Abstract
In order to better understand the biochemical mechanisms of DNA metabolism in chloroplasts, repair of UV induced plastome damage in vivo was determined by exposure of soybean suspension cells to UV light and subsequent quantitation of the damage remaining in nuclear and chloroplast encoded genes with time by quantitative polymerase chain reaction (QPCR). The kinetics of damage rapir in the nuclear rbcS gene suggest that photoreactivation and dark mechanisms are active, while for the plastome encoded psbA gene only a light-dependent repair process was detected which is considerably slower than would be expected for photolyase-mediated photoreactivation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bensen RJ, Warner HR: Partial purification and characterization of uracil-DNA glycosylase activity from chloroplasts of Zea mays seedlings. Plant Physiol 84: 1102–1106 (1987).
Berry-Lowe SL, McKnight TD, Shah DM, Meagher RB: The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Apl Genet 1: 483–498 (1982).
Bohr VA, Smith CA, Okumoto DS, Hanawalt PC: DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40: 359–369 (1985).
Brit AB, Chen J-J, Wykoff D, Mitchell D: A UV-sensitive mutant of Arabidopsis defective in the repair of pyrimidine-pyrimidone(6–4) dimers. Science 261: 1571–1574 (1993).
Cannon GC, Heinhorst S, Weissbach A: Plastid DNA content in a cultured soybean line capable of photoavtotrophic growth. Plant Physiol 80: 601–603 (1985).
Cannon GC, Heinhorst S, Siedlecki J, Weissbach A: Chloroplast DNA synthesis in light and dark grown cultured Nicotiana tabacum cells as determined by molecular hybridization. Plant Cell Rep 4: 41–45 (1985).
Cerutti H, Osman M, Grandoni P, Jagendorf AT: A homology of Escherichia coli RecA protein in plastids of higher plants. Proc Natl Acad Sci USA 89: 8068–8072 (1992).
Cerutti H, Ibrahim H-Z, Jagendorf AT: Treatment of pea (Pisum sativum) protoplasts with DNA-damaging agents induces a 30-kilodalton chloroplast protein immunologically related to Escherichia coli RecA. Plant Physiaol 102: 155–163 (1993).
Cox JL, Small GD: Isolation of a photoreactivation-deficient mutant of Chlamydomonas. Mutation Res 146: 249–255 (1985).
Crouse EJ, Schmitt JM, Bohnert HJ: Chloroplast and cyanobacterial genomes, genes and RNAs: a compilation. Plant Mol Biol Rep 3: 43–49 (1985).
Gillott M, Erdös G, Buetow DE: Light-induced chloroplasts differentiation in soybean cells in suspension culture. Plant Physiol 96: 962–970 (1991).
Govan HL, Valles-Ayoub Y, Braun J: Fine-mapping of DNA damage and repair in specific genomic segments. Nucl Acids Res 18: 3823–3830 (1990).
Grimaldi KA, Bingham JP, Souhami RL, Hartley JA: DNA damage by anticancer agents and its repair: Mapping in cells at the subgene level with quantitative polymerase chain reaction. Anal Biochem 222: 236–242 (1994).
Heinhorst S, Cannon GC, Weissbach A: Chloroplast and mitochondrial DNA polymerases from cultured soybean cells. Plant Physiol 92: 939–945 (1990).
Horn ME, Sherrard JJ, Widholm JM: Photoautotrophic growth of soybean cells in suspension culture. Plant Physiol 72: 426–429 (1983).
Howland GP: Dark-repair of ultraviolet-induced pyrimidine dimers in the DNA of wild carrot protoplasts. Nature 254: 160–161 (1975).
Kalinowski DP, Illenye S, van Houten B: Analysis of DNA damage and repair in murine leukemia L1210 cells using a quantitative polymerase chain reaction assay. Nucl Acids Res 20: 3485–3494 (1992).
Lamppa G, Bendich A: Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol 64: 126–130 (1979).
Lawrence ME, Possingham JV: Microspectrofluorometric measurement of chloroplast DNA in dividing and expanding leaf cells of Spinacea oleracea. Plant Physiol 81: 708–710 (1986).
