1932

Abstract

Ultraviolet-B (UV-B) radiation is an intrinsic fraction of sunlight that plants perceive through the UVR8 photoreceptor. UVR8 is a homodimer in its ground state that monomerizes upon UV-B photon absorption via distinct tryptophan residues. Monomeric UVR8 competitively binds to the substrate binding site of COP1, thus inhibiting its E3 ubiquitin ligase activity against target proteins, which include transcriptional regulators such as HY5. The UVR8–COP1 interaction also leads to the destabilization of PIF bHLH factor family members. Additionally, UVR8 directly interacts with and inhibits the DNA binding of a different set of transcription factors. Each of these UVR8 signaling mechanisms initiates nuclear gene expression changes leading to UV-B-induced photomorphogenesis and acclimation. The two WD40-repeat proteins RUP1 and RUP2 provide negative feedback regulation and inactivate UVR8 by facilitating redimerization. Here, we review the molecular mechanisms of the UVR8 pathway from UV-B perception and signal transduction to gene expression changes and physiological UV-B responses.

Keyword(s): acclimationCOP1HY5photoreceptorUV-BUVR8
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050718-095946
2021-06-17
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-050718-095946.html?itemId=/content/journals/10.1146/annurev-arplant-050718-095946&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abbas N, Maurya JP, Senapati D, Gangappa SN, Chattopadhyay S. 2014. Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cell 26:1036–52
    [Google Scholar]
  2. 2. 
    Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB et al. 2016. UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. PNAS 113:14864–69Demonstrates that Chlamydomonas UVR8 signaling induces key nonphotochemical quenching genes and thereby promotes photoprotection in high light.
    [Google Scholar]
  3. 3. 
    Allorent G, Petroutsos D. 2017. Photoreceptor-dependent regulation of photoprotection. Curr. Opin. Plant Biol. 37:102–8
    [Google Scholar]
  4. 4. 
    Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K et al. 1998. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1:213–22
    [Google Scholar]
  5. 5. 
    Aphalo PJ 2017. Quantification of UV radiation. UV-B Radiation and Plant Life: Molecular Biology to Ecology BR Jordan 10–22 Egham, UK: CABI.
    [Google Scholar]
  6. 6. 
    Arongaus AB, Chen S, Pireyre M, Glöckner N, Galvão VC et al. 2018. Arabidopsis RUP2 represses UVR8-mediated flowering in noninductive photoperiods. Genes Dev 32:1332–43
    [Google Scholar]
  7. 7. 
    Ballaré CL, Mazza CA, Austin AT, Pierik R. 2012. Canopy light and plant health. Plant Physiol 160:145–55
    [Google Scholar]
  8. 8. 
    Bernula P, Crocco CD, Arongaus AB, Ulm R, Nagy F, Viczián A. 2017. Expression of the UVR8 photoreceptor in different tissues reveals tissue-autonomous features of UV-B signalling. Plant Cell Environ 40:1104–14
    [Google Scholar]
  9. 9. 
    Binkert M, Crocco CD, Ekundayo B, Lau K, Raffelberg S et al. 2016. Revisiting chromatin binding of the Arabidopsis UV-B photoreceptor UVR8. BMC Plant Biol 16:42
    [Google Scholar]
  10. 10. 
    Binkert M, Kozma-Bognár 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 26:4200–13
    [Google Scholar]
  11. 11. 
    Bornman JF, Barnes PW, Robson TM, Robinson SA, Jansen MAK et al. 2019. Linkages between stratospheric ozone, UV radiation and climate change and their implications for terrestrial ecosystems. Photochem. Photobiol. Sci. 18:681–716
    [Google Scholar]
  12. 12. 
    Brown BA, Cloix C, Jiang GH, Kaiserli E, Herzyk P et al. 2005. A UV-B-specific signaling component orchestrates plant UV protection. PNAS 102:18225–30Shows that UVR8 is a UV-B-specific signaling component and that HY5 is a key effector of the UVR8 pathway.
    [Google Scholar]
  13. 13. 
    Brown BA, Headland LR, Jenkins GI. 2009. UV-B action spectrum for UVR8-mediated HY5 transcript accumulation in Arabidopsis. Photochem. Photobiol. 85:1147–55
    [Google Scholar]
  14. 14. 
    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 146:576–88
    [Google Scholar]
  15. 15. 
    Burko Y, Seluzicki A, Zander M, Pedmale UV, Ecker JR, Chory J. 2020. Chimeric activators and repressors define HY5 activity and reveal a light-regulated feedback mechanism. Plant Cell 32:967–83
    [Google Scholar]
  16. 16. 
    Bursch K, Toledo-Ortiz G, Pireyre M, Lohr M, Braatz C, Johansson H. 2020. Identification of BBX proteins as rate-limiting cofactors of HY5. Nat. Plants 6:921–28
    [Google Scholar]
  17. 17. 
    Camacho IS, Theisen A, Johannissen LO, Díaz-Ramos LA, Christie JM et al. 2019. Native mass spectrometry reveals the conformational diversity of the UVR8 photoreceptor. PNAS 116:1116–25
    [Google Scholar]
  18. 18. 
    Chen D, Gibson ES, Kennedy MJ. 2013. A light-triggered protein secretion system. J. Cell Biol. 201:631–40
    [Google Scholar]
  19. 19. 
    Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS et al. 2010. Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22:108–23
    [Google Scholar]
  20. 20. 
    Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ et al. 2012. Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–96Describes X-ray structures of homodimers of the UVR8 core and the monomerization mechanism of the recombinant proteins.
    [Google Scholar]
  21. 21. 
    Clayton WA, Albert NW, Thrimawithana AH, McGhie TK, Deroles SC et al. 2018. UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. Plant J 96:503–17
    [Google Scholar]
  22. 22. 
    Cloix C, Jenkins GI. 2008. Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. Mol. Plant 1:118–28
    [Google Scholar]
  23. 23. 
    Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA et al. 2012. C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein. PNAS 109:16366–70
    [Google Scholar]
  24. 24. 
    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 40:2250–60
    [Google Scholar]
  25. 25. 
    Crefcoeur RP, Yin R, Ulm R, Halazonetis TD. 2013. Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat. Commun. 4:1779
    [Google Scholar]
  26. 26. 
    Davey MP, Susanti NI, Wargent JJ, Findlay JE, Quick WP et al. 2012. The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B. Photosynth. Res. 114:121–31
    [Google Scholar]
  27. 27. 
    Demarsy E, Goldschmidt-Clermont M, Ulm R. 2018. Coping with ‘dark sides of the sun’ through photoreceptor signaling. Trends Plant Sci 23:260–71
    [Google Scholar]
  28. 28. 
    Demkura PV, Ballaré CL. 2012. UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol. Plant 5:116–26
    [Google Scholar]
  29. 29. 
    Díaz-Ramos LA, O'Hara A, Kanagarajan S, Farkas D, Strid Å, Jenkins GI 2018. Difference in the action spectra for UVR8 monomerisation and HY5 transcript accumulation in Arabidopsis. Photochem. Photobiol. Sci. 17:1108–17
    [Google Scholar]
  30. 30. 
    Dotto M, Gómez MS, Soto MS, Casati P. 2018. UV-B radiation delays flowering time through changes in the PRC2 complex activity and miR156 levels in Arabidopsis thaliana. Plant Cell Environ 41:1394–406
    [Google Scholar]
  31. 31. 
    Duek PD, Elmer MV, van Oosten VR, Fankhauser C. 2004. The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr. Biol. 14:2296–301
    [Google Scholar]
  32. 32. 
    Enderle B, Sheerin DJ, Paik I, Kathare PK, Schwenk P et al. 2017. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nat. Commun. 8:2221
    [Google Scholar]
  33. 33. 
    Fairchild CD, Schumaker MA, Quail PH. 2000. HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14:2377–91
    [Google Scholar]
  34. 34. 
    Fankhauser C, Christie JM. 2015. Plant phototropic growth. Curr. Biol. 25:R384–89
    [Google Scholar]
  35. 35. 
    Fasano R, Gonzalez N, Tosco A, Dal Piaz F, Docimo T et al. 2014. Role of Arabidopsis UV RESISTANCE LOCUS 8 in plant growth reduction under osmotic stress and low levels of UV-B. Mol. Plant 7:773–91
    [Google Scholar]
  36. 36. 
    Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A et al. 2009. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28:591–601Shows that UVR8 and COP1 directly interact and that UVR8 functions in UV-B acclimation and the inhibition of hypocotyl elongation.
    [Google Scholar]
  37. 37. 
    Fehér B, Kozma-Bognár L, Kevei É, Hajdu A, Binkert M et al. 2011. Functional interaction of the circadian clock and UV RESISTANCE LOCUS 8-controlled UV-B signaling pathways in Arabidopsis thaliana. Plant J 67:37–48
    [Google Scholar]
  38. 38. 
    Fernández 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
    [Google Scholar]
  39. 39. 
    Fierro AC, Leroux O, De Coninck B, Cammue BP, Marchal K et al. 2015. Ultraviolet-B radiation stimulates downward leaf curling in Arabidopsis thaliana. Plant Physiol. Biochem. 93:9–17
    [Google Scholar]
  40. 40. 
    Findlay KM, Jenkins GI. 2016. Regulation of UVR8 photoreceptor dimer/monomer photo-equilibrium in Arabidopsis plants grown under photoperiodic conditions. Plant Cell Environ 39:1706–14
    [Google Scholar]
  41. 41. 
    Gabilly ST, Baker CR, Wakao S, Crisanto T, Guan K et al. 2019. Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. PNAS 116:17556–62
    [Google Scholar]
  42. 42. 
    Galvão VC, Fankhauser C. 2015. Sensing the light environment in plants: photoreceptors and early signaling steps. Curr. Opin. Neurobiol. 34:46–53
    [Google Scholar]
  43. 43. 
    González Besteiro MA, Bartels S, Albert A, 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 68:727–37
    [Google Scholar]
  44. 44. 
    González Besteiro MA, Ulm R 2013. ATR and MKP1 play distinct roles in response to UV-B stress in Arabidopsis. Plant J 73:1034–43
    [Google Scholar]
  45. 45. 
    Greiner A, Kelterborn S, Evers H, Kreimer G, Sizova I, Hegemann P. 2017. Targeting of photoreceptor genes in Chlamydomonas reinhardtii via zinc-finger nucleases and CRISPR/Cas9. Plant Cell 29:2498–518
    [Google Scholar]
  46. 46. 
