Local infection with oilseed rape mosaic virus promotes genetic rearrangements in systemic Arabidopsis tissue

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 709-710, Issue , 2011, Pages 7-14

  Yao, Youli ^a   Bilichak, Andriy ^a   Golubov, Andrey ^a   Kovalchuk, Igor ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Arabidopsis thaliana; DNA repair gene expression; Double strand breaks; Homologous recombination frequency; Methylation; Microsatellite instability; Mutation frequency; Oilseed rape mosaic virus

Indexed keywords

BETA GLUCURONIDASE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA; KU ANTIGEN; PROTEIN MSH2; RAD51 PROTEIN;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DNA STRAND BREAKAGE; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE INSERTION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ASSOCIATION; GENETIC RECOMBINATION; GENOME; HOMOLOGOUS RECOMBINATION; MICROSATELLITE INSTABILITY; MUTATION RATE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; TOBACCO MOSAIC VIRUS; TRANSGENE;

ARABIDOPSIS; BRASSICA NAPUS; DNA METHYLATION; GENOME, PLANT; GENOMIC INSTABILITY; MICROSATELLITE INSTABILITY; MOSAIC VIRUSES; MUTATION; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CHINESE RAPE MOSAIC VIRUS; NICOTIANA OBTUSIFOLIA; TOBACCO MOSAIC VIRUS;

EID: 79954583925     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.02.014     Document Type: Article

References (69)

