Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Light sensing and responses in fungi

Nature Reviews Microbiology volume 17, pages 25–36 (2019)Cite this article

Subjects

Abstract

Light controls important physiological and morphological responses in fungi. Fungi can sense near-ultraviolet, blue, green, red and far-red light using up to 11 photoreceptors and signalling cascades to control a large proportion of the genome and thereby adapt to environmental conditions. The blue-light photoreceptor functions directly as a transcriptional regulator in the nucleus, whereas the red-light-sensing and far-red-light-sensing phytochrome induces a signalling pathway to transduce the signal from the cytoplasm to the nucleus. Green light can be sensed by retinal-binding proteins, known as opsins, but the signalling mechanisms are not well understood. In this Review, we discuss light signalling processes in fungi, their signalling cascades and recent insights into the integration of light signalling pathways with other regulatory circuits in fungal cells.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Photoreceptors in filamentous fungi and overview of light-controlled processes.
Fig. 2: Light responses in model fungi.
Fig. 3: Structure of fungal photoreceptors and their chromophores.
Fig. 4: Current model of light responses in fungi.
Fig. 5: Links between light signalling pathways and other cellular pathways.

Similar content being viewed by others

References

  1. Fuller, K. K., Loros, J. J. & Dunlap, J. C. Fungal photobiology: visible light as a signal for stress, space and time. Curr. Genet. 61, 275–288 (2015).

    CAS  PubMed  Google Scholar 

  2. Dasgupta, A., Fuller, K. K., Dunlap, J. C. & Loros, J. J. Seeing the world differently: variability in the photosensory mechanisms of two model fungi. Environ. Microbiol. 18, 5–20 (2015).

    PubMed  PubMed Central  Google Scholar 

  3. Fischer, R., Aguirre, J., Herrera-Estrella, A. & Corrochano, L. M. The complexity of fungal vision. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0020-2016 (2016).

  4. Schumacher, J. How light affects the life of Botrytis. Fungal Genet. Biol. 106, 26–41 (2017).

    CAS  PubMed  Google Scholar 

  5. Schmoll, M. Light, stress, sex and carbon – the photoreceptor ENVOY as a central checkpoint in the physiology of Trichoderma reesei. Fungal Biol. 122, 479–486 (2018).

    CAS  PubMed  Google Scholar 

  6. Riquelme, M. et al. Fungal morphogenesis: from the polarized growth of hyphae to complex reproduction and infection structures. Microbiol. Mol. Biol. Rev. 82, e00068–17 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Ruger-Herreros, C. et al. Regulation of conidiation by light in Aspergillus nidulans. Genetics 188, 809–822 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen, C. H., Ringelberg, C. S., Gross, R. H., Dunlap, J. C. & Loros, J. J. Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J. 28, 1029–1042 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Rosales-Saavedra, T. et al. Novel light-regulated genes in Trichoderma atroviride: a dissection by cDNA microarrays. Microbiology 152, 3305–3317 (2006).

    CAS  PubMed  Google Scholar 

  10. Esquivel-Naranjo, E. U. et al. A Trichoderma atroviride stress-activated MAPK pathway integrates stress and light signals. Mol. Microbiol. 100, 860–876 (2016).

    CAS  PubMed  Google Scholar 

  11. Yu, Z., Armant, O. & Fischer, R. Fungi use the SakA (HogA) pathway for phytochrome-dependent light signaling. Nat. Microbiol. 1, 16019 (2016). This paper presents the discovery of the link between red-light signalling and the HOG pathway.

    CAS  PubMed  Google Scholar 

  12. Atoui, A. et al. Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet. Biol. 47, 962–972 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Fuller, K. K., Ringelberg, C. S., Loros, J. J. & Dunlap, J. C. The fungal pathogen Aspergillus fumigatus regulates growth, metabolism, and stress resistance in response to light. mBio 4, e00142–13 (2013).

    PubMed  PubMed Central  Google Scholar 

  14. Schmoll, M., Schuster, A., Silva Rdo, N. & Kubicek, C. P. The G-alpha protein GNA3 of Hypocrea jecorina (Anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light. Eukaryot. Cell 8, 410–420 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Bayram, O. et al. Changes of global gene expression and secondary metabolite accumulation during light-dependent Aspergillus nidulans development. Fungal Genet. Biol. 87, 30–53 (2016).

