Abstract
Sunlight regulates transcriptional programs and triggers the shaping of the genome throughout plant development. Among the different sunlight wavelengths that reach the surface of the Earth, UV-B (280–315 nm) controls the expression of hundreds of genes for the photomorphogenic responses and also induces the formation of photodamage that interfere with genome integrity and transcriptional programs. The combination of cytogenetics and deep-learning-based analyses allowed determining the location of UV-B-induced photoproducts and quantifying the effects of UV-B irradiation on constitutive heterochromatin content in different Arabidopsis natural variants acclimated to various UV-B regimes. We identified that UV-B-induced photolesions are enriched within chromocenters. Furthermore, we uncovered that UV-B irradiation promotes constitutive heterochromatin dynamics that differs among the Arabidopsis ecotypes having divergent heterochromatin contents. Finally, we identified that the proper restoration of the chromocenter shape, upon DNA repair, relies on the UV-B photoreceptor, UV RESISTANCE LOCUS 8 (UVR8). These findings shed the light on the effect of UV-B exposure and perception in the modulation of constitutive heterochromatin content in Arabidopsis thaliana.
Graphical abstract
Similar content being viewed by others
Data availability
Data (i.e microscopy images) will be available on demand.
References
Heslop-Harrison (Pat), J. S., & Schwarzacher, T. (2011). Organisation of the plant genome in chromosomes. Plant Journal, 66, 18–33. https://doi.org/10.1111/j.1365-313X.2011.04544.x
Fransz, P., Soppe, W., & Schubert, I. (2003). Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Research, 11, 227–240. https://doi.org/10.1023/a:1022835825899
Pavet, V., Quintero, C., Cecchini, N. M., Rosa, A. L., & Alvarez, M. E. (2006). Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. MPMI, 19, 577–587. https://doi.org/10.1094/MPMI-19-0577
Pecinka, A., Dinh, H. Q., Baubec, T., Rosa, M., Lettner, N., & Scheid, O. M. (2010). Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. The Plant Cell, 22, 3118–3129. https://doi.org/10.1105/tpc.110.078493
Perrella, G., & Kaiserli, E. (2016). Light behind the curtain: photoregulation of nuclear architecture and chromatin dynamics in plants. New Phytologist, 212, 908–919. https://doi.org/10.1111/nph.14269
Barneche, F., Malapeira, J., & Mas, P. (2014). The impact of chromatin dynamics on plant light responses and circadian clock function. Journal of Experimental Botany, 65, 2895–2913. https://doi.org/10.1093/jxb/eru011
Probst, A. V., & Mittelsten Scheid, O. (2015). Stress-induced structural changes in plant chromatin. Current Opinion in Plant Biology, 27, 8–16. https://doi.org/10.1016/j.pbi.2015.05.011
Patitaki, E., Schivre, G., Zioutopoulou, A., Perrella, G., Bourbousse, C., Barneche, F., & Kaiserli, E. (2022). Light, chromatin, action: nuclear events regulating light signaling in Arabidopsis. New Phytologist, 236, 333–349. https://doi.org/10.1111/nph.18424
Bourbousse, C., Mestiri, I., Zabulon, G., Bourge, M., Formiggini, F., Koini, M. A., Brown, S. C., Fransz, P., Bowler, C., & Barneche, F. (2015). Light signaling controls nuclear architecture reorganization during seedling establishment. Proceedings of the National academy of Sciences of the United States of America, 112, E2836-2844. https://doi.org/10.1073/pnas.1503512112
Jiang, J., Liu, J., Sanders, D., Qian, S., Ren, W., Song, J., Liu, F., & Zhong, X. (2021). UVR8 interacts with de novo DNA methyltransferase and suppresses DNA methylation in Arabidopsis. Nat Plants, 7, 184–197. https://doi.org/10.1038/s41477-020-00843-4
Walbot, V. (1999). UV-B damage amplified by transposons in maize. Nature, 397, 398–399. https://doi.org/10.1038/17043
Questa, J., Walbot, V., & Casati, P. (2013). UV-B radiation induces Mu element somatic transposition in maize. Molecular Plant, 6, 2004–2007. https://doi.org/10.1093/mp/sst112
Alonso-Blanco, C., Andrade, J., Becker, C., Bemm, F., Bergelson, J., Borgwardt, K. M., Cao, J., Chae, E., Dezwaan, T. M., Ding, W., Ecker, J. R., Exposito-Alonso, M., Farlow, A., Fitz, J., Gan, X., Grimm, D. G., Hancock, A. M., Henz, S. R., Holm, S., … Zhou, X. (2016). 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. Cell, 166, 481–491. https://doi.org/10.1016/j.cell.2016.05.063
