Abstract
The important issue of photoreactivation DNA repair in plants has become even more interesting in recent years because a family of genes that are highly homologous to photoreactivating DNA repair enzymes but that function as blue light photoreceptors has been isolated. Here, we report the isolation of a novel photolyase-like sequence from Arabidopsis designated PHR1 (for photoreactivating enzyme). It shares little sequence similarity with either type I photolyases or the cryptochrome family of blue light photoreceptors. Instead, the PHR1 gene encodes an amino acid sequence with significant homology to the recently characterized type II photolyases identified in a number of prokaryotic and animal systems. PHR1 is a single-copy gene and is not expressed in dark-grown etiolated seedlings: the message is light inducible, which is similar to the expression profile for photoreactivation activity in plants. The PHR1 protein complements a photolyase-deficient mutant of Escherichia coli and thus confers photoreactivation activity. In addition, an Arabidopsis mutant that is entirely lacking in photolyase activity has been found to contain a lesion within this Arabidopsis type II photolyase sequence. We conclude that PHR1 represents a genuine plant photolyase gene and that the plant genes with homology to type I photolyases (the cryptochrome family of blue light photoreceptors) do not contribute to photoreactivation repair, at least in the case of Arabidopsis.
Full Text
The Full Text of this article is available as a PDF (2.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ahmad M., Cashmore A. R. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature. 1993 Nov 11;366(6451):162–166. doi: 10.1038/366162a0. [DOI] [PubMed] [Google Scholar]
- Ahmad M., Lin C., Cashmore A. R. Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J. 1995 Nov;8(5):653–658. doi: 10.1046/j.1365-313x.1995.08050653.x. [DOI] [PubMed] [Google Scholar]
- Akasaka S., Yamamoto K. Construction of Escherichia coli K12 phr deletion and insertion mutants by gene replacement. Mutat Res. 1991 Jan;254(1):27–35. doi: 10.1016/0921-8777(91)90037-p. [DOI] [PubMed] [Google Scholar]
- Beggs C. J., Stolzer-Jehle A., Wellmann E. Isoflavonoid Formation as an Indicator of UV Stress in Bean (Phaseolus vulgaris L.) Leaves : The Significance of Photorepair in Assessing Potential Damage by Increased Solar UV-B Radiation. Plant Physiol. 1985 Nov;79(3):630–634. doi: 10.1104/pp.79.3.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buchholz G., Ehmann B., Wellmann E. Ultraviolet Light Inhibition of Phytochrome-Induced Flavonoid Biosynthesis and DNA Photolyase Formation in Mustard Cotyledons (Sinapis alba L.). Plant Physiol. 1995 May;108(1):227–234. doi: 10.1104/pp.108.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiang T., Rupert C. S. Action spectrum for photoreactivation of ultraviolet-irradiated marsupial cells in tissue culture. Photochem Photobiol. 1979 Oct;30(4):525–528. doi: 10.1111/j.1751-1097.1979.tb07173.x. [DOI] [PubMed] [Google Scholar]
- Creusot F., Fouilloux E., Dron M., Lafleuriel J., Picard G., Billault A., Le Paslier D., Cohen D., Chabouté M. E., Durr A. The CIC library: a large insert YAC library for genome mapping in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):763–770. doi: 10.1046/j.1365-313x.1995.08050763.x. [DOI] [PubMed] [Google Scholar]
- Harm H. Damage and repair in mammalian cells after exposure to non-ionizing radiations. III. Ultraviolet and visible light irradiation of cells of placental mammals, including humans, and determination of photorepairable damage in vitro. Mutat Res. 1980 Jan;69(1):167–176. doi: 10.1016/0027-5107(80)90186-4. [DOI] [PubMed] [Google Scholar]
- Kato T., Jr, Todo T., Ayaki H., Ishizaki K., Morita T., Mitra S., Ikenaga M. Cloning of a marsupial DNA photolyase gene and the lack of related nucleotide sequences in placental mammals. Nucleic Acids Res. 1994 Oct 11;22(20):4119–4124. doi: 10.1093/nar/22.20.4119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kato T., Jr, Todo T., Ayaki H., Ishizaki K., Morita T., Mitra S., Ikenaga M. Cloning of a marsupial DNA photolyase gene and the lack of related nucleotide sequences in placental mammals. Nucleic Acids Res. 1994 Oct 11;22(20):4119–4124. doi: 10.1093/nar/22.20.4119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klimczak L. J., Farini D., Lin C., Ponti D., Cashmore A. R., Giuliano G. Multiple isoforms of Arabidopsis casein kinase I combine conserved catalytic domains with variable carboxyl-terminal extensions. Plant Physiol. 1995 Oct;109(2):687–696. doi: 10.1104/pp.109.2.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