    CAS  PubMed  Google Scholar 

  16. Silva, F., Torres-Martinez, S. & Garre, V. Distinct white collar-1 genes control specific light responses in Mucor circinelloides. Mol. Microbiol. 61, 1023–1037 (2006).

    CAS  PubMed  Google Scholar 

  17. Mooney, J. L. & Yager, L. N. Light is required for conidiation in Aspergillus nidulans. Genes Dev. 4, 1473–1482 (1990).

    CAS  PubMed  Google Scholar 

  18. Kües, U. et al. The A mating type and blue light regulate all known differentiation processes in the basidiomycete Coprinus cinereus. Mol. Gen. Genet. 260, 81–91 (1998).

    PubMed  Google Scholar 

  19. Grünbacher, A. et al. Six hydrophobins are involved in hydrophobin rodlet formation in Aspergillus nidulans and contribute to hydrophobicity of the spore surface. PLOS ONE 9, e94546 (2014).

    PubMed  PubMed Central  Google Scholar 

  20. Röhrig, J., Kastner, C. & Fischer, R. Light inhibits spore germination through phytochrome in Aspergillus nidulans. Curr. Genet. 59, 55–62 (2013).

    PubMed  Google Scholar 

  21. Duran, R., Cary, J. W. & Calvo, A. M. Role of the osmotic stress regulatory pathway in morphogenesis and secondary metabolism in fialmentous fungi. Toxins 2, 367–381 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Dunlap, J. C. & Loros, J. J. Making time: conservation of biological clocks from fungi to animals. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0039-2016 (2017).

  23. Montenegro-Montero, A., Canessa, P. & Larrondo, L. F. Around the fungal clock: recent advances in the molecular study of circadian clocks in Neurospora and other fungi. Adv. Genet. 92, 107–184 (2015).

    CAS  PubMed  Google Scholar 

  24. Lee, K., Loros, J. J. & Dunlap, J. C. Interconnected feedback loops in the Neurospora circadian system. Science 290, 277 (2000).

    Google Scholar 

  25. Arpaia, G., Loros, J. J., Dunlap, J. C., Morelli, G. & Macino, G. The interplay of light and the circadian clock. Independent dual regulation of clock-controlled gene ccg-2 (eas). Plant Physiol. 102, 1299–1305 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Cohen, R. & Delbrück, M. Photo-reactions in Phycomyces; growth and tropic responses to the stimulation of narrow test areas. J. Gen. Physiol. 42, 677–695 (1959).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Corrochano, L. M. & Galland, P. in The Mycota: Growth, differentiation and sexuality (ed. Wendland, J.) 235–256 (Springer, 2016).

  28. O’Hara, A. & Jenkins, J. I. In vivo function of tryptophans in the Arabidopsis UV-B photoreceptor UVR8. Plant Cell 24, 3755–3766 (2012).

    PubMed  PubMed Central  Google Scholar 

  29. Losi, A. & Gärtner, W. The evolution of flavin-binding photoreceptors: an ancient chromophore serving trendy blue-light sensors. Annu. Rev. Plant Biol. 63, 49–72 (2012).

    CAS  PubMed  Google Scholar 

  30. Pfeifer, A. et al. Time-resolved Fourier transform infrared study on photoadduct formation and secondary structural changes within the phototropin LOV domain. Biophys. J. 96, 1462–1470 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Crosson, S. & Moffat, K. Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14, 1067–1075 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Heintzen, C., Loros, J. J. & Dunlap, J. C. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104, 453–464 (2001).

    CAS  PubMed  Google Scholar 

  33. Zoltowski, B. D. et al. Conformational switching in the fungal light sensor Vivid. Science 316, 1054–1057 (2007). This is the first study to report the crystal structure of the LOV domain-containing protein VVD.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Dasgupta, A. et al. Biological significance of photoreceptor photocycle length: VIVID photocycle governs the dynamic VIVID-White Collar Complex pool mediating photo-adaptation and response to changes in light intensity. PLOS Genet. 11, e1005215 (2015).

    PubMed  PubMed Central  Google Scholar 

  35. Zoltowski, B. D., Vaccaro, B. & Crane, B. R. Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5, 827–834 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Zoltowski, B. D. & Crane, B. R. Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47, 7012–7019 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Vaidya, A. T., Chen, C. H., Dunlap, J. C., Loros, J. J. & Crane, B. R. Structure of a light-activated LOV protein dimer that regulates transcription. Sci. Signal. 4, ra50 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Lee, C. T., Malzahn, E., Brunner, M. & Mayer, M. P. Light-induced differences in conformational dynamics of the circadian clock regulator VIVID. J. Mol. Biol. 426, 601–610 (2014).

