Photoactivated UVR8-COP1 Module Determines Photomorphogenic UV-B Signaling Output in

English version České info

Higher plants are able to sense and interpret diverse light signals to modulate their growth. In response to long-wavelength and low-intensity ultraviolet-B (UV-B) light, plants establish photomorphogenic development and stress acclimation. UV RESISTANCE LOCUS 8 (UVR8) is a unique UV-B photoreceptor that triggers photomorphogenesis in Arabidopsis thaliana. However, the signaling process following UV-B light perception by plants is not fully understood. In this study, by generating transgenic UVR8 variants in Arabidopsis, we have extensively analyzed the biological significance of key residues in UVR8 for UV-B-induced photomorphogenesis. Furthermore, by engineering and characterizing two constitutively active UVR8 variants, we have provided the biochemical insight that the in vivo association between UVR8 and CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) critically determines the photomorphogenic UV-B signaling output.

Vyšlo v časopise: Photoactivated UVR8-COP1 Module Determines Photomorphogenic UV-B Signaling Output in. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004218
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004218

Souhrn

Zdroje

1. QuailPH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85–93.

2. ChenM, ChoryJ (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21: 664–671.

3. CashmoreAR, JarilloJA, WuYJ, LiuD (1999) Cryptochromes: blue light receptors for plants and animals. Science 284: 760–765.

4. BriggsWR, ChristieJM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7: 204–210.

5. LiuH, LiuB, ZhaoC, PepperM, LinC (2011) The action mechanisms of plant cryptochromes. Trends Plant Sci 16: 684–691.

6. ChristieJM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58: 21–45.

7. RizziniL, FavoryJJ, CloixC, FaggionatoD, O'HaraA, et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103–106.

8. FrohnmeyerH, StaigerD (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133: 1420–1428.

9. UlmR, NagyF (2005) Signalling and gene regulation in response to ultraviolet light. Curr Opin Plant Biol 8: 477–482.

10. HectorsK, PrinsenE, De CoenW, JansenMA, GuisezY (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.

11. JenkinsGI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60: 407–431.

12. KliebensteinDJ, LimJE, LandryLG, LastRL (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.

13. BrownBA, CloixC, JiangGH, KaiserliE, HerzykP, et al. (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci U S A 102: 18225–18230.

14. FavoryJJ, StecA, GruberH, RizziniL, OraveczA, et al. (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28: 591–601.

15. ChristieJM, ArvaiAS, BaxterKJ, HeilmannM, PrattAJ, et al. (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335: 1492–1496.

16. WuD, HuQ, YanZ, ChenW, YanC, et al. (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484: 214–219.

17. HuangX, OuyangX, YangP, LauOS, ChenL, 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. Proc Natl Acad Sci U S A 110: 16669–16674.

18. HeijdeM, UlmR (2013) Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc Natl Acad Sci U S A 110: 1113–1118.

19. GruberH, HeijdeM, HellerW, AlbertA, SeidlitzHK, et al. (2010) Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc Natl Acad Sci U S A 107: 20132–20137.

20. HeilmannM, JenkinsGI (2013) Rapid reversion from monomer to dimer regenerates the ultraviolet-B photoreceptor UV RESISTANCE LOCUS8 in intact Arabidopsis plants. Plant Physiol 161: 547–555.

21. CloixC, KaiserliE, HeilmannM, BaxterKJ, BrownBA, et al. (2012) C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein. Proc Natl Acad Sci U S A 109: 16366–16370.

22. O'HaraA, JenkinsGI (2012) In vivo function of tryptophans in the Arabidopsis UV-B photoreceptor UVR8. Plant Cell 24: 3755–3766.

23. GardnerG, LinC, TobinEM, LoehrerH, BrinkmanD (2009) Photobiological properties of the inhibition of etiolated Arabidopsis seedling growth by ultraviolet-B irradiation. Plant Cell Environ 32: 1573–1583.

24. HuangX, OuyangX, YangP, LauOS, LiG, et al. (2012) Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell 24: 4590–4606.

25. OraveczA, BaumannA, MateZ, BrzezinskaA, MolinierJ, et al. (2006) CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18: 1975–1990.

26. CrefcoeurRP, YinR, UlmR, HalazonetisTD (2013) Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat Commun 4: 1779.

27. HeijdeM, BinkertM, YinR, Ares-OrpelF, RizziniL, et al. (2013) Constitutively active UVR8 photoreceptor variant in Arabidopsis. Proc Natl Acad Sci USA 110: 20326–20331.

28. SuYS, LagariasJC (2007) Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 19: 2124–2139.

29. GuNN, ZhangYC, YangHQ (2012) Substitution of a conserved glycine in the PHR domain of Arabidopsis cryptochrome 1 confers a constitutive light response. Mol Plant 5: 85–97.

30. OsterlundMT, AngLH, DengXW (1999) The role of COP1 in repression of Arabidopsis photomorphogenic development. Trends Cell Biol 9: 113–118.

31. OsterlundMT, HardtkeCS, WeiN, DengXW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462–466.

32. FeherB, Kozma-BognarL, KeveiE, HajduA, BinkertM, 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.

33. BrownBA, JenkinsGI (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.

34. WargentJJ, GegasVC, JenkinsGI, DoonanJH, PaulND (2009) UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation. New Phytol 183: 315–326.

35. GitzDC, Liu-GitzL (2003) How do UV photomorphogenic responses confer water stress tolerance? Photochem Photobiol 78: 529–534.

36. DemkuraPV, BallareCL (2012) UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol Plant 5: 642–652.

37. ChenD, GibsonES, KennedyMJ (2013) A light-triggered protein secretion system. J Cell Biol 201: 631–640.

38. MullerK, EngesserR, SchulzS, SteinbergT, TomakidiP, et al. (2013) Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res 41: e124.

39. McNellisTW, von ArnimAG, ArakiT, KomedaY, MiseraS, et al. (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6: 487–500.

40. ChenH, ShenY, TangX, YuL, WangJ, et al. (2006) Arabidopsis CULLIN4 Forms an E3 Ubiquitin Ligase with RBX1 and the CDD Complex in Mediating Light Control of Development. Plant Cell 18: 1991–2004.

41. WeigelD, AhnJH, BlazquezMA, BorevitzJO, ChristensenSK, et al. (2000) Activation tagging in Arabidopsis. Plant Physiol 122: 1003–1013.

42. NohB, SpaldingEP (1998) Anion channels and the stimulation of anthocyanin accumulation by blue light in Arabidopsis seedlings. Plant Physiol 116: 503–509.