Footprints of the sun: Memory of UV and light stress in plants

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Müller Xing, Ralf ^a   Xing, Qian ^a   Goodrich, Justin ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Abiotic plant stress; Arabidopsis; Epigenetic memory; Stress signaling; UV B

Indexed keywords

EID: 84908180805     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00474     Document Type: Review

References (127)

1. Alexandre, C., Moller-Steinbach, Y., Schonrock, N., Gruissem, W., and Hennig, L. (2009). Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol. Plant 2, 675-687. doi: 10.1093/mp/ssp012
2. Ballare, C. L. (2014). Light regulation of plant defense. Annu. Rev. Plant Biol. 65, 335-363. doi: 10.1146/annurev-arplant-050213-040145
3. Bandurska, H., and Cieślak, M. (2013). The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environ. Exp. Bot. 94, 9-18. doi: 10.1016/j.envexpbot.2012.03.001
4. Bandurska, H., Pietrowska-Borek, M., and Cieślak, M. (2012). Response of barley seedlings to water deficit and enhanced UV-B irradiation acting alone and in combination. Acta Physiol. Plant 34, 161-171. doi: 10.1007/s11738-011-0814-9
5. Bandurska, H., Niedziela, J., and Chadzinikolau, T. (2013). Separate and combined responses to water deficit and UV-B radiation. Plant Sci. 213, 98-105. doi: 10.1016/j.plantsci.2013.09.003
6. Benhamed, M., Bertrand, C., Servet, C., and Zhou, D. X. (2006). Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18, 2893-2903. doi: 10.1105/tpc.106.043489
7. Benhamed, M., Martin-Magniette, M.-L., Taconnat, L., Bitton, F., Servet, C., De Clercq, R.,et al. (2008). Genome-scale Arabidopsis promoter array identifies targets of the histone acetyltransferase GCN5. Plant J. 56, 493-504. doi: 10.1111/j.1365-313X.2008.03606.x
8. Bertrand, C., Benhamed, M., Li, Y. F., Ayadi, M., Lemonnier, G., Renou, J. P.,et al. (2005). Arabidopsis HAF2 gene encoding TATA-binding protein (TBP)-associated factor TAF1, is required to integrate light signals to regulate gene expression and growth. J. Biol. Chem. 280, 1465-1473. doi: 10.1074/jbc.M409000200
9. Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21. doi: 10.1101/gad.947102
10. Bird, A. (2007). Perceptions of epigenetics. Nature 447, 396-398. doi: 10.1038/nature05913
11. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y.,et al. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS ONE 5:e9514. doi: 10.1371/journal.pone.0009514
12. Brosché, M., and Strid, Å. (2003). Molecular events following perception of ultraviolet-B radiation by plants. Physiol. Plant. 117, 1-10. doi: 10.1034/j.1399-3054.2003.1170101.x
13. Brown, B. A., Cloix, C., Jiang, G. H., Kaiserli, E., Herzyk, P., Kliebenstein, D. J.,et al. (2005). A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102, 18225-18230. doi: 10.1073/pnas.0507187102
14. Brown, B. A., and Jenkins, G. I. (2008). UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiol. 146, 576-588. doi: 10.1104/pp.107.108456
15. Campi, M., D'Andrea, L., Emiliani, J., and Casati, P. (2012). Participation of chromatin-remodeling proteins in the repair of ultraviolet-B-damaged DNA. Plant Physiol. 158, 981-995. doi: 10.1104/pp.111.191452
16. Campos, Â. D., Ferreira, A. G., Hampe, M. M. V., Antunes, I. F., Brancão, N., Silveira, E. P.,et al. (2003). Induction of chalcone synthase and phenylalanine ammonia-lyase by salicylic acid and Colletotrichum lindemuthianum in common bean. Braz. J. Plant Physiol. 15, 129-134. doi: 10.1590/S1677-04202003000300001
