Silencing of CPD Photolyase Makes Arabidopsis Hypersensitive and Hypermutable in Response to UV-B Radiation
-
- Yoshihara Ryouhei YOSHIHARA Ryouhei
- Quantum Beam Science Directorate Radiation-Applied Biology Division, Japan Atomic Energy Agency, Gunma, Japan
-
- Nakane Chiyoko NAKANE Chiyoko
- Graduate School of Agriculture, Yamaguchi University
-
- Sato Ryohei [他] SATO Ryohei
- Graduate School of Agriculture, Yamaguchi University
-
- YASUDA Ai
- Graduate School of Agriculture, Yamaguchi University
-
- TAKIMOTO Koichi
- Faculty of Agriculture, Yamaguchi University
Access this Article
Search this Article
Author(s)
-
- Yoshihara Ryouhei YOSHIHARA Ryouhei
- Quantum Beam Science Directorate Radiation-Applied Biology Division, Japan Atomic Energy Agency, Gunma, Japan
-
- Nakane Chiyoko NAKANE Chiyoko
- Graduate School of Agriculture, Yamaguchi University
-
- Sato Ryohei [他] SATO Ryohei
- Graduate School of Agriculture, Yamaguchi University
-
- YASUDA Ai
- Graduate School of Agriculture, Yamaguchi University
-
- TAKIMOTO Koichi
- Faculty of Agriculture, Yamaguchi University
Abstract
Plants are exposed to solar ultraviolet radiation (UV), which has deleterious effects on plant growth, development and physiology. Cyclobutane pyrimidine dimers (CPDs) are a major form of UV-induced DNA damage. It is conceivable that the reversal of CPDs is important for the reduction of lethal and mutagenic effects. Photoreactivation catalyzed by CPD photolyase is an efficient CPD repair system with a mechanism dependent on UV-A/visible light, which is contained in solar radiation. Photoreactivation presumably functions to protect plants from solar UV. We generated a CPD photolyase knock-down in <i>Arabidopsis thaliana</i> by RNA interference (RNAi) to investigate the role of CPD photorepair for protection of plants from solar UV. These knock-down lines exhibited hypersensitivity to UV-B and an increased occurrence of mutation induced by UV-B radiation compared with <i>Arabidopsis</i> proficient in CPD photolyase. Mutations induced by UV-B were determined by an <i>rpsL</i> mutation assay system. G:C to A:T transitions were frequently observed in CPD photolyase knock-down lines at the site of dipyrimidine sequences. A high incidence of frameshifts was observed in irradiated knock-down lines. These results indicate that CPD photoreactivation plays an important role for UV resistance of <i>Arabidopsis</i> and suppression of UV-induced mutagenesis.<br>
Journal
-
- Genes and Environment
-
Genes and Environment 30(2), 53-61, 2008-05-20
The Environmental Mutagen Society of Japan
References: 57
-
1
- One pyrimidine dimer inactivates expression of a transfected gene in xeroderma pigmentosum cells
-
PROTIC-SABLJIC M
Proc Natl Acad Sci USA 82, 6622-6626, 1985
Cited by (1)
-
2
- Inhibition of transient gene expression in Chinese hamster ovary cells by cyclobutane dimers and (6-4) photoproducts in transfected ultraviolet-irradiated plasmid DNA
-
MITCHELL DL
Plasmid 21, 21-30, 1989
Cited by (1)
-
3
- DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae
-
BROOMFIELD S
Mutat Res 486, 167-184, 2001
Cited by (1)
-
4
- The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis
-
WAGNER J
Mol Cell 4, 281-286, 1999
Cited by (1)
-
5
- UmuD'_2C is an error-prone DNA polymerase, Escherichia coli pol V
-
TANG M
Proc Natl Acad Sci USA 96, 8919-8924, 1999
Cited by (1)
-
6
- Deoxycytidyl transferase activity of yeast REV1 protein
-
NELSON JR
Nature 382, 729-731, 1996
Cited by (1)
-
7
- The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by UV light
-
GIBBS PE
Proc Natl Acad Sci USA 97, 4186-4191, 2000
Cited by (1)
-
8
- Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line
-
SIMPSON LJ
EMBO J 22, 1654-1664, 2003
Cited by (1)
-
9
- Thymine-thymine dimer bypass by yeast DNA polymerase ζ
-
NELSON JR
Science 272, 1646-1649, 1996
Cited by (1)
-
10
