Expression of the Beet necrotic yellow vein virus p25 protein induces hormonal changes and a root branching phenotype in Arabidopsis thaliana

Transgenic Research

Volumn 20, Issue 3, 2011, Pages 443-466

  Peltier, Claire ^a   Schmidlin, Laure ^a   Klein, Elodie ^a   Taconnat, Ludivine ^d   Prinsen, Els ^b   Erhardt, Mathieu ^a   Heintz, Dimitri ^a   Weyens, Guy ^c   Lefebvre, Marc ^c   Renou, Jean Pierre ^d   Gilmer, David ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c SESVanderHave NV/SA   (Belgium)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Auxin; BNYVV; Hormonal changes; Jasmonate; Microarray; Root

Indexed keywords

BACTERIAL DNA; CYCLOPENTANE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE; T DNA; T-DNA; VIRUS PROTEIN;

ARABIDOPSIS; ARTICLE; BEET; CELL NUCLEUS; CYTOPLASM; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PLANT VIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA VIRUS; TRANSGENIC PLANT; VIROLOGY;

ARABIDOPSIS; BETA VULGARIS; CELL NUCLEUS; CYCLOPENTANES; CYTOPLASM; DNA, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INDOLEACETIC ACIDS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYLIPINS; PHENOTYPE; PLANT DISEASES; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT ROOTS; PLANT VIRUSES; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA VIRUSES; VIRAL PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BEET NECROTIC YELLOW VEIN VIRUS; BETA VULGARIS; BETA VULGARIS SUBSP. VULGARIS;

EID: 79955857281     PISSN: 09628819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11248-010-9424-3     Document Type: Article