17. Casati, P., Campi, M., Chu, F., Suzuki, N., Maltby, D., Guan, S.,et al. (2008). Histone acetylation and chromatin remodeling are required for UV-B-dependent transcriptional activation of regulated genes in maize. Plant Cell 20, 827-842. doi: 10.1105/tpc.107.056457
18. Casati, P., Morrow, D. J., Fernandes, J. F., and Walbot, V. (2011a). UV-B signaling in maize: transcriptomic and metabolomic studies at different irradiation times. Plant Signal. Behav. 6, 1926-1931. doi: 10.4161/psb.6.12.18164
19. Casati, P., Campi, M., Morrow, D. J., Fernandes, J. F., and Walbot, V. (2011b). Transcriptomic, proteomic and metabolomic analysis of UV-B signaling in maize. BMC Genomics 12:321. doi: 10.1186/1471-2164-12-321
20. Casati, P., Stapleton, A. E., Blum, J. E., and Walbot, V. (2006). Genome-wide analysis of high-altitude maize and gene knockdown stocks implicates chromatin remodeling proteins in response to UV-B. Plant J. 46, 613-627. doi: 10.1111/j.1365-313X.2006.02721.x
21. Casati, P., and Walbot, V. (2004). Rapid transcriptome responses of maize (Zea mays) to UV-B in irradiated and shielded tissues. Genome Biol. 5:R16. doi: 10.1186/gb-2004-5-3-r16
22. Chandler, V. L., and Walbot, V. (1986). DNA modification of a maize transposable element correlates with loss of activity. Proc. Natl. Acad. Sci. U.S.A. 83, 1767-1771. doi: 10.1073/pnas.83.6.1767
23. Chen, H., Huang, X., Gusmaroli, G., Terzaghi, W., Lau, O. S., Yanagawa, Y.,et al. (2010a). Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22, 108-123. doi: 10.1105/tpc.109.065490
24. Chen, M., Lv, S., and Meng, Y. (2010b). Epigenetic performers in plants. Dev. Growth Differ. 52, 555-566. doi: 10.1111/j.1440-169X.2010.01192.x
25. Chen, Y. P. (2009). Response of antioxidant defense system to laser radiation apical meristem of Isatis indigoticaseedlings exposed to UV-B. Plant Signal. Behav. 4, 571-573. doi: 10.4161/psb.4.7.8794
26. Chinnusamy, V., and Zhu, J.-K. (2009). Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol.12, 133-139. doi: 10.1016/j.pbi.2008.12.006
27. Christie, J. M., Arvai, A. S., Baxter, K. J., Heilmann, M., Pratt, A. J., O'Hara, A.,et al. (2012). Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335, 1492-1496. doi: 10.1126/science.1218091
28. Christie, J. M., and Jenkins, G. I. (1996). Distinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells. Plant Cell 8, 1555-1567. doi: 10.1105/tpc.8.9.1555
29. Cloix, C., and Jenkins, G. I. (2008). Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. Mol. Plant 1, 118-128. doi: 10.1093/mp/ssm012
30. D'Urso, A., and Brickner, J. H. (2014). Mechanisms of epigenetic memory. Trends Genet. 30, 230-236. doi: 10.1016/j.tig.2014.04.004
31. Deal, R. B., and Henikoff, S. (2011). Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14, 116-122. doi: 10.1016/j.pbi.2010.11.005
32. Ding, Y., Fromm, M., and Avramova, Z. (2012). Multiple exposures to drought "train" transcriptional responses inArabidopsis. Nat. Commun. 3:740. doi: 10.1038/ncomms1732
33. Dumbliauskas, E., Lechner, E., Jaciubek, M., Berr, A., Pazhouhandeh, M., Alioua, M.,et al. (2011). The ArabidopsisCUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J. 30, 731-743. doi: 10.1038/emboj.2010.359
34. Emiliani, J., Grotewold, E., Falcone Ferreyra, M. L., and Casati, P. (2013). Flavonols protect Arabidopsis plants against UV-B deleterious effects. Mol. Plant 6, 1376-1379. doi: 10.1093/mp/sst021
35. Ervin, E. H., Zhang, X., and Fike, J. H. (2004). Ultraviolet-B radiation damage on kentucky bluegrass II: hormone supplement effects. HortScience 39, 1471-1474.
