Abstract
Light is increasingly recognized as an efficient means of controlling diverse biological processes with high spatiotemporal resolution. Optogenetic switches are molecular devices for regulating light-controlled gene expression, protein localization, signal transduction and protein-protein interactions. Such molecular components have been mainly developed through the use of photoreceptors, which upon light stimulation undergo conformational changes passing to an active state. The current repertoires of optogenetic switches include red, blue and UV-B light photoreceptors and have been implemented in a broad spectrum of biological platforms. In this review, we revisit different optogenetic switches that have been used in diverse biological platforms, with emphasis on those used for light-controlled gene expression in the budding yeast Saccharomyces cerevisiae. The implementation of these switches overcomes the use of traditional chemical inducers, allowing precise control of gene expression at lower costs, without leaving chemical traces, and positively impacting the production of high-value metabolites and heterologous proteins. Additionally, we highlight the potential of utilizing this technology beyond laboratory strains, by optimizing it for use in yeasts tamed for industrial processes. Finally, we discuss how fungal photoreceptors could serve as a source of biological parts for the development of novel optogenetic switches with improved characteristics. Although optogenetic tools have had a strong impact on basic research, their use in applied sciences is still undervalued. Therefore, the invitation for the future is to utilize this technology in biotechnological and industrial settings.
Similar content being viewed by others
References
Aravanis AM, Wang LP, Zhang F, Meltzer LA, Mogri MZ, Schneider MB, Deisseroth K (2007) An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng 4(3):S143–S156. doi:10.1088/1741-2560/4/3/S02
Avalos JL, Fink GR, Stephanopoulos G (2013) Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat Biotechnol 31(4):335–341. doi:10.1038/nbt.2509
Baker CL, Loros JJ, Dunlap JC (2012) The circadian clock of Neurospora crassa. FEMS Microbiol Rev 36(1):95–110. doi:10.1111/j.1574-6976.2011.00288.x
Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, Macino G (1996) White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J 15(7):1650–1657
Bayram O, Braus GH, Fischer R, Rodriguez-Romero J (2010) Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet Biol 47(11):900–908. doi:10.1016/j.fgb.2010.05.008
Bergström A, Simpson JT, Salinas F, Barre B, Parts L, Zia A, Nguyen Ba AN, Moses AM, Louis EJ, Mustonen V, Warringer J, Durbin R, Liti G (2014) A high-definition view of functional genetic variation from natural yeast genomes. Mol Biol Evol 31(4):872–888. doi:10.1093/molbev/msu037
Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fischer R (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15(20):1833–1838. doi:10.1016/j.cub.2005.08.061
Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8(9):1263–1268. doi:10.1038/nn1525
Canessa P, Schumacher J, Hevia MA, Tudzynski P, Larrondo LF (2013) Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: characterization of the white collar complex. PLoS One 8(12):e84223. doi:10.1371/journal.pone.0084223
Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ (2009) Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 28(8):1029–1042. doi:10.1038/emboj.2009.54
Chen D, Gibson ES, Kennedy MJ (2013) A light-triggered protein secretion system. J Cell Biol 201(4):631–640. doi:10.1083/jcb.201210119
Cheng P, He Q, Yang Y, Wang L, Liu Y (2003) Functional conservation of light, oxygen, or voltage domains in light sensing. Proc Natl Acad Sci U S A 100(10):5938–5943. doi:10.1073/pnas.1031791100
Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335(6075):1492–1496. doi:10.1126/science.1218091
Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA, O’Hara A, Smith BO, Christie JM, Jenkins GI (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(40):16366–16370. doi:10.1073/pnas.1210898109