    CAS  PubMed  Google Scholar 

  39. Ganguly, A., Thiel, W. & Crane, B. R. Glutamine amide flip elicits long distance allosteric responses in the lov protein VIVID. J. Am. Chem. Soc. 139, 2972–2980 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Schwerdtfeger, C. & Linden, H. Blue light adaptation and desensitization of light signal transduction in Neurospora crassa. Mol. Microbiol. 39, 1080–1087 (2001).

    CAS  PubMed  Google Scholar 

  41. Schwerdtfeger, C. & Linden, H. VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J. 22, 4846–4855 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Ballario, P. et al. White collar-1, a central regulator of blue light responses in Neurospora crassa, is a zinc finger protein. EMBO J. 15, 1650–1657 (1996). This is the first study first to clone the photoreceptor gene.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Froehlich, A. C., Liu, Y., Loros, J. J. & Dunlap, J. C. White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297, 815–819 (2002).

    CAS  PubMed  Google Scholar 

  44. He, Q. et al. White collar-1, a DNA binding transcription factor and a light sensor. Science 297, 840–843 (2002). References 43 and 44 show the breakthrough discovery of the chromophore attached to the photoreceptor, which is a transcription factor.

    CAS  PubMed  Google Scholar 

  45. Cheng, P., He, Q., Yang, Y., Wang, L. & Liu, Y. Functional conservation of light, oxygen, or voltage domains in light sensing. Proc. Natl Acad. Sci. USA 100, 5938–5943 (2003).

    CAS  PubMed  Google Scholar 

  46. Wang, B., Zhou, X., Loros, J. J. & Dunlap, J. C. Alternative use of DNA binding domains by the Neurospora white collar complex dictates circadian regulation and light responses. Mol. Cell. Biol. 36, 781–793 (2016).

    CAS  PubMed Central  Google Scholar 

  47. Linden, H. & Macino, G. White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J. 16, 98–109 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Schwerdtfeger, C. & Linden, H. Localization and light-dependent phosphorylation of white collar 1 and 2, the two central components of blue light signaling in Neurospora crassa. Eur. J. Biochem. 267, 414–421 (2000).

    CAS  PubMed  Google Scholar 

  49. Cheng, P., Yang, Y., Wang, L., He, Q. & Liu, Y. WHITE COLLAR-1, a multifunctional Neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J. Biol. Chem. 278, 3801–3808 (2003).

    CAS  PubMed  Google Scholar 

  50. Sanz, C. et al. Phycomyces MADB interacts with MADA to form the primary photoreceptor complex for fungal phototropism. Proc. Natl Acad. Sci. USA 106, 7095–7100 (2009).

    CAS  PubMed  Google Scholar 

  51. Idnurm, A. et al. The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc. Natl Acad. Sci. USA 103, 4546–4551 (2006).

    CAS  PubMed  Google Scholar 

  52. Sancar, A. Structure and function of DNA photolyase and cryptochrome blue light-photoreceptors. Chem. Rev. 103, 2203–2237 (2003).

    CAS  PubMed  Google Scholar 

  53. Bayram, Ö., Biesemann, C., Krappmann, S., Galland, P. & Braus, G. H. More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol. Biol. Cell 19, 3254–3262 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Berrocal-Tito, G. M., Esquivel-Naranjo, E. U., Horwitz, B. A. & Herrera-Estrella, A. Trichoderma atroviride PHR1, a fungal photolyase responsible for DNA repair, autoregulates its own photoinduction. Eukaryot. Cell 6, 1682–1692 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Cohrs, K. C. & Schumacher, J. The two cryptochrome/photolyase family proteins fulfill distinct roles in DNA photorepair and regulation of conidiation in the gray mold fungus Botrytis cinerea. Appl. Environ. Microbiol. 83, e00812–17 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Brych, A. et al. White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis. MicrobiologyOpen 5, 224–243 (2016).

    CAS  PubMed  Google Scholar 

  57. Scheerer, P. et al. Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497–502 (2008).

    CAS  PubMed  Google Scholar 

  58. Spudich, J. L. The multitalented microbial sensory rhodopsins. Trends Microbiol. 14, 480–487 (2006).

    CAS  PubMed  Google Scholar 

  59. Bieszke, J. A. et al. The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. Proc. Natl Acad. Sci. USA 96, 8034–8039 (1999).

