Host-induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors

Molecular Plant-Microbe Interactions

Volumn 26, Issue 6, 2013, Pages 633-642

  Pliego, Clara ^a   Nowara, Daniela ^b   Bonciani, Giulia ^a   Gheorghe, Dana M ^a   Xu, Ruo ^c   Surana, Priyanka ^d   Whigham, Ehren ^d   Nettleton, Dan ^d   Bogdanove, Adam J ^d,f   Wise, Roger P ^d   Schweizer, Patrick ^b   Bindschedler, Laurence V ^e,g   Spanu, Pietro D ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

^d IOWA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF READING   (United Kingdom)

^f Department of Obstetrics Gynecology   (United States)

^g UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PLANT RNA; RIBONUCLEASE;

ARTICLE; ASCOMYCETES; CELL DEATH; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC COMPLEMENTATION; GENETICS; HORDEUM; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; SEEDLING; SPECIES DIFFERENCE;

ASCOMYCOTA; CELL DEATH; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; GENETIC COMPLEMENTATION TEST; HORDEUM; HOST-PATHOGEN INTERACTIONS; MUTATION; PLANT DISEASES; PLANT LEAVES; RIBONUCLEASES; RNA, PLANT; SEEDLING; SPECIES SPECIFICITY;

BLUMERIA; BLUMERIA GRAMINIS F. SP. HORDEI; ERYSIPHALES; FUNGI; HORDEUM;

EID: 84877125481     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-01-13-0005-R     Document Type: Article

References (48)

