Evidence for involvement of Dicer-like, Argonaute and histone deacetylase proteins in gene silencing in Phytophthora infestans

Molecular Plant Pathology

Volumn 12, Issue 8, 2011, Pages 772-785

  Vetukuri, Ramesh R ^a   Avrova, Anna O ^b   Grenville Briggs, Laura J ^c   Van West, Pieter ^c   Söderbom, Fredrik ^a   Savenkov, Eugene I ^a   Whisson, Stephen C ^b   Dixelius, Christina ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; HISTONE DEACETYLASE; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; RNA DIRECTED RNA POLYMERASE;

ARTICLE; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYTOPHTHORA INFESTANS; PLANT DISEASE; POTATO; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TOMATO;

ARGONAUTE PROTEINS; GENE SILENCING; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; LYCOPERSICON ESCULENTUM; PHYLOGENY; PHYTOPHTHORA INFESTANS; PLANT DISEASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA REPLICASE; SOLANUM TUBEROSUM;

EUKARYOTA; LYCOPERSICON ESCULENTUM; OOMYCETES; PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

EID: 80052394968     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2011.00710.x     Document Type: Article

References (69)

1. Ah Fong, A.M.V. and Judelson, H.S. (2003) Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol. Microbiol. 50, 487-494.
2. Ah Fong, A.M.V., Bormann-Chung, C.A. and Judelson, H.S. (2008) Optimization of transgene-mediated silencing in Phytophthora infestans and its association with small-interfering RNAs. Fungal Genet. Biol. 45, 1197-1205.
3. Alder, M.N., Dames, S., Gaudet, J. and Mango, S.E. (2003) Gene silencing in Caenorhabditis elegans by transitive RNA interference. RNA 9, 25-32.
4. Ansel, K.M., Pastor, W.A., Rath, N., Lapan, A.D., Glasmacher, E., Wolf, C., Smith, L.C., Papadopoulou, N., Lamperti, E.D., Tahiliani, M., Ellwart, J.W., Shi, Y., Kremmer, E., Rao, A. and Heissmeyer, V. (2008) Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat. Struct. Mol. Biol. 15, 523-530.
5. Avrova, A.O., Venter, E., Birch, P.R.J. and Whisson, S.C. (2003) Profiling and quantifying differential gene transcription in Phytophthora infestans prior to and during the early stages of potato infection. Fungal Genet. Biol. 40, 4-14.
6. Avrova, A.O., Boevink, P.C., Young, V., Grenville-Briggs, L.J., Van West, P., Birch, P.R.J. and Whisson, S.C. (2008) A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cell. Microbiol. 10, 2271-2284.
7. Baldauf, S.L., Roger, A.J., Wenk-Siefert, I. and Doolittle, W.F. (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science, 290, 972-977.
8. Baumberger, N. and Baulcombe, D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA, 102, 11928-11933.
9. Bernstein, E., Caudy, A.A., Hammond, S.M. and Hannon, G.J. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 409, 363-366.
10. Bos, J.I., Armstrong, M.R., Gilroy, E.M., Boevink, P.C., Hein, I., Taylor, R.M., Zhendong, T., Engelhardt, S., Vetukuri, R.R., Harrower, B., Dixelius, C., Bryan, G., Sadanandom, A., Whisson, S.C., Kamoun, S. and Birch, P.R.J. (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc. Natl. Acad. Sci. USA, 107, 9909-9914.
11. Burki, F., Shalchian-Tabrizi, K., Minge, M., Skjaeveland, A., Nikolaev, S.I., Jakobsen, K.S. and Pawlowsk, J. (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One, 2, e790 (doi: 10.1371/journal.pone.0000790).
12. Caten, C.E. and Jinks, J.L. (1968) Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can. J. Bot. 46, 329-348.
13. Cerutti, H. and Casas-Mollano, J. (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81-99.
14. Cogoni, C. and Macino, G. (1999) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature, 399, 166-169.
15. Cogoni, C. and Macino, G. (2000) Post-transcriptional gene silencing across kingdoms. Curr. Opin. Genet. Dev. 10, 638-643.
16. Colmenares, S.U., Buker, S.M., Buhler, M. and Dlakic, D. (2007) Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol. Cell, 27, 449-461.
17. Date, S.V. (2008) The Rosetta stone method. Methods Mol. Biol. 453, 169-180.
18. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783-791.
19. Fry, W. (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol. Plant Pathol. 9, 385-402.
20. Gabel, H.W. and Ruvkun, G. (2008) The exonuclease ERI-1 has a conserved dual role in 5.8S rRNA processing and RNAi. Nat. Struct. Mol. Biol. 15, 531-533.
21. Gaulin, E., Haget, N., Khatib, M., Herbert, C., Rickauer, M. and Bottin, A. (2007) Transgenic sequences are frequently lost in Phytophthora parasitica transformants without reversion of the transgene-induced silenced state. Can. J. Microbiol. 53, 152-157.
