Abstract
UV-B exposure of plants regulates expression of numerous genes concerned with various responses. Sudden exposure of non-acclimated plants to high fluence rate, short wavelength UV-B induces expression via stress-related signaling pathways that are not specific to the UV-B stimulus, whereas low fluence rates of UV-B can regulate expression via the UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8). However, there is little information about whether non-stressful, low fluence rate UV-B treatments can activate gene expression independently of UVR8. Here, transcriptomic analysis of wild-type and uvr8 mutant Arabidopsis exposed to low fluence rate UV-B showed that numerous genes were regulated independently of UVR8. Moreover, nearly all of these genes were distinct to those induced by stress treatments. A small number of genes were expressed at all UV-B fluence rates employed and may be concerned with activation of eustress responses that facilitate acclimation to changing conditions. Expression of the gene encoding the transcription factor ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN 13 (ANAC13) was studied to characterise a low fluence rate, UVR8-independent response. ANAC13 is induced by as little as 0.1 μmol m−2 s−1 UV-B and its regulation is independent of components of the canonical UVR8 signaling pathway COP1 and HY5/HYH. Furthermore, UV-B induced expression of ANAC13 is independent of the photoreceptors CRY1, CRY2, PHOT1 and PHOT2 and phytochromes A, B, D and E. ANAC13 expression is induced over a range of UV-B wavelengths at low doses, with maximum response at 310 nm. This study provides a basis for further investigation of UVR8 and stress independent, low fluence rate UV-B signaling pathway(s).
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L. Rizzini, J.-J. Favory, C. Cloix, D. Faggionato, A. O’Hara, E. Kaiserli, R. Baumeister, E. Schäfer, F. Nagy, G. I. Jenkins and R. Ulm, Science, 2011, 332, 103–106.
J. M. Christie, A. S. Arvai, K. J. Baxter, M. Heilmann, A. J. Pratt, A. O’Hara, S. M. Kelly, M. Hothorn, B. O. Smith, K. Hitomi, G. I. Jenkins and E. D. Getzoff, Science, 2012, 335, 1492–1496.
D. Wu, Q. Hu, Z. Yan, W. Chen, C. Yan, X. Huang, J. Zhang, P. Yang, H. Deng, J. Wang, X. W. Deng and Y. Shi, Nature, 2012, 484, 214–219.
D. J. Kliebenstein, J. E. Lim, L. G. Landry and R. L. Last, Plant Physiol., 2002, 130, 234–243.
P. V. Demkura and C. L. Ballaré, Mol. Plant, 2002, 5, 642–652.
L. O. Morales, M. Brosché, J. Vainonen, G. I. Jenkins, J. J. Wargent, N. Sipari, Å. Strid, A. V. Lindfors, R. Tegelberg and P. J. Aphalo, Plant Physiol., 2013, 161, 744–7597.
G. I. Jenkins, Plant Cell, 2014, 26, 21–37.
S. Hayes, A. Sharma, D. P. Fraser, M. Trevisan, C. K. Cragg-Barber, E. Tavridou, C. Fankhauser, G. I. Jenkins and K. A. Franklin, Curr. Biol., 2016, 27, 120–127.
G. I. Jenkins, Plant, Cell Environ., 2017, 40, 2544–2557.
R. Yin and R. Ulm, Curr. Opin. Plant Biol., 2017, 37, 42–48.
M. Wu, Å. Strid and L. A. Eriksson, J. Phys. Chem. B, 2014, 118, 951–965.
T. Mathes, M. Heilmann, A. Pandit, J. Zhu, J. Ravensbergen, M. Klos, Y. Fu, B. O. Smith, J. M. Christie, G. I. Jenkins and J. T. M. Kennis, J. Am. Chem. Soc., 2015, 137, 8113–8120.
X. Zeng, Z. Ren, Q. Wu, J. Fan, P. Peng, K. Tang, R. Zhang, K.-H. Zhao and X. Yang, Nat. Plants, 2015, 1, 14006.
A. Oravecz, A. Baumann, Z. Máté, A. Brzezinska, J. Molinier, E. J. Oakeley, É. Adám, E. Schäfer, F. Nagy and R. Ulm, Plant Cell, 2006, 18, 1975–1990.
J. J. Favory, A. Stec, H. Gruber, L. Rizzini, A. Oravecz, M. Funk, A. Albert, C. Cloix, G. I. Jenkins, E. J. Oakeley, H. K. Seidlitz, F. Nagy and R. Ulm, EMBO J., 2009, 28, 591–601.
C. Cloix, E. Kaiserli, M. Heilmann, K. J. Baxter, B. A. Brown, A. O’Hara, B. O. Smith, J. M. Christie and G. I. Jenkins, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 16366–16370.
R. Yin, M. Y. Skvortsova, S. Loubéry and R. Ulm, Proc. Natl. Acad. Sci. U. S. A., 2016, 113, E4415–E4422.
B. A. Brown, C. Cloix, G. H. Jiang, E. Kaiserli, P. Herzyk, D. J. Kliebenstein and G. I. Jenkins, Proc. Natl. Acad. Sci. U. S. A., 2005, 102, 18225–18230.
Y. Yang, T. Liang, L. Zhang, K. Shao, X. Gu, R. Shang, N. Shi, X. Li, P. Zhang and H. Liu, Nat. Plants, 2018, 4, 980–107.
T. Liang, S. Mei, C. Shi, Y. Yang, Y. Peng, L. Ma, F. Wang, X. Li, X. Huang, Y. Yin and H. Liu, Dev. Cell, 2018, 44, 1–12.
