Functional and topological diversity of LOV domain photoreceptors
Light–oxygen–voltage sensitive (LOV) flavoproteins are ubiquitous photoreceptors that mediate responses to environmental cues. Photosensory inputs are transduced into signaling outputs via structural rearrangements in sensor domains that consequently modulate the activity of an effector domain or mu...
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2017
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| Online Access: | http://hdl.handle.net/1721.1/106825 https://orcid.org/0000-0002-0419-3351 |
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| author | Glantz, Spencer T. Carpenter, Eric J. Melkonian, Michael Gardner, Kevin H. Wong, Gane Ka-Shu Chow, Brian Y. Boyden, Edward |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Glantz, Spencer T. Carpenter, Eric J. Melkonian, Michael Gardner, Kevin H. Wong, Gane Ka-Shu Chow, Brian Y. Boyden, Edward |
| author_sort | Glantz, Spencer T. |
| collection | MIT |
| description | Light–oxygen–voltage sensitive (LOV) flavoproteins are ubiquitous photoreceptors that mediate responses to environmental cues. Photosensory inputs are transduced into signaling outputs via structural rearrangements in sensor domains that consequently modulate the activity of an effector domain or multidomain clusters. Establishing the diversity in effector function and sensor–effector topology will inform what signaling mechanisms govern light-responsive behaviors across multiple kingdoms of life and how these signals are transduced. Here, we report the bioinformatics identification of over 6,700 candidate LOV domains (including over 4,000 previously unidentified sequences from plants and protists), and insights from their annotations for ontological function and structural arrangements. Motif analysis identified the sensors from ∼42 million ORFs, with strong statistical separation from other flavoproteins and non-LOV members of the structurally related Per-aryl hydrocarbon receptor nuclear translocator (ARNT)-Sim family. Conserved-domain analysis determined putative light-regulated function and multidomain topologies. We found that for certain effectors, sensor–effector linker length is discretized based on both phylogeny and the preservation of α-helical heptad repeats within an extended coiled-coil linker structure. This finding suggests that preserving sensor–effector orientation is a key determinant of linker length, in addition to ancestry, in LOV signaling structure–function. We found a surprisingly high prevalence of effectors with functions previously thought to be rare among LOV proteins, such as regulators of G protein signaling, and discovered several previously unidentified effectors, such as lipases. This work highlights the value of applying genomic and transcriptomic technologies to diverse organisms to capture the structural and functional variation in photosensory proteins that are vastly important in adaptation, photobiology, and optogenetics. |
| first_indexed | 2024-09-23T12:03:33Z |
| format | Article |
| id | mit-1721.1/106825 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T12:03:33Z |
| publishDate | 2017 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/1068252022-09-27T23:50:20Z Functional and topological diversity of LOV domain photoreceptors Glantz, Spencer T. Carpenter, Eric J. Melkonian, Michael Gardner, Kevin H. Wong, Gane Ka-Shu Chow, Brian Y. Boyden, Edward Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Massachusetts Institute of Technology. Media Laboratory McGovern Institute for Brain Research at MIT Program in Media Arts and Sciences (Massachusetts Institute of Technology) Boyden, Edward Light–oxygen–voltage sensitive (LOV) flavoproteins are ubiquitous photoreceptors that mediate responses to environmental cues. Photosensory inputs are transduced into signaling outputs via structural rearrangements in sensor domains that consequently modulate the activity of an effector domain or multidomain clusters. Establishing the diversity in effector function and sensor–effector topology will inform what signaling mechanisms govern light-responsive behaviors across multiple kingdoms of life and how these signals are transduced. Here, we report the bioinformatics identification of over 6,700 candidate LOV domains (including over 4,000 previously unidentified sequences from plants and protists), and insights from their annotations for ontological function and structural arrangements. Motif analysis identified the sensors from ∼42 million ORFs, with strong statistical separation from other flavoproteins and non-LOV members of the structurally related Per-aryl hydrocarbon receptor nuclear translocator (ARNT)-Sim family. Conserved-domain analysis determined putative light-regulated function and multidomain topologies. We found that for certain effectors, sensor–effector linker length is discretized based on both phylogeny and the preservation of α-helical heptad repeats within an extended coiled-coil linker structure. This finding suggests that preserving sensor–effector orientation is a key determinant of linker length, in addition to ancestry, in LOV signaling structure–function. We found a surprisingly high prevalence of effectors with functions previously thought to be rare among LOV proteins, such as regulators of G protein signaling, and discovered several previously unidentified effectors, such as lipases. This work highlights the value of applying genomic and transcriptomic technologies to diverse organisms to capture the structural and functional variation in photosensory proteins that are vastly important in adaptation, photobiology, and optogenetics. United States. Defense Advanced Research Projects Agency. Living Foundries Program (Grant HR0011-12-C-0068) Massachusetts Institute of Technology. Media Laboratory. Harvard-MIT Joint Research Grants Program in Basic Neuroscience Office of the Assistant Secretary of Defense for Research and Engineering National Science Foundation (U.S.) (Grants CBET 1053233 and EFRI 0835878) National Institutes of Health (U.S.) (Grants 1DP2OD002002, 1R01NS067199, 1R01DA029639, 1R01GM104948, 1RC1MH088182, and 1R01NS075421) Wallace H. Coulter Foundation Alfred P. Sloan Foundation Human Frontier Science Program (Strasbourg, France) New York Stem Cell Foundation (Robertson Neuroscience Investigator Award) Institution of Engineering and Technology (A. F. Harvey Prize) Skolkovo Institute of Science and Technology 2017-02-02T16:22:00Z 2017-02-02T16:22:00Z 2016-02 2015-05 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/106825 Glantz, Spencer T. et al. “Functional and Topological Diversity of LOV Domain Photoreceptors.” Proceedings of the National Academy of Sciences 113.11 (2016): E1442–E1451. © 2016 National Academy of Sciences https://orcid.org/0000-0002-0419-3351 en_US http://dx.doi.org/10.1073/pnas.1509428113 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Glantz, Spencer T. Carpenter, Eric J. Melkonian, Michael Gardner, Kevin H. Wong, Gane Ka-Shu Chow, Brian Y. Boyden, Edward Functional and topological diversity of LOV domain photoreceptors |
| title | Functional and topological diversity of LOV domain photoreceptors |
| title_full | Functional and topological diversity of LOV domain photoreceptors |
| title_fullStr | Functional and topological diversity of LOV domain photoreceptors |
| title_full_unstemmed | Functional and topological diversity of LOV domain photoreceptors |
| title_short | Functional and topological diversity of LOV domain photoreceptors |
| title_sort | functional and topological diversity of lov domain photoreceptors |
| url | http://hdl.handle.net/1721.1/106825 https://orcid.org/0000-0002-0419-3351 |
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