    Gruber H, Heijde M, Heller W, Albert A, Seidlitz HK, Ulm R 2010. Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. PNAS 107:20132–37
    [Google Scholar]
  47. 47. 
    Han X, Chang X, Zhang Z, Chen H, He H et al. 2019. Origin and evolution of core components responsible for monitoring light environment changes during plant terrestrialization. Mol. Plant 12:847–62
    [Google Scholar]
  48. 48. 
    Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B et al. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–13
    [Google Scholar]
  49. 49. 
    Hayes S, Sharma A, Fraser DP, Trevisan M, Cragg-Barber CK et al. 2017. UV-B perceived by the UVR8 photoreceptor inhibits plant thermomorphogenesis. Curr. Biol. 27:120–27
    [Google Scholar]
  50. 50. 
    Hayes S, Velanis CN, Jenkins GI, Franklin KA 2014. UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance. PNAS 111:11894–99
    [Google Scholar]
  51. 51. 
    Heijde M, Binkert M, Yin R, Ares-Orpel F, Rizzini L et al. 2013. Constitutively active UVR8 photoreceptor variant in Arabidopsis. PNAS 110:20326–31
    [Google Scholar]
  52. 52. 
    Heijde M, Ulm R. 2013. Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homo-dimeric ground state. PNAS 110:1113–18Demonstrates that RUP1 and RUP2 facilitate UVR8 redimerization and ground state reversion.
    [Google Scholar]
  53. 53. 
    Heilmann M, Christie JM, Kennis JT, Jenkins GI, Mathes T. 2015. Photoinduced transformation of UVR8 monitored by vibrational and fluorescence spectroscopy. Photochem. Photobiol. Sci. 14:252–57
    [Google Scholar]
  54. 54. 
    Heilmann M, Jenkins GI. 2013. Rapid reversion from monomer to dimer regenerates the ultraviolet-B photoreceptor UV RESISTANCE LOCUS8 in intact Arabidopsis plants. Plant Physiol 161:547–55
    [Google Scholar]
  55. 55. 
    Heilmann M, Velanis CN, Cloix C, Smith BO, Christie JM, Jenkins GI. 2016. Dimer/monomer status and in vivo function of salt-bridge mutants of the plant UV-B photoreceptor UVR8. Plant J 88:71–81
    [Google Scholar]
  56. 56. 
    Heng Y, Lin F, Jiang Y, Ding M, Yan T et al. 2019. B-box containing proteins BBX30 and BBX31, acting downstream of HY5, negatively regulate photomorphogenesis in Arabidopsis. Plant Physiol 180:497–508
    [Google Scholar]
  57. 57. 
    Hoecker U. 2017. The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr. Opin. Plant Biol. 37:63–69
    [Google Scholar]
  58. 58. 
    Holm M, Ma L-G, Qu L-J, Deng X-W. 2002. Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–59
    [Google Scholar]
  59. 59. 
    Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C. 2009. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28:3893–902
    [Google Scholar]
  60. 60. 
    Hu Z, Cools T, De Veylder L. 2016. Mechanisms used by plants to cope with DNA damage. Annu. Rev. Plant Biol. 67:439–62
    [Google Scholar]
  61. 61. 
    Huang X, Ouyang X, Yang P, Lau OS, Chen L et al. 2013. Conversion from CUL4-based COP1-SPA E3 apparatus to UVR8-COP1-SPA complexes underlies a distinct biochemical function of COP1 under UV-B. PNAS 110:16669–74
    [Google Scholar]
  62. 62. 
    Huang X, Ouyang X, Yang P, Lau OS, Li G et al. 2012. Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell 24:4590–606
    [Google Scholar]
  63. 63. 
    Huang X, Yang P, Ouyang X, Chen L, Deng XW 2014. Photoactivated UVR8-COP1 module determines photomorphogenic UV-B signaling output in Arabidopsis. PLOS Genet 10:e1004218
    [Google Scholar]
  64. 64. 
    Indorf M, Cordero J, Neuhaus G, Rodríguez-Franco M. 2007. Salt tolerance (STO), a stress-related protein, has a major role in light signalling. Plant J 51:563–74
    [Google Scholar]
  65. 65. 
    Inoue S, Takemiya A, Shimazaki K. 2010. Phototropin signaling and stomatal opening as a model case. Curr. Opin. Plant Biol. 13:587–93
    [Google Scholar]
  66. 66. 
    Izumi M, Ishida H, Nakamura S, Hidema J. 2017. Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29:377–94
    [Google Scholar]
  67. 67. 
    Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W et al. 2008. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27:1277–88
    [Google Scholar]
  68. 68. 
    Jansen MAK, Gaba V, Greenberg BM. 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–35
    [Google Scholar]
  69. 69. 
    Jenkins GI. 2014. The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26:21–37
    [Google Scholar]
  70. 70. 
    Jenkins GI. 2017. Photomorphogenic responses to ultraviolet-B light. Plant Cell Environ 40:2544–57
    [Google Scholar]
  71. 71. 
    Jiang L, Wang Y, Li QF, Björn LO, He JX, Li SS. 2012. Arabidopsis STO/BBX24 negatively regulates UV-B signaling by interacting with COP1 and repressing HY5 transcriptional activity. Cell Res 22:1046–57
    [Google Scholar]
  72. 72. 