36. Falcone Ferreyra, M. L., Rius, S., Emiliani, J., Pourcel, L., Feller, A., Morohashi, K.,et al. (2010). Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J. 62, 77-91. doi: 10.1111/j.1365-313X.2010.04133.x
37. Fankhauser, C., and Ulm, R. (2011). Light-regulated interactions with SPA proteins underlie cryptochrome-mediated gene expression. Genes Dev. 25, 1004-1009. doi: 10.1101/gad.2053911
38. Favory, J. J., Stec, A., Gruber, H., Rizzini, L., Oravecz, A., Funk, M.,et al. (2009). Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28, 591-601. doi: 10.1038/emboj.2009.4
39. Fuglevand, G., Jackson, J. A., and Jenkins, G. I. (1996). UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell 8, 2347-2357. doi: 10.1105/tpc.8.12.2347
40. Gendrel, A. V., Lippman, Z., Yordan, C., Colot, V., and Martienssen, R. A. (2002). Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297, 1871-1873. doi: 10.1126/science.1074950
41. Gonzalez Besteiro, M. A., Bartels, S., Albert, A., and Ulm, R. (2011). Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway. Plant J. 68, 727-737. doi: 10.1111/j.1365-313X.2011.04725.x
42. Gruber, H., Heijde, M., Heller, W., Albert, A., Seidlitz, H. K., and Ulm, R. (2010). Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 20132-20137. doi: 10.1073/pnas.0914532107
43. Guo, L., Zhou, J., Elling, A. A., Charron, J. B., and Deng, X. W. (2008). Histone modifications and expression of light-regulated genes in Arabidopsis are cooperatively influenced by changing light conditions. Plant Physiol. 147, 2070-2083. doi: 10.1104/pp.108.122929
44. Hartmann, U., Valentine, W. J., Christie, J. M., Hays, J., Jenkins, G. I., and Weisshaar, B. (1998). Identification of UV/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system. Plant Mol. Biol. 36, 741-754. doi: 10.1023/A:1005921914384
45. Hayat, Q., Hayat, S., Irfan, M., and Ahmad, A. (2010). Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 68, 14-25. doi: 10.1016/j.envexpbot.2009.08.005
46. Hectors, K., Jacques, E., Prinsen, E., Guisez, Y., Verbelen, J. P., Jansen, M. A.,et al. (2010). UV radiation reduces epidermal cell expansion in leaves of Arabidopsis thaliana. J. Exp. Bot. 61, 4339-4349. doi: 10.1093/jxb/erq235
47. Hectors, K., Prinsen, E., De Coen, W., Jansen, M. A., and Guisez, Y. (2007). Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation show specific changes in morphology and gene expression in the absence of stress symptoms. New Phytol. 175, 255-270. doi: 10.1111/j.1469-8137.2007.02092.x
48. Hectors, K., Van Oevelen, S., Geuns, J., Guisez, Y., Jansen, M. A., and Prinsen, E. (2014). Dynamic changes in plant secondary metabolites during UV acclimation in Arabidopsis thaliana. Physiol. Plant. doi: 10.1111/ppl.12168 [Epub ahead of print].
49. Heddad, M., Norén, H., Reiser, V., Dunaeva, M., Andersson, B., and Adamska, I. (2006). Differential expression and localization of early light-induced proteins in Arabidopsis. Plant Physiol. 142, 75-87. doi: 10.1104/pp.106.081489
50. Heijde, M., and Ulm, R. (2013). Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc. Natl. Acad. Sci. U.S.A. 110, 1113-1118. doi: 10.1073/pnas.1214237110
51. Hideg, E., Jansen, M. A., and Strid, A. (2013). UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci. 18, 107-115. doi: 10.1016/j.tplants.2012.09.003
52. Hong, E. J., West, A. E., and Greenberg, M. E. (2005). Transcriptional control of cognitive development. Curr. Opin. Neurobiol. 15, 21-28. doi: 10.1016/j.conb.2005.01.002
53. Ishibashi, T., Kimura, S., Yamamoto, T., Furukawa, T., Takata, K., Uchiyama, Y.,et al. (2003). Rice UV-damaged DNA binding protein homologues are most abundant in proliferating tissues. Gene 308, 79-87. doi: 10.1016/S0378-1119(03)00447-5
54. Iwasaki, M., and Paszkowski, J. (2014). Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc. Natl. Acad. Sci. U.S.A. 111, 8547-8552. doi: 10.1073/pnas.1402275111
55. Jansen, M. A. K., Gaba, V., and Greenberg, B. M. (1998). Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3, 131-135. doi: 10.1016/S1360-1385(98)01215-1
56. Jaskiewicz, M., Conrath, U., and Peterhansel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50-55. doi: 10.1038/embor.2010.186
57. Jenkins, G. I. (2009). Signal transduction in responses to UV-B radiation. Annu. Rev. Plant Biol. 60, 407-431. doi: 10.1146/annurev.arplant.59.032607.092953
58. Jenkins, G. I., and Brown, B. A. (2007). "UV-B perception and signal transduction," in Annual Plant Reviews, Vol. 30, Light and Plant Development, eds C. G. Whitelam and K. J. Halliday (Oxford: Blackwell Publishing Ltd), 155-182.
