Expression of geminiviral AC2 RNA silencing suppressor changes sugar and jasmonate responsive gene expression in transgenic tobacco plants

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Soitamo, Arto J ^a   Jada, Balaji ^a   Lehto, Kirsi ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BEGOMOVIRUS; GEMINIVIRIDAE; MANIHOT ESCULENTA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

AC2 PROTEIN, GEMINIVIRUS; CHLOROPHYLL; CYCLOPENTANE DERIVATIVE; CYSTEINE PROTEINASE; DNA BINDING PROTEIN; HC PRO PROTEIN, POTYVIRUS; HC-PRO PROTEIN, POTYVIRUS; JASMONIC ACID; MESSENGER RNA; OXYLIPIN; RIBOSOME PROTEIN; VEGETABLE PROTEIN; VIRUS PROTEIN;

ARTICLE; BIOSYNTHESIS; CARBOHYDRATE METABOLISM; DNA MICROARRAY; DOWN REGULATION; DRUG EFFECT; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; IMMUNOLOGY; METABOLISM; OXIDATIVE STRESS; PHENOTYPE; PHOTOSYNTHESIS; PLANT GENE; PLANT LEAF; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPPRESSOR GENE; TOBACCO; TRANSGENIC PLANT; UPREGULATION; VIROLOGY;

CARBOHYDRATE METABOLISM; CHLOROPHYLL; CYCLOPENTANES; CYSTEINE ENDOPEPTIDASES; DNA-BINDING PROTEINS; DOWN-REGULATION; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; GENES, SUPPRESSOR; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; OXYLIPINS; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEINS; RNA, MESSENGER; TOBACCO; UP-REGULATION; VIRAL PROTEINS;

EID: 84868308343     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-204     Document Type: Article

References (56)