    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 19:2662–73
    [Google Scholar]
  73. 73. 
    Kim SH, Kim H, Chung S, Lee JH. 2017. DHU1 negatively regulates UV-B signaling via its direct interaction with COP1 and RUP1. Biochem. Biophys. Res. Commun. 491:285–90
    [Google Scholar]
  74. 74. 
    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 chromatincondensation 1. Plant Physiol. 130:234–43Discovered the first uvr8 mutant and UVR8 involvement in UV-B tolerance.
    [Google Scholar]
  75. 75. 
    Kondou Y, Miyagi Y, Morito T, Fujihira K, Miyauchi W et al. 2019. Physiological function of photoreceptor UVR8 in UV-B tolerance in the liverwort Marchantia polymorpha. Planta 249:1349–64
    [Google Scholar]
  76. 76. 
    Lämmermann N, Wulf D, Chang KS, Wichmann J, Jang J et al. 2020. Ubiquitin ligase component LRS1 and transcription factor CrHy5 act as a light switch for photoprotection in Chlamydomonas. bioRxiv 2020.02.10.942334. https://doi.org/10.1101/2020.02.10.942334
    [Crossref]
  77. 77. 
    Lau K, Podolec R, Chappuis R, Ulm R, Hothorn M. 2019. Plant photoreceptors and their signaling components compete for COP1 binding via VP peptide motifs. EMBO J 38:e102140
    [Google Scholar]
  78. 78. 
    Lau OS, Deng XW. 2012. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17:584–93
    [Google Scholar]
  79. 79. 
    Lee J, He K, Stolc V, Lee H, Figueroa P et al. 2007. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–49
    [Google Scholar]
  80. 80. 
    Li FC, Wang J, Wu MM, Fan CM, Li X, He JM. 2017. Mitogen-activated protein kinase phosphatases affect UV-B-induced stomatal closure via controlling NO in guard cells. Plant Physiol 173:760–70
    [Google Scholar]
  81. 81. 
    Li H, Li Y, Deng H, Sun X, Wang A et al. 2018. Tomato UV-B receptor SlUVR8 mediates plant acclimation to UV-B radiation and enhances fruit chloroplast development via regulating SlGLK2. Sci. Rep. 8:6097
    [Google Scholar]
  82. 82. 
    Li N, Teranishi M, Yamaguchi H, Matsushita T, Watahiki MK et al. 2015. UV-B-induced CPD photolyase gene expression is regulated by UVR8-dependent and -independent pathways in Arabidopsis. Plant Cell Physiol 56:2014–23
    [Google Scholar]
  83. 83. 
    Li X, Chung LW, Morokuma K, Li G. 2014. Theoretical study on the UVR8 photoreceptor: sensing ultraviolet-B by tryptophan and dissociation of homodimer. J. Chem. Theory Comput. 10:3319–30
    [Google Scholar]
  84. 84. 
    Li X, Liu Z, Ren H, Kundu M, Wang L et al. 2020. Dynamics and mechanism of light harvesting in UV photoreceptor UVR8. Chem. Sci. 11:12553–69
    [Google Scholar]
  85. 85. 
    Li X, Ren H, Kundu M, Liu Z, Zhong FW et al. 2020. A leap in quantum efficiency through light harvesting in photoreceptor UVR8. Nat. Commun. 11:4316
    [Google Scholar]
  86. 86. 
    Liang T, Mei S, Shi C, Yang Y, Peng Y et al. 2018. UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev. Cell 44:512–23.e5Shows that UVR8 directly interacts with transcription factors, inhibiting their DNA-binding activity.
    [Google Scholar]
  87. 87. 
    Liang T, Shi C, Peng Y, Tan H, Xin P et al. 2020. Brassinosteroid-activated BRI1-EMS-SUPPRESSOR 1 inhibits flavonoid biosynthesis and coordinates growth and UV-B stress responses in plants. Plant Cell 32:3224–39
    [Google Scholar]
  88. 88. 
    Liang T, Yang Y, Liu H. 2019. Signal transduction mediated by the plant UV-B photoreceptor UVR8. New Phytol 221:1247–52
    [Google Scholar]
  89. 89. 
    Liao X, Liu W, Yang HQ, Jenkins GI. 2020. A dynamic model of UVR8 photoreceptor signalling in UV-B-acclimated Arabidopsis. New Phytol 227:857–66
    [Google Scholar]
  90. 90. 
    Liao X, Zhang B, Blatt MR, Jenkins GI. 2019. A FRET method for investigating dimer/monomer status and conformation of the UVR8 photoreceptor. Photochem. Photobiol. Sci. 18:367–74
    [Google Scholar]
  91. 91. 
    Lin L, Dong H, Yang G, Yin R 2020. The C-terminal 17 amino acids of the photoreceptor UVR8 is involved in the fine-tuning of UV-B signaling. J. Integr. Plant Biol. 62:1327–40
    [Google Scholar]
  92. 92. 
    Liu LJ, Zhang YC, Li QH, Sang Y, Mao J et al. 2008. COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20:292–306
    [Google Scholar]
  93. 93. 
