The physiological importance of MpUVR8 in UV-B resistance and translocation in a UV-B-dependent manner from the cytosol into the nucleus is characterized in Marchantia polymorpha.
UV RESISTANCE LOCUS 8 (UVR8) is an ultraviolet-B (UV-B) light receptor functioning for UV-B sensing and tolerance in Arabidopsis thaliana and other species. It is unclear whether UVR8 physiologically functions in UV-B-induced defense responses in Marchantia polymorpha, which belongs to the earliest diverging group of embryophyte lineages. Here, we demonstrate that UVR8 has a physiological function in UV-B tolerance and that there is a UVR8-dependent pathway involved. In addition, a UVR8-independent pathway is revealed. We examine the tissue-specific expression pattern of M. polymorpha UVR8 (MpUVR8), showing that it is highly expressed in the apical notch in thalli and gametangiophores, as well as in antheridial and archegonial heads. Furthermore, Mpuvr8KO plant transformants, in which the MpUVR8 locus was disrupted, were produced and analyzed to understand the physiological and molecular function of MpUVR8. Analysis using these plants indicates the important roles of MpUVR8 and MpUVR8-regulated genes, and of MpUVR8-independent pathways in UV-B tolerance. Subcellular localization of Citrine-fused MpUVR8 in M. polymorpha cells was also investigated. It was found to translocate from the cytosol into the nucleus in response to UV-B irradiation. Our findings indicate strong conservation of the physiological function of UVR8 and the molecular mechanisms for UVR8-dependent signal transduction through regulation of gene expression in embryophytes.
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CONSTITUTIVELY PHOTOMORPHOGENIC 1
Cyclobutane pyrimidine dimers
ELONGATED HYPOCOTYL 5
Reactive oxygen species
Albert NW, Thrimawithana AH, McGhie TK, Clayton WA, Deroles SC, Schwinn KE, Bowman JL, Jordan BR, Davies KM (2018) Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytol 218(2):554–566. https://doi.org/10.1111/nph.15002
Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB, Niyogi KK, Ulm R, Goldschmidt-Clermont M (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 113(51):14864–14869. https://doi.org/10.1073/pnas.1607695114
Bernula P, Crocco CD, Arongaus AB, Ulm R, Nagy F, Viczian A (2017) Expression of the UVR8 photoreceptor in different tissues reveals tissue-autonomous features of UV-B signalling. Plant Cell Environ 40(7):1104–1114. https://doi.org/10.1111/pce.12904
Binkert M, Kozma-Bognar L, Terecskei K, De Veylder L, Nagy F, Ulm R (2014) UV-B-responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. Plant Cell 26(10):4200–4213. https://doi.org/10.1105/tpc.114.130716
Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12(12):2383–2394. https://doi.org/10.1105/tpc.12.12.2383
Bowman JL, Kohchi T, Yamato KT et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171(2):287–304.e215. https://doi.org/10.1016/j.cell.2017.09.030
Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Physiol Plant Mol Biol 47:75–100. https://doi.org/10.1146/annurev.arplant.47.1.75
Brosché M, Strid A (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117:1–10. https://doi.org/10.1034/j.1399-3054.2003.1170101.x
Brown BA, Jenkins GI (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(2):576–588. https://doi.org/10.1104/pp.107.108456
Brown BA, Cloix C, Jiang GH, Kaiserli E, Herzyk P, Kliebenstein DJ, Jenkins GI (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA 102(50):18225–18230. https://doi.org/10.1073/pnas.0507187102
Chiyoda S, Ishizaki K, Kataoka H, Yamato KT, Kohchi T (2008) Direct transformation of the liverwort Marchantia polymorpha L. by particle bombardment using immature thalli developing from spores. Plant Cell Rep 27(9):1467–1473. https://doi.org/10.1007/s00299-008-0570-5
Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335(6075):1492–1496. https://doi.org/10.1126/science.1218091
Clayton WA, Albert NW, Thrimawithana AH, McGhie TK, Deroles SC, Schwinn KE, Warren BA, McLachlan ARG, Bowman JL, Jordan BR, Davies KM (2018) UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. Plant J 96(3):503–517. https://doi.org/10.1111/tpj.14044
Coffey A, Prinsen E, Jansen MAK, Conway J (2017) The UVB photoreceptor UVR8 mediates accumulation of UV-absorbing pigments, but not changes in plant morphology, under outdoor conditions. Plant Cell Environ 40(10):2250–2260. https://doi.org/10.1111/pce.13025
Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, Albert A, Cloix C, Jenkins GI, Oakeley EJ, Seidlitz HK, Nagy F, Ulm R (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28(5):591–601. https://doi.org/10.1038/emboj.2009.4
Fernandez MB, Tossi V, Lamattina L, Cassia R (2016) A comprehensive phylogeny reveals functional conservation of the UV-B photoreceptor UVR8 from green algae to higher plants. Front Plant Sci 7:1698. https://doi.org/10.3389/fpls.2016.01698
Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133(4):1420–1428. https://doi.org/10.1104/pp.103.030049
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50(1):151–158. https://doi.org/10.1016/0014-4827(68)90403-5
Heijde M, Binkert M, Yin R, Ares-Orpel F, Rizzini L, Van De Slijke E, Persiau G, Nolf J, Gevaert K, De Jaeger G, Ulm R (2013) Constitutively active UVR8 photoreceptor variant in Arabidopsis. Proc Natl Acad Sci USA 110(50):20326–20331
Hideg E, Jansen MA, Strid A (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18(2):107–115. https://doi.org/10.1016/j.tplants.2012.09.003
Hidema J, Taguchi T, Ono T, Teranishi M, Yamamoto K, Kumagai T (2007) Increase in CPD photolyase activity functions effectively to prevent growth inhibition caused by UVB radiation. Plant J 50(1):70–79. https://doi.org/10.1111/j.1365-313X.2007.03041.x
Ishizaki K, Chiyoda S, Yamato KT, Kohchi T (2008) Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol 49(7):1084–1091. https://doi.org/10.1093/pcp/pcn085
Ishizaki K, Nonomura M, Kato H, Yamato KT, Kohchi T (2012) Visualization of auxin-mediated transcriptional activation using a common auxin-responsive reporter system in the liverwort Marchantia polymorpha. J Plant Res 125(5):643–651. https://doi.org/10.1007/s10265-012-0477-7
Ishizaki K, Johzuka-Hisatomi Y, Ishida S, Iida S, Kohchi T (2013) Homologous recombination-mediated gene targeting in the liverwort Marchantia polymorpha L. Sci Rep 3:1532. https://doi.org/10.1038/srep01532
Ishizaki K, Nishihama R, Ueda M, Inoue K, Ishida S, Nishimura Y, Shikanai T, Kohchi T (2015) Development of Gateway binary vector series with four different selection markers for the liverwort Marchantia polymorpha. PLoS One 10(9):e0138876. https://doi.org/10.1371/journal.pone.0138876
Ishizaki K, Nishihama R, Yamato KT, Kohchi T (2016) Molecular genetic tools and techniques for Marchantia polymorpha research. Plant Cell Physiol 57(2):262–270. https://doi.org/10.1093/pcp/pcv097
Jansen M (2002) Ultraviolet-B radiation effects on plants: induction of morphogenic responses. Physiol Plant 116:423–429. https://doi.org/10.1034/j.1399-3054.2002.1160319.x
Jenkins GI (2008) Environmental regulation of flavonoid biosynthesis. In: Givens DI, Minihane AM, Shaw E (eds) Health benefits of organic food: effects of the environment. CABI, Wallingford, pp 1147–1155
Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431. https://doi.org/10.1146/annurev.arplant.59.032607.092953
Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26(1):21–37. https://doi.org/10.1105/tpc.113.119446
Jenkins GI, Brown BA (2007) UV-B perception and signal transduction. Light and plant development. Annual Plant Review, vol 30. Blackwell, Oxford, pp 155–182. https://doi.org/10.1002/9780470988893.ch7
Jordan BR (1996) The effects of ultraviolet-B radiation on plants: a molecular perspective. Adv Bot Res 22:97–162
Kaiserli E, Jenkins GI (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(8):2662–2673. https://doi.org/10.1105/tpc.107.053330
Kliebenstein DJ, Lim JE, Landry LG, Last RL (2002) Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol 130(1):234–243. https://doi.org/10.1104/pp.005041
Kubo H, Nozawa S, Hiwatashi T, Kondou Y, Nakabayashi R, Mori T, Saito K, Takanashi K, Kohchi T, Ishizaki K (2018) Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha. J Plant Res 131(5):849–864. https://doi.org/10.1007/s10265-018-1044-7
Kubota A, Ishizaki K, Hosaka M, Kohchi T (2013) Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating thalli. Biosci Biotechnol Biochemy 77(1):167–172. https://doi.org/10.1271/bbb.120700
Kucera B, Leubner-Metzger G, Wellmann E (2003) Distinct ultraviolet-signaling pathways in bean leaves. DNA damage is associated with beta-1,3-glucanase gene induction, but not with flavonoid formation. Plant Physiol 133(4):1445–1452. https://doi.org/10.1104/pp.103.029520
