Non-Visual Light Sensing Enhances Behavioral Memory and Drives Gene Expression in

Overview

Journal bioRxiv

Date 2025 Feb 20

PMID 39975403

Authors

Zhijian Ji

Bingying Wang

Rashmi Chandra

Junqiang Liu

Supeng Yang

Yong Long

Michael Egan

Noelle LEtoile

Dengke K Ma

Affiliations

Soon will be listed here.

Abstract

Visible light influences a range of physiological processes, yet how animals respond to it independently of the visual system remains largely unknown. Here, we uncover a previously undescribed light-induced transcriptional pathway that modulates behavioral plasticity in , a roundworm without eyes. We demonstrate that ambient visible light or controlled-intensity visible-spectrum LED activates an effector gene in non-neuronal tissues through the bZIP transcription factors ZIP-2 and CEBP-2. Light induction of is more prominent at shorter wavelengths but is independent of the known blue light receptors LITE-1 and GUR-3 in . This bZIP-dependent genetic pathway in non-neuronal tissues enhances behavioral adaptability and olfactory memory, suggesting a body-brain communication axis. Furthermore, we use the light-responsive promoter to drive ectopic gene expression, causing synthetic light-induced sleep and rapid aging phenotypes in . These findings advance our understanding of light-responsive mechanisms outside the visual system and offer a new genetic tool for visible light-inducible gene expression in non-neuronal tissues.

References

Shi Y, Zhang J, Li X, Han Y, Guan J, Li Y . Non-image-forming photoreceptors improve visual orientation selectivity and image perception. Neuron. 2024; 113(3):486-500.e13. DOI: 10.1016/j.neuron.2024.11.015. View

Wei X, Potter C, Luo L, Shen K . Controlling gene expression with the Q repressible binary expression system in Caenorhabditis elegans. Nat Methods. 2012; 9(4):391-5. PMC: 3846601. DOI: 10.1038/nmeth.1929. View

Cronin T, Johnsen S . Extraocular, Non-Visual, and Simple Photoreceptors: An Introduction to the Symposium. Integr Comp Biol. 2016; 56(5):758-763. DOI: 10.1093/icb/icw106. View

Estes K, Dunbar T, Powell J, Ausubel F, Troemel E . bZIP transcription factor zip-2 mediates an early response to Pseudomonas aeruginosa infection in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2010; 107(5):2153-8. PMC: 2836710. DOI: 10.1073/pnas.0914643107. View

Pandey T, Ma D . Stress-Induced Phenoptosis: Mechanistic Insights and Evolutionary Implications. Biochemistry (Mosc). 2023; 87(12):1504-1511. DOI: 10.1134/S0006297922120082. View

Berson D, Dunn F, Takao M . Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002; 295(5557):1070-3. DOI: 10.1126/science.1067262. View

Brenner S . The genetics of Caenorhabditis elegans. Genetics. 1974; 77(1):71-94. PMC: 1213120. DOI: 10.1093/genetics/77.1.71. View

Bringmann H . Sleep-Active Neurons: Conserved Motors of Sleep. Genetics. 2018; 208(4):1279-1289. PMC: 5887131. DOI: 10.1534/genetics.117.300521. View

Genuth N, Barna M . Heterogeneity and specialized functions of translation machinery: from genes to organisms. Nat Rev Genet. 2018; 19(7):431-452. PMC: 6813789. DOI: 10.1038/s41576-018-0008-z. View

10.

Aghayeva U, Bhattacharya A, Sural S, Jaeger E, Churgin M, Fang-Yen C . DAF-16/FoxO and DAF-12/VDR control cellular plasticity both cell-autonomously and via interorgan signaling. PLoS Biol. 2021; 19(4):e3001204. PMC: 8099054. DOI: 10.1371/journal.pbio.3001204. View

11.

Ma D, Rothe M, Zheng S, Bhatla N, Pender C, Menzel R . Cytochrome P450 drives a HIF-regulated behavioral response to reoxygenation by C. elegans. Science. 2013; 341(6145):554-8. PMC: 3969381. DOI: 10.1126/science.1235753. View

12.

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

13.

Liu Y, Zhou J, Zhang N, Wu X, Zhang Q, Zhang W . Two sensory neurons coordinate the systemic mitochondrial stress response via GPCR signaling in C. elegans. Dev Cell. 2022; 57(21):2469-2482.e5. DOI: 10.1016/j.devcel.2022.10.001. View

14.

Keller J, Ellieva A, Ma D, Ju J, Nehk E, Konkel A . CYP-13A12 of the nematode Caenorhabditis elegans is a PUFA-epoxygenase involved in behavioural response to reoxygenation. Biochem J. 2014; 464(1):61-71. DOI: 10.1042/BJ20140848. View

15.

Stringham E, Dixon D, Jones D, Candido E . Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol Biol Cell. 1992; 3(2):221-33. PMC: 275521. DOI: 10.1091/mbc.3.2.221. View

16.

Hattar S, Lucas R, Mrosovsky N, Thompson S, Douglas R, Hankins M . Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003; 424(6944):76-81. PMC: 2885907. DOI: 10.1038/nature01761. View

17.

Denisov I, Makris T, Sligar S, Schlichting I . Structure and chemistry of cytochrome P450. Chem Rev. 2005; 105(6):2253-77. DOI: 10.1021/cr0307143. View

18.

Neve E, Ingelman-Sundberg M . Cytochrome P450 proteins: retention and distribution from the endoplasmic reticulum. Curr Opin Drug Discov Devel. 2010; 13(1):78-85. View

19.

Hanson S, Scholuke J, Liewald J, Sharma R, Ruse C, Engel M . Structure-function analysis suggests that the photoreceptor LITE-1 is a light-activated ion channel. Curr Biol. 2023; 33(16):3423-3435.e5. DOI: 10.1016/j.cub.2023.07.008. View

20.

Love M, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. PMC: 4302049. DOI: 10.1186/s13059-014-0550-8. View