Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae
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- 作者：Cristiano C Nunes (1)
Malali Gowda (1) (2)
Joshua Sailsbery (1)
Minfeng Xue (1) (3)
Feng Chen (4)
Douglas E Brown (1)
YeonYee Oh (1)
Thomas K Mitchell (5)
Ralph A Dean (1) - 刊名：BMC Genomics
- 出版年：2011
- 出版时间：December 2011
- 年：2011
- 卷：12
- 期：1
- 全文大小：1834KB
- 参考文献：1. Lee RC, Feinbaum RL, Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. / Cell 1993,75(5):843鈥?54. CrossRef
2. Abbott AL, Alvarez-Saavedra E, Miska EA, Lau NC, Bartel DP, Horvitz HR, Ambros V: The let-7 microRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans . / Dev Cell 2005, 9:403鈥?14. CrossRef
3. Kawaoka S, Hayashi N, Katsuma S, Kishino H, Kohara Y, Mita K, Shimada T: Bombyx small RNAs: Genomic defense system against transposons in the silkworm, Bombyx mori . / Insect Biochem Mol Biol 2008, 38:1058鈥?065. CrossRef
4. Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M, Bamford DH, Liu Y: qiRNA is a new type of small interfering RNA induced by DNA damage. / Nature 2009,459(7244):274鈥?77. CrossRef
5. Arnvig KB, Young DB: Identification of small RNAs in Mycobacterium tuberculosis . / Mol Microbiol 2009,73(3):397鈥?08. CrossRef
6. Kim VN, Han J, Siomi MC: Biogenesis of small RNAs in animals. / Nat Rev Mol Cell Biol 2009,10(2):126鈥?39. CrossRef
7. Ghildiyal M, Zamore PD: Small silencing RNAs: an expanding universe. / Nat Rev Genet 2009,10(2):94鈥?08. CrossRef
8. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, Bartel DP: RNAi in budding yeast. / Science 2009,326(5952):544鈥?50. CrossRef
9. J枚chl C, Rederstorff M, Hertel J, Stadler PF, Hofacker IL, Schrettl M, Haas H, Huttenhofer A: Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. / Nucleic Acids Res 2008,36(8):2677鈥?689. CrossRef
10. Kawaji H, Nakamura M, Takahashi Y, Sandelin A, Katayama S, Fukuda S, Daub CO, Kai C, Kawai J, Yasuda J, Carninci P, Hayashizaki Y: Hidden layers of human small RNAs. / BMC Genomics 2008, 9:157. CrossRef
11. Thompson DM, Parker R: The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae . / J Cell Biol 2009,185(1):43鈥?0. CrossRef
12. Lee YS, Shibata Y, Malhotra A, Dutta A: A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). / Genes Dev 2009,23(22):2639鈥?649. CrossRef
13. Yamasaki S, Ivanov P, Hu GF, Anderson P: Angiogenin cleaves tRNA and promotes stress-induced translational repression. / J Cell Biol 2009,185(1):35鈥?2. CrossRef
14. Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, Pertsemlidis A, Lewis ZA, Freitag M, Selker EU, Mello CC, Liu Y: Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. / Mol Cell 2010,38(6):803鈥?14. CrossRef
15. Nicolas FE, Moxon S, de Haro JP, Calo S, Grigoriev IV, Torres-Martinez S, Moulton V, Ruiz-Vazquez RM, Dalmay T: Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides . / Nucleic Acids Res 2010,38(16):5535鈥?541. CrossRef
16. Valent B, Chumley FG: Molecular genetic analysis of the rice blast fungus, Magnaporthe grisea . / Annu Rev Phytopathol 1991,29(1):443鈥?67. CrossRef
17. Urashima AS, Grosso CRF, Stabili A, Freitas EG, Silva CP, Netto DCS, Franco I, Bottan JHM: Effect of Magnaporthe grisea on seed germination, yield and quality of wheat. In / Advances in Genetics, Genomics and Control of Rice Blast Disease. Edited by: Wang G, Valent B. Springer Netherlands; 2009:267鈥?77. CrossRef
18. Talbot NJ: On the trail of a cereal killer: exploring the biology of Magnaporthe grisea . / Annu Rev Microbiol 2003,57(1):177鈥?02. CrossRef
19. Dean R: Signal pathways and appressorium morphogenesis. / Annu Rev Phytopathol 1997, 35:211鈥?34. CrossRef
20. Oh Y, Donofrio N, Pan H, Coughlan S, Brown D, Meng S, Mitchell T, Dean R: Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae . / Genome Biol 2008,9(5):R85. CrossRef
21. Gowda M, Venu RC, Raghupathy MB, Nobuta K, Li H, Wing R, Stahlberg E, Couglan S, Haudenschild CD, Dean R, Nahm BH, Meyers BC, Wang GL: Deep and comparative analysis of the mycelium and appressorium transcriptomes of Magnaporthe grisea using MPSS, RL-SAGE, and oligoarray methods. / BMC Genomics 2006, 7:310. CrossRef
22. Lee Y, Dean R: cAMP regulates infection structure formation in the plant-pathogenic fungus Magnaporthe grisea . / Plant Cell 1993, 5:693鈥?00. CrossRef
23. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan HQ, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li WX, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ: The genome sequence of the rice blast fungus Magnaporthe grisea . / Nature 2005, 434:980鈥?86. CrossRef
24. Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean RA, Wing RA, Soderlund C, Wang GL: Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. / Plant Physiol 2005,138(1):105鈥?15. CrossRef
25. Gowda M, Nunes CC, Sailsbery J, Xue M, Chen F, Nelson CA, Brown DE, Oh Y, Meng S, Mitchell T, Hagedorn CH, Dean RA: Genome-wide characterization of methylguanosine-capped and polyadenylated small RNAs in the rice blast fungus Magnaporthe oryzae . / Nucl Acids Res 2010, 38:7558鈥?569. CrossRef
26. Ebbole DJ: Magnaporthe as a model for understanding host-pathogen interactions. / Annu Rev Phytopathol 2007, 45:437鈥?56. CrossRef
27. Jeon J, Park S, Chi M, Choi J, Park J, Rho H, Kim S, Goh J, Yoo S, Park J, Yi M, Yang S, Kwon M, Han S, Kim B, Khang C, Park B, Lim S, Jung K, Kong S, Karunakaran M, Oh H, Kim H, Kang S, Choi W, Lee Y: Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. / Nat Genet 2007, 39:561鈥?65. CrossRef
28. Kadotani N, Nakayashiki H, Tosa Y, Mayama S: RNA silencing in the phytopathogenic fungus Magnaporthe oryzae . / Mol Plant Microbe Interact 2003,16(9):769鈥?76. CrossRef
29. Kadotani N, Nakayashiki H, Tosa Y, Mayama S: One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-triggered RNA silencing and related small interfering RNA accumulation. / J Biol Chem 2004,279(43):44467鈥?4474. CrossRef
30. Ebhardt HA, Tsang HH, Dai DC, Liu Y, Bostan B, Fahlman RP: Meta-analysis of small RNA-sequencing errors reveals ubiquitous post-transcriptional RNA modifications. / Nucleic Acids Res 2009,37(8):2461鈥?470. CrossRef
31. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP: Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans . / Cell 2006,127(6):1193鈥?207. CrossRef
32. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA: Human tRNA-derived small RNAs in the global regulation of RNA silencing. / RNA 2010,16(4):673鈥?95. CrossRef
33. Chen P, Jager G, Zheng B: Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana . / BMC Plant Biol 2010, 10:201. CrossRef
34. Hopper AK, Pai DA, Engelke DR: Cellular dynamics of tRNAs and their genes. / FEBS Lett 2010,584(2):310鈥?17. CrossRef
35. Johansson M, Bystr枚m A: Transfer RNA modifications and modifying enzymes in Saccharomyces cerevisiae . In / Fine-Tuning of RNA Functions by Modification and Editing. / Volume 12. Edited by: Grosjean H. Springer Berlin/Heidelberg: Topics in Current Genetics; 2005:87鈥?20.
36. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM: Rapid tRNA decay can result from lack of nonessential modifications. / Mol Cell 2006,21(1):87鈥?6. CrossRef
37. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B: Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1鈥? as biotrophy-associated secreted proteins in rice blast disease. / Plant Cell 2009,21(4):1273鈥?290. CrossRef
38. Donofrio NM, Oh Y, Lundy R, Pan H, Brown DE, Jeong JS, Coughlan S, Mitchell TK, Dean RA: Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea . / Fungal Genet Biol 2006,43(9):605鈥?17. CrossRef
39. Friedl盲nder MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N: Discovering microRNAs from deep sequencing data using miRDeep. / Nat Biotechnol 2008, 26:407鈥?15. CrossRef
40. Nakayashiki H, Nguyen QB: RNA interference: roles in fungal biology. / Curr Opin Microbiol 2008,11(6):494鈥?02. CrossRef
41. Schumann U, Ayliffe M, Kazan K, Wang M: RNA silencing in fungi. / Frontiers in Biology 2010,5(6):478鈥?94. CrossRef
42. Thon MR, Pan H, Diener S, Papalas J, Taro A, Mitchell TK, Dean RA: The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae . / Genome Biol 2006,7(2):R16. CrossRef
43. Kang S, Lebrun MH, Farrall L, Valent B: Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. / Mol Plant Microbe Interact 2001,14(5):671鈥?74. CrossRef
44. Fudal I, Bohnert HU, Tharreau D, Lebrun MH: Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea . / Fungal Genet Biol 2005,42(9):761鈥?72. CrossRef
45. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B: A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. / Plant Cell 2000,12(11):2019鈥?032. CrossRef
46. Hamilton A, Voinnet O, Chappell L, Baulcombe D: Two classes of short interfering RNA in RNA silencing. / EMBO J 2002,21(17):4671鈥?679. CrossRef
47. Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, Xu J, Kittler EL, Zapp ML, Weng Z, Zamore PD: Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. / Science 2008,320(5879):1077鈥?081. CrossRef
48. Yang N, Kazazian HH Jr: L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. / Nat Struct Mol Biol 2006,13(9):763鈥?71. CrossRef
49. Siomi MC, Miyoshi T, Siomi H: piRNA-mediated silencing in Drosophila germlines. / Semin Cell Dev Biol 2010,21(7):754鈥?59. CrossRef