    CAS  PubMed  Google Scholar 

  60. Bieszke, J. A., Spudich, E. N., Scott, K. L., Borkovich, K. A. & Spudich, J. L. A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38, 14138–14145 (1999).

    CAS  PubMed  Google Scholar 

  61. Ernst, O. P. et al. Microbial and animal rhodopsins: structures, functions and molecular mechanisms. Chem. Rev. 114, 126–163 (2014).

    CAS  PubMed  Google Scholar 

  62. Waschuk, S. A., Bezerra, A. G. J., Shi, L. & Brown, L. S. Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc. Natl Acad. Sci. USA 102, 6879–6883 (2005).

    CAS  PubMed  Google Scholar 

  63. Brown, L. S., Dioumaev, A. K., Lanyi, J. K., Spudich, E. N. & Spudich, J. L. Photochemical reaction cycle and proton transfer in Neurospora rhodopsin. J. Biol. Chem. 276, 32495–32505 (2001).

    CAS  PubMed  Google Scholar 

  64. Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98–102 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Rodriguez-Romero, J., Hedtke, M., Kastner, C., Müller, S. & Fischer, R. Fungi, hidden in soil or up in the air: light makes a difference. Annu. Rev. Microbiol. 64, 585–510 (2010).

    CAS  PubMed  Google Scholar 

  66. Smith, H. Phytochromes and light signal perception by plants — an emerging synthesis. Nature 407, 585–591 (2000).

    CAS  PubMed  Google Scholar 

  67. Inoue, K., Nishihama, R. & Kohchi, T. Evolutionary origin of phytochrome responses and signaling in land plants. Plant Cell Environ. 40, 2502–2508 (2017).

    CAS  PubMed  Google Scholar 

  68. Rockwell, N. C., Su, Y. S. & Lagarias, J. C. Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57, 837–858 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Blumenstein, A. et al. The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 15, 1833–1838 (2005).

    CAS  PubMed  Google Scholar 

  70. Froehlich, A. C., Noh, B., Vierstra, R. D., Loros, J. & Dunlap, J. C. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot. Cell 4, 2140–2152 (2005). References 69 and 70 are the first to characterize the fungal phytochromes.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Buchberger, T. & Lamparter, T. Streptophyte phytochromes exhibit an N-terminus of cyanobacterial origin and a C-terminus of proteobacterial origin. BMC Res. Notes 8, 1–13 (2015).

    CAS  Google Scholar 

  72. Li, F. W. et al. Phytochrome diversity in green plants and the origin of canonical plant phytochromes. Nat. Commun. 6, 7852 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Wagner, J. R., Brunzelle, J. S., Forest, K. T. & Vierstra, R. D. A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438, 325–331 (2005). This is the first study to report the crystal structure of the photosensory domain of a phytochrome.

    CAS  PubMed  Google Scholar 

  74. Brandt, S., von Stetten, D., Günther, M., Hildebrandt, P. & Frankenberg-Dinkel, N. The fungal phytochrome FphA from Aspergillus nidulans. J. Biol. Chem. 283, 34605–34614 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Adams, T. H., Wieser, J. K. & Yu, J.-H. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62, 35–54 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Smith, K. M. et al. Transcription factors in light and circadian clock signaling networks revealed by genomewide mapping of direct targets for Neurospora white collar complex. Eukaryot. Cell 9, 1549–1556 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Wu, C. et al. Genome-wide characterization of light-regulated genes in Neurospora crassa. G3 (Bethesda) 4, 1731–1745 (2014).

    Google Scholar 

  78. Sancar, C. et al. Combinatorial control of light induced chromatin remodeling and gene activation in Neurospora. PLOS Genet. 11, e1005105 (2015).

    PubMed  PubMed Central  Google Scholar 

  79. He, Q. & Liu, Y. Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation. Genes Dev. 19, 2888–2899 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Schafmeier, T., Kaldi, K., Diernfellner, A., Mohr, C. & Brunner, M. Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toword a cytoplasmic activator. Genes Dev. 20, 297–306 (2005).

    Google Scholar 

  81. Cha, J., Chang, S. S., Huang, G., Cheng, P. & Liu, Y. Control of WHITE COLLAR localization by phosphorylation is a critical step in the circadian negative feedback process. EMBO J. 27, 3246–3255 (2008). This study reports the detailed mechanism of light activation through the WCC.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Talora, C., Franchi, L., Linden, H., Ballario, P. & Macino, G. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 18, 4961–4968 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. He, Q. et al. CKI and CKII mediate the frequency-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev. 20, 2552–2565 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Huang, G. et al. Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop. Genes Dev. 21, 3283–3295 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Schafmeier, T. et al. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122, 235–246 (2005).