Corrochano LM, Garre V (2010) Photobiology in the Zygomycota: multiple photoreceptor genes for complex responses to light. Fungal Genet Biol 47(11):893–899. doi:10.1016/j.fgb.2010.04.007
Crefcoeur RP, Yin R, Ulm R, Halazonetis TD (2013) Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat Commun 4:1779. doi:10.1038/ncomms2800
Dai Z, Liu Y, Guo J, Huang L, Zhang X (2014) Yeast synthetic biology for high-value metabolites. FEMS Yeast Res. doi:10.1111/1567-1364.12187
Deisseroth K (2011) Optogenetics. Nat Methods 8(1):26–29. doi:10.1038/nmeth.f.324
Deisseroth K, Feng G, Majewska AK, Miesenbock G, Ting A, Schnitzer MJ (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. J Neurosci 26(41):10380–10386. doi:10.1523/JNEUROSCI.3863-06.2006
Deiters A (2010) Principles and applications of the photochemical control of cellular processes. Chembiochem 11(1):47–53. doi:10.1002/cbic.200900529
Drepper T, Krauss U, Meyer zu Berstenhorst S, Pietruszka J, Jaeger KE (2011) Lights on and action! Controlling microbial gene expression by light. Appl Microbiol Biotechnol 90(1):23–40. doi:10.1007/s00253-011-3141-6
Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, Albert A, Cloix C, Jenkins GI, Oakeley EJ, Seidlitz HK, Nagy F, Ulm R (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28(5):591–601. doi:10.1038/emboj.2009.4
Folcher M, Oesterle S, Zwicky K, Thekkottil T, Heymoz J, Hohmann M, Christen M, Daoud El-Baba M, Buchmann P, Fussenegger M (2014) Mind-controlled transgene expression by a wireless-powered optogenetic designer cell implant. Nat Commun 5:5392. doi:10.1038/ncomms6392
Froehlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297(5582):815–819. doi:10.1126/science.1073681
Froehlich AC, Noh B, Vierstra RD, Loros J, Dunlap JC (2005) Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot Cell 4(12):2140–2152. doi:10.1128/EC.4.12.2140-2152.2005
Gautier A, Gauron C, Volovitch M, Bensimon D, Jullien L, Vriz S (2014) How to control proteins with light in living systems. Nat Chem Biol 10(7):533–541. doi:10.1038/nchembio.1534
Gerhardt KP, Olson EJ, Castillo-Hair SM, Hartsough LA, Landry BP, Ekness F, Yokoo R, Gomez EJ, Ramakrishnan P, Suh J, Savage DF, Tabor JJ (2016) An open-hardware platform for optogenetics and photobiology. Sci Rep 6:35363. doi:10.1038/srep35363
Giaever G, Nislow C (2014) The yeast deletion collection: a decade of functional genomics. Genetics 197(2):451–465. doi:10.1534/genetics.114.161620
Gibson DG (2009) Synthesis of DNA fragments in yeast by one-step assembly of overlapping oligonucleotides. Nucleic Acids Res 37(20):6984–6990. doi:10.1093/nar/gkp687
Gibson DG, Benders GA, Axelrod KC, Zaveri J, Algire MA, Moodie M, Montague MG, Venter JC, Smith HO, Hutchison CA 3rd (2008) One-step assembly in yeast of 25 overlapping DNA fragments to form a complete synthetic Mycoplasma genitalium genome. Proc Natl Acad Sci U S A 105(51):20404–20409. doi:10.1073/pnas.0811011106
Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274(5287):546 563-7
Guntas G, Hallett RA, Zimmerman SP, Williams T, Yumerefendi H, Bear JE, Kuhlman B (2015) Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins. Proc Natl Acad Sci U S A 112(1):112–117. doi:10.1073/pnas.1417910112
Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301(5639):1541–1544. doi:10.1126/science.1086810
He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297(5582):840–843. doi:10.1126/science.1072795
Heintzen C, Loros JJ, Dunlap JC (2001) The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104(3):453–464
Hevia MA, Canessa P, Muller-Esparza H, Larrondo LF (2015) A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. Proc Natl Acad Sci U S A 112(28):8744–8749. doi:10.1073/pnas.1508432112
Hughes RM, Bolger S, Tapadia H, Tucker CL (2012) Light-mediated control of DNA transcription in yeast. Methods 58(4):385–391. doi:10.1016/j.ymeth.2012.08.004
Idnurm A, Heitman J (2005) Photosensing fungi: phytochrome in the spotlight. Curr Biol 15(20):R829–R832. doi:10.1016/j.cub.2005.10.001
Jensen MK, Keasling JD (2014) Recent applications of synthetic biology tools for yeast metabolic engineering. FEMS Yeast Res. doi:10.1111/1567-1364.12185
Jost AP, Weiner OD (2015) Probing yeast polarity with acute, reversible, optogenetic inhibition of protein function. ACS Synth Biol 4(10):1077–1085. doi:10.1021/acssynbio.5b00053