50. Ikeda K, Nakayashiki H, Takagi M, Tosa Y, Mayama S: Heat shock, copper sulfate and oxidative stress activate the retrotransposon MAGGY resident in the plant pathogenic fungus Magnaporthe grisea . / Mol Genet Genomics 2001,266(2):318鈥?25. CrossRef
51. Murata T, Kadotani N, Yamaguchi M, Tosa Y, Mayama S, Nakayashiki H: siRNA-dependent and -independent post-transcriptional cosuppression of the LTR-retrotransposon MAGGY in the phytopathogenic fungus Magnaporthe oryzae . / Nucleic Acids Res 2007,35(18):5987鈥?994. CrossRef
52. Thompson DM, Lu C, Green PJ, Parker R: tRNA cleavage is a conserved response to oxidative stress in eukaryotes. / RNA 2008,14(10):2095鈥?103. CrossRef
53. Haiser HJ, Karginov FV, Hannon GJ, Elliot MA: Developmentally regulated cleavage of tRNAs in the bacterium Streptomyces coelicolor . / Nucleic Acids Res 2008,36(3):732鈥?41. CrossRef
54. Li Y, Luo J, Zhou H, Liao JY, Ma LM, Chen YQ, Qu LH: Stress-induced tRNA-derived RNAs: a novel class of small RNAs in the primitive eukaryote Giardia lamblia . / Nucleic Acids Res 2008,36(19):6048鈥?055. CrossRef
55. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, Lyko F: RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. / Genes Dev 2010,24(15):1590鈥?595. CrossRef
56. Tinoco ML, Dias BB, Dall'Astta RC, Pamphile JA, Arag茫o FJ: In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. / BMC Biol 2010, 8:27. CrossRef
57. Gowda M, Li H, Wang GL: Robust analysis of 5'-transcript ends: a high-throughput protocol for characterization of sequence diversity of transcription start sites. / Nat Protoc 2007,2(7):1622鈥?632. CrossRef
58. Lu C, Meyers BC, Green PJ: Construction of small RNA cDNA libraries for deep sequencing. / Methods 2007,43(2):110鈥?17. CrossRef
59. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, / et al.: Genome sequencing in microfabricated high-density picolitre reactors. / Nature 2005,437(7057):376鈥?80.
60. Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. / Genome Res 2004,14(6):1188鈥?190. CrossRef - 作者单位：Cristiano C Nunes (1)
Malali Gowda (1) (2)
Joshua Sailsbery (1)
Minfeng Xue (1) (3)
Feng Chen (4)
Douglas E Brown (1)
YeonYee Oh (1)
Thomas K Mitchell (5)
Ralph A Dean (1)
1. Fungal Genomics Laboratory, Center for Integrated Fungal Research, Department of Plant Pathology, North Carolina State University, Raleigh, NC, 27606, USA
2. Next-Generation Genomics Laboratory, Center for Cellular and Molecular Platform, NCBS-GKVK Campus, Bangalore, 560065, India
3. Department of Plant Pathology, China Agricultural University, Beijing, 1000193, China
4. US DOE Joint Genome Institute, Walnut Creek, CA, 94598, USA
5. Department of Plant Pathology, The Ohio State University, Columbus, OH, 43210, USA
文摘
Background Emerging knowledge of the impact of small RNAs as important cellular regulators has prompted an explosion of small transcriptome sequencing projects. Although significant progress has been made towards small RNA discovery and biogenesis in higher eukaryotes and other model organisms, knowledge in simple eukaryotes such as filamentous fungi remains limited. Results Here, we used 454 pyrosequencing to present a detailed analysis of the small RNA transcriptome (~ 15 - 40 nucleotides in length) from mycelia and appressoria tissues of the rice blast fungal pathogen, Magnaporthe oryzae. Small RNAs mapped to numerous nuclear and mitochondrial genomic features including repetitive elements, tRNA loci, rRNAs, protein coding genes, snRNAs and intergenic regions. For most elements, small RNAs mapped primarily to the sense strand with the exception of repetitive elements to which small RNAs mapped in the sense and antisense orientation in near equal proportions. Inspection of the small RNAs revealed a preference for U and suppression of C at position 1, particularly for antisense mapping small RNAs. In the mycelia library, small RNAs of the size 18 - 23 nt were enriched for intergenic regions and repetitive elements. Small RNAs mapping to LTR retrotransposons were classified as LTR retrotransposon-siRNAs (LTR-siRNAs). Conversely, the appressoria library had a greater proportion of 28 - 35 nt small RNAs mapping to tRNA loci, and were classified as tRNA-derived RNA fragments (tRFs). LTR-siRNAs and tRFs were independently validated by 3' RACE PCR and northern blots, respectively. Conclusions Our findings suggest M. oryzae small RNAs differentially accumulate in vegetative and specialized-infection tissues and may play an active role in genome integrity and regulating growth and development.