References (59)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135: 745-755.
3. Bialek K, Cohen JD (1989) Quantitation of indoleacetic acid conjugates in bean seeds by direct tissue hydrolysis. Plant Physiol 90: 398-400.
4. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
5. Bülow L, Schindler M, Hehl R (2007) PathoPlant®: a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses. Nucleic Acids Res 35: D841-845.
6. Canet JV, Dobon A, Ibanez F, Perales L, Tornero P (2010) Resistance and biomass in Arabidopsis: a new model for salicylic acid perception. Plant Biotechnol J 8: 126-141.
7. Chauvaux N, van Dongen W, Esmans EL, van Onckelen HA (1993) Liquid chromatographic-mass spectrometric determination of 1-aminocyclopropane-1-carboxylic acid in tobacco. J Chromatogr A 657: 337-343.
8. Chiba S, Miyanishi M, Andika IB, Kondo H, Tamada T (2008) Identification of amino acids of the beet necrotic yellow vein virus p25 protein required for induction of the resistance response in leaves of Beta vulgaris plants. J Gen Virol 89: 1314-1323.
9. Cho H-T, Cosgrove DJ (2002) Regulation of root hair initiation and expansin gene expression in arabidopsis. Plant Cell 14: 3237-3253.
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
11. Corbineau F, Rudnicki RM, Come D (1988) The effect of methyl jasmonate on sunflower (Helianthus annuus L.) seed germination and seedling development. Plant Growth Regul 7: 157-169.
12. Crowe ML, Serizet C, Thareau V, Aubourg S, Rouze P, Hilson P, Beynon J, Weisbeek P, van Hummelen P, Reymond P, Paz-Ares J, Nietfeld W, Trick M (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31: 156-158.
13. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16: 1235-1250.
14. Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA 96: 3292-3297.
15. Finkelstein R (1994) Mutations at two new Arabidospis ABA response loci are similar to the abi3 mutations. Plant J 5: 765-771.
16. Gagnot S, Tamby JP, Martin-Magniette ML, Bitton F, Taconnat L, Balzergue S, Aubourg S, Renou JP, Lecharny A, Brunaud V (2008) CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res 36: D986-D990.
17. Ge Y, Dudoit S, Speed TP (2003) Resampling-based testing for microarray data analysis. Test 12.
18. Haeberle AM, Stussi-Garaud C (1995) In situ localization of the non-structural protein P25 encoded by beet necrotic yellow vein virus RNA 3. J Gen Virol 76: 643-650.
19. Hand DJ, Taylor CC (1987) Multivariate analysis of variance and repeated measures. Chapman and Hall/CRC, London.
20. Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B, Chardakov V, Cognet-Holliger C, Colot V, Crowe M, Darimont C, Durinck S, Eickhoff H, de Longevialle AF, Farmer EE, Grant M, Kuiper MT, Lehrach H, Leon C, Leyva A, Lundeberg J, Lurin C, Moreau Y, Nietfeld W, Paz-Ares J, Reymond P, Rouze P, Sandberg G, Segura MD, Serizet C, Tabrett A, Taconnat L, Thareau V, van Hummelen P, Vercruysse S, Vuylsteke M, Weingartner M, Weisbeek PJ, Wirta V, Wittink FR, Zabeau M, Small I (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14: 2176-2189.
21. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22: 4523-4533.
22. Holsters M, Silva B, van Vliet F, Genetello C, De Block M, Dhaese P, Depicker A, Inze D, Engler G, Villarroel R et al (1980) The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 3: 212-230.
23. Huckelhoven R, Dechert C, Kogel KH (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proc Natl Acad Sci USA 100: 5555-5560.
24. Ishikawa M, Naito S, Ohno T (1993) Effects of the tom1 mutation of Arabidopsis thaliana on the multiplication of tobacco mosaic virus RNA in protoplasts. J Virol 67: 5328-5338.
25. Jupin I, Guilley H, Richards KE, Jonard G (1992) Two proteins encoded by beet necrotic yellow vein virus RNA 3 influence symptom phenotype on leaves. EMBO J 11: 479-488.
26. Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol 132: 1177-1185.
27. Klein E, Link D, Schirmer A, Erhardt M, Gilmer D (2007) Sequence variation within Beet necrotic yellow vein virus p25 protein influences its oligomerization and isolate pathogenicity on Tetragonia expansa. Virus Res 126: 53-61.
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
29. Larson RL, Wintermantel WM, Hill A, Fortis L, Nunez A (2008) Proteome changes in sugar beet in response to Beet necrotic yellow vein virus. Physiol Mol Plant Pathol 72: 62-72.
30. Lauber E, Guilley H, Tamada T, Richards KE, Jonard G (1998) Vascular movement of beet necrotic yellow vein virus in Beta macrocarpa is probably dependent on an RNA 3 sequence domain rather than a gene product. J Gen Virol 79: 385-393.
31. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