- Multiple roles of Rev3, the catalytic subunit of polζ in maintaining genome stability in vertebrates
-
SONODA E
EMBO J 22, 3188-3197, 2003
Cited by (1)
-
11
- The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism
-
MCDONALD JP
Genetics 147, 1557-1568, 1997
Cited by (1)
-
12
- The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η
-
MASUTANI C
Nature 399, 700-704, 1999
Cited by (1)
-
13
- DNA repair in plants
-
KIMURA S
Chem Rev 106, 753-766, 2006
Cited by (1)
-
14
- An enzyme similar to animal type II photolyases mediates photoreactivation in Arabidopsis
-
AHMAD M
Plant Cell 9, 199-207, 1997
Cited by (1)
-
15
- Cloning and characterization of a gene (UVR3) required for photorepair of 6-4 photoproducts in Arabidopsis thaliana
-
NAKAJIMA S
Nucleic Acids Res 26, 638-644, 1998
Cited by (1)
-
16
- Cloning of the phr gene and amplification of photolyase in Escherichia coli
-
SANCAR A
Gene 4, 295-308, 1978
Cited by (1)
-
17
- Sequence of the Saccharomyces cerevisiae PHR1 gene and homology of the PHR1 photolyase to E. coli photolyase
-
SANCAR GB
Nucleic Acids Res 13, 8231-8246, 1985
Cited by (1)
-
18
- DNA photoreactivating enzyme from the cyanobacterium Anacystis nidulans
-
EKER AP
J Biol Chem 265, 8009-8015, 1990
Cited by (1)
-
19
- Visible light-inducible photolyase gene from the goldfish Carassius auratus
-
YASUHIRA S
J Biol Chem 267, 25644-25647, 1992
Cited by (1)
-
20
- Cloning of a marsupial DNA photolyase gene and the lack of related nucleotide sequences in placental mammals
-
KATO T Jr
Nucleic Acids Res 22, 4119-4124, 1994
Cited by (1)
-
21
- High-level expression of the photorepair gene in Drosophila ovary and its evolutionary implications
-
TODO T
Mutat Res 315, 213-228, 1994
Cited by (1)
-
22
- A gene for a class II DNA photolyase from Oryza sativa : cloning of the cDNA by dilution-amplification
-
HIROUCHI T
Mol Genet Genomics 269, 508-516, 2003
Cited by (1)
-
23
- An Arabidopsis photolyase mutant is hypersensitive to ultraviolet-B radiation
-
LANDRY LG
Proc Natl Acad Sci USA 94, 328-332, 1997
Cited by (1)
-
24
- UV radiation-sensitive norin 1 rice contains defective cyclobutane pyrimidine dimer photolyase
-
HIDEMA J
Plant Cell 12, 1569-1578, 2000
Cited by (1)
-
25
- Construct design for efficient, effective and high-throughput gene silencing in plants
-
WESLEY SV
Plant J 27, 581-590, 2001
Cited by (1)
-
26
- Floral dip : a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
-
CLOUGH SJ
Plant J 16, 735-743, 1998
Cited by (1)
-
27
- Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA
-
MORI T
Photochem Photobiol 54, 225-232, 1991
Cited by (1)
-
28
- Rapid isolation of high molecular weight plant DNA
-
MURRAY MG
Nucleic Acid Res 8, 4321-4325, 1980
Cited by (1)
-
29
- Mutagenic specificity of ultraviolet light
-
MILLER HJ
J Mol Biol 182, 45-65, 1985
Cited by (1)
-
30
- UV light-induced cyclobutane pyrimidine dimers are mutagenic in mammalian cells
-
PROTIC-SABLJIC M
Mol Cell Biol 6, 3349-3356, 1986
Cited by (1)
-
31
- The specificity of UV-induced mutations at an endogenous locus in mammalian cells
-
DROBETSKY EA
Proc Natl Acad Sci USA 84, 9103-9107, 1987
Cited by (1)
-
32
- Increase in CPD photolyase activity functions effectively to prevent growth inhibition caused by UVB radiation
-
HIDEMA J
Plant J 50, 70-79, 2007
Cited by (1)
-
33
- Genome-wide variation of the somatic mutation frequency in transgenic plants
-
KOVALCHUK I
EMBO J 19, 4431-4438, 2000
Cited by (1)
-
34
- The mutagenesis protein UmuC is a DNA polymerase activated by UmuD', RecA, and SSB and is specialized for translesion replication
-
REUVEN NB
J Biol Chem 274, 31763-31766, 1999
Cited by (1)
-
35
- Low fidelity DNA synthesis by human DNA polymerase-η
-
MATSUDA T
Nature 404, 1011-1013, 2000
Cited by (1)
-
36
- Disruption of the AtREV3 gene causes hypersensitivity to ultraviolet B light and y-rays in Arabidopsis : implication of the presence of a translesion synthesis mechanism in plants