22. Grenville-Briggs, L.J., Avrova, A.O., Bruce, C.R., Williams, A., Whisson, S.C., Birch, P.R.J. and van West, P. (2005) Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genet. Biol. 42, 244-256.
23. Grenville-Briggs, L.J., Anderson, V.L., Fugelstad, J., Avrova, A.O., Bouzenzana, J., Williams, A., Wawra, S., Whisson, S.C., Birch, P.R.J., Bulone, V. and van West, P. (2008) Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell, 20, 720-738.
24. Grishok, A. (2005) RNAi mechanisms in Caenorhabditis elegans. FEBS Lett. 579, 5932-5939.
25. Grouffaud, S., van West, P., Avrova, A.O., Birch, P.R.J. and Whisson, S.C. (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology, 154, 3743-3751.
26. Grunstein, M. (1990) Histone function in transcription. Annu. Rev. Cell Biol. 6, 643-676.
27. Guru, T. (2000) A silence that speaks volumes. Nature, 404, 804-808.
28. Haas, B.J., Kamoun, S., Zody, M.C., Jiang, R.H., Handsaker, R.E., Cano, L.M., Grabherr, M., Kodira, C.D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T.O., Ah-Fong, A.M., Alvarado, L., Anderson, V.L., Armstrong, M.R., Avrova, A., Baxter, L., Beynon, J., Boevink, P.C., Bollmann, S.R., Bos, J.I., Bulone, V., Cai, G., Cakir, C., Carrington, J.C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M.A., Fugelstad, J., Gilroy, E.M., Gnerre, S., Green, P.J., Grenville-Briggs, L.J., Griffith, J., Grünwald, N.J., Horn, K., Horner, N.R., Hu, C.H., Huitema, E., Jeong, D.H., Jones, A.M., Jones, J.D., Jones, R.W., Karlsson, E.K., Kunjeti, S.G., Lamour, K., Liu, Z., Ma, L., Maclean, D., Chibucos, M.C., McDonald, H., McWalters, J., Meijer, H.J., Morgan, W., Morris, P.F., Munro, C.A., O'Neill, K., Ospina-Giraldo, M., Pinzón, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D.C., Schumann, U.D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D.J., Sykes, S., Thines, M., van de Vondervoort, P.J., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zhou, S., Fry, W., Meyers, B.C., van West, P., Ristaino, J., Govers, F., Birch, P.R., Whisson, S.C., Judelson, H.S. and Nusbaum, C. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461, 393-398.
29. Hall, I.M., Shankaranarayana, G.D., Noma, K.-, Ayoub, N., Cohen, A. and Grewal, S.I.S. (2002) Establishment and maintenance of a heterochromatin domain. Science, 297, 2232-2237.
30. Höck, J. and Meister, G. (2008) The Argonaute protein family. Genome Biol. 9, 210 (doi: 10.1186/gb-2008-9-2-210).
31. Huettel, B., Kanno, T., Daxinger, L., Bucher, E., van der Winden, J., Matzke, A.J. and Matzke, M. (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim. Biophys. Acta, 1769, 358-374.
32. Irvine, D.V., Zaratiegui, M., Tolia, N.H., Goto, D.B., Chitwood, D.H., Vaughn, M.W., Joshua-Tor, L. and Martienssen, R. (2006) Argonaute slicing is required for heterochromatic silencing and spreading. Science, 313, 1134-1137.
33. Jinek, M. and Doudna, J.A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature, 457, 405-412.
34. Judelson, H.S. and Tani, S. (2007) Transgene-induced silencing of the zoosporogenesis-specific NIFC gene cluster of Phytophthora infestans involves chromatin alterations. Eukaryot Cell, 6, 1200-1209.
35. Judelson, H.S., Tyler, B.M. and Michelmore, R.W. (1991) Transformation of the oomycete pathogen, Phytophthora infestans. Mol. Plant-Microbe Interact. 4, 602-607.
36. Judelson, H.S., Ah-Fong, A.M.V., Aux, G., Avrova, A.O., Bruce, C., Cakir, C., da Cunha, L., Grenville-Briggs, L., Latijnhouwers, M., Ligterink, W., Meijer, H.J.G., Roberts, S., Thurber, C.S., Whisson, S.C., Birch, P.R.J., Govers, F., Kamoun, S., van West, P. and Windass, J. (2008) Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol. Plant-Microbe Interact. 21, 433-447.
37. Kim, D.H., Villeneuve, L.M., Morris, K.V. and Rossi, J.J. (2006) Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat. Struct. Mol. Biol. 13, 793-797.
38. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S. and Kim, V.N. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature, 425, 415-419.
39. Makeyev, E.V. and Bamford, D.H. (2002) Cellular RNA-dependent RNA polymerase involved in posttranscriptional gene silencing has two distinct activity modes. Mol. Cell, 10, 1417-1427.
40. Malone, C.D. and Hannon, G.J. (2009) Small RNAs as guardians of the genome. Cell, 136, 656-668.
41. Martens, H., Novotny, J., Oberstrass, J., Steck, T.L., Postlethwait, P. and Nellen, W. (2002) RNAi in Dictyostelium: the role of RNA-directed RNA polymerases and double-stranded RNase. Mol. Biol. Cell, 13, 445-453.
42. Moazed, D. (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature, 457, 413-420.
