UVR2 Ensures Transgenerational Genome Stability Under Simulated Natural UV-B in Arabidopsis Thaliana

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Dec 2

PMID 27905394

Citations 20

Authors

Eva-Maria Willing

Thomas Piofczyk

Andreas Albert

J Barbro Winkler

Korbinian Schneeberger

Ales Pecinka

Affiliations

Soon will be listed here.

Abstract

Ground levels of solar UV-B radiation induce DNA damage. Sessile phototrophic organisms such as vascular plants are recurrently exposed to sunlight and require UV-B photoreception, flavonols shielding, direct reversal of pyrimidine dimers and nucleotide excision repair for resistance against UV-B radiation. However, the frequency of UV-B-induced mutations is unknown in plants. Here we quantify the amount and types of mutations in the offspring of Arabidopsis thaliana wild-type and UV-B-hypersensitive mutants exposed to simulated natural UV-B over their entire life cycle. We show that reversal of pyrimidine dimers by UVR2 photolyase is the major mechanism required for sustaining plant genome stability across generations under UV-B. In addition to widespread somatic expression, germline-specific UVR2 activity occurs during late flower development, and is important for ensuring low mutation rates in male and female cell lineages. This allows plants to maintain genome integrity in the germline despite exposure to UV-B.

Citing Articles

Characterization of radiations-induced genomic structural variations in Arabidopsis thaliana.

Sall S, Alioua A, Staerck S, Graindorge S, Pellicioli M, Schuler J Plant J. 2024; 121(1):e17180.

PMID: 39616610 PMC: 11712536. DOI: 10.1111/tpj.17180.

The photoreactivation of 6 - 4 photoproducts in chloroplast and nuclear DNA depends on the amount of the Arabidopsis UV repair defective 3 protein.

Zglobicki P, Hermanowicz P, Klodawska K, Bazant A, Labuz J, Grzyb J BMC Plant Biol. 2024; 24(1):723.

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The vast majority of somatic mutations in plants are layer-specific.

Goel M, Campoy J, Krause K, Baus L, Sahu A, Sun H Genome Biol. 2024; 25(1):194.

PMID: 39049052 PMC: 11267851. DOI: 10.1186/s13059-024-03337-0.

Global repair is the primary nucleotide excision repair subpathway for the removal of pyrimidine-pyrimidone (6-4) damage from the Arabidopsis genome.

Kaya S, Erdogan D, Sancar A, Adebali O, Oztas O Sci Rep. 2024; 14(1):3308.

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Reply to: Re-evaluating evidence for adaptive mutation rate variation.

Monroe J, Murray K, Xian W, Srikant T, Carbonell-Bejerano P, Becker C Nature. 2023; 619(7971):E57-E60.

PMID: 37495874 PMC: 10371858. DOI: 10.1038/s41586-023-06315-x.

References

Mazza C, Boccalandro H, Giordano C, Battista D, Scopel A, Ballare C . Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol. 2000; 122(1):117-26. PMC: 58850. DOI: 10.1104/pp.122.1.117. View

Martincorena I, Roshan A, Gerstung M, Ellis P, Van Loo P, McLaren S . Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science. 2015; 348(6237):880-6. PMC: 4471149. DOI: 10.1126/science.aaa6806. View

Kimura S, Tahira Y, Ishibashi T, Mori Y, Mori T, Hashimoto J . 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. Nucleic Acids Res. 2004; 32(9):2760-7. PMC: 419598. DOI: 10.1093/nar/gkh591. View

Lynch M . Evolution of the mutation rate. Trends Genet. 2010; 26(8):345-52. PMC: 2910838. DOI: 10.1016/j.tig.2010.05.003. View

Scharer O . Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 2013; 5(10):a012609. PMC: 3783044. DOI: 10.1101/cshperspect.a012609. View

Pecinka A, Rosa M, Schikora A, Berlinger M, Hirt H, Luschnig C . Transgenerational stress memory is not a general response in Arabidopsis. PLoS One. 2009; 4(4):e5202. PMC: 2668180. DOI: 10.1371/journal.pone.0005202. View

Yadegari R, Drews G . Female gametophyte development. Plant Cell. 2004; 16 Suppl:S133-41. PMC: 2643389. DOI: 10.1105/tpc.018192. View

Kimura S, Sakaguchi K . DNA repair in plants. Chem Rev. 2006; 106(2):753-66. DOI: 10.1021/cr040482n. View

Brown B, Cloix C, Jiang G, Kaiserli E, Herzyk P, Kliebenstein D . A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci U S A. 2005; 102(50):18225-30. PMC: 1312397. DOI: 10.1073/pnas.0507187102. View

10.

Li J, Ou-Lee T, Raba R, Amundson R, Last R . Arabidopsis Flavonoid Mutants Are Hypersensitive to UV-B Irradiation. Plant Cell. 1993; 5(2):171-179. PMC: 160260. DOI: 10.1105/tpc.5.2.171. View

11.

Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley E . Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci U S A. 2004; 101(5):1397-402. PMC: 337064. DOI: 10.1073/pnas.0308044100. View

12.

Castells E, Molinier J, Drevensek S, Genschik P, Barneche F, Bowler C . det1-1-induced UV-C hyposensitivity through UVR3 and PHR1 photolyase gene over-expression. Plant J. 2010; 63(3):392-404. DOI: 10.1111/j.1365-313X.2010.04249.x. View

13.

Kliebenstein D, Lim J, Landry L, Last R . Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol. 2002; 130(1):234-43. PMC: 166556. DOI: 10.1104/pp.005041. View

14.

Kami C, Lorrain S, Hornitschek P, Fankhauser C . Light-regulated plant growth and development. Curr Top Dev Biol. 2010; 91:29-66. DOI: 10.1016/S0070-2153(10)91002-8. View

15.

Favory J, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M . Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 2009; 28(5):591-601. PMC: 2657586. DOI: 10.1038/emboj.2009.4. View

16.

Rochette P, Lacoste S, Therrien J, Bastien N, Brash D, Drouin R . Influence of cytosine methylation on ultraviolet-induced cyclobutane pyrimidine dimer formation in genomic DNA. Mutat Res. 2009; 665(1-2):7-13. DOI: 10.1016/j.mrfmmm.2009.02.008. View

17.

Schneeberger K, Hagmann J, Ossowski S, Warthmann N, Gesing S, Kohlbacher O . Simultaneous alignment of short reads against multiple genomes. Genome Biol. 2009; 10(9):R98. PMC: 2768987. DOI: 10.1186/gb-2009-10-9-r98. View

18.

Lister R, OMalley R, Tonti-Filippini J, Gregory B, Berry C, Millar A . Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008; 133(3):523-36. PMC: 2723732. DOI: 10.1016/j.cell.2008.03.029. View

19.

Feng S, Jacobsen S, Reik W . Epigenetic reprogramming in plant and animal development. Science. 2010; 330(6004):622-7. PMC: 2989926. DOI: 10.1126/science.1190614. View

20.

Crooks G, Hon G, Chandonia J, Brenner S . WebLogo: a sequence logo generator. Genome Res. 2004; 14(6):1188-90. PMC: 419797. DOI: 10.1101/gr.849004. View