    CAS  PubMed  Google Scholar 

  86. Cesbron, F., Oehler, M., Ha, N., Sancar, G. & Brunner, M. Transcriptional refractoriness is dependent on core promoter architecture. Nat. Commun. 6, 6753 (2015).

    CAS  PubMed  Google Scholar 

  87. Li, C., Cesbron, F., Oehler, M., Brunner, M. & Höfer, T. Frequency modulation of transcriptional bursting enables sensitive and rapid gene regulation. Cell Syst. 25, 409–423.e11 (2018).

    Google Scholar 

  88. Brenna, A., Grimaldi, B., Filetici, P. & Ballario, P. Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in Neurospora crassa. Mol. Biol. Cell 23, 3863–3872 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Grimaldi, B. et al. The Neurospora crassa White Collar-1 dependent bluit light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol. Biol. Cell 17, 4576–4583 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Ruesch, C. E. et al. The histone H3 lysine 9 methyltransferase DIM-5 modifies chromatin at frequency and represses light-activated gene expression. G3 (Bethesda) 5, 93–101 (2014).

    Google Scholar 

  91. Raduwan, H., Isola, A. L. & Belden, W. J. Methylation of histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock gene expression. J. Biol. Chem. 288, 8380–8390 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Hurley, J. M. et al. Analysis of clock-regulated genes in Neurospora reveals widespread posttranscriptional control of metabolic potential. Proc. Natl Acad. Sci. USA 111, 16995–17002 (2014).

    CAS  PubMed  Google Scholar 

  93. Purschwitz, J. et al. Functional and physical interaction of blue and red-light sensors in Aspergillus nidulans. Curr. Biol. 18, 255–259 (2008).

    CAS  PubMed  Google Scholar 

  94. Casas-Flores, S., Rios-Momberg, M., Bibbins, M., Ponce-Noyola, P. & Herrera-Estrella, A. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 150, 3561–3569 (2004).

    CAS  PubMed  Google Scholar 

  95. Casas-Flores, S. et al. Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot. Cell 5, 499–506 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Sánchez-Arrguín, A., Pérez-Martínez, A. S. & Herrera-Estrella, A. Proteomic analysis of Trichoderma atroviride reveals independent roles for transcription factors BLR-1 and BLR-2 in light and darkness. Eukaryot. Cell 11, 30–41 (2012).

    Google Scholar 

  97. Lokhandwala, J. et al. Structural biochemistry of a fungal LOV domain photoreceptor reveals an evolutionarily conserved pathway integrating light and oxidative stress. Structure 23, 116–125 (2015). This study reports the link between light and stress.

    CAS  PubMed  Google Scholar 

  98. Chen, C. H., DeMay, B. S., Gladfelter, A. S., Dunlap, J. C. & Loros, J. J. Physical interraction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proc. Natl Acad. Sci. USA 107, 16715–16720 (2010).

    CAS  PubMed  Google Scholar 

  99. Malzahn, E., Ciprianidis, S., Káldi, K., Schafmeier, T. & Brunner, M. Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142, 762–772 (2010).

    CAS  PubMed  Google Scholar 

  100. Ruger-Herreros, C., Gil-Sanchez Mdel, M., Sancar, G., Brunner, M. & Corrochano, L. M. Alteration of light-dependent gene regulation by the absence of the RCO-1/RCM-1 repressor complex in the fungus Neurospora crassa. PLOS ONE 9, e95069 (2014).

    PubMed  PubMed Central  Google Scholar 

  101. Schumacher, J., Simon, A., Cohrs, K. C., Viaud, M. & Tudzynski, P. The transcription factor BcLTF1 regulates virulence and light responses in the necrotrophic plant pathogen Botrytis cinerea. PLOS Genet. 10, e1004040 (2014).

    PubMed  PubMed Central  Google Scholar 

  102. Corrochano, L. M. et al. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr. Biol. 26, 1577–1584 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Idnurm, A. & Heitman, J. Light controls growth and development via a conserved pathway in the fungal kingdom. PLOS Biol. 3, 615–626 (2005). This study clones the blue-light photoreceptor in Phycomyces blakesleeanus more than 30 years after the isolation of the corresponding mutant.

