1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 74, 2023
  5. Article

Annual Review of Plant Biology

Volume 74, 2023

Optogenetic Methods in Plant Biology

Abstract

Optogenetics is a technique employing natural or genetically engineered photoreceptors in transgene organisms to manipulate biological activities with light. Light can be turned on or off, and adjusting its intensity and duration allows optogenetic fine-tuning of cellular processes in a noninvasive and spatiotemporally resolved manner. Since the introduction of Channelrhodopsin-2 and phytochrome-based switches nearly 20 years ago, optogenetic tools have been applied in a variety of model organisms with enormous success, but rarely in plants. For a long time, the dependence of plant growth on light and the absence of retinal, the rhodopsin chromophore, prevented the establishment of plant optogenetics until recent progress overcame these difficulties. We summarize the recent results of work in the field to control plant growth and cellular motion via green light–gated ion channels and present successful applications to light-control gene expression with single or combined photoswitches in plants. Furthermore, we highlight the technical requirements and options for future plant optogenetic research.

Keyword(s): biosensors, optoswitches, photoreceptors, plant optogenetics, rhodopsins
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-071122-094840
2023-05-22
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/arplant/74/1/annurev-arplant-071122-094840.html?itemId=/content/journals/10.1146/annurev-arplant-071122-094840&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abdelfattah AS, Ahuja S, Akkin T, Allu SR, Brake J et al. 2022. Neurophotonic tools for microscopic measurements and manipulation: status report. Neurophotonics 9:013001
     [Google Scholar]
  2. 2.
    Adamantidis A, Arber S, Bains JS, Bamberg E, Bonci A et al. 2015. Optogenetics: 10 years after ChR2 in neurons—views from the community. Nat. Neurosci. 18:1202–12
     [Google Scholar]
  3. 3.
    Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M et al. 2013. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6:2
     [Google Scholar]
  4. 4.
    Ando E, Kinoshita T. 2018. Red light-induced phosphorylation of plasma membrane H+-ATPase in stomatal guard cells. Plant Physiol. 178:838–49
     [Google Scholar]
  5. 5.
    Andreeva AV, Kutuzov MA. 2001. Do plants have rhodopsin after all? A mystery of plant G protein-coupled signalling. Plant Physiol. Biochem. 39:1027–35
     [Google Scholar]
  6. 6.
    Avelar GM, Schumacher RI, Zaini PA, Leonard G, Richards TA, Gomes SL. 2014. A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24:1234–40
     [Google Scholar]
  7. 7.
    Bansal A, Shikha S, Zhang Y. 2022. Towards translational optogenetics. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-021-00829-3
    [Google Scholar]
  8. 8.
    Beck S, Yu-Strzelczyk J, Pauls D, Constantin OM, Gee CE et al. 2018. Synthetic light-activated ion channels for optogenetic activation and inhibition. Front. Neurosci. 12:643
     [Google Scholar]
  9. 9.
    Benman W, Berlew EE, Deng H, Parker C, Kuznetsov IA et al. 2022. Temperature-responsive optogenetic probes of cell signaling. Nat. Chem. Biol. 18:152–60
     [Google Scholar]
  10. 10.
    Berlew EE, Kuznetsov IA, Yamada K, Bugaj LJ, Boerckel JD, Chow BY. 2021. Single-component optogenetic tools for inducible RhoA GTPase signaling. Adv. Biol. 5:2100810
     [Google Scholar]
  11. 11.
    Bi A, Cui J, Ma Y-P, Olshevskaya E, Pu M et al. 2006. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23–33
     [Google Scholar]
  12. 12.
    Boswell M, Lu Y, Boswell W, Savage M, Hildreth K et al. 2019. Fluorescent light incites a conserved immune and inflammatory genetic response within vertebrate organs (Danio rerio, Oryzias latipes and Mus musculus). Genes 10:271
     [Google Scholar]
  13. 13.
    Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:1263–68
     [Google Scholar]
  14. 14.
    Bracha D, Walls MT, Wei M-T, Zhu L, Kurian M et al. 2018. Mapping local and global liquid phase behavior in living cells using photo-oligomerizable seeds. Cell 175:1467–80.e13
     [Google Scholar]
  15. 15.
    Burgie ES, Vierstra RD. 2014. Phytochromes: an atomic perspective on photoactivation and signaling. Plant Cell 26:4568–83
     [Google Scholar]
  16. 16.
    Chatelle C, Ochoa-Fernandez R, Engesser R, Schneider N, Beyer HM et al. 2018. A green-light-responsive system for the control of transgene expression in mammalian and plant cells. ACS Synth. Biol. 7:1349–58
     [Google Scholar]
  17. 17.