-
SAKAMOTO A
Plant Cell 15, 2042-2057, 2003
Cited by (1)
-
37
- Roles of Arabidopsis AtREV1 and AtREV7 in translesion synthesis
-
TAKAHASHI S
Plant Physiol 138, 870-881, 2005
Cited by (1)
-
38
- AtREV1, a Y-family DNA polymerase in Arabidopsis, has deoxynucleotidyl transferase activity in vitro
-
TAKAHASHI S
Plant Physiol 145, 1052-1060, 2007
Cited by (1)
-
39
- Sequence and time-dependent deamination of cytosine bases in UVB-induced cyclobutane pyrimidine dimers in vivo
-
TU Y
J Mol Biol 284, 297-311, 1998
Cited by (1)
-
40
- hRAD30 mutations in the variant form of xeroderma pigmentosum
-
JOHNSON RE
Science 285, 263-265, 1999
Cited by (1)
-
41
- Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη
-
JOHNSON RE
Science 283, 1001-1004, 1999
Cited by (1)
-
42
- Requirement of DNA polymerase η for error-free bypass of UV-induced CC and TC photoproducts
-
YU SL
Mol Cell Biol 21, 185-188, 2001
Cited by (1)
-
43
- Deamination of 5-methylcytosines within cyclobutane pyrimidine dimers is an important component of UVB mutagenesis
-
LEE DH
J Biol Chem 278, 10314-10321, 2003
Cited by (1)
-
44
- Chemical synthesis and translesion replication of a cis-syn cyclobutane thymine-uracil dimer
-
TAKASAWA K
Nucl Acids Res 32, 1738-1745, 2004
Cited by (1)
-
45
- Mutations induced by ultraviolet light
-
PFEIFER GP
Mutat Res 571, 19-31, 2005
Cited by (1)
-
46
- Analysis of UV-induced mutation spectra in Escherichia coli by DNA polymerase η from Arabidopsis thaliana
-
SANTIAGO MJ
Mutat Res 601, 51-60, 2006
Cited by (1)
-
47
- Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday
-
STREISINGER G
Cold Spring Harb Symp Quant Biol 31, 77-84, 1966
Cited by (1)
-
48
- Mutagenesis by transient misalignment
-
KUNKEL TA
J Biol Chem 263, 14784-14789, 1988
Cited by (1)
-
49
- Frameshift errors initiated by nucleotide misincorporation
-
BEBENEK K
Proc Natl Acad Sci USA 87, 4946-4950, 1990
Cited by (1)
-
50
- Abasic translesion synthesis by DNA polymerase β violates the "A-rule"
-
EFRATI E
J Biol Chem 272, 2559-2569, 1997
Cited by (1)
-
51
- Fidelity of Escherichia coli DNA polymerase III holoenzyme
-
BLOOM LB
J Biol Chem 272, 27919-27930, 1997
Cited by (1)
-
52
- DNA repair in higher plants ; photoreactivation is the major DNA repair pathway in non-proliferating cells while excision repair (nucleotide excision repair and base excision repair) is active in proliferating cells
-
KIMURA S
Nucleic Acids Res 32, 2760-2767, 2004
Cited by (1)
-
53
- Studies of in vivo mutations in rpsL transgene in UVB-irradiated epidermis of XPA-deficient mice
-
MURAI H
Mutat Res 450, 181-192, 2000
Cited by (1)
-
54
- CPD Photolyase Gene from Spinacia oleracea : Repair of UV-Damaged DNA and Expression in Plant Organs
-
YOSHIHARA Ryouhei , IMAKI Toshiyuki , HORI Manabu , WATANABE Chihiro , YAMAMOTO Kazuo , TAKIMOTO Koichi
Journal of Radiation Research 46(2), 157-164, 2005-06-30
J-STAGE NDL Digital Collections References (48) Cited by (3)
-
55
- Relationship between Ultraviolet-B Sensitivity and Cyclobutane Pyrimidine Dimer Photorepair in Rice
-
HIDEMA Jun , SONG Il-Kyung , SATO Tadashi , KUMAGA Tadashi
Journal of Radiation Research 42(3), 295-303, 2001-09-01
J-STAGE NDL Digital Collections References (26) Cited by (6)
-
56
- A New System for Detecting Mutations in Arabidopsis thaliana and the Mutational Spectra Resulting from Ethylmethanesulfonate Treatment
-
YOSHIHARA Ryouhei , NAKANE Chiyoko , TAKIMOTO Koichi
Journal of Radiation Research 47(3/4), 223-228, 2006
J-STAGE NDL Digital Collections Cited by (1)
-
57
- Diurnal Change of Cucumber CPD Photolyase Gene (CsPHR) Expression and Its Physiological Role in Growth under UV-B Irradiation
-
TAKAHASHI Shinya , NAKAJIMA Nobuyoshi , SAJI Hikaru , KONDO Noriaki
Plant and Cell Physiology 43(3), 342-349, 2002-03-01
References (44) Cited by (3)