    CAS  Google Scholar 

  104. Schmoll, M., Franchi, L. & Kubicek, C. P. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (anamorph Trichoderma reesei), modulates cellulase gene transcription in reponse to light. Eukaryot. Cell 4, 1998–2007 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Hedtke, M. et al. Light-dependent gene activation in Aspergillus nidulans is strictly dependent on phytochrome and involves the interplay of phytochrome and white collar-regulated histone H3 acetylation. Mol. Microbiol. 97, 733–745 (2015).

    CAS  PubMed  Google Scholar 

  106. Cervantes-Badillo, M. G., Muñoz-Centeno, T., Uresti-Rivera, E. E., Argüello-Astorga, G. R. & Casas-Flores, S. The Trichoderma atroviride photolyase-encoding gene is transcriptionally regulated by non-canonical light response elements. FEBS J. 280, 3697–3708 (2013).

    CAS  PubMed  Google Scholar 

  107. Olmedo, M., Ruger-Herreros, C., Luque, E. M. & Corrochano, L. M. A complex photoreceptor system mediates the regulation by light of the conidiation genes con-10 and con-6 in Neurospora crassa. Fungal Genet. Biol. 47, 352–363 (2010).

    CAS  PubMed  Google Scholar 

  108. Wang, Z. et al. Light sensing by opsins and fungal ecology: NOP-1 modulates entry into sexual reproduction in response to environmental cues. Mol. Ecol. 27, 216–232 (2017).

    PubMed  PubMed Central  Google Scholar 

  109. García-Martínez, J., B., M., Avalos, J. & Termpitz, U. The CarO rhodopsin of the fungus Fusarium fujikuroi is a light-driven protein pump that retards spore germination. Sci. Rep. 5, 7798 (2015). This paper provides the first demonstration of fast proton-pumping activity of a fungal opsin.

    PubMed  PubMed Central  Google Scholar 

  110. Peñalva, M. A., Tilburn, J., Bignell, E. & Arst, H. N. J. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 16, 291–300 (2008).

    PubMed  Google Scholar 

  111. Alkan, N. et al. Global aspects of pacC regulation of pathogenicity genes in Colletotrichum gloeosporioides as revealed by transcriptome analysis. Mol. Plant Microbe Interact. 26, 1345–1358 (2013).

    CAS  PubMed  Google Scholar 

  112. Avelar, G. M. et al. A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24, 1234–1240 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Avelar, G. M. et al. A cyclic GMP-dependent K+ channel in the blastocladiomycete fungus Blastocladiella emersonii. Eukaryot. Cell 14, 958–963 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Bhoo, S.-H., Davis, S. J., Walker, J., Karniol, B. & Vierstra, R. D. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414, 776–779 (2001).

    CAS  PubMed  Google Scholar 

  115. Nagatani, K. Plant biology. Lighting up the nucleus. Science 288, 821–822 (2000).

    CAS  PubMed  Google Scholar 

  116. Bayram, O. et al. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320, 1504–1506 (2008).

    CAS  PubMed  Google Scholar 

  117. Bayram, Ö. & Braus, G. H. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36, 1–24 (2012).

    CAS  PubMed  Google Scholar 

  118. Azuma, N. et al. In vitro analysis of His-Asp phosphorelays in Aspergillus nidulans: the first direct biochemical evidence for the existence of His-Asp phosphotransfer system in filamentous fungi. Biosci. Biotechnol. Biochem. 71, 2493–2502 (2007).

    CAS  PubMed  Google Scholar 

  119. Wang, Z. et al. The fast-evolving phy-2 gene modulates sexual development in response to light in the model fungus Neurospora crassa. mBio https://doi.org/10.1128/mBio.02148-15 (2016).

  120. Fuller, K. K., Cramer, R. A., Zegans, M. E., Dunlap, J. C. & Loros, J. J. Aspergillus fumigatus photobiology illuminates the marked heterogeneity between isolates. mBio 7, e01517-16 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Lukens, R. J. Reversal by red light of blue light inhibition of sporulation in Alternaria solani. Phytophathology 55, 1032 (1965).

    Google Scholar 

  122. Pruß, S. et al. Role of the Alternaria alternata blue-light receptor WC-1 (LreA) in spore formation and secondary metabolism. Appl. Environ. Microbiol. 80, 2582–2591 (2014).