Lommel L, Hanawalt PC: Increased UV resistance of a Xeroderma pigmentosum revertant cell line is correlated with selective repair of the transcribed strand of and expressed gene. Mol Cell Biol 13: 970–976 (1993).
McLennan AG: The repair of ultraviolet-induced DNA damage in plant cells. Mutation Res 181: 1–7 (1987).
McLennan AG, Eastwood AC: An endonuclease activity from suspension cultures of Daucus carota which acts upon pyrimidine dimers. Plant Sci 46: 151–157 (1986).
Mellon I, Hanawalt P: Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature 342: 95–98 (1989).
Nicolas P, Hussein Y, Heizmann P, Nigon V: Comparative studies of chloroplastic and nuclear DNA repair abilities after ultraviolet irradiation of Euglena gracilis. Mol Gen Genet 178: 567–572 (1980).
Opperman T, Hong T-H, Surzyki S: Chloroplast and nuclear genomes of Chlamodomas reinhardtii share homology with Escherichia coli genes for DNA replication, repair and transcription. Curr Genet 15: 39–46 (1989).
Pang Q, Hays JB: UV-B-inducible and temperature-sensitive photoreactivation of cyclobutane pyrimidine dimers in Arabidopsis thaliana. Plant Physiol 95: 536–543 (1991).
Pang Q, Hays JB, Rajagopal I, Schaefer TS: Selection of Arabidopsis cDNAs that partially correct phenotypes of Escherichia coli DNA-damage-sensitive mutants and analysis of two plant cDNSs that appear to express UV-specific dark repair activities. Plant Mol Biol 22: 411–426 (1993).
Palmer JD: Comparative organization of chloroplast genomes. Annu Rev Genet 19: 325–354 (1985).
Scott NS, Possingham JV: Changes in chloroplast DNA levels during growth of spinach leaves. J Exp Bot 34: 1756–1767 (1983).
Shirley BW, Ham DP, Senecoff JF, Berry-Lowe SL, Zurfluh LL, Shah DM, Meagher RB: Comparison of the expression of two highly homologous members of the soybean ribulose-1,5-bisphosphate carboxylase small subunit gene family. Plant Mol Biol 14: 909–925 (1990).
Small GD: Loss of nuclear photoreactivating enzyme following UV irradiation of Chlamydomonas. Biochim Biophys Acta 606: 105–112 (1980).
Small GD: Repair systems for nuclear and chloroplast DNA in Chlamydomonas reinhardtii. Mutation Res 181: 31–35 (1987).
Spielmann A, Stutz E: Nucleotide sequence of soybean chloroplast DNA regions which contain the psbA and trnH genes and cover the ends of the large single copy region and one end of the inverted repeats. Nucl Acids Res 11: 7157–7167 (1983).
Stapleton AE: Ultraviolet radiation and plants: burning questions. Plant Cell 4: 1353–1358 (1992).
Svachulova J, Veleminsky J, Savata J: Nucleases of barley Chloroplasts acting on DNA modified by UV-light and by methyl methanesulphonate. In: Zadrazil S, Sponar J (eds), DNA Recombination, Interactions and Repair, pp. 495–499. Pergamon Press, Oxford, (1980).
Tymms MJ, Scott NS, Possingham JV: DNA Content of Beta vulgaris chloroplasts during leaf cell expansion. Plant Physiol 71: 785–788 (1983).
Veleminsky J, Svachulova J, Gichner T: Endonucleases for UV-irradiated and depurinated DNA in barley chloroplasts Nucl Acids Res 8: 1373–1381 (1980).
Vytasek R: A sensitive fluorometric asay for the determination of DNA. Anal Biochem 120: 243–248 (1982).
Widholm JM: Properties and uses of photoautotrophic plant cell cultures. Int Rev Cytol 132: 109–175 (1992).
Willmitzer L, Wagner KG: The isolation of nuclei from tissue-cultured plant cells. Exp Cell Res 135: 70–76 (1981).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cannon, G.C., Hedrick, L.A. & Heinhorst, S. Repair mechanisms of UV-induced DNA damage in soybean chloroplasts. Plant Mol Biol 29, 1267–1277 (1995). https://doi.org/10.1007/BF00020467
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00020467