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UVR8-dependent reporters reveal spatial characteristics of signal spreading in plant tissues

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Abstract

The UV Resistance Locus 8 (UVR8) photoreceptor controls UV-B mediated photomorphogenesis in Arabidopsis. The aim of this work is to collect and characterize different molecular reporters of photomorphogenic UV-B responses. Browsing available transcriptome databases, we identified sets of genes responding specifically to this radiation and are controlled by pathways initiated from the UVR8 photoreceptor. We tested the transcriptional changes of several reporters and found that they are regulated differently in different parts of the plant. Our experimental system led us to conclude that the examined genes are not controlled by light piping of UV-B from the shoot to the root or signalling molecules which may travel between different parts of the plant body but by local UVR8 signalling. The initiation of these universal signalling steps can be the induction of Elongated Hypocotyl 5 (HY5) and its homologue, HYH transcription factors. We found that their transcript and protein accumulation strictly depends on UVR8 and happens in a tissue autonomous manner. Whereas HY5 accumulation correlates well with the UVR8 signal across cell layers, the induction of flavonoids depends on both UVR8 signal and a yet to be identified tissue-dependent or developmental determinant.

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References

  1. A. B. Britt, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, 47, 75–100.

    Article  CAS  PubMed  Google Scholar 

  2. P. Casati and V. Walbot, Plant Physiol., 2003, 132, 1739–1754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. E. Hideg, M. A. Jansen and A. Strid, Trends Plant Sci., 2013, 18, 107–115.

    Article  CAS  PubMed  Google Scholar 

  4. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. D. J. Kliebenstein, J. E. Lim, L. G. Landry and R. L. Last, Plant Physiol., 2002, 130, 234–243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. L. Rizzini, J. J. Favory, C. Cloix, D. Faggionato, A. O’Hara, E. Kaiserli, R. Baumeister, E. Schafer, F. Nagy, G. I. Jenkins and R. Ulm, Science, 2011, 332, 103–106.

    Article  CAS  PubMed  Google Scholar 

  8. G. I. Jenkins, Plant, Cell Environ., 2017, 40, 2544–2557.

    Article  CAS  Google Scholar 

  9. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. D. Wu, Q. Hu, Z. Yan, W. Chen, C. Yan, X. Huang, J. Zhang, P. Yang, H. Deng, J. Wang, X. Deng and Y. Shi, Nature, 2012, 484, 214–219.

    Article  PubMed  CAS  Google Scholar 

  11. T. Mathes, M. Heilmann, A. Pandit, J. Zhu, J. Ravensbergen, M. Kloz, Y. Fu, B. O. Smith, J. M. Christie, G. I. Jenkins and J. T. Kennis, J. Am. Chem. Soc., 2015, 137, 8113–8120.

    Article  CAS  PubMed  Google Scholar 

  12. X. Li, L. W. Chung, K. Morokuma and G. Li, J. Chem. Theory Comput., 2014, 10, 3319–3330.

    Article  CAS  PubMed  Google Scholar 

  13. A. A. Voityuk, R. A. Marcus and M. E. Michel-Beyerle, Proc. Natl. Acad. Sci. U. S. A., 2014, 111, 5219–5224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. M. Wu, A. Strid and L. A. Eriksson, J. Phys. Chem. B, 2014, 118, 951–965.

    Article  CAS  PubMed  Google Scholar 

  15. Z. Liu, X. Li, F. W. Zhong, J. Li, L. Wang, Y. Shi and D. Zhong, J. Phys. Chem. Lett., 2014, 5, 69–72.

    Article  CAS  PubMed  Google Scholar 

  16. M. Heilmann, J. M. Christie, J. T. Kennis, G. I. Jenkins and T. Mathes, Photochem. Photobiol. Sci., 2015, 14, 252–257.

    Article  CAS  PubMed  Google Scholar 

  17. T. Miyamori, Y. Nakasone, K. Hitomi, J. M. Christie, E. D. Getzoff and M. Terazima, Photochem. Photobiol. Sci., 2015, 14, 995–1004.

    Article  CAS  PubMed  Google Scholar 

  18. X. Zeng, Z. Ren, Q. Wu, J. Fan, P. P. Peng, K. Tang, R. Zhang, K. H. Zhao and X. Yang, Nat. Plants, 2015, 1, 14006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. X. Huang, X. Ouyang and X. W. Deng, Curr. Opin. Plant Biol., 2014, 21, 96–103.