Li N, Teranishi M, Yamaguchi H, Matsushita T, Watahiki MK, Tsuge T, Li SS, Hidema J (2015) UV-B-induced CPD photolyase gene expression is regulated by UVR8-dependent and -independent pathways in Arabidopsis. Plant Cell Physiol 56(10):2014–2023. https://doi.org/10.1093/pcp/pcv121
Oravecz A, Baumann A, Mate Z, Brzezinska A, Molinier J, Oakeley EJ, Adam E, Schafer E, Nagy F, Ulm R (2006) CONSTITUTIVELY PHOTOMORPHOGENIC 1 is required for the UV-B response in Arabidopsis. Plant Cell 18(8):1975–1990. https://doi.org/10.1105/tpc.105.040097
Paul ND, Gwyn-Jones D (2003) Ecological roles of solar UV radiation: towards an integrated approach. Trends Ecol Evol 18:48–55
Qiu YL, Li L, Wang B et al (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103(42):15511–15516. https://doi.org/10.1073/pnas.0603335103
Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schafer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332(6025):103–106. https://doi.org/10.1126/science.1200660
Robson TM, Klem K, Urban O, Jansen MA (2015) Re-interpreting plant morphological responses to UV-B radiation. Plant Cell Environ 38(5):856–866. https://doi.org/10.1111/pce.12374
Rozema J, van de Staaij J, Bjorn LO, Caldwell M (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol Evol 12(1):22–28. https://doi.org/10.1016/S0169-5347(96)10062-8
Saint-Marcoux D, Proust H, Dolan L, Langdale JA (2015) Identification of reference genes for real-time quantitative PCR experiments in the liverwort Marchantia polymorpha. PLoS One 10(3):e0118678. https://doi.org/10.1371/journal.pone.0118678
Sancar A (2004) Photolyase and cryptochrome blue-light photoreceptors. Adv Protein Chem 69:73–100. https://doi.org/10.1016/S0065-3233(04)69003-6
Soriano G, Cloix C, Heilmann M, Nunez-Olivera E, Martinez-Abaigar J, Jenkins GI (2017) Evolutionary conservation of structure and function of the UVR8 photoreceptor from the liverwort Marchantia polymorpha and the moss Physcomitrella patens. New Phytol. https://doi.org/10.1111/nph.14767
Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R (2010) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ 33(1):88–103. https://doi.org/10.1111/j.1365-3040.2009.02061.x
Tilbrook K, Dubois M, Crocco CD, Yin R, Chappuis R, Allorent G, Schmid-Siegert E, Goldschmidt-Clermont M, Ulm R (2016) UV-B perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28(4):966–983. https://doi.org/10.1105/tpc.15.00287
Ulm R, Nagy F (2005) Signalling and gene regulation in response to ultraviolet light. Curr Opin Plant Biol 8(5):477–482. https://doi.org/10.1016/j.pbi.2005.07.004
Wickett NJ, Mirarab S, Nguyen N et al (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci USA 111(45):E4859–E4868. https://doi.org/10.1073/pnas.1323926111
Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P, Deng H, Wang J, Deng X, Shi Y (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484(7393):214–219. https://doi.org/10.1038/nature10931
Yin R, Ulm R (2017) How plants cope with UV-B: from perception to response. Curr Opin Plant Biol 37:42–48. https://doi.org/10.1016/j.pbi.2017.03.013
Yin R, Arongaus AB, Binkert M, Ulm R (2015) Two distinct domains of the UVR8 photoreceptor interact with COP1 to initiate UV-B signaling in Arabidopsis. Plant Cell 27(1):202–213. https://doi.org/10.1105/tpc.114.133868
Yin R, Skvortsova MY, Loubery S, Ulm R (2016) COP1 is required for UV-B-induced nuclear accumulation of the UVR8 photoreceptor. Proc Natl Acad Sci USA 113(30):E4415–E4422. https://doi.org/10.1073/pnas.1607074113
We appreciate the helpful discussions with Jun Hidema, Mika Teranishi, Shohei Yamaoka, Tianhong Li and Shinya Takahashi. We also thank Tatsuya Takizawa, Yasumasa Uemura, Moemi Sekikawa, Keisuke Takeda, Masahiko Ebisawa, Miho Yamaoki, Syun Sugama, Toshiki Takeda, Seika Sadahisa, Koichiro Seto, Syota Takei, Takao Masuda, Masaki Ishida, and Syota Yokoi for technical support. This work was supported by JSPS KAKENHI Grant no. 25450158 to YK and 17K15145 to KI.
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Kondou, Y., Miyagi, Y., Morito, T. et al. Physiological function of photoreceptor UVR8 in UV-B tolerance in the liverwort Marchantia polymorpha. Planta 249, 1349–1364 (2019). https://doi.org/10.1007/s00425-019-03090-w
- Land plant
- Nuclear translocation
- UV-B-absorbing compounds
- UV-B signal transduction
- UVR8-independent pathway