Tessadori, F., van Zanten, M., Pavlova, P., Clifton, R., Pontvianne, F., Snoek, L. B., Millenaar, F. F., Schulkes, R. K., van Driel, R., Voesenek, L. A. C. J., Spillane, C., Pikaard, C. S., Fransz, P., & Peeters, A. J. M. (2009). Phytochrome B and histone deacetylase 6 control light-induced chromatin compaction in Arabidopsis thaliana. PLoS Genetics, 5, e1000638. https://doi.org/10.1371/journal.pgen.1000638
Snoek, B. L., Pavlova, P., Tessadori, F., Peeters, A. J. M., Bourbousse, C., Barneche, F., de Jong, H., Fransz, P. F., & van Zanten, M. (2017). Genetic dissection of morphometric traits reveals that phytochrome B affects nucleus size and heterochromatin organization in Arabidopsis thaliana. G3 (Bethesda), 7, 2519–2531. https://doi.org/10.1534/g3.117.043539
Pavlova, P., van Zanten, M., Snoek, B. L., de Jong, H., & Fransz, P. (2022). 2D morphometric analysis of Arabidopsis thaliana nuclei reveals characteristic profiles of different cell types and accessions. Chromosome Research, 30, 5–24. https://doi.org/10.1007/s10577-021-09673-2
Schuch, A. P., Moreno, N. C., Schuch, N. J., Menck, C. F. M., & Garcia, C. C. M. (2017). Sunlight damage to cellular DNA: focus on oxidatively generated lesions. Free Radical Biology & Medicine, 107, 110–124. https://doi.org/10.1016/j.freeradbiomed.2017.01.029
Markovitsi, D. (2016). UV-induced DNA Damage: the role of electronic excited states. Photochemistry and Photobiology, 92, 45–51. https://doi.org/10.1111/php.12533
Britt, A. B. (1995). Repair of DNA damage induced by ultraviolet radiation. Plant Physiology, 108, 891–896.
Banaś, A. K., Zgłobicki, P., Kowalska, E., Bażant, A., Dziga, D., & Strzałka, W. (2020). All you need is light. Photorepair of UV-induced pyrimidine dimers. Genes, 11, 1304. https://doi.org/10.3390/genes11111304
Kimura, S., & Sakaguchi, K. (2006). DNA repair in plants. Chemical Reviews, 106, 753–766. https://doi.org/10.1021/cr040482n
Green, C. M., & Almouzni, G. (2002). When repair meets chromatin. First in series on chromatin dynamics. EMBO Reports, 3, 28–33. https://doi.org/10.1093/embo-reports/kvf005
Polo, S. E., & Almouzni, G. (2015). Chromatin dynamics after DNA damage: The legacy of the access-repair-restore model. DNA Repair (Amst), 36, 114–121. https://doi.org/10.1016/j.dnarep.2015.09.014
Fei, J., Kaczmarek, N., Luch, A., Glas, A., Carell, T., & Naegeli, H. (2011). Regulation of nucleotide excision repair by UV-DDB: prioritization of damage recognition to internucleosomal DNA. PLoS Biology. https://doi.org/10.1371/journal.pbio.1001183
Gale, J. M., Nissen, K. A., & Smerdon, M. J. (1987). UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. Proceedings of the National academy of Sciences of the United States of America, 84, 6644–6648. https://doi.org/10.1073/pnas.84.19.6644
Banyasz, A., Esposito, L., Douki, T., Perron, M., Lepori, C., Improta, R., & Markovitsi, D. (2016). Effect of C5-methylation of cytosine on the UV-induced reactivity of duplex DNA: conformational and electronic factors. The Journal of Physical Chemistry B, 120, 4232–4242. https://doi.org/10.1021/acs.jpcb.6b03340
Rochette, P. J., Lacoste, S., Therrien, J.-P., Bastien, N., Brash, D. E., & Drouin, R. (2009). Influence of cytosine methylation on ultraviolet-induced cyclobutane pyrimidine dimer formation in genomic DNA. Mutation Research, 665, 7–13. https://doi.org/10.1016/j.mrfmmm.2009.02.008
Hu, J., Adar, S., Selby, C. P., Lieb, J. D., & Sancar, A. (2015). Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution. Genes & Development, 29, 948–960. https://doi.org/10.1101/gad.261271.115
Wang, J., Li, X., Do Kim, K., Scanlon, M. J., Jackson, S. A., Springer, N. M., & Yu, J. (2019). Genome-wide nucleotide patterns and potential mechanisms of genome divergence following domestication in maize and soybean. Genome Biology, 20, 74. https://doi.org/10.1186/s13059-019-1683-6
Beckmann, M., Václavík, T., Manceur, A. M., Šprtová, L., von Wehrden, H., Welk, E., & Cord, A. F. (2014). glUV: a global UV-B radiation data set for macroecological studies. Methods in Ecology and Evolution, 5, 372–383. https://doi.org/10.1111/2041-210X.12168
Johann to Berens, P., Schivre, G., Theune, M., Peter, J., Sall, S. O., Mutterer, J., Barneche, F., Bourbousse, C., & Molinier, J. (2022). Advanced image analysis methods for automated segmentation of subnuclear chromatin domains. Epigenomes, 6, 34. https://doi.org/10.3390/epigenomes6040034