59. Jenkins, G. I., Long, J. C., Wade, H. K., Shenton, M. R., and Bibikova, T. N. (2001). UV and blue light signalling: pathways regulating chalcone synthase gene expression in Arabidopsis. New Phytol. 151, 121-131. doi: 10.1046/j.1469-8137.2001.00151.x
60. Jia, X., Ren, L., Chen, Q. J., Li, R., and Tang, G. (2009). UV-B-responsive microRNAs in Populus tremula. J. Plant Physiol. 166, 2046-2057. doi: 10.1016/j.jplph.2009.06.011
61. Kaiserli, E., and Jenkins, G. I. (2007). UV-B promotes rapid nuclear translocation of the Arabidopsis UV-B-specific signaling component UVR8 and activates its function in the nucleus. Plant Cell 19, 2662-2673. doi: 10.1105/tpc.107.053330
62. Kim, J. M., To, T. K., Ishida, J., Matsui, A., Kimura, H., and Seki, M. (2012). Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol. 53, 847-856. doi: 10.1093/pcp/pcs053
63. Kim, M. Y., and Zilberman, D. (2014). DNA methylation as a system of plant genomic immunity. Trends Plant Sci.19, 320-326. doi: 10.1016/j.tplants.2014.01.014
64. Kliebenstein, D. J., Lim, J. E., Landry, L. G., and Last, R. L. (2002). Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol. 130, 234-243. doi: 10.1104/pp.005041
65. Kravets, E. A., Zelena, L. B., Zabara, E. P., and Blume, Y. B. (2012). Adaptation strategy of barley plants to UV-B radiation. Emir. J. Food Agric. 24, 632-645. doi: 10.9755/ejfa.v24i6.632645
66. Kumar, S. V., and Wigge, P. A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response inArabidopsis. Cell 140, 136-147. doi: 10.1016/j.cell.2009.11.006
67. Landry, L. G., Stapleton, A. E., Lim, J., Hoffman, P., Hays, J. B., Walbot, V.,et al. (1997). An Arabidopsis photolyase mutant is hypersensitive to ultraviolet-B radiation. Proc. Natl. Acad. Sci. U.S.A. 94, 328-332. doi: 10.1073/pnas.94.1.328
68. Lang-Mladek, C., Popova, O., Kiok, K., Berlinger, M., Rakic, B., Aufsatz, W.,et al. (2010). Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol. Plant 3, 594-602. doi: 10.1093/mp/ssq014
69. Lang-Mladek, C., Xie, L., Nigam, N., Chumak, N., Binkert, M., Neubert, S.,et al. (2012). UV-B signaling pathways and fluence rate dependent transcriptional regulation of ARIADNE12. Physiol. Plant. 145, 527-539. doi: 10.1111/j.1399-3054.2011.01561.x
70. Lario, L. D., Ramirez-Parra, E., Gutierrez, C., Casati, P., and Spampinato, C. P. (2011). Regulation of plant MSH2 and MSH6 genes in the UV-B-induced DNA damage response. J. Exp. Bot. 62, 2925-2937. doi: 10.1093/jxb/err001
71. Lario, L. D., Ramirez-Parra, E., Gutierrez, C., Spampinato, C. P., and Casati, P. (2013). ANTI-SILENCING FUNCTION1 proteins are involved in ultraviolet-induced DNA damage repair and are cell cycle regulated by E2F transcription factors in Arabidopsis. Plant Physiol. 162, 1164-1177. doi: 10.1104/pp.112.212837