    Chen F, Duan XD, Yu Y, Yang S, Chen YY et al. 2022. Visual function restoration with a highly sensitive and fast Channelrhodopsin in blind mice. Signal. Transduct. Tar. 7:104
     [Google Scholar]
  18. 18.
    Cheng M-C, Kathare PK, Paik I, Huq E. 2021. Phytochrome signaling networks. Annu. Rev. Plant Biol. 72:217–44
     [Google Scholar]
  19. 19.
    Choi AR, Shi L, Brown LS, Jung K-H. 2014. Cyanobacterial light-driven proton pump, Gloeobacter rhodopsin: complementarity between rhodopsin-based energy production and photosynthesis. PLOS ONE 9:e110643
     [Google Scholar]
  20. 20.
    Christie JM. 2007. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58:21–45
     [Google Scholar]
  21. 21.
    Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ et al. 2012. Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–96
     [Google Scholar]
  22. 22.
    Christie JM, Gawthorne J, Young G, Fraser NJ, Roe AJ. 2012. LOV to BLUF: flavoprotein contributions to the optogenetic toolkit. Mol. Plant 5:533–44
     [Google Scholar]
  23. 23.
    Christie JM, Zurbriggen MD. 2021. Optogenetics in plants. New Phytol. 229:3108–15
     [Google Scholar]
  24. 24.
    Chuong AS, Miri ML, Busskamp V, Matthews GAC, Acker LC et al. 2014. Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nat. Neurosci. 17:1123–29
     [Google Scholar]
  25. 25.
    Cosentino C, Alberio L, Gazzarrini S, Aquila M, Romano E et al. 2015. Engineering of a light-gated potassium channel. Science 348:707–10
     [Google Scholar]
  26. 26.
    Coville FV. 1913. The agricultural utilization of acid lands by means of acid-tolerant crops. Bull. US Dept. Agric. 6:1–13
     [Google Scholar]
  27. 27.
    Dagliyan O, Hahn KM. 2019. Controlling protein conformation with light. Curr. Opin. Struct. Biol. 57:17–22
     [Google Scholar]
  28. 28.
    Dana H, Mohar B, Sun Y, Narayan S, Gordus A et al. 2016. Sensitive red protein calcium indicators for imaging neural activity. eLife 5:e12727
     [Google Scholar]
  29. 29.
    Dawydow A, Gueta R, Ljaschenko D, Ullrich S, Hermann M et al. 2014. Channelrhodopsin-2–XXL, a powerful optogenetic tool for low-light applications. PNAS 111:13972–77
     [Google Scholar]
  30. 30.
    Di W, Hu Q, Yan Z, Chen W, Yan C et al. 2012. Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–19
     [Google Scholar]
  31. 31.
    Dodd AN, Kudla J, Sanders D. 2010. The language of calcium signaling. Annu. Rev. Plant Biol. 61:593–620
     [Google Scholar]
  32. 32.
    Doering J, Fu T, Arnoux I, Stroh A 2018. Concepts of all-optical physiology. Optogenetics: A Roadmap A Stroh 153–74. New York: Springer
     [Google Scholar]
  33. 33.
    Duan XD, Nagel G, Gao SQ. 2019. Mutated channelrhodopsins with increased sodium and calcium permeability. Appl. Sci. 9:664
     [Google Scholar]
  34. 34.
    Emiliani V, Cohen AE, Deisseroth K, Häusser M. 2015. All-optical interrogation of neural circuits. J. Neurosci. 35:13917–26
     [Google Scholar]
  35. 35.
    Entcheva E, Kay MW. 2021. Cardiac optogenetics: a decade of enlightenment. Nat. Rev. Cardiol. 18:349–67
     [Google Scholar]
  36. 36.
    Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H. 2014. Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem. Rev. 114:126–63
     [Google Scholar]
  37. 37.
    Farahani PE, Reed EH, Underhill EJ, Aoki K, Toettcher JE. 2021. Signaling, deconstructed: using optogenetics to dissect and direct information flow in biological systems. Annu. Rev. Biomed. Eng. 23:61–87
     [Google Scholar]
  38. 38.
    Favory J-J, Stec A, Gruber H, Rizzini L, Oravecz A et al. 2009. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28:591–601
     [Google Scholar]
  39. 39.
    Felle HH. 2001. pH: signal and messenger in plant cells. Plant Biol. 3:577–91
     [Google Scholar]
  40. 40.
    Fraikin GY, Strakhovskaya MG, Belenikina NS, Rubin AB. 2016. LOV and BLUF flavoproteins’ regulatory photoreceptors of microorganisms and photosensory actuators in optogenetic systems. Mosc. Univ. Biol. Sci. Bull. 71:50–57
     [Google Scholar]
  41. 41.