1. Banerjee, B., Kurup, V. P., Phadnis, S., Greenberger, P. A., and Fink, J. N. 1996. Molecular cloning and expression of a recombinant Aspergillus fumigatus protein Asp f II with significant immunoglobulin E reactivity in allergic bronchopulmonary aspergillosis. J. Lab. Clin. Med. 127:253-262.
2. Bindschedler, L. V., McGuffin, L. J., Burgis, T. A., Spanu, P. D., and Cramer, R. 2011. Proteogenomics and in silico structural and functional annotation of the barley powdery mildew Blumeria graminis f. sp. hordei. Methods 54:432-441.
3. Bindschedler, L. V., Burgis, T. A., Mills, D. J. S., Ho, J. T. C., Cramer, R., and Spanu, P. D. 2009. In planta proteomics and proteogenomics of the biotrophic barley fungal pathogen Blumeria graminis f. sp. hordei. Mol. Cell. Proteomics 8:2368-2381.
4. Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Ann. Rev. Plant Biol. 60:379-406.
5. Both, M., and Spanu, P. 2004. Blumeria graminis f. sp. hordei, an obligate pathogen of barley. Pages 202-218 in: Plant Pathogen Interactions, N. Talbot, ed. Blackwell Publishing, Oxford.
6. Both, M., Eckert, S. E., Csukai, M., Müller, E., Dimopoulos, G., and Spanu, P. D. 2005. Transcript profiles of Blumeria graminis development during infection reveal a cluster of genes that are potential virulence determinants. Mol. Plant-Microbe Interact. 18:125-133.
7. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. 2009. The Carbohydrate-Active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acid Res. 37:D233-D238.
8. Dodds, P. N., and Rathjen, J. P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548.
9. Dong, W. B., Nowara, D., and Schweizer, P. 2006. Protein polyubiquitination plays a role in basal host resistance of barley. Plant Cell 18:3321-3331.
10. Douchkov, D., Nowara, D., Zierold, U., and Schweizer, P. 2005. A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol. Plant-Microbe Interact. 18:755-761.
11. Dunnett, C. W. 1955. A Multiple comparison procedure for comparing several treatments with a control. J. Am. Stat. Assn. 50:1096-1121.
12. Eichmann, R., Bischof, M., Weis, C., Shaw, J., Lacomme, C., Schweizer, P., Duchkov, D., Hensel, G., Kumlehn, J., and Hückelhoven, R. 2010. BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol. Plant-Microbe Interact. 23:1217-1227.
13. Ellis, J. G., and Dodds, P. N. 2011. Showdown at the RXLR motif: Serious differences of opinion in how effector proteins from filamentous eukaryotic pathogens enter plant cells. Proc. Natl. Acad. Sci. U.S.A. 108:14381-14382.
14. Glawe, D. A. 2008. The powdery mildews: A review of the world's most familiar (yet poorly known) plant pathogens. Annu. Rev. Phytopathol. 46:27-51.
15. Godfrey, D., Bohlenius, H., Pedersen, C., Zhang, Z., Emmersen, J., and Thordal-Christensen, H. 2010. Powdery mildew and rust fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11:317.
16. Goldman, R.C., Sullivan, P.A., Zakula, D., and Capobianco, J.O. 1995. Kinetics of β-1,3 glucan interaction at the donor and acceptor sites of the fungal glucosyltransferase encoded by the BGL2 gene. Eur. J. Biochem. 227:372-378.
17. Haas, B., Kamoun, S., Zody, M., Jiang, R., Handsaker, R., and Cano, L. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398.
18. Hacquard, S., Joly, D. L., Lin, Y.-C., Tisserant, E., Feau, N., Delaruelle, C., Legué, V., Kohler, A., Tanguay, P., Petre, B., Frey, P., Van de Peer, Y., Rouzé, P., Martin, F., Hamelin, R. C., and Duplessis, S. 2012. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (Poplar leaf rust). Mol. Plant-Microbe Interact. 25:279-293.
19. Hann, D. 2010. Bacterial virulence effectors and their activities. Curr. Opin. Plant Biol. 13:388-393.
20. Hoefle, C., and Huckelhoven, R. 2008. Enemy at the gates: Traffic at the plant cell pathogen interface. Cell. Microbiol. 10:2400-2407.
21. Hsu, J. 1992. The factor analytic approach to simultaneous inference in the general linear model. J. Comput. Graph. Stat. 1:151-168.
22. International Barley Genome Sequencing Consortium, Mayer, K, F., Waugh, R., Brown, J, W., Schulman, A., Langridge, P., Platzer, M., Fincher. G. B., Muehlbauer, G. J., Sato, K., Close, T. J., Wise, R. P., and Stein, N. 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711-716.
23. Kämper, J., Kahmann, R., Bolker, M., Ma, L. J., Brefort, T., Saville, B. J., Banuett, F., Kronstad, J. W., Gold, S. E., Muller, O., Perlin, M. H., Wosten, H. A. B., de Vries, R., Ruiz-Herrera, J., Reynaga-Pena, C. G., Snetselaar, K., McCann, M., Perez-Martin, J., Feldbrugge, M., Basse, C. W., Steinberg, G., Ibeas, J. I., Holloman, W., Guzman, P., Farman, M., Stajich, J. E., Sentandreu, R., Gonzalez-Prieto, J. M., Kennell, J. C., Molina, L., Schirawski, J., Mendoza-Mendoza, A., Greilinger, D., Munch, K., Rossel, N., Scherer, M., Vranes, M., Ladendorf, O., Vincon, V., Fuchs, U., Sandrock, B., Meng, S., Ho, E. C. H., Cahill, M. J., Boyce, K. J., Klose, J., Klosterman, S. J., Deelstra, H. J., Ortiz-Castellanos, L., Li, W. X., Sanchez-Alonso, P., Schreier, P. H., Hauser-Hahn, I., Vaupel, M., Koopmann, E., Friedrich, G., Voss, H., Schluter, T., Margolis, J., Platt, D., Swimmer, C., Gnirke, A., Chen, F., Vysotskaia, V., Mannhaupt, G., Guldener, U., Munsterkotter, M., Haase, D., Oesterheld, M., Mewes, H. W., Mauceli, E. W., DeCaprio, D., Wade, C. M., Butler, J., Young, S., Jaffe, D. B., Calvo, S., Nusbaum, C., Galagan, J., and Birren, B.W. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97-101.
