Efficiency of different strategies for gene silencing in Botrytis cinerea

Applied Microbiology and Biotechnology

Volumn 98, Issue 22, 2014, Pages 9413-9424

  Espino, José ^a,b   González, Mario ^a   González, Celedonio ^a   Brito, Nélida ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Botrytis; GFP; Hairpin RNA; niaD; Opposing dual promoter; Post transcriptional gene silencing; RNA interference

Indexed keywords

GENETIC ENGINEERING; RNA;

BOTRYTIS; GFP; HAIRPIN RNA; NIAD; OPPOSING DUAL-PROMOTER; POST-TRANSCRIPTIONAL GENE SILENCING; RNA INTERFERENCE;

GENE EXPRESSION;

FUNGAL RNA; GREEN FLUORESCENT PROTEIN; MULTIPROTEIN COMPLEX; NITRATE REDUCTASE; FUNGAL DNA; SMALL INTERFERING RNA;

AJELLOMYCES DERMATITIDIS; ARABIDOPSIS THALIANA; ARTICLE; BOTRYTIS CINEREA; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CRYPHONECTRIA PARASITICA; DIMERIZATION; FUNGAL GENOME; FUNGUS MUTANT; GENE EXPRESSION; GENE SILENCING; GENETIC CODE; GENETIC TRANSFORMATION; INTRON; NONHUMAN; PROMOTER REGION; RICE; RNA BINDING; RNA INTERFERENCE; BOTRYTIS; CHEMISTRY; EVALUATION STUDY; GENE VECTOR; GENETICS; METABOLISM; MICROBIAL GENETICS; PLASMID; PROCEDURES; REPORTER GENE;

BOTRYTIS; DNA, FUNGAL; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; GENETIC VECTORS; GENETICS, MICROBIAL; PLASMIDS; RNA, SMALL INTERFERING;

EID: 84925484263     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6087-7     Document Type: Article

References (53)