    Liu X, Zhang Q, Yang G, Zhang C, Dong H et al. 2020. Pivotal roles of Tomato photoreceptor SlUVR8 in seedling development and UV-B stress tolerance. Biochem. Biophys. Res. Commun. 522:177–83
    [Google Scholar]
  94. 94. 
    Liu Z, Li X, Zhong FW, Li J, Wang L et al. 2014. Quenching dynamics of ultraviolet-light perception by UVR8 photoreceptor. J. Phys. Chem. Lett. 5:69–72
    [Google Scholar]
  95. 95. 
    Loyola R, Herrera D, Mas A, Wong DC, Höll J et al. 2016. The photomorphogenic factors UV-B RECEPTOR 1, ELONGATED HYPOCOTYL 5, and HY5 HOMOLOGUE are part of the UV-B signalling pathway in grapevine and mediate flavonol accumulation in response to the environment. J. Exp. Bot. 67:5429–45
    [Google Scholar]
  96. 96. 
    Mao K, Wang L, Li YY, Wu R. 2015. Molecular cloning and functional analysis of UV RESISTANCE LOCUS 8 (PeUVR8) from Populus euphratica. PLOS ONE 10:e0132390
    [Google Scholar]
  97. 97. 
    Mathes T, Heilmann M, Pandit A, Zhu J, Ravensbergen J et al. 2015. Proton-coupled electron transfer constitutes the photoactivation mechanism of the plant photoreceptor UVR8. J. Am. Chem. Soc. 137:8113–20
    [Google Scholar]
  98. 98. 
    Mazza CA, Ballaré CL. 2015. Photoreceptors UVR8 and phytochrome B cooperate to optimize plant growth and defense in patchy canopies. New Phytol 207:4–9
    [Google Scholar]
  99. 99. 
    Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL. 2000. Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122:117–26
    [Google Scholar]
  100. 100. 
    Miyamori T, Nakasone Y, Hitomi K, Christie JM, Getzoff ED, Terazima M. 2015. Reaction dynamics of the UV-B photosensor UVR8. Photochem. Photobiol. Sci. 14:995–1004
    [Google Scholar]
  101. 101. 
    Molinier J. 2017. Genome and epigenome surveillance processes underlying UV exposure in plants. Genes 8:316
    [Google Scholar]
  102. 102. 
    Morales LO, Brosché M, Vainonen J, Jenkins GI, Wargent JJ et al. 2013. Multiple roles for UV RESISTANCE LOCUS8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar ultraviolet radiation. Plant Physiol 161:744–59
    [Google Scholar]
  103. 103. 
    Moriconi V, Binkert M, Costigliolo C, Sellaro R, Ulm R, Casal JJ. 2018. Perception of sunflecks by the UV-B photoreceptor UV RESISTANCE LOCUS8. Plant Physiol 177:75–81
    [Google Scholar]
  104. 104. 
    Müller K, Engesser R, Schulz S, Steinberg T, Tomakidi P et al. 2013. Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res 41:e124
    [Google Scholar]
  105. 105. 
    Oakenfull RJ, Davis SJ. 2017. Shining a light on the Arabidopsis circadian clock. Plant Cell Environ 40:2571–85
    [Google Scholar]
  106. 106. 
    O'Hara A, Headland LR, Díaz-Ramos LA, Morales LO, Strid Å, Jenkins GI. 2019. Regulation of Arabidopsis gene expression by low fluence rate UV-B independently of UVR8 and stress signaling. Photochem. Photobiol. Sci. 18:1675–84
    [Google Scholar]
  107. 107. 
    O'Hara A, Jenkins GI. 2012. In vivo function of tryptophans in the Arabidopsis UV-B photoreceptor UVR8. Plant Cell 24:3755–66
    [Google Scholar]
  108. 108. 
    Olsen JL, Rouzé P, Verhelst B, Lin YC, Bayer T et al. 2016. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331–35
    [Google Scholar]
  109. 109. 
    Oravecz A, Baumann A, Máté Z, Brzezinska A, Molinier J et al. 2006. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18:1975–90
    [Google Scholar]
  110. 110. 
    Osterlund MT, Hardtke CS, Wei N, Deng XW. 2000. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–66
    [Google Scholar]
  111. 111. 
    Ouyang X, Huang X, Jin X, Chen Z, Yang P et al. 2014. Coordinated photomorphogenic UV-B signaling network captured by mathematical modeling. PNAS 111:11539–44
    [Google Scholar]
  112. 112. 
    Pacín M, Legris M, Casal JJ. 2013. COP1 re-accumulates in the nucleus under shade. Plant J 75:631–41
    [Google Scholar]
  113. 113. 
    Pacín M, Legris M, Casal JJ. 2014. Rapid decline in nuclear CONSTITUTIVE PHOTOMORPHOGENESIS1 abundance anticipates the stabilization of its target ELONGATED HYPOCOTYL5 in the light. Plant Physiol 164:1134–38
    [Google Scholar]
  114. 114. 
    Paul ND, Gwynn-Jones D. 2003. Ecological roles of solar UV radiation: towards an integrated approach. Trends Ecol. Evol. 18:48–55
    [Google Scholar]
  115. 115. 
    Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A et al. 2016. A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537:563–66
    [Google Scholar]
  116. 116. 
    Podolec R, Lau K, Wagnon TB, Hothorn M, Ulm R. 2021. A constitutively monomeric UVR8 photoreceptor confers enhanced UV-B photomorphogenesis. PNAS 118:e2017284118
    [Google Scholar]
  117. 117. 