Kaberniuk AA, Shemetov AA, Verkhusha VV (2016) A bacterial phytochrome-based optogenetic system controllable with near-infrared light. Nat Methods 13(7):591–597. doi:10.1038/nmeth.3864
Kawano F, Suzuki H, Furuya A, Sato M (2015) Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat Commun 6:6256. doi:10.1038/ncomms7256
Kawano F, Okazaki R, Yazawa M, Sato M (2016) A photoactivatable Cre-loxP recombination system for optogenetic genome engineering. Nat Chem Biol 12(12):1059–1064. doi:10.1038/nchembio.2205
Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL (2010) Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods 7(12):973–975. doi:10.1038/nmeth.1524
Kim H, Yoo SJ, Kang HA (2014) Yeast synthetic biology for the production of recombinant therapeutic proteins. FEMS Yeast Res. doi:10.1111/1567-1364.12195
Larrondo LF, Olivares-Yanez C, Baker CL, Loros JJ, Dunlap JC (2015) Circadian rhythms. Decoupling circadian clock protein turnover from circadian period determination. Science 347(6221):1257277. doi:10.1126/science.1257277
Leung DW, Otomo C, Chory J, Rosen MK (2008) Genetically encoded photoswitching of actin assembly through the Cdc42-WASP-Arp2/3 complex pathway. Proc Natl Acad Sci U S A 105(35):12797–12802. doi:10.1073/pnas.0801232105
Levskaya A, Weiner OD, Lim WA, Voigt CA (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461(7266):997–1001. doi:10.1038/nature08446
Li M, Borodina I (2014) Application of synthetic biology for production of chemicals in yeast Saccharomyces cerevisiae. FEMS Yeast Res. doi:10.1111/1567-1364.12213
Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJ, van Oudenaarden A, Barton DB, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ (2009) Population genomics of domestic and wild yeasts. Nature 458(7236):337–341. doi:10.1038/nature07743
Liu H, Yu X, Li K, Klejnot J, Yang H, Lisiero D, Lin C (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322(5907):1535–1539. doi:10.1126/science.1163927
Lopez J, Essus K, Kim IK, Pereira R, Herzog J, Siewers V, Nielsen J, Agosin E (2015) Production of beta-ionone by combined expression of carotenogenic and plant CCD1 genes in Saccharomyces cerevisiae. Microb Cell Factories 14:84. doi:10.1186/s12934-015-0273-x
Lungu OI, Hallett RA, Choi EJ, Aiken MJ, Hahn KM, Kuhlman B (2012) Designing photoswitchable peptides using the AsLOV2 domain. Chem Biol 19(4):507–517. doi:10.1016/j.chembiol.2012.02.006
Ma Z, Du Z, Chen X, Wang X, Yang Y (2013) Fine tuning the LightOn light-switchable transgene expression system. Biochem Biophys Res Commun 440(3):419–423. doi:10.1016/j.bbrc.2013.09.092
Malzahn E, Ciprianidis S, Kaldi K, Schafmeier T, Brunner M (2010) Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142(5):762–772. doi:10.1016/j.cell.2010.08.010
Melendez J, Patel M, Oakes BL, Xu P, Morton P, McClean MN (2014) Real-time optogenetic control of intracellular protein concentration in microbial cell cultures. Integr Biol (Camb) 6(3):366–372. doi:10.1039/c3ib40102b
Milias-Argeitis A, Rullan M, Aoki SK, Buchmann P, Khammash M (2016) Automated optogenetic feedback control for precise and robust regulation of gene expression and cell growth. Nat Commun 7:12546. doi:10.1038/ncomms12546
Mokdad-Gargouri R, Abdelmoula-Soussi S, Hadiji-Abbes N, Amor IY, Borchani-Chabchoub I, Gargouri A (2012) Yeasts as a tool for heterologous gene expression. Methods Mol Biol 824:359–370. doi:10.1007/978-1-61779-433-9_18
Montenegro-Montero A, Canessa P, Larrondo LF (2015) Around the fungal clock: recent advances in the molecular study of circadian clocks in Neurospora and other fungi. Adv Genet 92:107–184. doi:10.1016/bs.adgen.2015.09.003
Motta-Mena LB, Reade A, Mallory MJ, Glantz S, Weiner OD, Lynch KW, Gardner KH (2014) An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat Chem Biol 10(3):196–202. doi:10.1038/nchembio.1430
Müller K, Engesser R, Metzger S, Schulz S, Kampf MM, Busacker M, Steinberg T, Tomakidi P, Ehrbar M, Nagy F, Timmer J, Zubriggen MD, Weber W (2013a) A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells. Nucleic Acids Res 41(7):e77. doi:10.1093/nar/gkt002