1. Fang Y, Spector DL. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 2007, 17(9):818-823. 10.1016/j.cub.2007.04.005, 1950788, 17442570.
2. Yang Z, Ebright YW, Yu B, Chen X. HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2' OH of the 3' terminal nucleotide. Nucleic Acids Res 2006, 34(2):667-675. 10.1093/nar/gkj474, 1356533, 16449203.
3. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS. Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 2005, 102(10):3691-3696. 10.1073/pnas.0405570102, 553294, 15738428.
4. Vaucheret H. Plant ARGONAUTES. Trends Plant Sci 2008, 13(7):350-358. 10.1016/j.tplants.2008.04.007, 18508405.
5. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ. RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 2009, 21(3):367-376. 10.1016/j.ceb.2009.01.025, 19243928.
6. Wadsworth S, Dunoyer P. Plant RNA-silencing immunity and viral counter-defence strategies. pp. 1-35. In: Molecular Plant-Microbe Interactions. Eds. Bouarab et al. 2009, 1-35.
7. Navarro L, Jay F, Nomura K, He SY, Voinnet O. Suppression of the microRNA pathway by bacterial effector proteins. Science 2008, 321(5891):964-967. 10.1126/science.1159505, 2570098, 18703740.
8. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136(4):669-687. 10.1016/j.cell.2009.01.046, 19239888.
9. Jay F, Renou JP, Voinnet O, Navarro L. Biotic stress-associated microRNAs: identification, detection, regulation, and functional analysis. Methods Mol Biol 2010, 592:183-202. 10.1007/978-1-60327-005-2_13, 19802597.
10. Ruiz-Ferrer V, Voinnet O. Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 2009, 60:485-510. 10.1146/annurev.arplant.043008.092111, 19519217.
11. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 2008, 8:25. 10.1186/1471-2229-8-25, 2292181, 18312648.
12. Voinnet O. Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Curr Opin Plant Biol 2008, 11(4):464-470. 10.1016/j.pbi.2008.04.006, 18583181.
13. Chellappan P, Xia J, Zhou X, Gao S, Zhang X, Coutino G, Vazquez F, Zhang W, Jin H. siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Res 2010, 38(20):6883-6894. 10.1093/nar/gkq590, 2978365, 20621980.
14. Chapman EJ, Carrington JC. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 2007, 8(11):884-896. 10.1038/nrg2179, 17943195.
15. Moissiard G, Voinnet O. Viral suppression of RNA silencing in plants. Mol Plant Pathol 2004, 5(1):71-82. 10.1111/j.1364-3703.2004.00207.x, 20565584.
16. Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 1998, 17(22):6739-6746. 10.1093/emboj/17.22.6739, 1171019, 9822616.
17. Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 2005, 6(3):206-220. 10.1038/nrg1555, 15703763.
18. Lakatos L, Szittya G, Silhavy D, Burgyan J. Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J 2004, 23(4):876-884. 10.1038/sj.emboj.7600096, 381004, 14976549.
19. Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, Liu YP, Dolja VV, Calvino LF, Lopez-Moya JJ, Burgyan J. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J 2006, 25(12):2768-2780. 10.1038/sj.emboj.7601164, 1500863, 16724105.
20. Ding SW. RNA-based antiviral immunity. Nat Rev Immunol 2010, 10(9):632-644. 10.1038/nri2824, 20706278.
21. Vanitharani R, Chellappan P, Fauquet CM. Geminiviruses and RNA silencing. Trends Plant Sci 2005, 10(3):144-151. 10.1016/j.tplants.2005.01.005, 15749473.
22. Chellappan P, Masona MV, Vanitharani R, Taylor NJ, Fauquet CM. Broad spectrum resistance to ssDNA viruses associated with transgene-induced gene silencing in cassava. Plant Mol Biol 2004, 56(4):601-611. 10.1007/s11103-004-0147-9, 15630623.
23. Patil BL, Fauquet CM. Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Pathol 2009, 10(5):685-701. 10.1111/j.1364-3703.2009.00559.x, 19694957.
24. Raja P, Sanville BC, Buchmann RC, Bisaro DM. Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 2008, 82(18):8997-9007. 10.1128/JVI.00719-08, 2546898, 18596098.
25. Fauquet CM, Bisaro DM, Briddon RW, Brown JK, Harrison BD, Rybicki EP, Stenger DC, Stanley J. Revision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species. Arch Virol 2003, 148(2):405-421. 10.1007/s00705-002-0957-5, 12557003.
26. Soitamo AJ, Jada B, Lehto K. HC-Pro silencing suppressor significantly alters the gene expression profile in tobacco leaves and flowers. BMC Plant Biol 2011, 11:68. 10.1186/1471-2229-11-68, 3111369, 21507209.
27. Siddiqui SA, Sarmiento C, Truve E, Lehto H, Lehto K. Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol Plant Microbe Interact 2008, 21(2):178-187. 10.1094/MPMI-21-2-0178, 18184062.
28. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55(4):611-622. 10.1373/clinchem.2008.112797, 19246619.