72. Lau, O. S., and Deng, X. W. (2012). The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 17, 584-593. doi: 10.1016/j.tplants.2012.05.004
73. Levine, M. (2011). Paused RNA polymerase II as a developmental checkpoint. Cell 145, 502-511. doi: 10.1016/j.cell.2011.04.021
74. Li, F., Mao, G., Tong, D., Huang, J., Gu, L., Yang, W.,et al. (2013a). The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSα. Cell 153, 590-600. doi: 10.1016/j.cell.2013.03.025
75. Li, J., Yang, L., Jin, D., Nezames, C. D., Terzaghi, W., and Deng, X. W. (2013b). UV-B-induced photomorphogenesis in Arabidopsis. Protein Cell 4, 485-492. doi: 10.1007/s13238-013-3036-7
76. Li, J., Ou-Lee, T. M., Raba, R., Amundson, R. G., and Last, R. L. (1993). Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5, 171-179. doi: 10.1105/tpc.5.2.171
77. Liu, N., Fromm, M., and Avramova, Z. (2014). H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of Arabidopsis thaliana. Mol. Plant 7, 502-513. doi: 10.1093/mp/ssu001
78. Lu, F., Cui, X., Zhang, S., Jenuwein, T., and Cao, X. (2011). Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43, 715-719. doi: 10.1038/ng.854
79. Luo, M., Liu, X., Singh, P., Cui, Y., Zimmerli, L., and Wu, K. (2012). Chromatin modifications and remodeling in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 129-136. doi: 10.1016/j.bbagrm.2011.06.008
80. Mahdavian, K., Ghorbanli, M., and Kalantari, K. M. (2008). Role of salicylic acid in regulating ultraviolet radiation-induced oxidative stress in pepper leaves. Russ. J. Plant Physiol. 55, 560-563. doi: 10.1134/S1021443708040195
81. Margueron, R., and Reinberg, D. (2010). Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 11, 285-296. doi: 10.1038/nrg2752
82. Margueron, R., and Reinberg, D. (2011). The polycomb complex PRC2 and its mark in life. Nature 469, 343-349. doi: 10.1038/nature09784
83. Martinez, C., Pons, E., Prats, G., and Leon, J. (2004). Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J. 37, 209-217. doi: 10.1046/j.1365-313X.2003.01954.x
84. Martinez-Luscher, J., Morales, F., Delrot, S., Sanchez-Diaz, M., Gomes, E., Aguirreolea, J.,et al. (2013). Short- and long-term physiological responses of grapevine leaves to UV-B radiation. Plant Sci. 213, 114-122. doi: 10.1016/j.plantsci.2013.08.010
85. McKenzie, R. L., Aucamp, P. J., Bais, A. F., Bjorn, L. O., Ilyas, M., and Madronich, S. (2011). Ozone depletion and climate change: impacts on UV radiation. Photochem. Photobiol. Sci. 10, 182-198. doi: 10.1039/c0pp90034f
86. Moan, J. (2001). "Visible light and UV radiation," in Radiation at Home, Outdoors and in the Workplace, eds D. Brune, R. Hellborg, B. R. R. Persson, and R. Pääkkönen (Oslo: Scandinavian Science Publisher), 69-85.