    PubMed  PubMed Central  Google Scholar 

  123. García-Esquivel, M., Esquivel-Naranjo, E. U., Hernández-Oñate, M. A., Ibarra-Laclette, E. & Herrera-Estrella, A. The Trichoderma atroviride cryptochrome/photolyase genes regulate the expression of blr1-independent genes both in red and blue light. Fungal Biol. 120, 500–512 (2016).

    PubMed  Google Scholar 

  124. Verma, S. & Idnurm, A. The Uve1 endonuclease is regulated by the White Collar Complex to protect Cryptococcus neoformans from UV damage. PLOS Genet. 9, e1003769 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Rangel, D. E. N., Fernandes, E. K. K., Braga, G. U. L. & Roberts, D. W. Visible light during mycelial growth and conidiation of Metarhizium robertsii produces conidia with increased stress tolerance. FEMS Microbiol. Lett. 315, 81–86 (2011).

    CAS  PubMed  Google Scholar 

  126. Hu, Y. et al. Disruption of a phytochrome-like histidine kinase gene by homologous recombination leads to a significant reduction in vegetative growth, sclerotia production, and the pathogenicity of Botrytis cinerea. Physiol. Mol. Plant Pathol. 85, 25–33 (2014).

    CAS  Google Scholar 

  127. Qiu, L., Wang, J. J., Chu, Z. J., Ying, S. H. & Feng, M. G. Phytochrome controls conidiation in response to red/far-red light and daylight length and regulates multistress tolerance in Beauveria bassiana. Environ. Microbiol. 16, 2316–2328 (2014).

    CAS  PubMed  Google Scholar 

  128. Hérivaux, A. et al. Major sensing proteins in pathogenic fungi: the hybrid histidine kinase family. PLOS Genet. 12, e1005683 (2016).

    Google Scholar 

  129. de Castro, P. A. et al. ChIP-seq reveals a role for CrzA in the Aspergillus fumigatus high-osmolarity glycerol response (HOG) signalling pathway. Mol. Microbiol. 94, 655–674 (2014).

    PubMed  Google Scholar 

  130. Takeshita, N. et al. Pulses of Ca2+ coordinate actin assembly and exocytosis for stepwise cell extension. Proc. Natl Acad. Sci. USA 114, 5701–5706 (2017).

    CAS  PubMed  Google Scholar 

  131. Zhou, L. et al. Superresolution and pulse-chase imaging reveal the role of vesicle transport in polar growth of fungal cells. Sci. Adv. 4, e1701798 (2018).

    PubMed  PubMed Central  Google Scholar 

  132. Tisch, D., Kubicek, C. P. & Schmoll, M. New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet. Biol. 48, 631–640 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Schmoll, M., Esquivel-Naranjo, E. U. & Herrera-Estrella, A. Trichoderma in the light of day — physiology and development. Fungal Genet. Biol. 47, 909–916 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Bodvard, K., Jörhov, A., Blomberg, A., Molin, M. & Käll, M. The yeast transcription factor Crz1 is activated by light in a Ca2+/calcineurin-dependent and PKA-independent manner. PLOS ONE 8, e53404 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Bodvard, K. et al. Light-sensing via hydrogen peroxide and a peroxiredoxin. Nat. Commun. 8, 14791 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Hao, N. & O’Shea, E. K. Signal-dependent dynamics of transcription factor translocation controls gene expression. Nat. Struct. Mol. Biol. 19, 31–39 (2011).

    PubMed  PubMed Central  Google Scholar 

  137. Purschwitz, J., Müller, S. & Fischer, R. Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the white collar protein LreB. Mol. Genet. Genomics. 281, 35–42 (2009).

    CAS  Google Scholar 

  138. Rauscher, S., Pacher, S., Hedtke, M., Kniemeyer, O. & Fischer, R. A phosphorylation code of the Aspergillus nidulans global regulator VelvetA (VeA) determines specific functions. Mol. Microbiol. 99, 909–924 (2016).

    CAS  PubMed  Google Scholar 

  139. Smith, H. Light quality, photoperception, and plant strategy. Annu. Rev. Plant Physiol. 33, 481–518 (1982).

    CAS  Google Scholar 

  140. Njimona, I., Yang, R. & Lamparter, T. Temperature effects on bacterial phytochrome. PLOS ONE 9, e109794 (2014).

    PubMed  PubMed Central  Google Scholar 

  141. Legris, M. et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900 (2016).

    CAS  PubMed  Google Scholar 

  142. Jung, J. H. et al. Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889 (2016).

    CAS  PubMed  Google Scholar 

  143. Casal, J. J. & Qüesta, J. I. Light and temperature cues: multitasking receptors and transcriptional integrators. New Phytol. 217, 1029–1034 (2018).