32. Netting AG, Milborrow BV (1988) Methane chemical ionization Mass-Spectrometry of the pentafluorobenzyl derivatives of Abscisic-acid, its metabolites and other plant-growth regulators. Biomed Environ Mass Spectrom 17: 281-286.
33. Niesbach-Klosgen U, Guilley H, Jonard G, Richards K (1990) Immunodetection in vivo of beet necrotic yellow vein virus-encoded proteins. Virology 178: 52-61.
34. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 100: 2987-2991.
35. Pan X, Welti R, Wang X (2008) Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 1773-1781.
36. Pavli OI, Panopoulos NJ, Goldbach R, Skaracis GN (2010) BNYVV-derived dsRNA confers resistance to rhizomania disease of sugar beet as evidenced by a novel transgenic hairy root approach. Transgenic Res.
37. Peart JR, Cook G, Feys BJ, Parker JE, Baulcombe DC (2002) An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J 29: 569-579.
38. Peltier C, Hleibieh K, Thiel H, Klein E, Bragard C, Gilmer D (2008) Molecular biology of the beet necrotic yellow vein virus. Plant Viruses 2: 14-24.
39. Pfeffer S, Dunoyer P, Heim F, Richards KE, Jonard G, Ziegler-Graff V (2002) P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. J Virol 76: 6815-6824.
40. Pollini CP, Masia A, Giunchedi L (1990) Free indole-3-acetic acid in sugar-beet root of rhizomania-susceptible and moderately resistant cultivars. Phytopathol Mediterr 29: 191-195.
41. Prinsen E, Stijn van L, Sevgi Ö, Henri van O (2000) Auxin analysis. In: Iacobellis NS, Collmer A, Hutcheson SW, Mansfield JW, Morris CE, Murillo J, Schaad NW, Stead DE, Surico G, Ullrich M (eds) Plant hormone protocols. Kluwer Academic Humana Press, Dordrecht.
42. Quillet L, Guilley H, Jonard G, Richards K (1989) In vitro synthesis of biologically active beet necrotic yellow vein virus RNA. Virology 172: 293-301.
43. Rahim MD, Andika IB, Han C, Kondo H, Tamada T (2007) RNA4-encoded p31 of beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. J Gen Virol 88: 1611-1619.
44. Schmidlin L, De Bruyne E, Weyens G, Lefebvre M, Gilmer D (2008) Identification of differentially expressed root genes upon rhizomania disease. Mol Plant Pathol 9: 741-751.
45. Smets R, Claes V, van Onckelen HA, Prinsen E (2003) Extraction and quantitative analysis of 1-aminocyclopropane-1-carboxylic acid in plant tissue by gas chromatography coupled to mass spectrometry. J Chromatogr A 993: 79-87.
46. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89: 6837-6840.
47. Tamada T, Abe H (1989) Evidence that beet necrotic yellow vein virus RNA-4 is essential for transmission by the fungus Polymyxa betae. J Gen Virol 70: 3391-3398.
48. Tamada T, Shirako Y, Abe H, Saito M, Kigushi T, Harada T (1989) Production and pathogenicity of isolates of Beet necrotic yellow vein virus with different numbers of RNA components. J Gen Virol 70: 3399-3409.
49. Tamada T, Uchino H, Kusume T, Saito M (1999) RNA 3 deletion mutants of beet necrotic yellow vein virus do not cause rhizomania disease in sugar beets. Phytopathology 89: 1000-1006.
50. Thiel H, Varrelmann M (2009) Identification of beet necrotic yellow vein virus P25 pathogenicity factor-interacting sugar beet proteins that represent putative virus targets or components of plant resistance. Mol Plant Microbe Interact 22: 999-1010.
51. Tsujimoto Y, Numaga T, Ohshima K, Yano MA, Ohsawa R, Goto DB, Naito S, Ishikawa M (2003) Arabidopsis tobamovirus multiplication (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J 22: 335-343.
52. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
53. van Der Straeten D, Djudzman A, van Caeneghem W, Smalle J, van Montagu M (1993) Genetic and physiological analysis of a new locus in Arabidopsis that confers resistance to 1-aminocyclopropane-1-carboxylic acid and ethylene and specifically affects the ethylene signal transduction pathway. Plant Physiol 102: 401-408.
54. Vetter G, Hily JM, Klein E, Schmidlin L, Haas M, Merkle T, Gilmer D (2004) Nucleo-cytoplasmic shuttling of the beet necrotic yellow vein virus RNA-3-encoded p25 protein. J Gen Virol 85: 2459-2469.
55. Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177-187.
56. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949-956.
57. Yamanaka T, Ohta T, Takahashi M, Meshi T, Schmidt R, Dean C, Naito S, Ishikawa M (2000) TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. Proc Natl Acad Sci USA 97: 10107-10112.
58. Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M, Tomita K, Kubota K, Meshi T, Naito S, Ishikawa M (2002) Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J Virol 76: 2491-2497.
59. Yoshida K, Kaothien P, Matsui T, Kawaoka A, Shinmyo A (2003) Molecular biology and application of plant peroxidase genes. Appl Microbiol Biotechnol 60: 665-670.