87. Molinier, J., Ries, G., Zipfel, C., and Hohn, B. (2006). Transgeneration memory of stress in plants. Nature 442, 1046-1049. doi: 10.1038/nature05022
88. Müller, R., and Goodrich, J. (2011). Sweet memories: epigenetic control in flowering. F1000 Biol. Rep. 3:13. doi: 10.3410/B3-13
89. Nawkar, G. M., Maibam, P., Park, J. H., Sahi, V. P., Lee, S. Y., and Kang, C. H. (2013). UV-induced cell death in plants. Int. J. Mol. Sci. 14, 1608-1628. doi: 10.3390/ijms14011608
90. Nawrath, C., and Métraux, J.-P. (1999). Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11, 1393-1404. doi: 10.1105/tpc.11.8.1393
91. Nechaev, S., and Adelman, K. (2011). Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim. Biophys. Acta 1809, 34-45. doi: 10.1016/j.bbagrm.2010.11.001
92. Ohlsson, A. B., Segerfeldt, P., Lindstrom, A., Borg-Karlson, A. K., and Berglund, T. (2013). UV-B exposure of indoor-grown Picea abies seedlings causes an epigenetic effect and selective emission of terpenes. Z. Naturforsch. C 68, 139-147. doi: 10.5560/ZNC.2013.68c0139
93. Pastor, V., Luna, E., Mauch-Mani, B., Ton, J., and Flors, V. (2013). Primed plants do not forget. Environ. Exp. Bot.94, 46-56. doi: 10.1016/j.envexpbot.2012.02.013
94. Pazhouhandeh, M., Molinier, J., Berr, A., and Genschik, P. (2011). MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A.108, 3430-3435. doi: 10.1073/pnas.1018242108
95. Pecinka, A., Rosa, M., Schikora, A., Berlinger, M., Hirt, H., Luschnig, C.,et al. (2009). Transgenerational stress memory is not a general response in Arabidopsis. PLoS ONE 4:e5202. doi: 10.1371/journal.pone.0005202
96. Pontin, M. A., Piccoli, P. N., Francisco, R., Bottini, R., Martinez-Zapater, J. M., and Lijavetzky, D. (2010). Transcriptome changes in grapevine (Vitis vinifera L.) cv. Malbec leaves induced by ultraviolet-B radiation. BMC Plant Biol. 10:224. doi: 10.1186/1471-2229-10-224
97. Questa, J. I., Fina, J. P., and Casati, P. (2013). DDM1 and ROS1 have a role in UV-B induced- and oxidative DNA damage in A. thaliana. Front. plant sci. 4:420. doi: 10.3389/fpls.2013.00420
98. Questa, J. I., Walbot, V., and Casati, P. (2010). Mutator transposon activation after UV-B involves chromatin remodeling. Epigenetics 5, 352-363. doi: 10.4161/epi.5.4.11751
99. Ries, G., Heller, W., Puchta, H., Sandermann, H., Seidlitz, H. K., and Hohn, B. (2000). Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98-101. doi: 10.1038/35017595
100. Rizzini, L., Favory, J. J., Cloix, C., Faggionato, D., O'Hara, A., Kaiserli, E.,et al. (2011). Perception of UV-B by theArabidopsis UVR8 protein. Science 332, 103-106. doi: 10.1126/science.1200660
101. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y., and Hunt, M. D. (1996). Systemic acquired resistance. Plant Cell 8, 1809-1819. doi: 10.1105/tpc.8.10.1809
102. Safrany, J., Haasz, V., Mate, Z., Ciolfi, A., Feher, B., Oravecz, A.,et al. (2008). Identification of a novel cis-regulatory element for UV-B-induced transcription in Arabidopsis. Plant J. 54, 402-414. doi: 10.1111/j.1365-313X.2008.03435.x
103. Sani, E., Herzyk, P., Perrella, G., Colot, V., and Amtmann, A. (2013). Hyperosmotic priming of Arabidopsisseedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 14:R59. doi: 10.1186/gb-2013-14-6-r59
104. Schäfer, E., and Nagy, F. (2006). Photomorphogenesis in Plants and Bacteria. 3rd Edn. Dordrecht: Springer.
105. Schenke, D., Cai, D., and Scheel, D. (2014). Suppression of UV-B stress responses by flg22 is regulated at the chromatin level via histone modification. Plant Cell Environ. 37, 1716-1721. doi: 10.1111/pce.12283
106. Schmidt, C. K., and Jackson, S. P. (2013). On your MARK, get SET(D2), go! H3K36me3 primes DNA mismatch repair. Cell 153, 513-515. doi: 10.1016/j.cell.2013.04.018
107. Shinkle, J. R., Edwards, M. C., Koenig, A., Shaltz, A., and Barnes, P. W. (2010). Photomorphogenic regulation of increases in UV-absorbing pigments in cucumber (Cucumis sativus) and Arabidopsis thaliana seedlings induced by different UV-B and UV-C wavebands. Physiol. Plant. 138, 113-121. doi: 10.1111/j.1399-3054.2009.01298.x
108. Sokolova, D., Vengzhen, G., and Kravets, A. (2014). The effect of DNA methylation modification polymorphism of corn seeds on their germination rate, seedling resistance and adaptive capacity under UV-C exposure. Am. J. Plant Biol. 1, 1-14.
