Research Progress on Blue-photoreceptors and Its Functions in Eukaryotic Microalgae

doi:10.13560/j.cnki.biotech.bull.1985.2017.04.007

Abstract

Abstract: Eukaryotic microalgae,as a kind of photosynthetic eukaryotes,originate from endosymbiotic events. Their broad varieties,wide distribution,and complexity of evolutionary history make it become an ideal experimental material for research in algal stress physiology. Light is one of the important signal factors in the environment,it is not only the energy source for eukaryotic microalgae,but also provides information,and regulates the growth and development. For adapting the information of light intensity,quality and cycles,eukaryotic microalgae form a set system of fine light signal receiving and transducing during the long-time evolution. Photoreceptor plays the critical linkage role of receiving and transforming in the light signal pathway. Based on the various wavelengths of light,there are four types of photoreceptors,i.e.,red/far-red,blue,green and ultraviolet. Blue-photoreceptors can perceive 320-400 nm light and play key roles in the regulation of multiple plant physiological processes. Referenced by the study advances on the structures and functions of blue-photoreceptors in higher plant Arabidopsis thaliana,we summarized the study advances on the photoreceptor of eukaryotic microalgae,mainly focusing on their gene cloning,protein structure,molecular evolution,photochemical characteristics,physiological functions,and light signal transduction. Moreover,we suggested the future issues and focuses on the studies of blue-photoreceptors in eukaryotic microalgae,which provide reference for the research of blue photoreceptors from eukaryotic microalgae.

Key words: microalgae, blue-photoreceptor, protein structure, photochemical properties, light signal transduction

CUI Hong-li, CHEN Jun, HOU Yi-long, WU Hai-ge, QIN Song. Research Progress on Blue-photoreceptors and Its Functions in Eukaryotic Microalgae[J]. Biotechnology Bulletin, 2017, 33(4): 51-62.