    Fraikin GY, Strakhovskaya MG, Rubin AB. 2013. Biological photoreceptors of light-dependent regulatory processes. Biochemistry 78:1238–53
     [Google Scholar]
  42. 42.
    Fudim R, Szczepek M, Vierock J, Vogt A, Schmidt A et al. 2019. Design of a light-gated proton channel based on the crystal structure of Coccomyxa rhodopsin. Sci. Signal. 12:573eaav4203
     [Google Scholar]
  43. 43.
    Gao SQ, Nagpal J, Schneider MW, Kozjak-Pavlovic V, Nagel G, Gottschalk A. 2015. Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat. Commun. 6:8046
     [Google Scholar]
  44. 44.
    Gil AA, Carrasco-López C, Zhu LY, Zhao EM, Ravindran PT et al. 2020. Optogenetic control of protein binding using light-switchable nanobodies. Nat. Commun. 11:4044
     [Google Scholar]
  45. 45.
    Gilroy S, Bialasek M, Suzuki N, Gorecka M, Devireddy AR et al. 2016. ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171:1606–15
     [Google Scholar]
  46. 46.
    Glantz ST, Carpenter EJ, Melkonian M, Gardner KH, Boyden ES et al. 2016. Functional and topological diversity of LOV domain photoreceptors. PNAS 113:E1442–51
     [Google Scholar]
  47. 47.
    Gómez-Consarnau L, González JM, Riedel T, Jaenicke S, Wagner-Döbler I et al. 2016. Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria. ISME J. 10:1102–12
     [Google Scholar]
  48. 48.
    Goto A, Bota A, Miya K, Wang JB, Tsukamoto S et al. 2021. Stepwise synaptic plasticity events drive the early phase of memory consolidation. Science 374:857–63
     [Google Scholar]
  49. 49.
    Govorunova EG, Gou Y, Sineshchekov OA, Li H, Lu X et al. 2022. Kalium channelrhodopsins are natural light-gated potassium channels that mediate optogenetic inhibition. Nat. Neurosci. 25:967–74
     [Google Scholar]
  50. 50.
    Govorunova EG, Sineshchekov OA, Janz R, Liu X, Spudich JL. 2015. Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics. Science 349:647–50
     [Google Scholar]
  51. 51.
    Govorunova EG, Sineshchekov OA, Li H, Spudich JL. 2017. Microbial rhodopsins: diversity, mechanisms, and optogenetic applications. Annu. Rev. Biochem. 86:845–72
     [Google Scholar]
  52. 52.
    Govorunova EG, Sineshchekov OA, Rodarte EM, Janz R, Morelle O et al. 2017. The expanding family of natural anion channelrhodopsins reveals large variations in kinetics, conductance, and spectral sensitivity. Sci. Rep. 7:43358
     [Google Scholar]
  53. 53.
    Guern J, Felle H, Mathieu Y, Kurkdjian A. 1991. Regulation of intracellular pH in plant cells. Int. Rev. Cytol. 127:111–73
     [Google Scholar]
  54. 54.
    Guntas G, Hallett RA, Zimmerman SP, Williams T, Yumerefendi H et al. 2015. Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins. PNAS 112:112–17
     [Google Scholar]
  55. 55.
    Gutermuth T, Herbell S, Lassig R, Brosche M, Romeis T et al. 2018. Tip-localized Ca2+-permeable channels control pollen tube growth via kinase-dependent R- and S-type anion channel regulation. New Phytol. 218:1089–105
     [Google Scholar]
  56. 56.
    Gutermuth T, Lassig R, Portes M-T, Maierhofer T, Romeis T et al. 2013. Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25:4525–43
     [Google Scholar]
  57. 57.
    Hart JE, Gardner KH. 2021. Lighting the way: recent insights into the structure and regulation of phototropin blue light receptors. J. Biol. Chem. 296:100594
     [Google Scholar]
  58. 58.
    Hartmann R, Sickinger HD, Oesterhelt D. 1980. Anaerobic growth of halobacteria. PNAS 77:3821–25
     [Google Scholar]
  59. 59.
    Hedrich R. 2012. Ion channels in plants. Physiol. Rev. 92:1777–811
     [Google Scholar]
  60. 60.
    Hegemann P, Nagel G. 2013. From channelrhodopsins to optogenetics. EMBO Mol. Med. 5:173–76
     [Google Scholar]
  61. 61.
    Herbell S, Gutermuth T, Konrad KR. 2018. An interconnection between tip-focused Ca2+ and anion homeostasis controls pollen tube growth. Plant Signal. Behav. 13:e1529521
     [Google Scholar]
  62. 62.
    Herrou J, Crosson S. 2011. Function, structure and mechanism of bacterial photosensory LOV proteins. Nat. Rev. Microbiol. 9:713–23
     [Google Scholar]
  63. 63.