109. Sokolova, D. A., Vengzhen, G. S., and Kravets, A. P. (2013). An analysis of the correlation between the changes in satellite DNA methylation patterns and plant cell responses to the stress. Cellbio (Irvine, Calif.) 2, 163-171. doi: 10.4236/cellbio.2013.23018
110. Song, J., Irwin, J., and Dean, C. (2013). Remembering the prolonged cold of winter. Curr. Biol. 23, R807-R811. doi: 10.1016/j.cub.2013.07.027
111. Stroud, H., Otero, S., Desvoyes, B., Ramirez-Parra, E., Jacobsen, S. E., and Gutierrez, C. (2012). Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 109, 5370-5375. doi: 10.1073/pnas.1203145109
112. Surplus, S. L., Jordan, B. R., Murphy, A. M., Carr, J. P., Thomas, B., and Mackerness, S. A. H. (1998). Ultraviolet-B-induced responses in Arabidopsis thaliana: role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ. 21, 685-694. doi: 10.1046/j.1365-3040.1998.00325.x
113. Tilbrook, K., Arongaus, A. B., Binkert, M., Heijde, M., Yin, R., and Ulm, R. (2013). The UVR8 UV-B photoreceptor: perception, signaling and response. Arabidopsis Book 11:e0164. doi: 10.1199/tab.0164
114. Ulm, R., Baumann, A., Oravecz, A., Máté, Z., Ádám, É., Oakeley, E. J.,et al. (2004). 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. 101, 1397-1402. doi: 10.1073/pnas.0308044100
115. Ulm, R., Ichimura, K., Mizoguchi, T., Peck, S. C., Zhu, T., Wang, X.,et al. (2002). Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J. 21, 6483-6493. doi: 10.1093/emboj/cdf646
116. Valledor, L., Canal, M. J., Pascual, J., Rodriguez, R., and Meijon, M. (2012). Early induced protein 1 (PrELIP1) and other photosynthetic, stress and epigenetic regulation genes are involved in Pinus radiata D. don UV-B radiation response. Physiol. Plant 146, 308-320. doi: 10.1111/j.1399-3054.2012.01629.x
117. van Dijk, K., Ding, Y., Malkaram, S., Riethoven, J. J., Liu, R., Yang, J.,et al. (2010). Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol. 10:238. doi: 10.1186/1471-2229-10-238
118. Volle, C., and Dalal, Y. (2014). Histone variants: the tricksters of the chromatin world. Curr. Opin. Genet. Dev. 25, 8-14. doi: 10.1016/j.gde.2013.11.006
119. Walbot, V. (1992). Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol. Gen. Genet.234, 353-360. doi: 10.1007/BF00538694
120. Walbot, V. (1999). UV-B damage amplified by transposons in maize. Nature 397, 398-399. doi: 10.1038/17043
121. Yalpani, N., Enyedi, A., León, J., and Raskin, I. (1994). Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193, 372-376. doi: 10.1007/BF00201815
122. Yao, Y., Danna, C. H., Zemp, F. J., Titov, V., Ciftci, O. N., Przybylski, R.,et al. (2011). UV-C-irradiated Arabidopsisand tobacco emit volatiles that trigger genomic instability in neighboring plants. Plant Cell 23, 3842-3852. doi: 10.1105/tpc.111.089003
123. Yelagandula, R., Stroud, H., Holec, S., Zhou, K., Feng, S., Zhong, X.,et al. (2014). The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158, 98-109. doi: 10.1016/j.cell.2014.06.006
124. Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y. V., Pellegrini, M., Goodrich, J.,et al. (2007). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5:e129. doi: 10.1371/journal.pbio.0050129
125. Zhou, D.-X. (2009). Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics 4, 15-18. doi: 10.4161/epi.4.1.7371
126. Zhu, J.-K. (2009). Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143-166. doi: 10.1146/annurev-genet-102108-134205
127. Zhu, Y., Dong, A., and Shen, W.-H. (2012). Histone variants and chromatin assembly in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 343-348. doi: 10.1016/j.bbagrm.2011.07.012