Kawakatsu, T., Huang, S.-S.C., Jupe, F., Sasaki, E., Schmitz, R. J., Urich, M. A., Castanon, R., Nery, J. R., Barragan, C., He, Y., Chen, H., Dubin, M., Lee, C.-R., Wang, C., Bemm, F., Becker, C., O’Neil, R., O’Malley, R. C., Quarless, D. X., … Ecker, J. R. (2016). Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell, 166, 492–505. https://doi.org/10.1016/j.cell.2016.06.044
Jiao, W. B., & Schneeberger, K. (2020). Chromosome-level assemblies of multiple Arabidopsis genomes reveal hotspots of rearrangements with altered evolutionary dynamics. Nature Communications, 1, 989. https://doi.org/10.1038/s41467-020-14779-y
Mathieu, O., Reinders, J., Čaikovski, M., Smathajitt, C., & Paszkowski, J. (2007). Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell, 130, 851–862. https://doi.org/10.1016/j.cell.2007.07.007
Law, J. A., & Jacobsen, S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics, 11, 204–220. https://doi.org/10.1038/nrg2719
Rozema, J., van de Staaij, J., Björn, L. O., & Caldwell, M. (1997). UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology & Evolution, 12, 22–28. https://doi.org/10.1016/S0169-5347(96)10062-8
Molinier, J. (2017). Genome and epigenome surveillance processes underlying UV exposure in plants. Genes (Basel). https://doi.org/10.3390/genes8110316
Sun, L., Jing, Y., Liu, X., Li, Q., Xue, Z., Cheng, Z., Wang, D., He, H., & Qian, W. (2020). Heat stress-induced transposon activation correlates with 3D chromatin organization rearrangement in Arabidopsis. Nature Communications, 11, 1886. https://doi.org/10.1038/s41467-020-15809-5
Graindorge, S., Cognat, V., Johann to Berens, P., Mutterer, J., & Molinier, J. (2019). Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure. PLoS Genetics, 15, e1008476. https://doi.org/10.1371/journal.pgen.1008476
Singer, T., Yordan, C., & Martienssen, R. A. (2001). Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene decrease in DNA Methylation (DDM1). Genes & Development, 15, 591–602. https://doi.org/10.1101/gad.193701
Lippman, Z., Gendrel, A.-V., Black, M., Vaughn, M. W., Dedhia, N., Richard McCombie, W., Lavine, K., Mittal, V., May, B., Kasschau, K. D., Carrington, J. C., Doerge, R. W., Colot, V., & Martienssen, R. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature, 430, 471–476. https://doi.org/10.1038/nature02651
Tittel-Elmer, M., Bucher, E., Broger, L., Mathieu, O., Paszkowski, J., & Vaillant, I. (2010). Stress-induced activation of heterochromatic transcription. PLOS Genetics, 6, e1001175. https://doi.org/10.1371/journal.pgen.1001175
Johann to Berens, P., & Molinier, J. (2020). Formation and recognition of UV-induced DNA damage within genome complexity. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms21186689
Jenkins, G. I. (2017). Photomorphogenic responses to ultraviolet-B light. Plant, Cell & Environment, 40, 2544–2557. https://doi.org/10.1111/pce.12934
Johnson, L. M., Law, J. A., Khattar, A., Henderson, I. R., & Jacobsen, S. E. (2008). SRA-domain proteins required for DRM2-mediated De Novo DNA methylation. PLOS Genetics, 4, e1000280. https://doi.org/10.1371/journal.pgen.1000280
Favory, J. J., Stec, A., Gruber, H., Rizzini, L., Oravecz, A., Funk, M., Albert, A., Cloix, C., Jenkins, G. I., Oakeley, E. J., Seidlitz, H. K., Nagy, F., & Ulm, R. (2009). Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO Journal, 5, 591–601. https://doi.org/10.1038/emboj.2009.4
Castells, E., Molinier, J., Drevensek, S., Genschik, P., Barneche, F., & Bowler, C. (2010). det1-1-induced UV-C hyposensitivity through UVR3 and PHR1 photolyase gene over-expression. The Plant Journal, 63, 392–404. https://doi.org/10.1111/j.1365-313X.2010.04249.x
Acknowledgements
We are grateful to Prof. Roman Ulm for providing the uvr8-6 seeds. This research was funded by a grant from the French National Research Agency (ANR-20-CE20-002) and supported by the EPIPLANT Groupement de Recherche (CNRS, France). K.G. was supported by the ERASMUS program for higher education.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Johann to Berens, P., Golebiewska, K., Peter, J. et al. UV-B-induced modulation of constitutive heterochromatin content in Arabidopsis thaliana. Photochem Photobiol Sci 22, 2153–2166 (2023). https://doi.org/10.1007/s43630-023-00438-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s43630-023-00438-w