    Hörner M, Eble J, Yousefi OS, Schwarz J, Warscheid B et al. 2019. Light-controlled affinity purification of protein complexes exemplified by the resting ZAP70 interactome. Front. Immunol. 10:226
     [Google Scholar]
  64. 64.
    Huang S, Ding M, Roelfsema MRG, Dreyer I, Scherzer S et al. 2021. Optogenetic control of the guard cell membrane potential and stomatal movement by the light-gated anion channel GtACR1. Sci. Adv. 7:eabg4619
     [Google Scholar]
  65. 65.
    Inoue K, Tsukamoto T, Shimono K, Suzuki Y, Miyauchi S et al. 2015. Converting a light-driven proton pump into a light-gated proton channel. J. Am. Chem. Soc. 137:3291–99
     [Google Scholar]
  66. 66.
    Iseki M, Matsunaga S, Murakami A, Ohno K, Shiga K et al. 2002. A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–51The first characterization of the Photoactivated Adenylyl Cyclase (PAC) as photoreceptor for negative phototaxis in Euglena gracilis.
     [Google Scholar]
  67. 67.
    Ishizuka T, Kakuda M, Araki R, Yawo H. 2006. Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci. Res. 54:85–94
     [Google Scholar]
  68. 68.
    Jiang HN, Li Y, Cui ZJ. 2017. Photodynamic physiology–photonanomanipulations in cellular physiology with protein photosensitizers. Front. Physiol. 8:191
     [Google Scholar]
  69. 69.
    Jost M, Fernández-Zapata J, Polanco MC, Ortiz-Guerrero JM, Chen PYT et al. 2015. Structural basis for gene regulation by a B12-dependent photoreceptor. Nature 526:536–41
     [Google Scholar]
  70. 70.
    Karasuyama M, Inoue K, Nakamura R, Kandori H, Takeuchi I. 2018. Understanding colour tuning rules and predicting absorption wavelengths of microbial rhodopsins by data-driven machine-learning approach. Sci. Rep. 8:15580
     [Google Scholar]
  71. 71.
    Karp G. 2009. Cell and Molecular Biology: Concepts and Experiments Hoboken, NJ: John Wiley & Sons. , 6th ed..
  72. 72.
    Keinath NF, Waadt R, Brugman R, Schroeder JI, Grossmann G et al. 2015. Live cell imaging with R-GECO1 sheds light on flg22- and chitin-induced transient [Ca2+]cyt patterns in Arabidopsis. Mol. Plant 8:1188–200
     [Google Scholar]
  73. 73.
    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 7:973–75
     [Google Scholar]
  74. 74.
    Kevei E, Schafer E, Nagy F. 2007. Light-regulated nucleo-cytoplasmic partitioning of phytochromes. J. Exp. Bot. 58:3113–24
     [Google Scholar]
  75. 75.
    Kim CK, Adhikari A, Deisseroth K. 2017. Integration of optogenetics with complementary methodologies in systems neuroscience. Nat. Rev. Neurosci. 18:222–35
     [Google Scholar]
  76. 76.
    Kim Y-S, Kim N-H, Yeom S-J, Kim S-W, Oh D-K. 2009. In vitro characterization of a recombinant Blh protein from an uncultured marine bacterium as a β-carotene 15,15′-dioxygenase. J. Biol. Chem. 284:15781–93
     [Google Scholar]
  77. 77.
    Kirilovsky D, Kerfeld CA. 2013. The orange carotenoid protein: a blue-green light photoactive protein. Photochem. Photobiol. Sci. 12:1135–43
     [Google Scholar]
  78. 78.
    Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A et al. 2014. Independent optical excitation of distinct neural populations. Nat. Methods 11:338–46
     [Google Scholar]
  79. 79.
    Kleinlogel S, Feldbauer K, Dempski RE, Fotis H, Wood PG et al. 2011. Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh. Nat. Neurosci. 14:513–18
     [Google Scholar]
  80. 80.
    Kolar K, Knobloch C, Stork H, Žnidarič M, Weber W. 2018. OptoBase: a web platform for molecular optogenetics. ACS Synth. Biol. 7:1825–28
     [Google Scholar]
  81. 81.
    Kumari A, Chételat A, Nguyen CT, Farmer EE. 2019. Arabidopsis H+-ATPase AHA1 controls slow wave potential duration and wound-response jasmonate pathway activation. PNAS 116:20226–31
     [Google Scholar]
  82. 82.
    Lamparter T. 2004. Evolution of cyanobacterial and plant phytochromes. FEBS Lett. 573:1–5
     [Google Scholar]
  83. 83.