1. Lexer C., Fay M.F. Adaptation to environmental stress: a rare or frequent driver of speciation?. J. Evol. Biol. 2005, 18:893-900.
2. Shimizu K.K., Purugganan M.D. Evolutionary and ecological genomics of Arabidopsis. Plant Physiol. 2005, 138:578-584.
3. Kathiria P., Golubov A., Sidler C., Kalischuk M., Kawchuk L.M., Kovalchuk I. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol. 2010.
4. Boyko A, Golubov A., Bilichak A., Kovalchuk I. Chlorine ions but not sodium ions alter genome stability of Arabidopsis thaliana. Plant Cell Physiol. 2010.
5. Boyko A., Blevins T., Yao Y., Golubov A., Bilichak A., Ilnytskyy Y., Hollander J., Meins F., Kovalchuk I. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS One 2010, 5:e9514.
6. Boyko A., Kovalchuk I. Epigenetic control of plant stress response. Environ. Mol. Mutagen. 2008, 49:61-72.
7. Boyko A., Kathiria P., Zemp F.J., Yao Y., Pogribny I., Kovalchuk I. Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Res. 2007, 35:1714-1725.
8. Kovalchuk I., Kovalchuk O., Kalck V., Boyko V., Filkowski J., Heinlein M., Hohn B. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 2003, 423:760-762.
9. Molinier J., Ries G., Zipfel C., Hohn B. Transgeneration memory of stress in plants. Nature 2006, 442:1046-1049.
10. Pecinka A., Rosa M., Schikora A., Berlinger M., Hirt H., Luschnig C., Mittelsten O. Scheid Transgenerational stress memory is not a general response in Arabidopsis. PLoS One 2009, 4:e5202.
11. Broekaert W.F., Delaure S.L., De Bolle M.F., Cammue B.P. The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol. 2006, 44:393-416.
12. Day B., Graham T. The plant host pathogen interface: cell wall and membrane dynamics of pathogen-induced responses. Ann. N.Y. Acad. Sci. 2007, 1113:123-134.
13. Hardham A.R., Jones D.A., Takemoto D. Cytoskeleton and cell wall function in penetration resistance. Curr. Opin. Plant Biol. 2007, 10:342-348.
14. Ryan C.A., Huffaker A., Yamaguchi Y. New insights into innate immunity in Arabidopsis. Cell. Microbiol. 2007, 9:1902-1908.
15. de P.J., Wit How plants recognize pathogens and defend themselves. Cell. Mol. Life Sci. 2007, 64:2726-2732.
16. Dong X. Genetic dissection of systemic acquired resistance. Curr. Opin. Plant Biol. 2001, 4:309-314.
17. Scholthof K.B. Tobacco mosaic virus: a model system for plant biology. Annu. Rev. Phytopathol. 2004, 42:13-34.
18. Kothari I.L., Patel M. Plant immunization. Indian J. Exp. Biol. 2004, 42:244-252.
19. Friedman A.R., Baker B.J. The evolution of resistance genes in multi-protein plant resistance systems. Curr. Opin. Genet. Dev. 2007, 17:493-499.
20. Richter T.E., Pryor T.J., Bennetzen J.L., Hulbert S.H. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 1995, 141:373-381.
21. Tornero P., Chao R.A., Luthin W.N., Goff S.A., Dangl J.L. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein. Plant Cell 2002, 14:435-450.
22. Azaiez A., Bouchard E.F., Jean M., Belzile F.J. Length, orientation, and plant host influence the mutation frequency in microsatellites. Genome 2006, 49:1366-1373.
23. Ilnytskyy Y, Boyko A., Kovalchuk I. Luciferase-based transgenic recombination assay is more sensitive than beta-glucoronidase-based. Mutat. Res. 2004, 559:189-197.
24. Kovalchuk I., Kovalchuk O., Hohn B. Genome-wide variation of the somatic mutation frequency in transgenic plants. EMBO J. 2000, 19:4431-4438.
25. Boyko A., Molinier J., Chatter W., Laroche A., Kovalchuk I. Acute but not chronic exposure to abiotic stress results in transient reduction of expression levels of the transgene driven by the 35S promoter. N Biotechnol. 2010, 27:70-77.
26. Wada Y., Miyamoto K., Kusano T., Sano H. Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol. Genet. Genomics 2004, 271:658-666.
27. Chen Z.J., Ni Z. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 2006, 28:240-252.
28. Hartlerode A.J., Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem. J. 2009, 423:157-168.
29. Boyko A., Zemp F., Filkowski J., Kovalchuk I. Double-strand break repair in plants is developmentally regulated. Plant Physiol. 2006, 141:488-497.
30. Garcia-Diaz M., Bebenek K. Multiple functions of DNA polymerases. CRC Crit. Rev. Plant Sci. 2007, 26:105-122.
31. Golubov A., Yao Y., Maheshwari P., Bilichak A., Boyko A., Belzile F., Kovalchuk I. Microsatellite instability in Arabidopsis increases with plant development. Plant Physiol. 2010, 154:1415-1427.
32. Kathiria P., Sidler C., Golubov A., Kalischuk M., Kawchuk L.M., Kovalchuk I. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol. 2010, 153:1859-1870.
33. Boyko A, Greer M., Kovalchuk I. Acute exposure to UVB has a more profound effect on plant genome stability than chronic exposure. Mutat. Res. 2006, 602:100-109.
34. Boyko A., Hudson D., Bhomkar P., Kathiria P., Kovalchuk I. Increase of homologous recombination frequency in vascular tissue of Arabidopsis plants exposed to salt stress. Plant Cell Physiol. 2006, 47:736-742.
35. Ilnytskyy Y., Yao Y., Kovalchuk I. Double-strand break repair machinery is sensitive to UV radiation. J. Mol. Biol. 2005, 345:707-715.
36. Besplug J., Filkowski J., Burke P., Kovalchuk I., Kovalchuk O. Atrazine induces homologous recombination but not point mutation in the transgenic plant-based biomonitoring assay. Arch. Environ. Contam. Toxicol. 2004, 46:296-300.
37. Filkowski J., Kovalchuk O., Kovalchuk I. Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant J. 2004, 38:60-69.
38. Filkowski J, Yeoman A., Kovalchuk O., Kovalchuk I. Systemic plant signal triggers genome instability. Plant J. 2004, 38:1-11.