B. Fehér, L. Kozma-Bognár, E. Kevei, A. Hajdu, M. Binkert, S. J. Davis, E. Schäfer, R. Ulm and F. Nagy, Plant J., 2011, 67, 37–48.
A. O’Hara and G. I. Jenkins, Plant Cell, 2012, 24, 3755–3766.
J. J. Wargent, V. C. Gegas, G. I. Jenkins, J. H. Doonan and N. D. Paul, New Phytol., 2009, 183, 315–326.
R. Ulm, A. Baumann, A. Oravecz, Z. Mate, E. Adam, E. J. Oakeley, E. Schäfer and F. Nagy, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 1397–1402.
B. A. Brown and G. I. Jenkins, Plant Physiol., 2008, 146, 576–588.
J. Kilian, D. Whitehead, J. Horak, D. Wanke, S. Weinl, O. Batistic, C. D’Angelo, E. Bornberg-Bauer, J. Kudla and K. Harter, Plant J., 2007, 50, 347–363.
J. Safrany, V. Haasz, Z. Mate, A. Ciolfi, B. Feher, A. Oravecz, A. Stec, G. Dallmann, G. Morelli, R. Ulm and F. Nagy, Plant J., 2008, 54, 402–414.
J. Takeda, R. Nakata, H. Ueno, A. Murakami, M. Iseki and M. Watanabe, Photochem. Photobiol., 2014, 90, 1043–1049.
N. Rai, S. Neugart, Y. Yan, F. Wang, S. M. Siipola, A. V. Lindfors, J. B. Winkler, A. Albert, M. Brosché, T. Lehto, L. O. Morales and P. J. Aphalo, J. Exp. Bot., 2019, DOI: 10.1093/jxb/erz236.
K. A. Franklin, U. Praekelt, W. M. Stoddart, O. E. Billingham, K. J. Halliday and G. C. Whitelam, Plant Physiol., 2003, 131, 1340–1346.
H. K. Wade, A. K. Sohal and G. I. Jenkins, Plant Physiol., 2003, 131, 707–715.
T. Kagawa, T. Sakai, N. Suetsugu, K. Oikawa, S. Ishiguro, T. Kato, S. Tabata, K. Okada and M. Wada, Science, 2001, 291, 2138–2141.
M. Holm, C. Hardtke, R. Gaudet and X. W. Deng, EMBO J., 2001, 20, 118–127.
X. W. Deng and P. H. Quail, Plant J., 1992, 2, 83–95.
L. A. Díaz-Ramos, A. O’Hara, S. Kanagarajan, D. Farkas, Å. Strid and G. I. Jenkins, Photochem. Photobiol. Sci., 2018, 17, 1108–1117.
R. A. Irizarry, B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs and T. P. Speed, Nucleic Acids Res., 2003, 31, e15.
R. Breitling, P. Armengaud, A. Amtmann and P. Herzyk, FEBS Lett., 2004, 573, 83–92.
P. Bardou, J. Mariette, F. Escudié, C. Djemiel and C. Klopp, BMC Bioinf., 2014, 15, 293.
G. Yu, L.-G. Wang, Y. Han and Q.-Y. He, OMICS, 2012, 16, 284–287.
K. Hectors, E. Prinsen, W. De Coen, M. A. K. Jansen and Y. Guisez, New Phytol., 2007, 175, 255–270.
M. Brosché and Å. Strid, Physiol. Plant., 2003, 117, 1–10.
G. I. Jenkins, Annu. Rev. Plant Biol., 2009, 60, 407–431.
R. Ulm and F. Nagy, Curr. Opin. Plant Biol., 2005, 8, 477–482.
M. A. González-Besteiro, S. Bartels, A. Albert and R. Ulm, Plant J., 2011, 68, 727–737.
É. Hideg, M. A. K. Jansen and Å. Strid, Trends Plant Sci., 2013, 18, 107–115.
A. N. Olsen, H. A. Ernst, L. L. Leggio and K. Skriver, Trends Plant Sci., 2005, 10, 79–87.
H. Ooka, K. Satoh, K. Doi, T. Nagata, Y. Otomo, K. Murakami, K. Matsubara, N. Osato, J. Kawai, P. Carninci, Y. Hayashizaki, K. Suzuki, K. Kojima, Y. Takahara, K. Yamamoto and S. Kikuchi, DNA Res., 2003, 10, 239–247.
K. Nakashima, H. Takasaki, J. Mizoi, K. Shinozaki and K. Yamaguchi-Shinozaki, Biochim. Biophys. Acta, 2012, 1819, 97–10.
I. De Clercq, V. Vermeirssen, O. Van Aken, K. Vandepoele, M. W. Murcha, S. R. Law, A. Inzé, S. Ng, A. Ivanova, D. Rombaut, B. van de Cotte, P. Jaspers, Y. Van de Peer, J. Kangasjärvi, J. Whelan and F. Van Breusegem, Plant Cell, 2013, 25, 3472–3490.
C. O’Shea, L. Staby, S. K. Bendsen, F. G. Tidemand, A. Redsted, M. Willemoës, B. B. Kragelund and K. Skriver, Biochem. J., 2015, 465, 281–294.
S. G. Yu and L. O. Björn, J. Photochem. Photobiol., B, 1997, 37, 212–218.
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O’Hara, A., Headland, L.R., Díaz-Ramos, L.A. et al. Regulation of Arabidopsis gene expression by low fluence rate UV-B independently of UVR8 and stress signaling. Photochem Photobiol Sci 18, 1675–1684 (2019). https://doi.org/10.1039/c9pp00151d
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DOI: https://doi.org/10.1039/c9pp00151d