29. Memelink J. Regulation of gene expression by jasmonate hormones. Phytochemistry 2009, 70(13-14):1560-1570.
30. Avanci NC, Luche DD, Goldman GH, Goldman MH. Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol Res 2010, 9(1):484-505. 10.4238/vol9-1gmr754, 20391333.
31. Lin Z, Zhong S, Grierson D. Recent advances in ethylene research. J Exp Bot 2009, 60(12):3311-3336. 10.1093/jxb/erp204, 19567479.
32. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 2003, 15(1):165-178. 10.1105/tpc.007468, 143489, 12509529.
33. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, Liu HL, Wang CS, Jin H, Zhu JK. An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 2009, 137(3):498-508. 10.1016/j.cell.2009.04.028, 2700824, 19410546.
34. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 2008, 49(4):493-500. 10.1093/pcp/pcn043, 18344228.
35. Sun JQ, Jiang HL, Li CY. Systemin/Jasmonate-mediated systemic defense signaling in tomato. Mol Plant 2011, 4(4):607-615. 10.1093/mp/ssr008, 21357647.
36. Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP. Mechanisms of plant resistance to viruses. Nat Rev Microbiol 2005, 3(10):789-798. 10.1038/nrmicro1239, 16132037.
37. Alvarez S, Zhu M, Chen S. Proteomics of Arabidopsis redox proteins in response to methyl jasmonate. J Proteomics 2009, 73(1):30-40. 10.1016/j.jprot.2009.07.005, 19628057.
38. Jung C, Lyou SH, Yeu S, Kim MA, Rhee S, Kim M, Lee JS, Choi YD, Cheong JJ. Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Rep 2007, 26(7):1053-1063. 10.1007/s00299-007-0311-1, 17297615.
39. Maslenkova LT, Zanev Y, Popova LP. Oxygen-evolving activity of thylakoids from barley plants cultivated on different concentrations of jasmonic Acid. Plant Physiol 1990, 93(4):1316-1320. 10.1104/pp.93.4.1316, 1062674, 16667619.
40. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J. A central integrator of transcription networks in plant stress and energy signalling. Nature 2007, 448(7156):938-942. 10.1038/nature06069, 17671505.
41. Baena-Gonzalez E, Sheen J. Convergent energy and stress signaling. Trends Plant Sci 2008, 13(9):474-482. 10.1016/j.tplants.2008.06.006, 3075853, 18701338.
42. Lozano-Duran R, Bejarano ER. Geminivirus C2 protein might be the key player for geminiviral co- option of SCF-mediated ubiquitination. Plant Signal Behav 2011, 6(7):999-1001. 10.4161/psb.6.7.15499, 3257777, 21691154.
43. Lozano-Duran R, Rosas-Diaz T, Gusmaroli G, Luna AP, Taconnat L, Deng XW, Bejarano ER. Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 2011, 23(3):1014-1032. 10.1105/tpc.110.080267, 3082251, 21441437.
44. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH. Î2C1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 2008, 22(18):2564-2577. 10.1101/gad.1682208, 2546693, 18794352.
45. Lewsey MG, Murphy AM, Maclean D, Dalchau N, Westwood JH, Macaulay K, Bennett MH, Moulin M, Hanke DE, Powell G, Smith AG, Carr JP. Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 2010, 23(7):835-845. 10.1094/MPMI-23-7-0835, 20521947.
46. Miao Y, Zentgraf U. The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 2007, 19(3):819-830. 10.1105/tpc.106.042705, 1867371, 17369373.
47. Ascencio-Ibanez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 2008, 148(1):436-454. 10.1104/pp.108.121038, 2528102, 18650403.
48. Nagar S, Hanley-Bowdoin L, Robertson D. Host DNA replication is induced by geminivirus infection of differentiated plant cells. Plant Cell 2002, 14(12):2995-3007. 10.1105/tpc.005777, 151198, 12468723.
49. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Biochem Mol Biol 2000, 35(2):105-140.
50. Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D. Control of Jasmonate Biosynthesis and Senescence by miR319 Targets. PLoS Biol 2008, 6(9).
51. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5(10):R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
52. Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 2005, 138(3):1195-1204. 10.1104/pp.105.060459, 1176394, 16009995.
53. Usadel B, Nagel A, Steinhauser D, Gibon Y, Blasing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, Fernie AR, Stitt M. PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinforma 2006, 7:535.
54. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR. Imaging of photo-oxidative stress responses in leaves. J Exp Bot 2002, 53(372):1249-1254. 10.1093/jexbot/53.372.1249, 11997373.
55. Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b with four different solvents: verification of the concentration of chlorophyll by atomic absorption spectroscopy. Biochim Biophys Acta 1989, 975:384-394.
56. Neff MM, Chory J. Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 1998, 118(1):27-35. 10.1104/pp.118.1.27, 34865, 9733523.