1. Benito E, Prins T, van Kan JAL (1996) Application of differential display RT-PCR to the analysis of gene expression in a plant-fungus interaction. Plant Mol Biol 32:947–957
2. Benito E, ten Have A, van’t Klooster J, van Kan JAL (1998) Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur J Plant Pathol 104:207–220
3. Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J (2013) RNAi function, diversity, and loss in the fungal kingdom. Chromosom Res 21:561–572
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
5. Brito N, Espino JJ, González C (2006) The endo-ß-1,4-xylanase Xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32
6. Bromley M, Gordon C, Rovira-Graells NA, Oliver J (2006) The Aspergillus fumigatus cellobiohydrolase B (cbhB) promoter is tightly regulated and can be exploited for controlled protein expression and RNAi. FEMS Microbiol Lett 264:246–254
7. Burroughs AM, Ando Y, Aravind L (2014) New perspectives on the diversification of the RNA interference system: insights from comparative genomics and small RNA sequencing. Wiley Interdiscip Rev RNA 5:141–181
8. Campbell WH (2001) Structure and function of eukaryotic NAD(P)H:nitrate reductase. Cell Mol Life Sci 58:194–204
9. Chang SS, Zhang Z, Liu Y (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305–323
10. Cools HJ, Hammond-Kosack KE (2013) Exploitation of genomics in fungicide research: current status and future perspectives. Mol Plant Pathol 14:197–210
11. Dang Y, Zhang Z, Liu Y (2014) Small RNA-mediated gene silencing in Neurospora. In: Sesma A, von der Haar T (eds) Fungal RNA biology. Springer International Publishing, Cham, pp 269–289
12. Delcan J, Moyano C, Raposo R, Melgarejo P (2002) Storage of Botrytis cinerea using different methods. J Plant Pathol 84:3–9
13. Elad Y, Williamson B, Tudzynski P, Delen N (2004) Botrytis spp. and diseases they cause in agricultural systems—an introduction. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Kluwer Academic Publishers, Dordrecht, pp 1–8
14. Espino JJ, Gutierrez-Sanchez G, Brito N, Shah P, Orlando R, Gonzalez C (2010) The Botrytis cinerea early secretome. Proteomics 10:3020–3034
15. Gagnon KT, Corey DR (2012) Argonaute and the nuclear RNAs: new pathways for RNA-mediated control of gene expression. Nucleic Acid Ther 22:3–16
16. Garre V, Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM (2014) The RNAi machinery in mucorales: the emerging role of endogenous small RNAs. In: Sesma A, von der Haar T (eds) Fungal RNA biology. Springer International Publishing, Cham, pp 291–313
17. Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, Haeuser-Hahn I, Schreier PH, Tudzynski P (2012) Identification of pathogenesis-associated genes by T-DNA-mediated insertional mutagenesis in Botrytis cinerea: a type 2A phosphoprotein phosphatase and an SPT3 transcription factor have significant impact on virulence. Mol Plant Microbe Interact 25:481–495
18. Giesbert S, Siegmund U, Schumacher J, Kokkelink L, Tudzynski P (2014) Functional analysis of BcBem1 and its interaction partners in Botrytis cinerea: impact on differentiation and virulence. PLoS One 9:e95172
19. González C, Noda J, Espino JJ, Brito N (2008) Drill-assisted genomic DNA extraction from Botrytis cinerea. Biotechnol Lett 30:1989–1992
20. Gronover CS, Schorn C, Tudzynski B (2004) Identification of Botrytis cinerea genes up-regulated during infection and controlled by the Galpha subunit BCG1 using suppression subtractive hybridization (SSH). Mol Plant Microbe Interact 17:537–546
21. Hamada W, Reignault P, Bompeix G, Boccara M (1994) Transformation of Botrytis cinerea with the hygromycin B resistance gene, hph. Curr Genet 26:251–255
22. Hammond TM, Xiao H, Boone EC, Decker LM, Lee SA, Perdue TD, Pukkila PJ, Shiu PK (2013) Novel proteins required for meiotic silencing by unpaired DNA and siRNA generation in Neurospora crassa. Genetics 194:91–100
23. Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94:2122–2127
24. Henry C, Mouyna I, Latgé JP (2007) Testing the efficacy of RNA interference constructs in Aspergillus fumigatus. Curr Genet 51:277–284
25. Jaskiewicz L, Filipowicz W (2008) Role of Dicer in posttranscriptional RNA silencing. Curr Top Microbiol Immunol 320:77–97
26. Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2004) 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 279:44467–44474
27. Kück U, Hoff B (2010) New tools for the genetic manipulation of filamentous fungi. Appl Microbiol Biotechnol 86:51–62
28. Kuhn CD, Joshua-Tor L (2013) Eukaryotic Argonautes come into focus. Trends Biochem Sci 38:263–271
29. Lacroix H, Spanu PD (2009) Silencing of six hydrophobins in Cladosporium fulvum: complexities of simultaneously targeting multiple genes. Appl Environ Microbiol 75:542–546
30. Leroch M, Kleber A, Silva E, Coenen T, Koppenhofer D, Shmaryahu A, Valenzuela PD, Hahn M (2013) Transcriptome profiling of Botrytis cinerea conidial germination reveals upregulation of infection-related genes during the prepenetration stage. Eukaryot Cell 12:614–626
31. Liu H, Cottrell TR, Pierini LM, Goldman WE, Doering TL (2002) RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160:463–470
32. Luna E, Bruce TJ, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiol 158:844–853
33. Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262
34. Nguyen QB, Itoh K, Van VB, Tosa Y, Nakayashiki H (2011) Simultaneous silencing of endo-ß-1,4 xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol Microbiol 81:1008–1019
35. Noda J, Brito N, Espino JJ, Gonzalez C (2007) Methodological improvements in the expression of foreign genes and in gene replacement in the phytopathogenic fungus Botrytis cinerea. Mol Plant Pathol 8:811–816
36. Nunes CC, Dean RA (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
37. Nunes CC, Sailsbery JK, Dean RA (2011) Characterization and application of small RNAs and RNA silencing mechanisms in fungi. Fungal Biol Rev 25:172–180
38. Patel RM, van Kan JAL, Bailey AM, Foster GD (2008) RNA-mediated gene silencing of superoxide dismutase (bcsod1) in Botrytis cinerea. Phytopathology 98:1334–1339
39. Patel RM, van Kan JAL, Bailey AM, Foster GD (2010) Inadvertent gene silencing of argininosuccinate synthase (bcass1) in Botrytis cinerea by the pLOB1 vector system. Mol Plant Pathol 11:613–624
40. Rolland SG, Bruel CA (2008) Sulphur and nitrogen regulation of the protease-encoding ACP1 gene in the fungus Botrytis cinerea: correlation with a phospholipase D activity. Microbiology 154:1464–1473
41. Romao-Dumaresq AS, de Araújo WL, Talbot NJ, Thornton CR (2012) RNA Interference of endochitinases in the sugarcane endophyte Trichoderma virens 223 reduces its fitness as a biocontrol agent of pineapple disease. PLoS One 7:e47888
42. Sambrook J, Russell DW (2001) Molecular cloning. A laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
43. T method. Nat Protoc 3:1101–1108
44. Schumacher J, Viaud M, Simon A, Tudzynski B (2008) The G α subunit BCG1, the phospholipase C (BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol Microbiol 67:1027–1050
45. Shiu PKT, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107:905–916
46. Snell FD, Snell CT (1949) Colorimetric methods of analysis. Van Nostrand, New York
47. Son H, Min K, Lee J, Raju NB, Lee YW (2011) Meiotic silencing in the homothallic fungus Gibberella zeae. Fungal Biol 115:1290–1302
48. Tauati S, Pearson M, Choquer M, Foster G, Bailey A (2014) Investigating the role of dicer 2 (dcr2) in gene silencing and the regulation of mycoviruses in Botrytis cinerea. Microbiology 83:140–148
49. Tudzynski P, Siewers V (2004) Approaches to molecular genetics and genomics of Botrytis. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Kluwer Academic Publisher, Dordrecht, pp 53–66
50. van Kan JAL, van’t Klooster JW, Wagemakers CAM, Dees DCT, van der Vlugt-Bergmans CJB (1997) Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol Plant Microbe Interact 10:30–38
51. Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151
52. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123
53. Ziv C, Yarden O (2010) Gene silencing for functional analysis: assessing RNAi as a tool for manipulation of gene expression. Methods Mol Biol 638:77–100