UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 51, 2016, Pages 14864-14869

  Allorent, Guillaume ^a   Lefebvre Legendre, Linnka ^a   Chappuis, Richard ^a   Kuntz, Marcel ^b   Truong, Thuy B ^c,d   Niyogi, Krishna K ^c,d   Ulm, Roman ^a   Goldschmidt Clermont, Michel ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIV GRENOBLE ALPES   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

LHCSR1; Nonphotochemical quenching; Photoprotection; PSBS; UV B photoreceptor

Indexed keywords

ACCLIMATIZATION; ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL FLUORESCENCE; CHLOROPLAST; CONTROLLED STUDY; ELECTRON TRANSPORT; GENE OVEREXPRESSION; LIGHT HARVESTING SYSTEM; NONHUMAN; PHOTOINHIBITION; PHOTORECEPTOR; PHOTOSYSTEM II; POINT MUTATION; PRIORITY JOURNAL; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; ULTRAVIOLET B RADIATION; ARABIDOPSIS; FLUORESCENCE; GENE EXPRESSION REGULATION; LIGHT; METABOLISM; PHOSPHORYLATION; PHOTON; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ARABIDOPSIS PROTEIN; CHLOROPHYLL; COP1 PROTEIN, ARABIDOPSIS; UBIQUITIN PROTEIN LIGASE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; FLUORESCENCE; GENE EXPRESSION REGULATION, PLANT; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOSPHORYLATION; PHOTONS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; ULTRAVIOLET RAYS;

EID: 85006515811     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1607695114     Document Type: Article

References (50)

1. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239-260.
2. Erickson E, Wakao S, Niyogi KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J 82(3):449-465.
3. Minagawa J, Tokutsu R (2015) Dynamic regulation of photosynthesis in Chlamydomonas reinhardtii. Plant J 82(3):413-428.
4. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16(3):307-314.
5. Wobbe L, Bassi R, Kruse O (2016) Multi-level light capture control in plants and green algae. Trends Plant Sci 21(1):55-68.
6. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170(4):1903-1916.
7. Ballottari M, et al. (2016) Identification of pH-sensing sites in the Light Harvesting Complex Stress-Related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J Biol Chem 291(14):7334-7346.
8. Bonente G, et al. (2011) Analysis of LhcSR3, a protein essential for feedback deexcitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9(1):e1000577.
9. Liguori N, Roy LM, Opacic M, Durand G, Croce R (2013) Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: The C-terminus of LHCSR is the knob of a dimmer switch. J Am Chem Soc 135(49):18339-18342.
10. Li XP, et al. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403(6768):391-395.
11. Peers G, et al. (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462(7272):518-521.
12. Niyogi KK, Bjorkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9(8):1369-1380.
13. Petroutsos D, et al. (2011) The chloroplast calcium sensor CAS is required for photo-acclimation in Chlamydomonas reinhardtii. Plant Cell 23(8):2950-2963.
14. Petroutsos D, et al. (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537(7621):563-566.
15. Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407-431.
16. Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 17(4):230-237.
17. Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: Balancing damage, repair and acclimation. Trends Plant Sci 3(4):131-135.
18. 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.
19. Favory JJ, et al. (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28(5):591-601.
20. 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(4):727-737.
21. Rizzini L, et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332(6025):103-106.
22. Christie JM, et al. (2012) Plant UVR8 photoreceptor senses UV-B by tryptophanmediated disruption of cross-dimer salt bridges. Science 335(6075):1492-1496.
23. Wu D, et al. (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484(7393):214-219.
24. 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.
25. 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.
26. Brown BA, et al. (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA 102(50):18225-18230.
27. Binkert M, et al. (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.
28. Yin R, Skvortsova MY, Loubéry 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.
29. Huang X, 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 USA 110(41):16669-16674.
30. Heijde M, Ulm R (2013) Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc Natl Acad Sci USA 110(3):1113-1118.
31. 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(1):547-555.
32. Tilbrook K, et al. (2016) UV-B perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28(4):966-983.
33. Takahashi S, et al. (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153(3):988-993.
34. Zavafer A, Chow WS, Cheah MH (2015) The action spectrum of photosystem II photoinactivation in visible light. J Photochem Photobiol B 152(Pt B):247-260.
35. Davey MP, et al. (2012) The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B. Photosynth Res 114(2):121-131.
36. Tibiletti T, Auroy P, Peltier G, Caffarri S (2016) Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol 171(4):2717-2730.
37. Correa-Galvis V, et al. (2016) Photosystem II subunit PsbS is involved in the induction of LHCSR protein-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 291(33):17478-17487.
38. Maruyama S, Tokutsu R, Minagawa J (2014) Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii. Plant Cell Physiol 55(7):1304-1310.
39. Allorent G, et al. (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25(2):545-557.
40. Dinc E, et al. (2016) LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells. Proc Natl Acad Sci USA 113(27):7673-7678.
41. Jenkins GI (2014) Structure and function of the UV-B photoreceptor UVR8. Curr Opin Struct Biol 29:52-57.
42. Li X, et al. (2016) An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell 28(2):367-387.
43. Oravecz A, et al. (2006) CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18(8):1975-1990.
44. Schierenbeck L, et al. (2015) Fast forward genetics to identify mutations causing a high light tolerant phenotype in Chlamydomonas reinhardtii by whole-genome-sequencing. BMC Genomics 16(1):57.
45. Serrato AJ, Fernández-Trijueque J, Barajas-López JD, Chueca A, Sahrawy M (2013) Plastid thioredoxins: A "one-for-all" redox-signaling system in plants. Front Plant Sci 4:463.
46. Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299(5612):1572-1575.
47. Naumann B, et al. (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7(21):3964-3979.
48. Hamel PP, Dreyfuss BW, Xie Z, Gabilly ST, Merchant S (2003) Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J Biol Chem 278(4):2593-2603.
49. Michelet L, Lefebvre-Legendre L, Burr SE, Rochaix JD, Goldschmidt-Clermont M (2011) Enhanced chloroplast transgene expression in a nuclear mutant of Chlamydomonas. Plant Biotechnol J 9(5):565-574.
50. Fraser PD, Pinto ME, Holloway DE, Bramley PM (2000) Technical advance: Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24(4):551-558.