    Podolec R, Ulm R. 2018. Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr. Opin. Plant Biol. 45:18–25
    [Google Scholar]
  118. 118. 
    Ponnu J, Riedel T, Penner E, Schrader A, Hoecker U 2019. Cryptochrome 2 competes with COP1 substrates to repress COP1 ubiquitin ligase activity during Arabidopsis photomorphogenesis. PNAS 116:27133–41
    [Google Scholar]
  119. 119. 
    Puchta H. 2017. Applying CRISPR/Cas for genome engineering in plants: The best is yet to come. Curr. Opin. Plant Biol. 36:1–8
    [Google Scholar]
  120. 120. 
    Qian C, Chen Z, Liu Q, Mao W, Chen Y et al. 2020. Coordinated transcriptional regulation by the UV-B photoreceptor and multiple transcription factors for plant UV-B responses. Mol. Plant 13:777–92
    [Google Scholar]
  121. 121. 
    Qian C, Mao W, Liu Y, Ren H, Lau OS et al. 2016. Dual-source nuclear monomers of UV-B light receptor direct photomorphogenesis in Arabidopsis. Mol. Plant 9:1671–74
    [Google Scholar]
  122. 122. 
    Rai N, Neugart S, Yan Y, Wang F, Siipola SM et al. 2019. How do cryptochromes and UVR8 interact in natural and simulated sunlight?. J. Exp. Bot. 70:4975–90Shows that UVR8 and cry1 are required for survival in sunlight.
    [Google Scholar]
  123. 123. 
    Rai N, O'Hara A, Farkas D, Safronov O, Ratanasopa K et al. 2020. The photoreceptor UVR8 mediates the perception of both UV-B and UV-A wavelengths up to 350 nm of sunlight with responsivity moderated by cryptochromes. Plant Cell Environ 43:1513–27
    [Google Scholar]
  124. 124. 
    Ren H, Han J, Yang P, Mao W, Liu X et al. 2019. Two E3 ligases antagonistically regulate the UV-B response in Arabidopsis. PNAS 116:4722–31
    [Google Scholar]
  125. 125. 
    Rizzini L, Favory JJ, Cloix C, Faggionato D, O'Hara A et al. 2011. Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–6Demonstrates that UVR8 is a UV-B photoreceptor and that it operates through Trp-based mechanisms and monomerization.
    [Google Scholar]
  126. 126. 
    Robson TM, Aphalo PJ, Banaś AK, Barnes PW, Brelsford CC et al. 2019. A perspective on ecologically relevant plant-UV research and its practical application. Photochem. Photobiol. Sci. 18:970–88
    [Google Scholar]
  127. 127. 
    Rozema J, Björn LO, Bornman JF, Gaberščik A, Häder DP et al. 2002. The role of UV-B radiation in aquatic and terrestrial ecosystems—an experimental and functional analysis of the evolution of UV-absorbing compounds. J Photochem. Photobiol. B Biol. 66:2–12
    [Google Scholar]
  128. 128. 
    Rozema J, van de Staaij J, Björn LO, Caldwell M. 1997. UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol. Evol. 12:22–28
    [Google Scholar]
  129. 129. 
    Safrany J, Haasz V, Mate Z, Ciolfi A, Feher B et al. 2008. Identification of a novel cis-regulatory element for UV-B-induced transcription in Arabidopsis. Plant J 54:402–14
    [Google Scholar]
  130. 130. 
    Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y et al. 2003. The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17:2642–47
    [Google Scholar]
  131. 131. 
    Santhanam R, Oh Y, Kumar R, Weinhold A, Luu VT et al. 2017. Specificity of root microbiomes in native-grown Nicotiana attenuata and plant responses to UVB increase Deinococcus colonization. Mol. Ecol. 26:2543–62
    [Google Scholar]
  132. 132. 
    Schierenbeck L, Ries D, Rogge K, Grewe S, Weisshaar B, Kruse O. 2015. Fast forward genetics to identify mutations causing a high light tolerant phenotype in Chlamydomonas reinhardtii by whole-genome-sequencing. BMC Genom 16:57
    [Google Scholar]
  133. 133. 
    Scrima A, Koníčková R, Czyzewski BK, Kawasaki Y, Jeffrey PD et al. 2008. Structural basis of UV DNA-damage recognition by the DDB1–DDB2 complex. Cell 135:1213–23
    [Google Scholar]
  134. 134. 
    Seo HS, Yang JY, Ishikawa M, Bolle C, Ballesteros ML, Chua NH. 2003. LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 424:995–99
    [Google Scholar]
  135. 135. 
    Sharma A, Sharma B, Hayes S, Kerner K, Hoecker U et al. 2019. UVR8 disrupts stabilisation of PIF5 by COP1 to inhibit plant stem elongation in sunlight. Nat. Commun. 10:4417
    [Google Scholar]
  136. 136. 
    Soriano G, Cloix C, Heilmann M, Núñez-Olivera E, Martínez-Abaigar J, Jenkins GI. 2018. Evolutionary conservation of structure and function of the UVR8 photoreceptor from the liverwort Marchantia polymorpha and the moss Physcomitrella patens. New Phytol 217:151–62
    [Google Scholar]
  137. 137. 