References

[1] Gould SB, Waller RF, Mcfadden GI. Plastid evolution[J]. Annual Review of Plant Biology, 2008, 59：491-517.
[2] Keeling PJ. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution[J]. Annual Review of Plant Biology, 2013, 64（4）：583-607.
[3] 范玉琴, 李德红. 植物的蓝光受体及其信号转导[J]. 激光生物学报, 2004, 13（4）：314-320.
[4] Cui HL, Yu XN, Wang Y, et al. Evolutionary origins, molecular cloning and expression of carotenoid hydroxylases in eukaryotic photosynthetic algae[J]. Bmc Genomics, 2013, 14（1）：135-143.
[5] Fumio T, Daisuke Y, Mié I, et al. Aureochrome, a photoreceptor required for photomorphogenesis in stramenopiles[J]. Proceedings of the National Academy of Science, 2007, 104（49）：19625-19630.
[6] Kianianmomeni A, Hallmann A. Algal photoreceptors：in vivo functions and potential applications[J]. Planta, 2014, 239（1）：1-26.
[7] Chaves I, Pokorny R, Byrdin M, et al. The cryptochromes：blue light photoreceptors in plants and animals[J]. Annual Review of Plant Biology, 2011, 62：335.
[8] 孙燕, 许志茹. 植物的蓝光受体[J]. 植物生理学报, 2008, 44（01）：144-150.
[9] Jean-Pierre B, Baldissera G, Armin D, et al. Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1[J]. European Journal of Biochemistry, 2003, 270（14）：2921-2928.
[10] Yu X, Klejnot J, Zhao X, et al. Arabidopsis cryptochrome 2 completes its posttranslational life cycle in the nucleus[J]. Plant Cell, 2007, 19（10）：3146-3156.
[11] 常立, 文国琴. 植物蓝光受体研究进展[J]. 生物技术通讯, 2004, 15（2）：169-171.
[12] Wang H, Ma LG, Li JM, et al. Direct interaction of Arabidopsis cryptochromes with COP1 in light control development[J]. Behavior Genetics, 2001, 294（5540）：154-158.
[13] Liu B, Zuo ZC, Liu HT, et al. Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light[J]. Genes & Development, 2011, 25（10）：1029-1034.
[14] Zuo ZC, Liu HT, Liu B, et al. Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis[J]. Current Biology, 2011, 21（10）：841-847.
[15] 李旭. 拟南芥蓝光受体隐花素CRY2光激发机理和功能的生化分析[D]. 长沙：湖南大学, 2012.
[16] Ahmad M, Jarillo JA, Smirnova O, et al. The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro[J]. Molecular Cell, 1998, 1（7）：939-948.
[17] 张云云. 拟南芥蓝光受体CRY2互作蛋白激酶的筛选及验证[D]. 长春：吉林大学, 2015.
[18] Berrocal-Tito GM, Esquivel-Naranjo EU, Horwitz BA, et al. Trichoderma atroviride PHR1, a fungal photolyase responsible for DNA repair, autoregulates its own photoinduction[J]. Eukaryotic Cell, 2007, 6（9）：1682-1692.
[19] Bayram O, Biesemann C, Krappmann S, et al. More than a repair enzyme：Aspergillus nidulans photolyase-like CryA is a regulator of sexual development[J]. Molecular Biology of the Cell, 2008, 19（8）：3254-3262.
[20] Heijde M, Zabulon G, Corellou F, et al. Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes[J]. Plant Cell & Environment, 2010, 33（10）：1614-1626.
[21] Yihua H, Richard B, Smith BS, et al. Crystal structure of cryptochrome 3 from Arabidopsis thaliana and its implications for photolyase activity[J]. Proceedings of the National Academy of Sciences, 2006, 103（47）：17701-17706.
[22] Brudler R, Hitomi K, Daiyasu H, et al. Identification of a new cryptochrome class, structure, function, and evolution[J]. Molecular Cell, 2003, 11（1）：59-67.
[23] Dominik I, Ramona S, Joachim H, et al. Blue light induces radical formation and autophosphorylation in the light-sensitive domain of Chlamydomonas cryptochrome[J]. Journal of Biological Chemistry, 2007, 282（30）：21720-21728.
[24] Dominik I, Richard P, Elena H, et al. Photoreaction of plant and DASH cryptochromes probed by infrared spectroscopy：the neutral radical state of flavoproteins[J]. Journal of Physical Chemistry B, 2010, 114（51）：17155-17161.
[25] Lariguet P, Dunand C. Plant photoreceptors：phylogenetic overview[J]. Journal of Molecular Evolution, 2005, 61（4）：559-569.
[26] Reisdorph NA, Small GD. The CPH1 Gene of Chlamydomonas reinhardtii encodes two forms of cryptochrome whose levels are controlled by light-induced proteolysis[J]. Plant Physiology, 2004, 134（4）：1546-1554.
[27] Thomas L, Dominik I, Bernhard D, et al. Microsecond light-induced proton transfer to flavin in the blue light sensor plant cryptochrome[J]. Journal of the American Chemical Society, 2009, 131（40）：14274-14280.