43. Morris, K.V. (2005) siRNA-mediated transcriptional gene silencing: the potential mechanism and a possible role in the histone code. Cell. Mol. Life Sci. 62, 3057-3066.
44. Motamedi, M.R., Verdel, A., Colmenares, S.U., Gerber, S.A., Gygi, S.P. and Moazed, D. (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell, 119, 789-802.
45. Phillips, A.J., Anderson, V.L., Robertson, E.J., Secombes, C.J. and van West, P. (2008) New insights into animal pathogenic oomycetes. Trends Microbiol. 16, 13-19.
46. Probst, A.V., Fagard, M., Proux, F., Mourrain, P., Boutet, S., Earley, K., Lawrence, R.J., Pikaard, C.S., Murfett, J., Furner, I., Vaucheret, H. and Scheid, O.M. (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell, 16, 1021-1034.
47. Raffaele, S., Farrer, R.A., Cano, L.M., Studholme, D.J., MacLean, D., Thines, M., Jiang, R.H., Zody, M.C., Kunjeti, S.G., Donofrio, N.M., Meyers, B.C., Nusbaum, C. and Kamoun, S. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science, 330, 1540-1543.
48. Sadaie, M., Iida, T., Urano, T. and Nakayama, J.-I. (2004) A chromodomain protein, Chp1, is required for the establishment of heterochromatin in fission yeast. EMBO J. 23, 3825-3835.
49. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
50. Sigova, A., Rhind, N. and Zamore, P.D. (2004) A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev. 18, 2359-2367.
51. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K.L., Parrish, S., Timmons, L., Plasterk, R.H. and Fire, A. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell, 107, 465-476.
52. Tabara, H., Sarkissian, M., Kelly, W.G., Fleenor, J., Grishok, A., Timmons, L., Fire, A. and Mello, C. (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell, 99, 123-132.
53. Takezaki, N., Rzhetsky, A. and Nei, M. (1995) Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12, 823-833.
54. Tamaru, H. and Selker, E.U. (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature, 414, 277-283.
55. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
56. Tani, S., Yatzkan, E. and Judelson, H.S. (2004) Multiple pathways regulate the induction of genes during zoosporogenesis in Phytophthora infestans. Mol. Plant-Microbe Interact. 17, 330-337.
57. Vastenhouw, N.L., Brunschwig, K., Okihara, K.L., Muller, F., Tijsterman, M. and Plasterk, R.H.A. (2006) Gene expression: long-term gene silencing by RNAi. Nature, 442, 882.
58. Vastenhouw, N.L., Fischer, S.E.J., Robert, V.J.P., Thijssen, K.L., Fraser, A.G., Kamath, R.S., Ahringer, J. and Plasterk, R.H.A. (2003) A genome-wide screen identifies 27 genes involved in transposon silencing in C. elegans. Curr. Biol. 13, 1311-1316.
59. Vaucheret, H. (2008) Plant ARGONAUTES. Trends Plant Sci. 13, 350-358.
60. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I.S. and Moazed, D. (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science, 303, 672-676.
61. Verdel, A. and Moazed, D. (2005) RNAi-directed assembly of heterochromatin in fission yeast. FEBS Lett. 579, 5872-5878.
62. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I.S. and Martienssen, R.A. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science, 297, 1833-1837.
63. Walker, C.A., Koppe, M., Grenville-Briggs, L.J., Avrova, A.O., Horner, N.R., McKinnon, A.D., Whisson, S.C., Birch, P.R.J. and van West, P. (2008) A putative DEAD-box RNA-helicase is required for normal zoospore development in the late blight pathogen Phytophthora infestans. Fungal Genet. Biol. 45, 954-962.
64. van West, P., Kamoun, S., van 't Klooster, J.W. and Govers, F. (1999) Internuclear gene silencing in Phytophthora infestans. Mol. Cell, 3, 339-348.
65. van West, P., Shepherd, S.J., Walker, C.A., Li, S., Appiah, A.A., Grenville-Briggs, L.J., Govers, F. and Gow, N.A.R. (2008) Internuclear gene silencing in Phytophthora infestans is established through chromatin remodelling. Microbiology, 154, 1482-1490.
66. Whisson, S.C., Avrova, A.O., Van West, P. and Jones, J.T. (2005) A method for double-stranded RNA-mediated transient gene silencing in Phytophthora infestans. Mol. Plant Pathol. 6, 153-163.
67. Whisson, S.C., Boevink, P.C., Moleleki, L., Avrova, A.O., Morales, J.G., Gilroy, E.M., Armstrong, M.R., Grouffaud, S., van West, P., Chapman, S., Hein, I., Toth, I.K., Pritchard, L. and Birch, P. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115-118.
68. Yang, S.-J., Carter, S.A., Cole, A.B., Cheng, N.-H. and Nelson, R.S. (2004) A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl. Acad. Sci. USA, 101, 6297-6302.
69. Zuckerkandl, E. and Pauling, L. (1965) Evolutionary divergence and convergence in proteins. In: Evolving Genes and Proteins (Bryson, V. and Vogel, H.J., eds), pp. 97-166. New York: Academic Press.