    Article  CAS  PubMed  Google Scholar 

  20. O. S. Lau and X. W. Deng, Trends Plant Sci., 2012, 17, 584–593.

    Article  CAS  PubMed  Google Scholar 

  21. D. Zhu, A. Maier, J. H. Lee, S. Laubinger, Y. Saijo, H. Wang, L. J. Qu, U. Hoecker and X. W. Deng, Plant Cell, 2008, 20, 2307–2323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. M. T. Osterlund, C. S. Hardtke, N. Wei and X. W. Deng, Nature, 2000, 405, 462–466.

    Article  CAS  PubMed  Google Scholar 

  23. X. Huang, X. Ouyang, P. Yang, O. S. Lau, L. Chen, N. Wei and X. W. Deng, Proc. Natl. Acad. Sci. U. S. A., 2013, 110, 16669–16674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. M. Binkert, L. Kozma-Bognar, K. Terecskei, L. De Veylder, F. Nagy and R. Ulm, Plant Cell, 2014, 26, 4200–4213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Y. Yang, T. Liang, L. Zhang, K. Shao, X. Gu, R. Shang, N. Shi, X. Li, P. Zhang and H. Liu, Nature, 2018, 4, 98–107.

    CAS  Google Scholar 

  26. R. Stracke, O. Jahns, M. Keck, T. Tohge, K. Niehaus, A. R. Fernie and B. Weisshaar, New Phytol., 2010, 188, 985–1000.

    Article  CAS  PubMed  Google Scholar 

  27. M. Heijde and R. Ulm, Trends Plant Sci., 2012, 17, 230–237.

    Article  CAS  PubMed  Google Scholar 

  28. B. A. Brown and G. I. Jenkins, Plant Physiol., 2008, 146, 576–588.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. L. Liu, S. Gregan, C. Winefield and B. Jordan, Plant, Cell Environ., 2015, 38, 905–919.

    Article  CAS  Google Scholar 

  30. W. A. Clayton, N. W. Albert, A. H. Thrimawithana, T. K. McGhie, S. C. Deroles, K. E. Schwinn, B. A. Warren, A. R. G. McLachlan, J. L. Bowman, B. R. Jordan and K. M. Davies, Plant J., 2018, 96, 503–517.

    Article  CAS  PubMed  Google Scholar 

  31. C. Cloix and G. I. Jenkins, Mol. Plant, 2008, 1, 118–128.

    Article  CAS  PubMed  Google Scholar 

  32. V. Moriconi, M. Binkert, C. Costigliolo, R. Sellaro, R. Ulm and J. J. Casal, Plant Physiol., 2018, 177, 75–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. R. Yin, A. B. Arongaus, M. Binkert and R. Ulm, Plant Cell, 2015, 27, 202–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. R. Ulm, A. Baumann, A. Oravecz, Z. Mate, E. Adam, E. J. Oakeley, E. Schafer and F. Nagy, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 1397–1402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. T. A. Day, G. Martin and T. C. Vogelmann, Plant, Cell Environ., 1993, 16(6), 735–741.

  36. P. W. Barnes, S. D. Flint, R. J. Ryel, M. A. Tobler, A. E. Barkley and J. J. Wargent, Plant Physiol. Biochem., 2015, 93, 94–100.

    Article  CAS  PubMed  Google Scholar 

  37. L. A. Diaz-Ramos, A. O’Hara, S. Kanagarajan, D. Farkas, A. Strid and G. I. Jenkins, Photochem. Photobiol. Sci., 2018, 17, 1108–1117.

    Article  CAS  PubMed  Google Scholar 

  38. T. Preuten, T. Hohm, S. Bergmann and C. Fankhauser, Curr. Biol., 2013, 23, 1934–1938.

    Article  CAS  PubMed  Google Scholar 

  39. K. Yamamoto, T. Suzuki, Y. Aihara, K. Haga, T. Sakai and A. Nagatani, Plant Cell Physiol., 2014, 55, 497–506.

    Article  CAS  PubMed  Google Scholar 

  40. F. Vandenbussche and D. Van Der Straeten, Plant Physiol., 2014, 166, 40–43.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. M. Endo, N. Mochizuki, T. Suzuki and A. Nagatani, Plant Cell, 2007, 19, 84–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. D. Kirchenbauer, A. Viczian, E. Adam, Z. Hegedus, C. Klose, M. Leppert, A. Hiltbrunner, S. Kircher, E. Schafer and F. Nagy, New Phytol., 2016, 211, 584–598.