    Lechno-Yossef S, Melnicki MR, Bao H, Montgomery BL, Kerfeld CA. 2017. Synthetic OCP heterodimers are photoactive and recapitulate the fusion of two primitive carotenoproteins in the evolution of cyanobacterial photoprotection. Plant J. 91:646–56
     [Google Scholar]
  84. 84.
    Leung DW, Otomo C, Chory J, Rosen MK. 2008. Genetically encoded photoswitching of actin assembly through the Cdc42-WASP-Arp2/3 complex pathway. PNAS 105:12797–802
     [Google Scholar]
  85. 85.
    Levskaya A, Weiner OD, Lim WA, Voigt CA. 2009. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997–1001
     [Google Scholar]
  86. 86.
    Li K, Prada J, Damineli DSC, Liese A, Romeis T et al. 2021. An optimized genetically encoded dual reporter for simultaneous ratio imaging of Ca2+ and H+ reveals new insights into ion signaling in plants. New Phytol. 230:2292–310
     [Google Scholar]
  87. 87.
    Li X, Gutierrez DV, Hanson MG, Han J, Mark MD et al. 2005. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. PNAS 102:17816–21
     [Google Scholar]
  88. 88.
    Makhijani K, To TL, Ruiz-Gonzalez R, Lafaye C, Royant A, Shu XK. 2017. Precision optogenetic tool for selective single- and multiple-cell ablation in a live animal model system. Cell Chem. Biol. 24:110–19
     [Google Scholar]
  89. 89.
    Man D, Wang W, Sabehi G, Aravind L, Post AF et al. 2003. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22:1725–31
     [Google Scholar]
  90. 90.
    Martinez A, Bradley AS, Waldbauer JR, Summons RE, DeLong EF. 2007. Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. PNAS 104:5590–95
     [Google Scholar]
  91. 91.
    Mary I, Tarran GA, Warwick PE, Terry MJ, Scanlan DJ et al. 2008. Light enhanced amino acid uptake by dominant bacterioplankton groups in surface waters of the Atlantic Ocean. FEMS Microbiol. Ecol. 63:36–45
     [Google Scholar]
  92. 92.
    Mathony J, Niopek D. 2021. Enlightening allostery: designing switchable proteins by photoreceptor fusion. Adv. Biol. 5:e2000181
     [Google Scholar]
  93. 93.
    Miller G 2006. Shining new light on neural circuits. Science 314:1674–76Report stated that the application of Channelrhodopsin-2 was the most feasible and straightforward method to light-control neuronal activity.
     [Google Scholar]
  94. 94.
    Miller G, Schlauch K, Tam R, Cortes D, Torres MA et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45
     [Google Scholar]
  95. 95.
    Mittler R, Shulaev V, Lam E. 1995. Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7:29–42
     [Google Scholar]
  96. 96.
    Möglich A, Yang X, Ayers RA, Moffat K. 2010. Structure and function of plant photoreceptors. Annu. Rev. Plant Biol. 61:21–47
     [Google Scholar]
  97. 97.
    Moldenhauer M, Sluchanko NN, Tavraz NN, Junghans C, Buhrke D et al. 2018. Interaction of the signaling state analog and the apoprotein form of the orange carotenoid protein with the fluorescence recovery protein. Photosynth. Res. 135:125–39
     [Google Scholar]
  98. 98.
    Morris RM, Nunn BL, Frazar C, Goodlett DR, Ting YS, Rocap G. 2010. Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. ISME J. 4:673–85
     [Google Scholar]
  99. 99.
    Mühlhäuser WWD, Fischer A, Weber W, Radziwill G. 2017. Optogenetics–bringing light into the darkness of mammalian signal transduction. Biochim. Biophys. Acta Mol. Cell Res. 1864:280–92
     [Google Scholar]
  100. 100.
    Müller K, Engesser R, Schulz S, Steinberg T, Tomakidi P et al. 2013. Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res. 41:e124
     [Google Scholar]
  101. 101.
    Müller K, Siegel D, Rodriguez Jahnke F, Gerrer K, Wend S et al. 2014. A red light-controlled synthetic gene expression switch for plant systems. Mol. BioSyst. 10:1679–88First optogenetic switch introduced into plant cells; a red/far-red light–activated/inactivated photoswitch for the control of gene expression in Arabidopsis, N. tabacum and Physcomitrium patens cells.
     [Google Scholar]
  102. 102.
    Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 2005. Light activation of Channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15:2279–84The first demonstration of completely noninvasive manipulation of animal (C. elegans) behavior by Channelrhodopsin-2 with blue light illumination.
     [Google Scholar]
  103. 103.
    Nagel G, Möckel B, Büldt G, Bamberg E. 1995. Functional expression of bacteriorhodopsin in oocytes allows direct measurement of voltage dependence of light induced H+ pumping. FEBS Lett. 377:263–66
     [Google Scholar]
  104. 104.
    Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM et al. 2002. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–98
     [Google Scholar]
  105. 105.
    Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N et al. 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. PNAS 100:13940–45First characterization of the light-gated cation channel Channelrhodopsin-2, showing its rapid response to light and depolarization of cells.
     [Google Scholar]
  106. 106.
    Ochoa-Fernandez R, Abel NB, Wieland F-G, Schlegel J, Koch L-A et al. 2020. Optogenetic control of gene expression in plants in the presence of ambient white light. Nat. Methods 17:717–25Optogenetic gene-expression switch for use in plants growing under normal growth conditions, leading to a system that is blind to white light and activated on command only by monochromatic red light.
     [Google Scholar]
  107. 107.
    Ochoa-Fernandez R, Samodelov SL, Brandl SM, Wehinger E, Müller K et al. 2016. Optogenetics in plants: red/far-red light control of gene expression. Optogenetics: Methods and Protocols A Kianianmomeni 125–39. New York: Springer
     [Google Scholar]
  108. 108.
    Onukwufor JO, Trewin AJ, Baran TM, Almast A, Foster TH, Wojtovich AP. 2020. Quantification of reactive oxygen species production by the red fluorescent proteins KillerRed, SuperNova and mCherry. Free Radic. Bio Med. 147:1–7
     [Google Scholar]
  109. 109.
    Ouyang X, Ren H, Huang X. 2021. Optogenetic tools controlled by ultraviolet-B light. aBIOTECH 2:170–75
     [Google Scholar]
  110. 110.
    Paik I, Huq E. 2019. Plant photoreceptors: multi-functional sensory proteins and their signaling networks. Semin. Cell Dev. Biol. 92:114–21
     [Google Scholar]
  111. 111.
    Panzer S, Zhang C, Konte T, Bräuer C, Diemar A et al. 2021. Modified rhodopsins from Aureobasidium pullulans excel with very high proton-transport rates. Front. Mol. Biosci. 8:750528
     [Google Scholar]
  112. 112.
    Papanatsiou M, Petersen J, Henderson L, Wang Y, Christie JM, Blatt MR. 2019. Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363:1456–59
     [Google Scholar]
  113. 113.
    Pham VN, Kathare PK, Huq E. 2018. Phytochromes and phytochrome interacting factors. Plant Physiol. 176:1025–38
     [Google Scholar]
  114. 114.
    Piccinini L, Iacopino S, Cazzaniga S, Ballottari M, Giuntoli B, Licausi F. 2022. A synthetic switch based on orange carotenoid protein to control blue-green light responses in chloroplasts. Plant Physiol. 189:1153–68A blue-green light switch based on orange carotenoid proteins for the control of gene expression in plant chloroplasts.
     [Google Scholar]
  115. 115.
    Pinhassi J, DeLong EF, Béjà O, González JM, Pedrós-Alió C. 2016. Marine bacterial and archaeal ion-pumping rhodopsins: genetic diversity, physiology, and ecology. Microbiol. Mol. Biol. Rev. 80:929–54
     [Google Scholar]
  116. 116.
    Podolec R, Demarsy E, Ulm R. 2021. Perception and signaling of ultraviolet-B radiation in plants. Annu. Rev. Plant Biol. 72:793–822
     [Google Scholar]
  117. 117.
    Pontier D, Mittler R, Lam E. 2002. Mechanism of cell death and disease resistance induction by transgenic expression of bacterio-opsin. Plant J. 30:499–509
     [Google Scholar]
  118. 118.
    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
     [Google Scholar]
  119. 119.
    Qi YCB, Garren EJ, Shu XK, Tsien RY, Jin YS. 2012. Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. PNAS 109:7499–504
     [Google Scholar]
  120. 120.
    Resentini F, Grenzi M, Ancora D, Cademartori M, Luoni L et al. 2021. Simultaneous imaging of ER and cytosolic Ca2+ dynamics reveals long-distance ER Ca2+ waves in plants. Plant Physiol. 187:603–17
     [Google Scholar]
  121. 121.
    Reyer A, Häßler M, Scherzer S, Huang S, Pedersen JT et al. 2020. Channelrhodopsin-mediated optogenetics highlights a central role of depolarization-dependent plant proton pumps. PNAS 117:20920–25
     [Google Scholar]
  122. 122.
    Rizhsky L, Mittler R. 2001. Inducible expression of bacterio-opsin in transgenic tobacco and tomato plants. Plant Mol. Biol. 46:313–23
     [Google Scholar]
  123. 123.
    Rozenberg A, Inoue K, Kandori H, Beja O. 2021. Microbial rhodopsins: the last two decades. Annu. Rev. Microbiol. 75:427–47
     [Google Scholar]
  124. 124.