    Stacey MG, Hicks SN, von Arnim AG 1999. Discrete domains mediate the light-responsive nuclear and cytoplasmic localization of Arabidopsis COP1. Plant Cell 11:349–64
    [Google Scholar]
  138. 138. 
    Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S et al. 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 33:88–103
    [Google Scholar]
  139. 139. 
    Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, Badger MR. 2010. The solar action spectrum of photosystem II damage. Plant Physiol 153:988–93
    [Google Scholar]
  140. 140. 
    Tavridou E, Pireyre M, Ulm R. 2020. Degradation of the transcription factors PIF4 and PIF5 under UV-B promotes UVR8-mediated inhibition of hypocotyl growth in Arabidopsis. Plant J 101:507–17
    [Google Scholar]
  141. 141. 
    Tavridou E, Schmid-Siegert E, Fankhauser C, Ulm R. 2020. UVR8-mediated inhibition of shade avoidance involves HFR1 stabilization in Arabidopsis. PLOS Genet 16:e1008797
    [Google Scholar]
  142. 142. 
    Tilbrook K, Arongaus AB, Binkert M, Heijde M, Yin R, Ulm R 2013. The UVR8 UV-B photoreceptor: perception, signaling and response. Arabidopsis Book 11:e0164
    [Google Scholar]
  143. 143. 
    Tilbrook K, Dubois M, Crocco CD, Yin R, Chappuis R et al. 2016. UV-B perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28:966–83
    [Google Scholar]
  144. 144. 
    Tissot N, Ulm R. 2020. Cryptochrome-mediated blue-light signalling modulates UVR8 photoreceptor activity and contributes to UV-B tolerance in Arabidopsis. Nat. Commun. 11:1323
    [Google Scholar]
  145. 145. 
    Tokutsu R, Fujimura-Kamada K, Matsuo T, Yamasaki T, Minagawa J. 2019. The CONSTANS flowering complex controls the protective response of photosynthesis in the green alga Chlamydomonas. Nat. Commun. 10:4099
    [Google Scholar]
  146. 146. 
    Tokutsu R, Fujimura-Kamada K, Yamasaki T, Matsuo T, Minagawa J. 2019. Isolation of photoprotective signal transduction mutants by systematic bioluminescence screening in Chlamydomonas reinhardtii. Sci. Rep. 9:2820
    [Google Scholar]
  147. 147. 
    Tossi V, Lamattina L, Jenkins GI, Cassia RO. 2014. Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV RESISTANCE LOCUS8 photoreceptor in a nitric oxide-dependent mechanism. Plant Physiol 164:2220–30
    [Google Scholar]
  148. 148. 
    Tossi VE, Regalado JJ, Iannicelli J, Laino LE, Burrieza HP et al. 2019. Beyond Arabidopsis: differential UV-B response mediated by UVR8 in diverse species. Front. Plant Sci. 10:780
    [Google Scholar]
  149. 149. 
    Uljon S, Xu X, Durzynska I, Stein S, Adelmant G et al. 2016. Structural basis for substrate selectivity of the E3 ligase COP1. Structure 24:687–96
    [Google Scholar]
  150. 150. 
    Ulm R, Baumann A, Oravecz A, Máté Z, Ádám É et al. 2004. Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. PNAS 101:1397–402Shows that HY5 is a crucial transcriptional regulator in the UV-B response.
    [Google Scholar]
  151. 151. 
    Vaishak KP, Yadukrishnan P, Bakshi S, Kushwaha AK, Ramachandran H et al. 2019. The B-box bridge between light and hormones in plants. J. Photochem. Photobiol. B 191:164–74
    [Google Scholar]
  152. 152. 
    Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. 2004. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–6
    [Google Scholar]
  153. 153. 
    Vandenbussche F, Tilbrook K, Fierro AC, Marchal K, Poelman D et al. 2014. Photoreceptor-mediated bending towards UV-B in Arabidopsis. Mol. Plant 7:1041–52
    [Google Scholar]
  154. 154. 
    Vandenbussche F, Van Der Straeten D. 2014. Differential accumulation of ELONGATED HYPOCOTYL5 correlates with hypocotyl bending to ultraviolet-B light. Plant Physiol 166:40–43
    [Google Scholar]
  155. 155. 
    Vandenbussche F, Yu N, Li W, Vanhaelewyn L, Hamshou M et al. 2018. An ultraviolet B condition that affects growth and defense in Arabidopsis. Plant Sci 268:54–63
    [Google Scholar]
  156. 156. 
    Vanhaelewyn L, Bernula P, Van Der Straeten D, Vandenbussche F, Viczián A. 2019. UVR8-dependent reporters reveal spatial characteristics of signal spreading in plant tissues. Photochem. Photobiol. Sci. 18:1030–45
    [Google Scholar]
  157. 157. 
    Vanhaelewyn L, Viczián A, Prinsen E, Bernula P, Serrano AM et al. 2019. Differential UVR8 signal across the stem controls UV-B-induced inflorescence phototropism. Plant Cell 31:2070–88
    [Google Scholar]
  158. 158. 
    Velanis CN, Herzyk P, Jenkins GI. 2016. Regulation of transcription by the Arabidopsis UVR8 photoreceptor involves a specific histone modification. Plant Mol. Biol. 92:425–43
    [Google Scholar]
  159. 159. 