    PubMed  Google Scholar 

  144. Shen, W. L. et al. Function of rhodopsin in temperature discrimination in Drosophila. Science 331, 1333–1336 (2011).

    CAS  PubMed  Google Scholar 

  145. Nakasone, Y., Ono, T.-A., Ishii, A., Masuda, S. & Terazima, M. Temperature-sensitive reaction of a photosensor protein YcgF: possibility of a role of temperature sensor. Biochemistry 49, 2288–2296 (2010).

    CAS  PubMed  Google Scholar 

  146. Fujii, Y. et al. Phototropin perceives temperature based on the lifetime of its photoactivated state. Proc. Natl Acad. Sci. USA 114, 9206–9211 (2017).

    CAS  PubMed  Google Scholar 

  147. Schafmeier, T. et al. Circadian activity and abundance rhythms of the Neurospora clock tanscription factor WCC associated with rapid nucleo-cytoplamic shuttling. Genes Dev. 22, 3397–3402 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Hunt, S. M., Thompson, S., Elvin, M. & Heintzen, C. VIVID interacts with the WHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora. Proc. Natl Acad. Sci. USA 107, 16709–16714 (2010).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work of the authors’ laboratory was supported by the German Science Foundation (DFG Fi 459/19-1) and the China Scholar Council (CSC). The authors thank A. Diernfellner (Heidelberg) and J. Schumacher (Münster) for Neurospora crassa strains and providing some images for Fig. 2.

Reviewer information

Nature Reviews Microbiology thanks A. Herrera-Estrella, J. Loros and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

  1. Karlsruhe Institute of Technology (KIT) — South Campus, Institute for Applied Biosciences, Department of Microbiology, Karlsruhe, Germany

    Zhenzhong Yu & Reinhard Fischer

Authors
  1. Zhenzhong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reinhard Fischer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Z.Y. and R.F. researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and/or edited the manuscript before submission.

Corresponding author

Correspondence to Reinhard Fischer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Chromophore

An organic molecule that absorbs light in the visible spectrum. Photoreceptors are proteins containing a chromophore, which upon light absorption cause structural changes of the attached protein.

Flavin

An organic molecule with a characteristic tricyclic heterocycle (isoalloxazine).

Linear tetrapyrrole

An organic molecule composed of four five-atom rings. They can be cyclic, as in haemoglobin, or linear, like in biliverdin.

Phytochrome

A protein that contains a linear tetrapyrrole as a chromophore and absorbs red and far-red light. It is the main photosensor of plants and controls morphogenesis.

Circadian clock

Describes a stable oscillation synchronized by light. The period is approximately (circa) a day (diem).

Sporangiophore

The morphological structure of fungi that produce (resistant) spores, which are small entities for dispersal or for survival.

Cryptochrome

A flavin-binding protein that senses blue light and is involved in circadian rhythms in higher eukaryotes.

Photolyase

An enzyme that repairs DNA damage caused by ultraviolet light. The enzyme contains flavin as cofactor and itself requires blue light for activity.

Photoadduct

A chromophore that attaches covalently to a protein.

Photoadaptation

The phenomenon in which after light signalling the system becomes insensitive for a certain time.

Rhodopsins

The photosensors of the retina. Rhodopsins contain retinal as a chromophore. Rhodopsins are also found in lower eukaryotes and in archaea.

FRQ

A negative regulator of the circadian clock in fungi. Oscillation of transcription of clock-controlled genes requires the positive element, white collar 1 (WC-1), and the negative FRQ protein.

Cleistothecia

The fruiting body of ascomycetes. Spores are produced after meiosis.

Conidiation

The process of the formation of vegetative (asexual) spores. Usually special morphological structures, the conidiophores, are produced, which generate the conidia.

Sclerotia

A multicellular structure used for survival of some fungi. In Botrytis cinerea, it is the prerequisite for sexual fruiting body (apothecia) formation.

High osmolarity glycerol pathway

(HOG pathway). A signalling pathway that is required for the adaptation of yeast and other organisms to high osmolarity conditions.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, Z., Fischer, R. Light sensing and responses in fungi. Nat Rev Microbiol 17, 25–36 (2019). https://doi.org/10.1038/s41579-018-0109-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-018-0109-x

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing