Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Chen, Yun ^a   Gao, Qixun ^a   Huang, Mengmeng ^a   Liu, Ye ^a   Liu, Zunyong ^a   Liu, Xin ^a   Ma, Zhonghua ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; FUNGAL RNA;

FUSARIUM; GENETICS; PHYSIOLOGY; RNA INTERFERENCE;

FUNGAL PROTEINS; FUSARIUM; RNA INTERFERENCE; RNA, FUNGAL;

EID: 84938225882     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12500     Document Type: Article

References (64)

1. Moazed, D. Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413-420 (2009).
2. Carreras-Villasenor, N., Esquivel-Naranjo, E. U., Villalobos-Escobedo, J. M., Abreu-Goodger, C. & Herrera-Estrella, A. The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride. Mol. Microbiol. 89, 96-112 (2013).
3. Nicolas, F. E., Torres-Martinez, S. & Ruiz-Vazquez, R. M. Loss and retention of RNA interference in fungi and parasites. PLoS Pathog. 9(1), e1003089 doi: 10.1371/journal.ppat.1003089 (2013).
4. Vaucheret, H., Vazquez, F., Crete, P. & Bartel, D. P. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18, 1187-1197 (2004).
5. Brodersen, P. & Voinnet, O. The diversity of RNA silencing pathways in plants. Trends Genet. 22, 268-280 (2006).
6. Romano, N. & Macino, G. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol. 6, 3343-3353 (1992).
7. Chang, S. S., Zhang, Z. & Liu, Y. RNA interference pathways in fungi: mechanisms and functions. Annu. Rev. Microbiol. 66, 305-323 (2012).
8. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
9. Li, X. & Carthew, R. W. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123, 1267-1277 (2005).
10. Croce, C. M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10, 704-714 (2009).
11. Xiao, C. & Rajewsky, K. MicroRNA control in the immune system: basic principles. Cell 136, 26-36 (2009).
12. Baulcombe, D. RNA silencing in plants. Nature 431, 356-363 (2004).
13. Jones-Rhoades, M. W., Bartel, D. P. & Bartel, B. MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53 (2006).
14. Lee, H. C. et al. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 38, 803-814 (2010).
15. Jiang, N., Yang, Y., Janbon, G., Pan, J. & Zhu, X. Identification and functional demonstration of miRNAs in the fungus Cryptococcus neoformans. PLoS One 7, e52734 doi: 10.1371/journal.pone.0052734 (2012).
16. Zhou, J. et al. Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol. Genet. Genomics 287, 275-282 (2012).
17. Zhou, Q., Wang, Z., Zhang, J., Meng, H. & Huang, B. Genome-wide identification and profiling of microRNA-like RNAs from Metarhizium anisopliae during development. Fungal Biol. 116, 1156-1162 (2012).
18. Goswami, R. S. & Kistler, H. C. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5, 515-525 (2004).
19. Starkey, D. E. et al. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet. Biol. 44, 1191-1204 (2007).
20. Bottalico, A. Fusarium diseases of cereals: species complex and related mycotoxin profiles, in Europe. J. Plant Pathol. 80, 85-103 (1998).
21. Jones, R. K. & Mirocha, C. J. Quality parameters in small grains from Minnesota affected by Fusarium head blight. Plant Dis. 83, 506-511 (1999).
22. Yin, Y., Liu, X., Li, B. & Ma, Z. Characterization of sterol demethylation inhibitor-resistant isolates of Fusarium asiaticum and F. graminearum collected from wheat in China. Phytopathology 99, 487-497 (2009).
23. Koch, A. et al. Host-induced gene silencing of cytochrome P450 lanosterol C14 alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. USA. 110, 19324-19329 (2013).
24. Cheng, W. et al. Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnol. J. doi: 10.1111/pbi.12352 (2015).
25. Liu, X. et al. Paralogous cyp51 genes in Fusarium graminearum mediate differential sensitivity to sterol demethylation inhibitors. Fungal Genet. Biol. 48, 113-123 (2011).
26. Nakayashiki, H. et al. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42, 275-283 (2005).
27. Ma, J. B., Ye, K. Q. & Patel, D. J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318-322 (2004).
28. Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293-296 (2000).
29. Lee, D. W., Pratt, R. J., McLaughlin, M. & Aramayo, R. An argonaute-like protein is required for meiotic silencing. Genetics 164, 821-828 (2003).
30. Alexander, W. G. et al. DCL-1 colocalizes with other components of the MSUD machinery and is required for silencing. Fungal Genet. Biol. 45, 719-727 (2008).
31. Segers, G. C., Zhang, X., Deng, F., Sun, Q. & Nuss, D. L. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc. Natl. Acad. Sci. USA. 104, 12902-12906 (2007).
32. Drinnenberg, I. A. et al. RNAi in budding yeast. Science 326, 544-550 (2009).
33. Janbon, G. et al. Characterizing the role of RNA silencing components in Cryptococcus neoformans. Fungal Genet. Biol. 47, 1070-1080 (2010).
34. Drinnenberg, I. A., Fink, G. R. & Bartel, D. P. Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333, 1592 (2011).
35. Lau, S. K. et al. Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLoS Negl. Trop. Dis. 7, e2398 doi: 10.1371/journal.pntd.0002398 (2013).
36. Rathjen, T. et al. High throughput sequencing of microRNAs in chicken somites. FEBS Lett. 583, 1422-1426 (2009).
37. Szittya, G. et al. High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9, 593 doi: 10.1186/1471-2164-9-593 (2008).
38. Bonnet, E., Wuyts, J., Rouze, P. & Van de Peer, Y. Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics 20, 2911-2917 (2004).
39. Kuck, U. & Hoff, B. New tools for the genetic manipulation of filamentous fungi. Appl. Microbiol. Biotechnol. 86, 51-62 (2010).
40. Nguyen, Q. B., Itoh, K., Van Vu, B., Tosa, Y. & Nakayashiki, H. Simultaneous silencing of endo-beta-1,4 xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol. Microbiol. 81, 1008-1019 (2011).
41. Abdel-Hadi, A. M., Caley, D. P., Carter, D. R. & Magan, N. Control of aflatoxin production of Aspergillus flavus and Aspergillus parasiticus using RNA silencing technology by targeting aflD (nor-1) gene. Toxins 3, 647-659 (2011).
42. Ghag, S. B., Shekhawat, U. K. & Ganapathi, T. R. Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant Biotechnol. J. 12, 541-553 (2014).
43. Khatri, M. & Rajam, M. V. Targeting polyamines of Aspergillus nidulans by siRNA specific to fungal ornithine decarboxylase gene. Med. Mycol. 45, 211-220 (2007).
44. Fitzgerald, A., Van Kan, J. A. & Plummer, K. M. Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet. Biol. 41, 963-971 (2004).
45. Nguyen, Q. B. et al. Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. Mol. Microbiol. 68, 1348-65 (2008).
46. Sigova, A., Rhind, N. & Zamore, P. D. A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev. 18, 2359-2367 (2004).
47. Iida, T., Nakayama, J. & Moazed, D. siRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol. Cell 31, 178-189 (2008).
48. Simmer, F. et al. Hairpin RNA induces secondary small interfering RNA synthesis and silencing in trans in fission yeast. EMBO Rep. 11, 112-118 (2010).
49. Smith, N. A. et al. Total silencing by intron-spliced hairpin RNAs. Nature 407, 319-320 (2000).
50. Hammond, T. M. et al. RNA silencing gene truncation in the filamentous fungus Aspergillus nidulans. Eukaryot. Cell 7, 339-349 (2008).
51. Nolan, T. et al. The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res. 33, 1564-1573 (2005).
52. Nicolas, F. E. et al. Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides. Nucleic Acids Res. 38, 5535-5541 (2010).
53. Nunes, C. C. et al. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genomics 12, 288 doi: 10.1186/1471-2164-12-28 (2011).
54. Sun, Q., Choi, G. H. & Nuss, D. L. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc. Natl. Acad. Sci. USA. 106, 17927-17932 (2009).
55. Wang, X. et al. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev. 24, 2566-2582 (2010).
56. Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837 (2002).
57. Martienssen, R. A., Zaratiegui, M. & Goto, D. B. RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet. 21, 450-456 (2005).
58. Liu, X. H. et al. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot. Cell 6, 997-1005 (2007).
59. Proctor, R. H., Hohn, T. M. & Mccormick, S. P. Reduced Virulence of Gibberella zeae Caused by Disruption of a Trichothecene Toxin Biosynthetic Gene. Mol. Plant Microbe Interact. 8, 593-601 (1995).
60. Hou, Z. et al. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe Interact. 15, 1119-1127 (2002).
61. Park, G., Bruno, K. S., Staiger, C. J., Talbot, N. J. & Xu, J. R. Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol. Microbiol. 53, 1695-1707 (2004).
62. Bruno, K. S., Tenjo, F., Li, L., Hamer, J. E. & Xu, J. R. Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot. Cell 3, 1525-1532 (2004).
63. Griffiths-Jones, S. et al. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 33, D121-124 (2005).
64. Enright, A. J. et al. MicroRNA targets in Drosophila. Genome Biol. 5, R1 (2003).