Heterologous expression screens in nicotiana benthamiana identify a candidate effector of the wheat yellow rust pathogen that associates with processing bodies

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Petre, Benjamin ^a,b,c   Saunders, Diane G O ^a,d,e   Sklenar, Jan ^a   Lorrain, Cécile ^a,b,c   Krasileva, Ksenia V ^a,d   Win, Joe ^a   Duplessis, Sébastien ^b,c   Kamoun, Sophien ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b UNIVERSITÉ DE LORRAINE   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

^d EARLHAM INSTITUTE   (United Kingdom)

^e JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EFFECTOR PROTEIN; ENHANCER OF MRNA DECAPPING PROTEIN 4; FUNGAL PROTEIN; MESSENGER RNA; PST02549 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; GREEN FLUORESCENT PROTEIN;

ARTICLE; CELL BODY; CELL COMPARTMENTALIZATION; COMPUTER MODEL; CONTROLLED STUDY; CYTOLOGY; FUNGAL STRAIN; HETEROLOGOUS EXPRESSION; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT CELL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PUCCINIA STRIIFORMIS; RNA CAPPING; RNA DEGRADATION; STRIPE RUST; WHEAT; BASIDIOMYCETES; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; OPEN READING FRAME; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; PROTEIN ANALYSIS; TANDEM MASS SPECTROMETRY; TOBACCO; VIRULENCE;

BASIDIOMYCOTA; CHROMATOGRAPHY, LIQUID; COMPUTER SIMULATION; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; OPEN READING FRAMES; PLANT DISEASES; PLANT LEAVES; PROTEIN INTERACTION MAPPING; RNA, MESSENGER; TANDEM MASS SPECTROMETRY; TOBACCO; TRITICUM; VIRULENCE;

EID: 84959440232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149035     Document Type: Article

References (39)

1. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539-48 doi: 10.1038/nrg2812 PMID: 20585331
2. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol 77:235-47 doi: 10.1101/sqb.2012.77.015933 PMID: 23223409
3. Dangl JL, Horvath DM, Staskawicz BJ. 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746-51 doi: 10.1126/science.1236011 PMID: 23950531
4. Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S. 2009. Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22:115-22 doi: 10.1094/MPMI-22-2-0115 PMID: 19132864
5. Martin F, Kamoun S. 2012. Effectors in Plant-Microbe Interactions. Wiley-Blackwell Eds. ISBN: 978-0-470-95822-3
6. Petre B, Joly DL, Duplessis S. 2014. Effector proteins of rust fungi. Front Plant Sci 5:416 doi: 10.3389/ fpls.2014.00416 PMID: 25191335
7. Upadhyaya NM, Mago R, Staskawicz BJ, Ayliffe MA, Ellis JG, Dodds PN. 2014. A Bacterial Type III Secretion Assay for Delivery of Fungal Effector Proteins into Wheat. Mol Plant Microbe Interact 27:255-264 doi: 10.1094/MPMI-07-13-0187-FI PMID: 24156769
8. Petre B, Saunders DG, Sklenar J, Lorrain C, Win J, Duplessis S, et al. 2015a. Candidate Effector Proteins of the Rust Pathogen Melampsora larici-populina Target Diverse Plant Cell Compartments. Mol Plant Microbe Interact 28:689-700
9. Goodin MM, Zaitlin D, Naidu RA, Lommel SA. 2008. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 21:1015-26 doi: 10.1094/MPMI-21-8-1015 PMID: 18616398
10. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB. 2012. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25:1523-30 doi: 10.1094/MPMI-06-12-0148-TA PMID: 22876960
11. Pais M, Win J, Yoshida K, Etherington GJ, Cano LM, Raffaele S, et al. 2013. From pathogen genomes to host plant processes: the power of plant parasitic oomycetes. Genome Biol 14:211 doi: 10.1186/gb-2013-14-6-211 PMID: 23809564
12. Petre B, Lorrain C, Saunders DG, Win J, Sklenar J, Duplessis S, et al. 2015b. Rust fungal effectors mimic host transit peptides to translocate into chloroplasts. Cell Microbiol doi: 10.1111/cmi.12530
13. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, et al. 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414-30 doi: 10.1111/j.1364-3703.2011.00783.x PMID: 22471698
14. Beddow JM, Pardey PG, Chai Y, Hurley TM, Kriticos DJ, Braun H-J, et al. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nat Plants 1:15132
15. Chen W, Wellings C, Chen X, Kang Z, Liu T. 2014. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Mol Plant Pathol 15:433-46 doi: 10.1111/mpp.12116 PMID: 24373199
16. Hubbard A, Lewis CM, Yoshida K, Ramirez-Gonzalez RH, de Vallavieille-Pope C, Thomas J, et al. 2015. Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol 16:23 doi: 10.1186/s13059-015-0590-8 PMID: 25723868
17. Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X, Kojima KK, et al. 2011. Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One 6:e24230 doi: 10.1371/journal.pone.0024230 PMID: 21909385
18. Garnica DP, Upadhyaya NM, Dodds PN, Rathjen JP. 2013. Strategies for Wheat Stripe Rust Pathogenicity Identified by Transcriptome Sequencing. PLoS One 8:e67150. PMID: 23840606
19. Zheng W, Huang L, Huang J, Wang X, Chen X, Zhao J, et al. 2013. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat Commun 4:2673 doi: 10.1038/ ncomms3673 PMID: 24150273
20. Cantu D, Segovia V, MacLean D, Bayles R, Chen X, Kamoun S, et al. 2013. Genome analyses of the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics 14:270 doi: 10.1186/1471-2164-14-270 PMID: 23607900
21. Chan EKL, Fritzler MJ. 2012. Ten years of progress in GW/P body research. Advances in Experimental Medicine and Biology. Springer Science and Business Media Eds.
22. Xu J, Yang JY, Niu QW, Chua NH. 2006. Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18:3386-98 PMID: 17158604
23. Xu J, Chua NH. 2009. Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell 21:3270-9 doi: 10.1105/ tpc.109.070078 PMID: 19855049
24. Steffens A, Bräutigam A, Jakoby M, Hülskamp M. 2015. The BEACH Domain Protein SPIRRIG Is Essential for Arabidopsis Salt Stress Tolerance and Functions as a Regulator of Transcript Stabilization and Localization. PLoS Biol 13:e1002188 doi: 10.1371/journal.pbio.1002188 PMID: 26133670
25. Maldonado-Bonilla LD, Eschen-Lippold L, Gago-Zachert S, Tabassum N, Bauer N, Scheel D, et al. 2014. The Arabidopsis tandem zinc finger 9 protein binds RNA and mediates pathogen-associated molecular pattern-triggered immune responses. Plant Cell Physiol 55:412-25 doi: 10.1093/pcp/pct175 PMID: 24285750
26. Eulalio A, Fröhlich KS, Mano M, Giacca M, Vogel J. 2011. A candidate approach implicates the secreted Salmonella effector protein SpvB in P-body disassembly. PLoS One 6:e17296. doi: 10.1371/ journal.pone.0017296 PMID: 21390246
27. Reineke LC, Lloyd RE. 2013. Diversion of stress granules and P-bodies during viral infection. Virology 436:255-67 doi: 10.1016/j.virol.2012.11.017 PMID: 23290869
28. Weiberg A, Wang M, Bellinger M, Jin H. 2014. Small RNAs: a new paradigm in plant-microbe interactions. Annu Rev Phytopathol 52:495-516 doi: 10.1146/annurev-phyto-102313-045933 PMID: 25090478
29. Qiao Y, Shi J, Zhai Y, Hou Y, Ma W. 2015. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. Proc Natl Acad Sci U S A 112:5850-5 doi: 10.1073/pnas. 1421475112 PMID: 25902521
30. Spanu PD. 2015. RNA-protein interactions in plant disease: hackers at the dinner table. New Phytol 207:991-5 doi: 10.1111/nph.13495 PMID: 26237564
31. Roux ME, Rasmussen MW, Palma K, Lolle S, Regué AM, Bethke G, et al. 2015. The mRNA decay factor PAT1 functions in a pathway including MAP kinase 4 and immune receptor SUMM2. EMBO J 34:593-608 doi: 10.15252/embj.201488645 PMID: 25603932
32. Ariumi Y, Kuroki M, Kushima Y, Osugi K, Hijikata M, Maki M, et al. 2011. Hepatitis C virus hijacks Pbody and stress granule components around lipid droplets. J Virol 85:6882-92 doi: 10.1128/JVI. 02418-10 PMID: 21543503
33. Pérez-Vilaró G, Fernández-Carrillo C, Mensa L, Miquel R, Sanjuan X, Forns X, et al. 2015. Hepatitis C virus infection inhibits P-body granule formation in human livers. J Hepatol 62:785-90 doi: 10.1016/j. jhep.2014.11.018 PMID: 25463546
34. Eulalio A, Behm-Ansmant I, Izaurralde E. 2007. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8:9-22 PMID: 17183357
35. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science. 333:596-601 doi: 10.1126/science.1203659 PMID: 21798943
36. Emanuelle S, Doblin MS, Stapleton DI, Bacic A, Gooley PR. 2015. Molecular Insights into the Enigmatic Metabolic Regulator, SnRK1. Trends Plant Sci doi: http://dx.doi.org/10.1016/j.tplants.2015.11.001
37. Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. 2014. A novel conserved mechanism for plant NLR protein pairs: the "integrated decoy" hypothesis. Front Plant Sci 5:606 doi: 10.3389/fpls.2014. 00606 PMID: 25506347
38. Wu CH, Krasileva KV, Banfield MJ, Terauchi R, Kamoun S. 2015. The "sensor domains" of plant NLR proteins: more than decoys? Front Plant Sci 6:134 doi: 10.3389/fpls.2015.00134 PMID: 25798142
39. Sarris PF, Jones JD. 2015. Plant immune receptors mimic pathogen virulence targets. Oncotarget 6:16824-5 PMID: 26219337