    Rungrat T, Awlia M, Brown T, Cheng R, Sirault X et al. 2016. Using phenomic analysis of photosynthetic function for abiotic stress response gene discovery. Arabidopsis Book 14:e0185
     [Google Scholar]
  125. 125.
    Ryu MH, Moskvin OV, Siltberg-Liberles J, Gomelsky M. 2010. Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J. Biol. Chem. 285:41501–8
     [Google Scholar]
  126. 126.
    Sahel JA, Boulanger-Scemama E, Pagot C, Arleo A, Galluppi F et al. 2021. Partial recovery of visual function in a blind patient after optogenetic therapy. Nat. Med. 27:1223–29
     [Google Scholar]
  127. 127.
    Scheib U, Broser M, Constantin OM, Yang S, Gao S et al. 2018. Rhodopsin-cyclases for photocontrol of cGMP/cAMP and 2.3 Å structure of the adenylyl cyclase domain. Nat. Commun. 9:2046
     [Google Scholar]
  128. 128.
    Scheib U, Stehfest K, Gee CE, Körschen HG, Fudim R et al. 2015. The rhodopsin–guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling. Sci. Signal. 8:rs8
     [Google Scholar]
  129. 129.
    Schneider F, Grimm C, Hegemann P. 2015. Biophysics of channelrhodopsin. Annu. Rev. Biophys. 44:167–86
     [Google Scholar]
  130. 130.
    Scholz N, Guan CL, Nieberler M, Grotemeyer A, Maiellaro I et al. 2017. Mechano-dependent signaling by Latrophilin/CIRL quenches cAMP in proprioceptive neurons. eLife 6:e28360
     [Google Scholar]
  131. 131.
    Schröder-Lang S, Schwärzel M, Seifert R, Strünker T, Kateriya S et al. 2007. Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods 4:39–42
     [Google Scholar]
  132. 132.
    Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T et al. 2006. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16:1741–47
     [Google Scholar]
  133. 133.
    Shcherbakova DM, Shemetov AA, Kaberniuk AA, Verkhusha VV. 2015. Natural photoreceptors as a source of fluorescent proteins, biosensors, and optogenetic tools. Annu. Rev. Biochem. 84:519–50
     [Google Scholar]
  134. 134.
    Shen B-R, Zhu C-H, Yao Z, Cui L-L, Zhang J-J et al. 2017. An optimized transit peptide for effective targeting of diverse foreign proteins into chloroplasts in rice. Sci. Rep. 7:46231
     [Google Scholar]
  135. 135.
    Shimizu-Sato S, Huq E, Tepperman JM, Quail PH. 2002. A light-switchable gene promoter system. Nat. Biotechnol. 20:1041–44First optogenetic tool to control a cellular process; a phytochrome-based split-transcription factor photoswitch was engineered into yeast cells to control gene expression.
     [Google Scholar]
  136. 136.
    Sierra YAB, Rost BR, Pofahl M, Fernandes AM, Kopton RA et al. 2018. Potassium channel-based optogenetic silencing. Nat. Commun. 9:4611
     [Google Scholar]
  137. 137.
    Spudich JL, Yang CS, Jung KH, Spudich EN. 2000. Retinylidene proteins: structures and functions from archaea to humans. Annu. Rev. Cell Dev. Biol. 16:365–92
     [Google Scholar]
  138. 138.
    Stamatakis AM, Schachter MJ, Gulati S, Zitelli KT, Malanowski S et al. 2018. Simultaneous optogenetics and cellular resolution calcium imaging during active behavior using a miniaturized microscope. Front. Neurosci. 12:496
     [Google Scholar]
  139. 139.
    Stierl M, Stumpf P, Udwari D, Gueta R, Hagedorn R et al. 2011. Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J. Biol. Chem. 286:1181–88
     [Google Scholar]
  140. 140.
    Sukhova E, Sukhov V. 2021. Electrical signals, plant tolerance to actions of stressors, and programmed cell death: Is interaction possible?. Plants 10:81704
     [Google Scholar]
  141. 141.
    Swanson SJ, Choi W-G, Chanoca A, Gilroy S. 2011. In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Annu. Rev. Plant Biol. 62:273–97
     [Google Scholar]
  142. 142.
    Tanaka T, Singh M, Shihoya W, Yamashita K, Kandori H, Nureki O. 2020. Structural basis for unique color tuning mechanism in heliorhodopsin. Biochem. Biophys. Res. Commun. 533:262–67
     [Google Scholar]
  143. 143.
    Tang RJ, Yang S, Nagel G, Gao SQ. 2021. mem-iLID, a fast and economic protein purification method. Biosci. Rep. 41:7BSR20210800
     [Google Scholar]
  144. 144.