Müller K, Engesser R, Schulz S, Steinberg T, Tomakidi P, Weber CC, Ulm R, Timmer J, Zurbriggen MD, Weber W (2013b) Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res 41(12):e124. doi:10.1093/nar/gkt340
Müller K, Engesser R, Timmer J, Nagy F, Zurbriggen MD, Weber W (2013c) Synthesis of phycocyanobilin in mammalian cells. Chem Commun (Camb) 49(79):8970–8972. doi:10.1039/c3cc45065a
Müller K, Engesser R, Timmer J, Zurbriggen MD, Weber W (2014a) Orthogonal optogenetic triple-gene control in mammalian cells. ACS Synth Biol 3(11):796–801. doi:10.1021/sb500305v
Müller K, Siegel D, Rodriguez Jahnke F, Gerrer K, Wend S, Decker EL, Reski R, Weber W, Zurbriggen MD (2014b) A red light-controlled synthetic gene expression switch for plant systems. Mol BioSyst 10(7):1679–1688. doi:10.1039/c3mb70579j
Nihongaki Y, Yamamoto S, Kawano F, Suzuki H, Sato M (2015) CRISPR-Cas9-based photoactivatable transcription system. Chem Biol 22(2):169–174. doi:10.1016/j.chembiol.2014.12.011
Niopek D, Benzinger D, Roensch J, Draebing T, Wehler P, Eils R, Di Ventura B (2014) Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells. Nat Commun 5:4404. doi:10.1038/ncomms5404
Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main A, Eng D, Polichuk DR, Teoh KH, Reed DW, Treynor T, Lenihan J, Fleck M, Bajad S, Dang G, Dengrove D, Diola D, Dorin G, Ellens KW, Fickes S, Galazzo J, Gaucher SP, Geistlinger T, Henry R, Hepp M, Horning T, Iqbal T, Jiang H, Kizer L, Lieu B, Melis D, Moss N, Regentin R, Secrest S, Tsuruta H, Vazquez R, Westblade LF, Xu L, Yu M, Zhang Y, Zhao L, Lievense J, Covello PS, Keasling JD, Reiling KK, Renninger NS, Newman JD (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496(7446):528–532. doi:10.1038/nature12051
Pathak GP, Vrana JD, Tucker CL (2013) Optogenetic control of cell function using engineered photoreceptors. Biol Cell 105(2):59–72. doi:10.1111/boc.201200056
Pathak GP, Strickland D, Vrana JD, Tucker CL (2014) Benchmarking of optical dimerizer systems. ACS Synth Biol 3(11):832–838. doi:10.1021/sb500291r
Polstein LR, Gersbach CA (2012) Light-inducible spatiotemporal control of gene activation by customizable zinc finger transcription factors. J Am Chem Soc 134(40):16480–16483. doi:10.1021/ja3065667
Polstein LR, Gersbach CA (2015) A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat Chem Biol 11(3):198–200. doi:10.1038/nchembio.1753
Pudasaini A, El-Arab KK, Zoltowski BD (2015) LOV-based optogenetic devices: light-driven modules to impart photoregulated control of cellular signaling. Front Mol Biosci 2:18. doi:10.3389/fmolb.2015.00018
Purschwitz J, Muller S, Kastner C, Schoser M, Haas H, Espeso EA, Atoui A, Calvo AM, Fischer R (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18(4):255–259. doi:10.1016/j.cub.2008.01.061
Purschwitz J, Muller S, Fischer R (2009) Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the white collar protein LreB. Mol Gen Genomics 281(1):35–42. doi:10.1007/s00438-008-0390-x
Renicke C, Schuster D, Usherenko S, Essen LO, Taxis C (2013) A LOV2 domain-based optogenetic tool to control protein degradation and cellular function. Chem Biol 20(4):619–626. doi:10.1016/j.chembiol.2013.03.005
Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schafer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332(6025):103–106. doi:10.1126/science.1200660
Robertson JB, Davis CR, Johnson CH (2013) Visible light alters yeast metabolic rhythms by inhibiting respiration. Proc Natl Acad Sci U S A 110(52):21130–21135. doi:10.1073/pnas.1313369110
Schierling B, Pingoud A (2012) Controlling the DNA cleavage activity of light-inducible chimeric endonucleases by bidirectional photoactivation. Bioconjug Chem 23(6):1105–1109. doi:10.1021/bc3001326
Schmidt D, Cho YK (2015) Natural photoreceptors and their application to synthetic biology. Trends Biotechnol 33(2):80–91. doi:10.1016/j.tibtech.2014.10.007
Shimizu-Sato S, Huq E, Tepperman JM, Quail PH (2002) A light-switchable gene promoter system. Nat Biotechnol 20(10):1041–1044. doi:10.1038/nbt734
Sorokina O, Kapus A, Terecskei K, Dixon LE, Kozma-Bognar L, Nagy F, Millar AJ (2009) A switchable light-input, light-output system modelled and constructed in yeast. J Biol Eng 3:15. doi:10.1186/1754-1611-3-15