39. Filkowski J., Besplug J., Burke P., Kovalchuk I., Kovalchuk O. Genotoxicity of 2 4-D and dicamba revealed by transgenic Arabidopsis thaliana plants harboring recombination and point mutation markers. Mutat. Res. 2003, 542:23-32.
40. Kovalchuk O., Kovalchuk I., Arkhipov A., Hohn B., Dubrova Y.E. Extremely complex pattern of microsatellite mutation in the germline of wheat exposed to the post-Chernobyl radioactive contamination. Mutat. Res. 2003, 525:93-101.
41. Kovalchuk O., Dubrova Y.E., Arkhipov A., Hohn B., Kovalchuk I. Wheat mutation rate after Chernobyl. Nature 2000, 407:583-584.
42. Geras'kin S.A., Oudalova A.A., Kim J.K., Dikarev V.G., Dikareva N.S. Cytogenetic effect of low dose gamma-radiation in Hordeum vulgare seedlings: non-linear dose-effect relationship. Radiat. Environ. Biophys. 2007, 46:31-41.
43. Mitchel R.E. Low doses of radiation are protective in vitro and in vivo: evolutionary origins. Dose Response 2006, 4:75-90.
44. Little M.P. Do non-targeted effects increase or decrease low dose risk in relation to the linear-non-threshold (LNT) model?. Mutat. Res. 2010, 687:17-27.
45. Smith R.W., Wang J., Mothersill C.E., Hinton T.G., Aizawa K., Seymour C.B. Proteomic changes in the gills of wild-type and transgenic radiosensitive medaka following exposure to direct irradiation and to X-ray induced bystander signals. Biochim. Biophys. Acta 2010.
46. Gow M.D., Seymour C.B., Byun S.H., Mothersill C.E. Effect of dose rate on the radiation-induced bystander response. Phys. Med. Biol. 2008, 53:119-132.
47. O'Neill-Mehlenbacher A., Kilemade M., Elliott A., Mothersill C., Seymour C. Comparison of direct and bystander effects induced by ionizing radiation in eight fish cell lines. Int. J. Radiat. Biol. 2007, 83:593-602.
48. Mothersill C., Seymour C. Radiation-induced bystander effects: past history and future directions. Radiat. Res. 2001, 155:759-767.
49. Seymour C.B., Mothersill C. Relative contribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Radiat. Res. 2000, 153:508-511.
50. Sedelnikova O.A., Redon C.E., Dickey J.S., Nakamura A.J., Georgakilas A.G., Bonner W.M. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat. Res. 2010, 704:152-159.
51. O'Neill P., Wardman P. Radiation chemistry comes before radiation biology. Int. J. Radiat. Biol. 2009, 85:9-25.
52. Li F., Liu P., Wang T., Bian P., Wu Y., Wu L., Yu Z. The induction of bystander mutagenic effects in vivo by alpha-particle irradiation in whole Arabidopsis thaliana plants. Radiat. Res. 2010, 174:228-237.
53. Yang G., Mei T., Yuan H., Zhang W., Chen L., Xue J., Wu L., Wang Y. Bystander/abscopal effects induced in intact Arabidopsis seeds by low-energy heavy-ion radiation. Radiat. Res. 2008, 170:372-380.
54. Yang G., Wu L., Chen L., Pei B., Wang Y., Zhan F., Wu Y., Yu Z. Targeted irradiation of shoot apical meristem of Arabidopsis embryos induces long-distance bystander/abscopal effects. Radiat. Res. 2007, 167:298-305.
55. Li K., Jiang S., Yu H., Zhao J., Zhang F., Carr C., Zhang J., Zhang G. Analysis of charge and mass effects on peroxidase expressions and activities in Arabidopsis thaliana after low-energy ion irradiation. Mutat. Res. 2009, 680:64-69.
56. Gorbunova V., Levy A.A. Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res. 1997, 25:4650-4657.
57. Choi C.S., Sano H. Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol. Genet. Genomics 2007, 277:589-600.
58. Mason G., Noris E., Lanteri S., Acquadro A., Accotto G.P., Portis E. Potentiality of methylation-sensitive amplification polymorphism (MSAP) in identifying genes involved in tomato response to tomato yellow leaf curl Sardinia virus. Plant Mol. Biol. Rep. 2008, 26:156-173.
59. Aina R., Sgorbati S., Santagostino A., Labra M., Ghiani A., Citterio S. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol. Plant. 2004, 121:472-480.
60. Verhoeven K.J., Jansen J.J., van Dijk P.J., Biere A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010, 185:1108-1118.
61. Labra M., Ghiani A., Citterio S., Sgorbati S., Sala F., Vannini C., Ruffini-Castiglione M., Bracale M. Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol. 2002, 4:694-699.
62. Klammer H., Kadhim M., Iliakis G. Evidence of an adaptive response targeting DNA nonhomologous end joining and its transmission to bystander cells. Cancer Res. 2010, 70:8498-8506.
63. Nagasawa H., Wilson P.F., Chen D.J., Thompson L.H., Bedford J.S., Little J.B. Low doses of alpha particles do not induce sister chromatid exchanges in bystander Chinese hamster cells defective in homologous recombination. DNA Repair (Amst.) 2008, 7:515-522.
64. Koturbash I., Rugo R.E., Hendricks C.A., Loree J., Thibault B., Kutanzi K., Pogribny I., Yanch J.C., Engelward B.P., Kovalchuk O. Irradiation induces DNA damage and modulates epigenetic effectors in distant bystander tissue in vivo. Oncogene 2006, 25:4267-4275.
65. Zhang Y., Zhou J., Held K.D., Redmond R.W., Prise K.M., Liber H.L. Deficiencies of double-strand break repair factors and effects on mutagenesis in directly gamma-irradiated and medium-mediated bystander human lymphoblastoid cells. Radiat. Res. 2008, 169:197-206.
66. Jefferson R.A., Kavanagh T.A., Bevan M.W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987, 6:3901-3907.
67. Bock C., Reither S., Mikeska T., Paulsen M., Walter J., Lengauer T. BiQ analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 2005, 21:4067-4068.
68. Li L.C., Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431.
69. Seki M., Narusaka M., Abe H., Kasuga M., Yamaguchi-Shinozaki K., Carninci P., Hayashizaki Y., Shinozaki K. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 2001, 13:61-72.