    Tyszkiewicz AB, Muir TW. 2008. Activation of protein splicing with light in yeast. Nat. Methods 5:303–5
     [Google Scholar]
  145. 145.
    Ulijasz AT, Cornilescu G, Cornilescu CC, Zhang J, Rivera M et al. 2010. Structural basis for the photoconversion of a phytochrome to the activated Pfr form. Nature 463:250–54
     [Google Scholar]
  146. 146.
    Ullrich S, Gueta R, Nagel G. 2013. Degradation of channelopsin-2 in the absence of retinal and degradation resistance in certain mutants. Biol. Chem. 394:271–80
     [Google Scholar]
  147. 147.
    Verma V, Ravindran P, Kumar PP. 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16:86
     [Google Scholar]
  148. 148.
    Vierock J, Grimm C, Nitzan N, Hegemann P. 2017. Molecular determinants of proton selectivity and gating in the red-light activated channelrhodopsin Chrimson. Sci. Rep. 7:9928
     [Google Scholar]
  149. 149.
    Vierock J, Rodriguez-Rozada S, Dieter A, Pieper F, Sims R et al. 2021. BiPOLES is an optogenetic tool developed for bidirectional dual-color control of neurons. Nat. Commun. 12:4527
     [Google Scholar]
  150. 150.
    Waadt R, Köster P, Andrés Z, Waadt C, Bradamante G et al. 2020. Dual-reporting transcriptionally linked genetically encoded fluorescent indicators resolve the spatiotemporal coordination of cytosolic abscisic acid and second messenger dynamics in Arabidopsis. Plant Cell 32:2582–601
     [Google Scholar]
  151. 151.
    Wang Q, Lin C. 2020. Mechanisms of cryptochrome-mediated photoresponses in plants. Annu. Rev. Plant Biol. 71:103–29
     [Google Scholar]
  152. 152.
    Wend S, Dal Bosco C, Kämpf MM, Ren F, Palme K et al. 2013. A quantitative ratiometric sensor for time-resolved analysis of auxin dynamics. Sci. Rep. 3:2052
     [Google Scholar]
  153. 153.
    Wondraczek L, Tyystjärvi E, Méndez-Ramos J, Müller FA, Zhang Q. 2015. Shifting the sun: solar spectral conversion and extrinsic sensitization in natural and artificial photosynthesis. Adv. Sci. 2:1500218
     [Google Scholar]
  154. 154.
    Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I et al. 2009. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104–8
     [Google Scholar]
  155. 155.
    Yang S, Constantin OM, Sachidanandan D, Hofmann H, Kunz TC et al. 2021. PACmn for improved optogenetic control of intracellular cAMP. BMC Biol. 19:227
     [Google Scholar]
  156. 156.
    Yang X, Montano S, Ren Z. 2015. How does photoreceptor UVR8 perceive a UV-B signal?. Photochem. Photobiol. 91:993–1003
     [Google Scholar]
  157. 157.
    Yu D, Lee H, Hong J, Jung H, Jo Y et al. 2019. Optogenetic activation of intracellular antibodies for direct modulation of endogenous proteins. Nat. Methods 16:1095–100
     [Google Scholar]
  158. 158.
    Zhang SX, Lutas A, Yang S, Diaz A, Fluhr H et al. 2021. Hypothalamic dopamine neurons motivate mating through persistent cAMP signalling. Nature 597:245–49
     [Google Scholar]
  159. 159.
    Zhao Y, Araki S, Wu J, Teramoto T, Chang Y-F et al. 2011. An expanded palette of genetically encoded Ca2+ indicators. Science 333:1888–91
     [Google Scholar]
  160. 160.
    Zhou Y, Ding M, Duan X, Konrad KR, Nagel G, Gao S. 2021. Extending the anion channelrhodopsin-based toolbox for plant optogenetics. Membranes 11:287
     [Google Scholar]
  161. 161.
    Zhou Y, Ding M, Gao S, Yu-Strzelczyk J, Krischke M et al. 2021. Optogenetic control of plant growth by a microbial rhodopsin. Nat. Plants 7:144–51First demonstration of retinal production in transgene plants (N. tabacum) that facilitated the expression and function of microbial opsins.
     [Google Scholar]
  162. 162.
    Zhou Y, Ding M, Nagel G, Konrad KR, Gao S. 2021. Advances and prospects of rhodopsin-based optogenetics in plant research. Plant Physiol. 187:572–89
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-071122-094840
Loading
Optogenetic Methods in Plant Biology
Annual Review of Plant Biology 74, 313 (2023); https://doi.org/10.1146/annurev-arplant-071122-094840
/content/journals/10.1146/annurev-arplant-071122-094840
/content/journals/10.1146/annurev-arplant-071122-094840
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error