24. Kelley, L., and Sternberg, M. 2009. Protein structure prediction on the Web: A case study using the Phyre server. Nat. Prot. 4:363-371.
25. Klink, T. A., Woycechowsky, K. J., Taylor, K. M., and Raines, R. T. 2000. Contribution of disulfide bonds to the conformational stability and catalytic activity of ribonuclease A. Eur. J. Biochem. 267:566-572.
26. -ΔΔCT method. Methods 25:402-408.
27. Mouyna, I., Morelle, W., Vai, M., Monod, M., Léchenne, B., Fontaine, T., Beauvais, A., Sarfati, J., Prévost, M.-C., Henry, C., and Latgé, J.-P. 2005. Deletion of GEL2 encoding for a β(1-3) glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol. Microbiol. 56:1675-1688.
28. Nelson, A. J., and Bushnell, W. R. 1997. Transient expression of anthocyanin genes in barley epidermal cells: Potential for use in evaluation of disease response genes. Trans. Res. 6:233-244.
29. Nishikawa, S., Morioka, H., Kim, H. J., Fuchimura, K., Tanaka, T., Uesugi, S., Hakoshima, T., Tomita, K., Ohtsuka, E., and Ikehara, M. 1987. Two histidine residues are essential for ribonuclease T1 activity as is the case for ribonuclease A. Biochemistry 26:8620-8624.
30. Nowara, D., Gay, A., Lacomme, C., Shaw, J., Ridout, C., Douchkov, D., Hensel, G., Kumlehn, J., and Schweizer, P. 2010. HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130-3141.
31. Nunes, C. C., and Dean, R. A. 2012. Host-induced gene silencing: A tool for understanding fungal host interaction and for developing novel disease control strategies. Mol. Plant Pathol. 13:519-529.
32. Pedersen, C., Ver Loren van Themaat, E., McGuffin, L. J., Abbott, J. C., Burgis, T. A., Barton, G., Bindschedler, L. V., Lu, X., Maekawa, T., Weßling, R., Cramer, R., Thordal-Christensen, H., Panstruga, R., and Spanu, P. D. 2012. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13:694.
33. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Meth. 8:785-786.
34. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., and Lopez, R. 2005. InterProScan: Protein domains identifier. Nucleic Acid Res. 33:W116-W120.
35. Ridout, C. J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J. D. G., and Brown, J. K. M. 2006. Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18:2402-2414.
36. Sacristán, S., Vigouroux, M., Pedersen, C., Skamnioti, P., Thordal-Christensen, H., Micali, C., Brown, J. K. M., and Ridout, C. J. 2009. Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons. PLoS ONE 4:e7463. Published online.
37. Schirawski, J., Mannhaupt, G., Munch, K., Brefort, T., Schipper, K., Doehlemann, G., Di Stasio, M., Rossel, N., Mendoza-Mendoza, A., Pester, D., Muller, O., Winterberg, B., Meyer, E., Ghareeb, H., Wollenberg, T., Munsterkotter, M., Wong, P., Walter, M., Stukenbrock, E., Guldener, U., and Kahmann, R. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546-1548.
38. Schweizer, P., Pokorny, J., Schulze-Lefert, P., and Dudler, R. 2000. Technical advance. Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J. 24:895-903.
39. Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stuber, K., van Themaat, E. V. L., Brown, J. K. M., Butcher, S. A., Gurr, S. J., Lebrun, M. H., Ridout, C. J., Schulze-Lefert, P., Talbot, N. J., Ahmadinejad, N., Ametz, C., Barton, G. R., Benjdia, M., Bidzinski, P., Bindschedler, L. V., Both, M., Brewer, M. T., Cadle-Davidson, L., Cadle-Davidson, M. M., Collemare, J., Cramer, R., Frenkel, O., Godfrey, D., Harriman, J., Hoede, C., King, B. C., Klages, S., Kleemann, J., Knoll, D., Koti, P. S., Kreplak, J., Lopez-Ruiz, F. J., Lu, X. L., Maekawa, T., Mahanil, S., Micali, C., Milgroom, M. G., Montana, G., Noir, S., O'Connell, R. J., Oberhaensli, S., Parlange, F., Pedersen, C., Quesneville, H., Reinhardt, R., Rott, M., Sacristan, S., Schmidt, S. M., Schon, M., Skamnioti, P., Sommer, H., Stephens, A., Takahara, H., Thordal-Christensen, H., Vigouroux, M., Wessling, R., Wicker, T., and Panstruga, R. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543-1546.
40. Stergiopoulos, I., and de Wit, P. 2009. Fungal effector proteins. Annu. Rev. Phytopathol. 47:233-263.
41. Takken, F., and Rep, M. 2010. The arms race between tomato and Fusarium oxysporum. Mol. Plant Pathol. 11:309-314.
42. Wang, Y., and Huang, Q. 2011. Assays for effector-mediated suppression of programmed cell death in yeast. Methods Mol. Biol. 712:173-180.
43. Zhang, W.-J., Pedersen, C., Kwaaitaal, M., Gregersen, P. L., Mørch, S. M., Hanisch, S., Kristensen, A., Fuglsang, A. T., Collinge, D. B., and Thordal-Christensen, H. 2012. Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol. Plant Pathol. 13:1110-1119.
44. Zimmermann, G., Baeumlein, H., Mock, H.-P., Himmelbach, A., and Schweizer, P. 2006. The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance. Plant Physiol 142:181-192.
45. 2 (Protein Homology/analogY Recognition Engine V 2.0) server: www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=index
46. SignalP 4.1 server: www.cbs.dtu.dk/services/SignalP
47. EMBL-EBI Clustal W server: www.ebi.ac.uk/Tools/msa/clustalw2
48. Labsoft's Si-Fi software: labtools.ipk-gatersleben.de