), 2009
PMID: 19400653
Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid
Wees, The Plant Journal 33(), 2003
Isochorismate synthase is required to synthesize salicylic acid for plant defence.
Wildermuth MC, Dewdney J, Wu G, Ausubel FM., Nature 414(6863), 2001
PMID: 11734859
The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.
Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Despres C., Cell Rep 1(6), 2012
PMID: 22813739
Arabidopsis transportin1 is the nuclear import receptor for the circadian clock-regulated RNA-binding protein AtGRP7.
Ziemienowicz A, Haasen D, Staiger D, Merkle T., Plant Mol. Biol. 53(1-2), 2003
PMID: 14756317

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 23961939
PubMed | Europe PMC

Suchen in

Google Scholar