Molecular Characteristics and Efficacy of 16D10 siRNAs in Inhibiting Root-Knot Nematode Infection in Transgenic Grape Hairy Roots

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Yang, Yingzhen ^a   Jittayasothorn, Yingyos ^a,b   Chronis, Demosthenis ^c   Wang, Xiaohong ^c   Cousins, Peter ^a,d   Zhong, Gan Yuan ^a  

^a Grape Genetics Research Unit   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

^c ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

^d E and J Gallo Winery ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SINGLE STRANDED RNA; SMALL INTERFERING RNA;

16D10 GENE; ARTICLE; CONTROLLED STUDY; GENE; GENE SILENCING; GRAPE; INFECTION SENSITIVITY; NONHUMAN; RNA INTERFERENCE; RNA SEQUENCE; ROOT KNOT; TRANSGENIC PLANT;

ANIMALS; NEMATODA; NEMATODE INFECTIONS; PLANT DISEASES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RNA, SMALL INTERFERING; VITIS;

EID: 84880465168     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069463     Document Type: Article

References (59)

1. Nicol JM, Stirling GR, Rose BJ, May P, Van Heeswijck R, (1999) Impact of nematodes on grapevine growth and productivity: current knowledge and future directions, with special reference to Australian viticulture. Australian Journal of Grape and Wine Research 5: 109-127.
2. Cain DW, Mckenry MV, Tarailo RE, (1984) A new pathotype of root-knot nematode on grape rootstocks. J Nematol 16: 207-208.
3. Cousins P, Johnston D, Switras-Meyer S, Boyden L, Vidmar J, et al. (2007) USDA ARS research in grape rootstock breeding and genetics. Acta Hort (ISHS) 733: 51-58.
4. Cousins P, Walker MA, (2002) Genetics of resistance to Meloidogyne incognita in crosses of grape rootstocks. Theor Appl Genet 105: 802-807.
5. Xu K, Riaz S, Roncoroni NC, Jin Y, Hu R, et al. (2008) Genetic and QTL analysis of resistance to Xiphinema index in a grapevine cross. Theor Appl Genet 116: 305-311.
6. Hwang CF, Xu KN, Hu R, Zhou R, Riaz S, et al. (2010) Cloning and characterization of XiR1, a locus responsible for dagger nematode resistance in grape. Theor Appl Genet 121: 789-799.
7. Davis EL, Hussey RS, Mitchum MG, Baum TJ, (2008) Parasitism proteins in nematode-plant interactions. Curr Opin Plant Biol 11: 360-366.
8. Lilley CJ, Davies LJ, Urwin PE, (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139: 630-640.
9. Huang GZ, Allen R, Davis EL, Baum TJ, Hussey RS, (2006) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. P Natl Acad Sci USA 103: 14302-14306.
10. Charlton WL, Harel HY, Bakhetia M, Hibbard JK, Atkinson HJ, et al. (2010) Additive effects of plant expressed double-stranded RNAs on root-knot nematode development. Int J Parasitol 40: 855-864.
11. Yadav BC, Veluthambi K, Subramaniam K, (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasit 148: 219-222.
12. Ibrahim HMM, Alkharouf NW, Meyer SLF, Aly MAM, El-Din AEYG, et al. (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol 127: 90-99.
13. Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL, et al. (2009) Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 60: 315-324.
14. Steeves RM, Todd TC, Essig JS, Trick HN, (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Funct Plant Biol 33: 991-999.
15. Klink VP, Kim KH, Martins V, MacDonald MH, Beard HS, et al. (2009) A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta 230: 53-71.
16. Li JR, Todd TC, Oakley TR, Lee J, Trick HN, (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232: 775-785.
17. Hirai S, Kodama H, (2008) RNAi vectors for manipulation of gene expression in higher plants. The Open Plant Science Journal 2: 21-30.
18. Li LM, Lin XY, Khvorova A, Fesik SW, Shen Y, (2007) Defining the optimal parameters for hairpin-based knockdown constructs. RNA 13: 1765-1774.
19. Miyagishi M, Sumimoto H, Miyoshi H, Kawakami Y, Taira K, (2004) Optimization of an siRNA-expression system with an improved hairpin and its significant suppressive effects in mammalian cells. J Gene Med 6: 715-723.
20. Mcintyre GJ, Yu YH, Lomas M, Fanning GC, (2011) The effects of stem length and core placement on shRNA activity. BMC Mol Biol 12: 34.
21. Liu YP, von Eije KJ, Schopman NCT, Westerink JT, ter Brake O, et al. (2009) Combinatorial RNAi against HIV-1 using extended short hairpin RNAs. Mol Ther 17: 1712-1723.
22. Bernstein E, Caudy AA, Hammond SM, Hannon GJ, (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
23. Schauer SE, Jacobsen SE, Meinke DW, Ray A, (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7: 487-491.
24. Runo S, Alakonya A, Machuka J, Sinha N, (2011) RNA interference as a resistance mechanism against crop parasites in Africa: a 'Trojan horse' approach. Pest Manag Sci 67: 129-136.
25. Sen GL, Blau HM, (2006) A brief history of RNAi: the silence of the genes. FASEB J 20: 1293-1299.
26. Boudreau RL, Spengler RM, Hylock RH, Kusenda BJ, Davis HA,et al. (2012) siSPOTR: a tool for designing highly specific and potent siRNAs for human and mouse. Nucleic Acids Res doi:10.1093/nar/gks1797.
27. Lamarcq LH, Scherer BJ, Phelan ML, Kalnine NN, Nguyen YH, et al. (2006) Large-scale, high-throughput validation of short hairpin RNA sequences for RNA interference. J Biomol Screen 11: 236-246.
28. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, et al. (2004) Rational siRNA design for RNA interference. Nat Biotechnol 22: 326-330.
29. Elbashir SM, Harborth J, Weber K, Tuschl T, (2002) Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26: 199-213.
30. Fellmann C, Zuber J, McJunkin K, Chang K, Malone CD, et al. (2011) Functional identification of optimized RNAi triggers using a massively parallel sensor assay. Mol Cell 41: 733-746.
31. Grimm D, Streetz KL, Jopling CL, Storm TA, Pandey K, et al. (2006) Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441: 537-541.
32. Huang GZ, Dong RH, Allen R, Davis EL, Baum TJ, et al. (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe In 19: 463-470.
33. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590.
34. Jittayasothorn Y, Yang Y, Chen S, Wang X, Zhong GY, (2011) Influences of Agrobacterium rhizogenes strains, plant genotypes, and tissue types on the induction of transgenic hairy roots in Vitis species. Vitis 50: 107-114.
35. Lambert KN, Tedford EC, Caswell EP, Williamson VM, (1992) A system for continuous production of root-knot nematode juveniles in hydroponic culture. Phytopathology 82: 512-515.
36. Hussey RS, Janssen GJW (2002) In:Starr JL, Cook R, Bridge J, editors. Plant Resistance to parasitic nematodes: CABI, Wallingford, UK. 43-70.
37. Daykin ME, Hussey RS (1985) Staining and histopathological techniques in nematology. In: Barker KR, Carter CC, Sasser JN, editors. An advanced treatise on Meloidogyne: North Carolina State University, Raleigh. 39-46.
38. Carra A, Gambino G, Schubert A, (2007) A cetyltrimethylammonium bromide-based method to extract low-molecular-weight RNA from polysaccharide-rich plant tissues. Anal Biochem 360: 318-320.
39. Claverie M, Dirlewanger E, Bosselut N, Van Ghelder C, Voisin R, et al. (2011) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol 156: 779-792.
40. Ho T, Wang H, Pallett D, Dalmay T, (2007) Evidence for targeting common siRNA hotspots and GC preference by plant Dicer-like proteins. FEBS Lett 581: 3267-3272.
41. Schwarz DS, Hutvagner G, Du T, Xu ZS, Aronin N, et al. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208.
42. Khvorova A, Reynolds A, Jayasena SD, (2003) Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216.
43. Hutvagner G, (2005) Small RNA asymmetry in RNAi: Function in RISC assembly and gene regulation. FEBS Lett 579: 5850-5857.
44. Freier SM, Kierzek R, Jaeger JA, Sugimoto N, Caruthers MH, et al. (1986) Improved free-energy parameters for predictions of RNA duplex stability. P Natl Acad Sci USA 83: 9373-9377.
45. Kim YK, Yeo J, Kim B, Ha M, Kim VN, (2012) Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 46: 893-895.
46. Wubben MJ, Callahan FE, Triplett BA, Jenkins JN, (2009) Phenotypic and molecular evaluation of cotton hairy roots as a model system for studying nematode resistance. Plant Cell Rep 28: 1399-1409.
47. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, et al. (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872-875.
48. Llave C, Kasschau KD, Rector MA, Carrington JC, (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619.
49. Ho T, Pilcher RLR, Edwards ML, Cooper I, Dalmay T, et al. (2008) Evidence for GC preference by monocot Dicer-like proteins. Biochem Bioph Res Co 368: 433-437.
50. Liu YP, Haasnoot J, Berkhout B, (2007) Design of extended short hairpin RNAs for HIV-1 inhibition. Nucleic Acids Res 35: 5683-5693.
51. Saayman S, Barichievy S, Capovilla A, Morris KV, Arbuthnot P, et al. (2008) The efficacy of generating three independent anti-HIV-1 siRNAs from a single U6 RNA Pol III-expressed long hairpin RNA. Plos One 3(7): e2602 doi:2610.1371/journal.pone.0002602.
52. Vlassov AV, Korba B, Farrar K, Mukerjee S, Seyhan AA, et al. (2007) shRNAs targeting hepatitis C: effects of sequence and structural features, and comparison with siRNA. Oligonucleotides 17: 223-236.
53. Jensen SMR, Schmitz A, Pedersen FS, Kjems J, Bramsen JB, (2012) Functional Selection of shRNA Loops from Randomized Retroviral Libraries. Plos One 7(8): e43095 doi:43010.41371/journal.pone.0043095.
54. Boudreau RL, Monteys AM, Davidson BL, (2008) Minimizing variables among hairpin-based RNAi vectors reveals the potency of shRNAs. RNA 14: 1834-1844.
55. Park JE, Heo I, Tian Y, Simanshu DK, Chang H, et al. (2011) Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature 475: 201-207.
56. Leibman D, Wolf D, Saharan V, Zelcer A, Arazi T, et al. (2011) A high level of transgenic viral small RNA is associated with broad potyvirus resistance in cucurbits. Mol Plant Microbe In 24: 1220-1238.
57. Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H, (2002) Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucleic Acids Res 30: 1757-1766.
58. Chan CY, Carmack CS, Long DD, Maliyekkel A, Shao Y,et al. (2009) A structural interpretation of the effect of GC-content on efficiency of RNA interference. BMC Bioinformatics (Suppl 1): S33.
59. Li Z, Fortin Y, Shen SH (2009) Forward and robust selection of the most potent and noncellular toxic siRNAs from RNAi libraries. Nucleic Acids Res 37: doi10.1093/nar/gkn1953.