- Li Y. F., Kim S. T., Sancar A. Evidence for lack of DNA photoreactivating enzyme in humans. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4389–4393. doi: 10.1073/pnas.90.10.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li Y. F., Sancar A. Active site of Escherichia coli DNA photolyase: mutations at Trp277 alter the selectivity of the enzyme without affecting the quantum yield of photorepair. Biochemistry. 1990 Jun 19;29(24):5698–5706. doi: 10.1021/bi00476a009. [DOI] [PubMed] [Google Scholar]
- Lin C., Ahmad M., Gordon D., Cashmore A. R. Expression of an Arabidopsis cryptochrome gene in transgenic tobacco results in hypersensitivity to blue, UV-A, and green light. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8423–8427. doi: 10.1073/pnas.92.18.8423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin C., Robertson D. E., Ahmad M., Raibekas A. A., Jorns M. S., Dutton P. L., Cashmore A. R. Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1. Science. 1995 Aug 18;269(5226):968–970. doi: 10.1126/science.7638620. [DOI] [PubMed] [Google Scholar]
- Mitchell D. L., Hartman P. S. The regulation of DNA repair during development. Bioessays. 1990 Feb;12(2):74–79. doi: 10.1002/bies.950120205. [DOI] [PubMed] [Google Scholar]
- Noonan F. P., De Fabo E. C. Ultraviolet-B dose-response curves for local and systemic immunosuppression are identical. Photochem Photobiol. 1990 Oct;52(4):801–810. doi: 10.1111/j.1751-1097.1990.tb08685.x. [DOI] [PubMed] [Google Scholar]
- O'Connor K. A., McBride M. J., West M., Yu H., Trinh L., Yuan K., Lee T., Zusman D. R. Photolyase of Myxococcus xanthus, a Gram-negative eubacterium, is more similar to photolyases found in Archaea and "higher" eukaryotes than to photolyases of other eubacteria. J Biol Chem. 1996 Mar 15;271(11):6252–6259. doi: 10.1074/jbc.271.11.6252. [DOI] [PubMed] [Google Scholar]
- Pang Q., Hays J. B. UV-B-Inducible and Temperature-Sensitive Photoreactivation of Cyclobutane Pyrimidine Dimers in Arabidopsis thaliana. Plant Physiol. 1991 Feb;95(2):536–543. doi: 10.1104/pp.95.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pruitt R. E., Meyerowitz E. M. Characterization of the genome of Arabidopsis thaliana. J Mol Biol. 1986 Jan 20;187(2):169–183. doi: 10.1016/0022-2836(86)90226-3. [DOI] [PubMed] [Google Scholar]
- Rosen H., Rehn M. M., Johnson B. A. The effect of caffeine on repair in Chlamydomonas reinhardtii. I. Enhancement of recombination repair. Mutat Res. 1980 May;70(3):301–309. doi: 10.1016/0027-5107(80)90020-2. [DOI] [PubMed] [Google Scholar]
- Sancar A. Structure and function of DNA photolyase. Biochemistry. 1994 Jan 11;33(1):2–9. doi: 10.1021/bi00167a001. [DOI] [PubMed] [Google Scholar]
- Small G. D., Min B., Lefebvre P. A. Characterization of a Chlamydomonas reinhardtii gene encoding a protein of the DNA photolyase/blue light photoreceptor family. Plant Mol Biol. 1995 Jun;28(3):443–454. doi: 10.1007/BF00020393. [DOI] [PubMed] [Google Scholar]
- Sutherland B. M., Bennett P. V. Human white blood cells contain cyclobutyl pyrimidine dimer photolyase. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9732–9736. doi: 10.1073/pnas.92.21.9732. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutherland J. C., Sutherland B. M. Human photoreactivating enzyme action spectrum and safelight conditions. Biophys J. 2009 Jan 1;15(5):435–440. doi: 10.1016/S0006-3495(75)85828-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- The electronic Plant Gene Register. Plant Physiol. 1996 Mar;110(3):1047–1048. doi: 10.1104/pp.110.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Todo T., Ryo H., Yamamoto K., Toh H., Inui T., Ayaki H., Nomura T., Ikenaga M. Similarity among the Drosophila (6-4)photolyase, a human photolyase homolog, and the DNA photolyase-blue-light photoreceptor family. Science. 1996 Apr 5;272(5258):109–112. doi: 10.1126/science.272.5258.109. [DOI] [PubMed] [Google Scholar]
- Trosko J. E., Mansour V. H. Response of tobacco and Haplopappus cells to ultraviolet irradiation after posttreatment with photoreactivating light. Radiat Res. 1968 Nov;36(2):333–343. [PubMed] [Google Scholar]
- Yasui A., Eker A. P., Yasuhira S., Yajima H., Kobayashi T., Takao M., Oikawa A. A new class of DNA photolyases present in various organisms including aplacental mammals. EMBO J. 1994 Dec 15;13(24):6143–6151. doi: 10.1002/j.1460-2075.1994.tb06961.x. [DOI] [PMC free article] [PubMed] [Google Scholar]