Strickland D, Moffat K, Sosnick TR (2008) Light-activated DNA binding in a designed allosteric protein. Proc Natl Acad Sci U S A 105(31):10709–10714. doi:10.1073/pnas.0709610105
Strickland D, Lin Y, Wagner E, Hope CM, Zayner J, Antoniou C, Sosnick TR, Weiss EL, Glotzer M (2012) TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat Methods 9(4):379–384. doi:10.1038/nmeth.1904
Taslimi A, Zoltowski B, Miranda JG, Pathak GP, Hughes RM, Tucker CL (2016) Optimized second-generation CRY2-CIB dimerizers and photoactivatable Cre recombinase. Nat Chem Biol 12(6):425–430. doi:10.1038/nchembio.2063
Toettcher JE, Gong D, Lim WA, Weiner OD (2011) Light-based feedback for controlling intracellular signaling dynamics. Nat Methods 8(10):837–839. doi:10.1038/nmeth.1700
Toettcher JE, Weiner OD, Lim WA (2013) Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 155(6):1422–1434. doi:10.1016/j.cell.2013.11.004
Tran MT, Tanaka J, Hamada M, Sugiyama Y, Sakaguchi S, Nakamura M, Takahashi S, Miwa Y (2014) In vivo image analysis using iRFP transgenic mice. Exp Anim 63(3):311–319
Tsai CS, Kwak S, Turner TL, Jin YS (2014) Yeast synthetic biology toolbox and applications for biofuel production. FEMS Yeast Res. doi:10.1111/1567-1364.12206
Tyszkiewicz AB, Muir TW (2008) Activation of protein splicing with light in yeast. Nat Methods 5(4):303–305. doi:10.1038/nmeth.1189
Usherenko S, Stibbe H, Musco M, Essen LO, Kostina EA, Taxis C (2014) Photo-sensitive degron variants for tuning protein stability by light. BMC Syst Biol 8:128. doi:10.1186/s12918-014-0128-9
Vos T, de la Torre CP, van Gulik WM, Pronk JT, Daran-Lapujade P (2015) Growth-rate dependency of de novo resveratrol production in chemostat cultures of an engineered Saccharomyces cerevisiae strain. Microb Cell Factories 14:133. doi:10.1186/s12934-015-0321-6
Wang X, Chen X, Yang Y (2012) Spatiotemporal control of gene expression by a light-switchable transgene system. Nat Methods 9(3):266–269. doi:10.1038/nmeth.1892
Wang Z, Li N, Li J, Dunlap JC, Trail F, Townsend JP (2016) The fast-evolving phy-2 gene modulates sexual development in response to light in the model fungus Neurospora crassa. MBio 7(2):e02148. doi:10.1128/mBio.02148-15
Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, Kuhlman B, Hahn KM (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461(7260):104–108. doi:10.1038/nature08241
Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P, Deng H, Wang J, Deng X, Shi Y (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484(7393):214–219. doi:10.1038/nature10931
Yang X, Jost AP, Weiner OD, Tang C (2013) A light-inducible organelle-targeting system for dynamically activating and inactivating signaling in budding yeast. Mol Biol Cell 24(15):2419–2430. doi:10.1091/mbc.E13-03-0126
Yazawa M, Sadaghiani AM, Hsueh B, Dolmetsch RE (2009) Induction of protein-protein interactions in live cells using light. Nat Biotechnol 27(10):941–945. doi:10.1038/nbt.1569
Zhu Y, Tepperman JM, Fairchild CD, Quail PH (2000) Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix-loop-helix factor PIF3 in a reaction requiring the PAS domain of PIF3. Proc Natl Acad Sci U S A 97(24):13419–13424. doi:10.1073/pnas.230433797
Zoltowski BD, Vaccaro B, Crane BR (2009) Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol 5(11):827–834. doi:10.1038/nchembio.210
Acknowledgements
We are grateful to all members of Larrondo’s lab for their constructive comments on this review and Michael Handford (Universidad de Chile) for language support. No yeast cells were harmed during the writing of this article. This work was supported by Millennium Nucleus for Fungal Integrative and Synthetic Biology (MN-FISB, grant no. NC120043), CONICYT/FONDECYT to L.F.L. (grant no. 1131030) and CONICYT/FONDECYT to E.A. (grant no. 1130822). F.S. was supported by CONICYT/FONDECYT postdoctoral fellowship (grant no. 3150156) and V.D. by CONICYT/PhD Scholarship (grant no. 6313018).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Salinas, F., Rojas, V., Delgado, V. et al. Optogenetic switches for light-controlled gene expression in yeast. Appl Microbiol Biotechnol 101, 2629–2640 (2017). https://doi.org/10.1007/s00253-017-8178-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8178-8