    Voityuk AA, Marcus RA, Michel-Beyerle ME 2014. On the mechanism of photoinduced dimer dissociation in the plant UVR8 photoreceptor. PNAS 111:5219–24
    [Google Scholar]
  160. 160. 
    Wang Q, Lin C. 2020. Mechanisms of cryptochrome-mediated photoresponses in plants. Annu. Rev. Plant Biol. 71:103–29
    [Google Scholar]
  161. 161. 
    Wang Q, Zuo Z, Wang X, Gu L, Yoshizumi T et al. 2016. Photoactivation and inactivation of Arabidopsis cryptochrome 2. Science 354:343–47
    [Google Scholar]
  162. 162. 
    Wang X, Wang Q, Han YJ, Liu Q, Gu L et al. 2017. A CRY-BIC negative-feedback circuitry regulating blue light sensitivity of Arabidopsis. Plant J 92:426–36
    [Google Scholar]
  163. 163. 
    Wargent J 2017. Turning UV photobiology into an agricultural reality. UV-B Radiation and Plant Life: Molecular Biology to Ecology BR Jordan 162–17 Egham, UK: CABI
    [Google Scholar]
  164. 164. 
    Wargent JJ, Gegas VC, Jenkins GI, Doonan JH, Paul ND. 2009. UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation. New Phytol 183:315–26
    [Google Scholar]
  165. 165. 
    Wargent JJ, Jordan BR. 2013. From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. New Phytol 197:1058–76
    [Google Scholar]
  166. 166. 
    Wu D, Hu Q, Yan Z, Chen W, Yan C et al. 2012. Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–19Describes X-ray structures of homodimers of the UVR8 core and the monomerization mechanism of the recombinant proteins.
    [Google Scholar]
  167. 167. 
    Wu M, Farkas D, Eriksson LA, Strid Å. 2019. Proline 411 biases the conformation of the intrinsically disordered plant UVR8 photoreceptor C27 domain altering the functional properties of the peptide. Sci. Rep. 9:818
    [Google Scholar]
  168. 168. 
    Wu M, Grahn E, Eriksson LA, Strid Å. 2011. Computational evidence for the role of Arabidopsis thaliana UVR8 as UV-B photoreceptor and identification of its chromophore amino acids. J. Chem. Inf. Model. 51:1287–95
    [Google Scholar]
  169. 169. 
    Wu M, Strid Å, Eriksson LA. 2014. Photochemical reaction mechanism of UV-B-induced monomerization of UVR8 dimers as the first signaling event in UV-B-regulated gene expression in plants. J. Phys. Chem. B 118:951–65
    [Google Scholar]
  170. 170. 
    Wu Q, Huang B, Niehaus TA, Yang X, Fan J, Zhang RQ 2015. The role of tryptophans in the UV-B absorption of a UVR8 photoreceptor—a computational study. Phys. Chem. Chem. Phys. 17:10786–94
    [Google Scholar]
  171. 171. 
    Yadav A, Bakshi S, Yadukrishnan P, Lingwan M, Dolde U et al. 2019. The B-box-containing microprotein miP1a/BBX31 regulates photomorphogenesis and UV-B protection. Plant Physiol 179:1876–92
    [Google Scholar]
  172. 172. 
    Yang Y, Liang T, Zhang L, Shao K, Gu X et al. 2018. UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis. Nat. Plants 4:98–107Shows that UVR8 directly interacts with transcription factors, inhibiting their DNA-binding activity.
    [Google Scholar]
  173. 173. 
    Yang Y, Zhang L, Chen P, Liang T, Li X, Liu H. 2020. UV-B photoreceptor UVR8 interacts with MYB73/MYB77 to regulate auxin responses and lateral root development. EMBO J 39:e101928
    [Google Scholar]
  174. 174. 
    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 27:202–13
    [Google Scholar]
  175. 175. 
    Yin R, Skvortsova MY, Loubéry S, Ulm R 2016. COP1 is required for UV-B-induced nuclear accumulation of the UVR8 photoreceptor. PNAS 113:E441522
    [Google Scholar]
  176. 176. 
    Yin R, Ulm R. 2017. How plants cope with UV-B: from perception to response. Curr. Opin. Plant Biol. 37:42–48
    [Google Scholar]
  177. 177. 
    Zeng X, Ren Z, Wu Q, Fan J, Peng P-P et al. 2015. Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8. Nat. Plants 1:14006
    [Google Scholar]
  178. 178. 
    Zhang X, Dong C, Huang W, Wang H, Wang L et al. 2015. Rational design of a photo-responsive UVR8-derived protein and a self-assembling peptide-protein conjugate for responsive hydrogel formation. Nanoscale 7:16666–70
    [Google Scholar]
  179. 179. 
    Zhang Y, Feng S, Chen F, Chen H, Wang J et al. 2008. Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 20:1437–55
    [Google Scholar]
  180. 180. 
    Zhao C, Mao K, You CX, Zhao XY, Wang SH et al. 2016. Molecular cloning and functional analysis of a UV-B photoreceptor gene, MdUVR8 (UV Resistance Locus 8), from apple. Plant Sci 247:115–26
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-050718-095946
Loading
/content/journals/10.1146/annurev-arplant-050718-095946
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error