[28] Benedikt B, Katja P, Meike S, et al. A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii[J]. Plant Cell, 2012, 24（7）：2992-3008.
[29] Benedikt B, Nico M, Tilman K, et al. News about cryptochrome photoreceptors in algae[J]. Plant Signaling & Behavior, 2013, 8（2）：1-4.
[30] Asimgil H, Kavakli IH. Purification and characterization of five members of photolyase/cryptochrome family from Cyanidioschyzon merolae[J]. Plant Science, 2012, 185-186（4）：190-198.
[31] Juhas M, Zadow A, Spexard M, et al. A novel cryptochrome in the diatom Phaeodactylumtricornutum influences the regulation of light-harvesting protein levels[J]. Febs Journal, 2014, 281（9）：2299-2311.
[32] Oliveri P, Fortunato AE, Petrone L, et al. The Cryptochrome/Photolyase Family in aquatic organisms[J]. Marine Genomics, 2014, 14（1）：23-37.
[33] Chris B, Allen AE, Badger JH, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes[J]. Nature, 2008, 456（7219）：239-244.
[34] Depauw FA, Rogato A, Ribera d'Alcalá M, et al. Exploring the molecular basis of responses to light in marine diatoms[J]. Journal of Experimental Botany, 2012, 63（4）：1575-1591.
[35] Sacha C, Manuela M, Tomoko I, et al. Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity[J]. Embo Reports, 2009, 10（6）：655-661.
[36] Cock JM, Sterck L, Rouzé P, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae[J]. Nature, 2010, 465（7298）：617-621.
[37] Vieler A, Wu G, Tsai CH, et al. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779[J]. PLoS Genetics, 2012, 8（11）：e1003064.
[38] Brunelle SA, Starr HE, Sotka EE, et al. Characterization of a dinoflagellate cryptochrome blue-light receptor with a possible role incircadian control of the cell cycle1[J]. Journal of Phycology, 2007, 43（3）：509-518.
[39] Asimgil H, Kavakli IH. Purification and characterization of five members of photolyase/cryptochrome family from Cyanidioschyzon merolae[J]. Plant Science, 2012, s 185-186（4）：190-198.
[40] Ulrich K, Bui Quang M, Aba L, et al. Distribution and phylogeny of light-oxygen-voltage-blue-light-signaling proteins in the three kingdoms of life[J]. Journal of Bacteriology, 2009, 191（23）：7234-7242.
[41] Christie JM, Salomon M, Nozue K, et al. LOV（light, oxygen, or voltage）domains of the blue-light photoreceptor phototropin（nph1）：binding sites for the chromophore flavin mononucleotide[J]. Proc Natl Acad Sci USA, 1999, 1999：8779-8783.
[42] 乔新荣, 陈琼. 植物向光素信号通路中NPH3蛋白的研究进展[J]. 植物生理学报, 2015（6）：829-834.
[43] 乔新荣, 段鸿斌, 叶兆伟. 植物向光素受体与信号转导机制研究进展[J]. 生物技术通报, 2014（8）：1-7.
[44] Harper SM, Neil LC, Gardner KH. Structural basis of a phototropin light switch[J]. Science, 2003, 301（5639）：1541-1545.
[45] Corchnoy SB, Swartz TE, Lewis JW, et al. Intramolecular proton transfers and structural changes during the photocycle of the LOV2 domain of phototropin 1[J]. Journal of Biological Chemistry, 2003, 278（2）：724-731.
[46] Briggs WR, Christie JM, Salomon M. Phototropins：a new family of flavin-binding blue light receptors in plants[J]. Antioxidants & Redox Signaling, 2001, 3（5）：775-788.
[47] Christie JM, Swartz TE, Bogomolni RA, et al. Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function[J]. Plant Journal, 2002, 32（2）：205-219.
[48] Salomon M, Christie JM, Knieb E, et al. Photochemical and mutational analysis of the FMN-binding domains of the plant bluelight receptor, phototropin[J]. Biochemistry, 2000, 39（31）：9401-9410.
[49] Hiroko K, Takeshi K, Steen C, et al. Responses of ferns to red light are mediated by an unconventional photoreceptor[J]. Nature, 2003, 421（6920）：287-290.
[50] Kennis JTM, Stokkum IHM, Van, Sean C, et al. The LOV2 domain of phototropin：A reversible photochromic switch[J]. Journal of the American Chemical Society, 2004, 126（14）：4512-4513.
[51] Christie JM. Phototropin blue-light receptors[J]. Annual Review of Plant Biology, 2007, 58（1）：21-45.
[52] Yuki T, Masayoshi N, Koji O, et al. Light-induced movement of the LOV2 domain in an Asp720Asn mutant LOV2-kinase fragment of Arabidopsis phototropin 2[J]. Biochemistry, 2011, 50（7）：1174-1183.