    Article  CAS  PubMed  Google Scholar 

  43. M. Endo, S. Nakamura, T. Araki, N. Mochizuki and A. Nagatani, Plant Cell, 2005, 17, 1941–1952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. P. Bernula, C. D. Crocco, A. B. Arongaus, R. Ulm, F. Nagy and A. Viczian, Plant, Cell Environ., 2017, 40, 1104–1114.

    Article  CAS  Google Scholar 

  45. J. Kim, K. Song, E. Park, K. Kim and G. Bae, Plant Cell, 2016, 28, 2770–2785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. H. J. Lee, J. H. Ha, S. G. Kim, H. K. Choi, Z. H. Kim, Y. J. Han, J. I. Kim, Y. Oh, V. Fragoso, K. Shin, T. Hyeon, H. G. Choi, K. H. Oh, I. T. Baldwin and C. M. Park, Sci. Signaling, 2016, 9, ra106.

  47. H. G. Nimmo, Plant, Cell Environ., 2018, 41, 1742–1748.

    Article  CAS  Google Scholar 

  48. P. Casati and V. Walbot, Genome Biol., 2004, 5, R16.

  49. M. Karimi, A. Bleys, R. Vanderhaeghen and P. Hilson, Plant Physiol., 2007, 145, 1183–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Z. Magyar, B. Horvath, S. Khan, B. Mohammed, R. Henriques, L. De Veylder, L. Bako, B. Scheres and L. Bogre, EMBO J., 2012, 31, 1480–1493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. J. C. Oliveros, Venny. An interactive tool for comparing lists with Venn’s diagrams, http://bioinfogp.cnb.csic.es/tools/venny/index.html).

  52. A. Oravecz, A. Baumann, Z. Mate, A. Brzezinska, J. Molinier, E. J. Oakeley, E. Adam, E. Schafer, F. Nagy and R. Ulm, Plant Cell, 2006, 18, 1975–1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. F. Vandenbussche, N. Yu, W. Li, L. Vanhaelewyn, M. Hamshou, D. Van Der Straeten and G. Smagghe, Plant Sci., 2018, 268, 54–63.

    Article  CAS  PubMed  Google Scholar 

  54. J. Wan, P. Zhang, R. Wang, L. Sun, W. Wang, H. Zhou and J. Xu, Front. Plant Sci., 2018, 9, 618.

    Article  PubMed  PubMed Central  Google Scholar 

  55. M. Heijde and R. Ulm, Proc. Natl. Acad. Sci. U. S. A., 2013, 110, 1113–1118.

    Article  CAS  PubMed  Google Scholar 

  56. 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. Cell Mol. Biol., 2007, 50, 347–363.

    Article  CAS  Google Scholar 

  57. L. O. Morales, M. Brosche, J. Vainonen, G. I. Jenkins, J. J. Wargent, N. Sipari, A. Strid, A. V. Lindfors, R. Tegelberg and P. J. Aphalo, Plant Physiol., 2013, 161, 744–759.

    Article  CAS  PubMed  Google Scholar 

  58. X. Chen, Q. Yao, X. Gao, C. Jiang, N. P. Harberd and X. Fu, Curr. Biol., 2016, 26, 640–646.

    Article  CAS  PubMed  Google Scholar 

  59. G. Soriano, C. Cloix, M. Heilmann, E. Nunez-Olivera, J. Martinez-Abaigar and G. I. Jenkins, New Phytol., 2018, 217, 151–162.

    Article  CAS  PubMed  Google Scholar 

  60. 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, 512–523.

    Article  CAS  PubMed  Google Scholar 

  61. R. Stracke, H. Ishihara, G. Huep, A. Barsch, F. Mehrtens, K. Niehaus and B. Weisshaar, Plant J. Cell Mol. Biol., 2007, 50, 660–677.

    Article  CAS  Google Scholar 

  62. F. Vandenbussche, Y. Habricot, A. S. Condiff, R. Maldiney, D. Van der Straeten and M. Ahmad, Plant J. Cell Mol. Biol., 2007, 49, 428–441.

    Article  CAS  Google Scholar 

  63. E. Georgii, M. Jin, J. Zhao, B. Kanawati, P. Schmitt-Kopplin, A. Albert, J. B. Winkler and A. R. Schaffner, BMC Plant Biol., 2017, 17, 120.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. R. A. Henry-Kirk, B. Plunkett, M. Hall, T. McGhie, A. C. Allan, J. J. Wargent and R. V. Espley, Plant, Cell Environ., 2018, 41, 675–688.

    Article  CAS  Google Scholar 

  65. Z. Liu, Y. Liu, Z. Pu, J. Wang, Y. Zheng, Y. Li and Y. Wei, Biotechnol. Lett., 2013, 35, 1765–1780.

    Article  CAS  PubMed  Google Scholar 

  66. S. Czemmel, J. Holl, R. Loyola, P. Arce-Johnson, J. A. Alcalde, J. T. Matus and J. Bogs, Front. Plant Sci., 2017, 8, 1084.

    Article  PubMed  PubMed Central  Google Scholar 

  67. C. S. Buer, F. Kordbacheh, T. T. Truong, C. H. Hocart and M. A. Djordjevic, Planta, 2013, 238, 171–189.

    Article  CAS  PubMed  Google Scholar 

  68. W. Grunewald, I. De Smet, D. R. Lewis, C. Lofke, L. Jansen, G. Goeminne, R. Vanden Bossche, M. Karimi, B. De Rybel, B. Vanholme, T. Teichmann, W. Boerjan, M. C. Van Montagu, G. Gheysen, G. K. Muday, J. Friml and T. Beeckman, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 1554–1559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. C. S. Buer and M. A. Djordjevic, J. Exp. Bot., 2009, 60, 751–763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. A. Kakuszi, E. Sarvari, A. Solti, G. Czegeny, E. Hideg, E. Hunyadi-Gulyas, K. Boka and B. Boddi, J. Photochem. Photobiol., B, 2016, 161, 422–429.

    Article  CAS  Google Scholar 

  71. C. Markstadter, I. Queck, J. Baumeister, M. Riederer, U. Schreiber and W. Bilger, Photosynth. Res., 2001, 67, 17–25.

    Article  CAS  PubMed  Google Scholar 

  72. Y. Zhang, C. Li, J. Zhang, J. Wang, J. Yang, Y. Lv, N. Yang, J. Liu, X. Wang, G. Palfalvi, G. Wang and L. Zheng, PLoS One, 2017, 12, e0180449.

  73. K. van Gelderen, C. Kang, R. Paalman, D. Keuskamp, S. Hayes and R. Pierik, Plant Cell, 2018, 30, 101–116.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. R. Stracke, J. J. Favory, H. Gruber, L. Bartelniewoehner, S. Bartels, M. Binkert, M. Funk, B. Weisshaar and R. Ulm, Plant, Cell Environ., 2010, 33, 88–103.

    CAS  Google Scholar 

  75. I. I. Vaseva, E. Qudeimat, T. Potuschak, Y. Du, P. Genschik, F. Vandenbussche and D. Van Der Straeten, Proc. Natl. Acad. Sci. U. S. A., 2018, 115, E4130–E4139.

  76. S. Savaldi-Goldstein, C. Peto and J. Chory, Nature, 2007, 446, 199–202.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Functional Plant Biology, Department of Biology, Faculty of Sciences, Ghent University, KL Ledeganckstraat 35, B-9000, Gent, Belgium

    Lucas Vanhaelewyn, Dominique Van Der Straeten & Filip Vandenbussche

  2. Institute of Plant Biology, Biological Research Centre, Temesvári krt. 62, H-6726, Szeged, Hungary

    Péter Bernula & András Viczián

  3. Doctoral School in Biology, Faculty of Science and Informatics, University of Szeged, Szeged, H-6726, Hungary

    Péter Bernula

Authors
  1. Lucas Vanhaelewyn
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  2. Péter Bernula
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  3. Dominique Van Der Straeten
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  4. Filip Vandenbussche
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  5. András Viczián
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Correspondence to András Viczián.

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Electronic supplementary information (ESI) available: Supplementary Tables 1–5 and Fig. 1–9. See DOI: 10.1039/c8pp00492g

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Vanhaelewyn, L., Bernula, P., Van Der Straeten, D. et al. UVR8-dependent reporters reveal spatial characteristics of signal spreading in plant tissues. Photochem Photobiol Sci 18, 1030–1045 (2019). https://doi.org/10.1039/c8pp00492g

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