[53] Sullivan S, Thomson CE, Lamont DJ, et al. In vivo phosphorylation site mapping and functional characterization of Arabidopsis phototropin 1[J]. Molecular Plant, 2008, 1（1）：178-194.
[54] Shin-Ichiro I, Toshinori K, Masaki M, et al. Blue light-induced autophosphorylation of phototropin is a primary step for signaling[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105（14）：5626-5631.
[55] Sullivan S, Petersen J, Blackwood L, et al. Functional characterization of Ostreococcus tauri phototropin[J]. New Phytologist, 2015, doi:10. 1111/nph. 13640.
[56] Huang K, Merkle T, Beck CF. Isolation and characterization of a Chlamydomonas gene that encodes a putative blue-light photoreceptor of the phototropin family[J]. Physiologia Plantarum, 2002, 115（4）：613-622.
[57] Kasahara M;Swartz TE;Olney MA;et al. Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii[J]. Plant Physiology, 2002, 129（2）：762-773.
[58] Huang K, Beck CF. Photoropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii[J]. Proceedings of the National Academy of Sciences, 2003, 100：762-73.
[59] Chung-Soon I, Stephan E, Huang K, et al. Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii[J]. Plant Journal, 2006, 48（1）：1-16.
[60] Christie JM. Phototropin blue-light receptors[J]. Annual Review of Plant Biology, 2007, 58（4）：21-45.
[61] Zorin B, Lu Y, Sizova I, et al. Nuclear gene targeting in Chlamydomonas as exemplified by disruption of the PHOT gene[J]. Gene, 2009, 432（s 1-2）：91-96.
[62] Jessica T, Andre G, Jana S, et al. Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii[J]. Plant Cell, 2012, 24（11）：4687-4702.
[63] Berthold P, Tsunoda SP, Oliver P, et al. Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization[J]. Plant Cell, 2008, 20（6）：1665-1677.
[64] El-Batoul DT, Christie JM, Sophie SF, et al. A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus[J]. Plant Journal, 2011, 65（4）：578-588.
[65] Losi A, Gärtner W. The evolution of flavin-binding photoreceptors：an ancient chromophore serving trendy blue-light sensors[J]. Annual Review of Plant Biology, 2012, 63（3）：49-72.
[66] Losi A, Gärtner W. Old chromophores, new photoactivation paradi- gms, trendy applications：flavins in blue light-sensing photorece-ptors[J]. Photochemi Photobiol, 2011, 87（3）：491-510.
[67] Tseng TS, Frederickson MA, Briggs WR, et al. Light-activated bacterial LOV-domain histidine kinases[J]. Methods in Enzymology, 2010, 471：125-134.
[68] Deng YY, Yao JT, Fu G, et al. Isolation, expression, and characterization of blue light receptor Aureochrome gene from Saccharina japonica（Laminariales, Phaeophyceae）[J]. Marine Biotechnology, 2013, 16（2）：135-143.
[69] Osamu H, Ken T, Kazunori Z, et al. Blue light-induced conformational changes in a light-regulated transcription factor, Aureochrome-1[J]. Plant & Cell Physiology, 2013, 54（1）：93-106.
[70] Herman E, Sachse M, Kroth PG, et al. Blue-light-induced unfolding of the Jα helix allows for the dimerization of aureochrome-LOV from the diatom Phaeodactylum tricornutum[J]. Biochemistry, 2013, 52（18）：3094-3101.
[71] Mitra D, Yang X, Moffat K. Crystal structures of aureochrome1 LOV suggest new design strategies for optogenetics[J]. Structure, 2012, 20（4）：698-706.
[72] 黄一江. 微拟球藻NgLACS和NgAUREO1基因的克隆表达与功能分析[D]. 泰安：山东农业大学, 2014.
[73] Noriyuki S, Masamitsu W. Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles：phototropin, ZTL/FKF1/LKP2 and aureochrome[J]. Plant & Cell Physiology, 2013, 54（1）：8-23.
[74] Huysman MJJ, Fortunato AE, Michiel M, et al. Aureochrome1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in diatoms（Phaeodactylum tricornutum）[J]. Plant Cell, 2013, 25（1）：215-228.
[75] Mié I, Fumio T, Hisayoshi N, et al. Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes[J]. Planta, 2009, 230（3）：543-552.
[76] Gaditana N, Radakovits O, Jinkerson RE, et al. Draft genome sequence and genetic transformation of the oleaginous alga[J]. Nature Communications, 2012, 3（2）：686-698.