No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

The Complexity of Fungal Vision

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    168.51 Kb
  • HTML
    182.77 Kb
  • PDF
    4.17 MB
  • Authors: Reinhard Fischer1, Jesus Aguirre2, Alfredo Herrera-Estrella3, Luis M. Corrochano4
  • Editors: Joseph Heitman5, Neil A. R. Gow6
    Affiliations: 1: Karlsruhe Institute of Technology (KIT), Institute of Applied Biosciences, Department of Microbiology, D-76131 Karlsruhe, Germany; 2: Departamento de Biología Celular y del Desarrollo, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico; 3: Laboratorio Nacional de Genómica para la Biodiversidad, CINVESTAV-Irapuato, Irapuato, Guanajuato 36821, Mexico; 4: Department of Genetics, University of Seville, 41012 Seville, Spain; 5: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 6: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0020-2016
  • Received 30 June 2016 Accepted 11 July 2016 Published 18 November 2016
  • Reinhard Fischer, [email protected]
image of The Complexity of Fungal Vision
    Preview this microbiology spectrum article:
    Zoom in

    The Complexity of Fungal Vision, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0020-2016-1.gif /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0020-2016-2.gif
  • Abstract:

    Life, as we know it, would not be possible without light. Light is not only a primary source of energy, but also an important source of information for many organisms. To sense light, only a few photoreceptor systems have developed during evolution. They are all based on an organic molecule with conjugated double bonds that allows energy transfer from visible (or UV) light to its cognate protein to translate the primary physical photoresponse to cell-biological actions. The three main classes of receptors are flavin-based blue-light, retinal-based green-light (such as rhodopsin), and linear tetrapyrrole-based red-light sensors. Light not only controls the behavior of motile organisms, but is also important for many sessile microorganisms including fungi. In fungi, light controls developmental decisions and physiological adaptations as well as the circadian clock. Although all major classes of photoreceptors are found in fungi, a good level of understanding of the signaling processes at the molecular level is limited to some model fungi. However, current knowledge suggests a complex interplay between light perception systems, which goes far beyond the simple sensing of light and dark. In this article we focus on recent results in several fungi, which suggest a strong link between light-sensing and stress-activated mitogen-activated protein kinases.

  • Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2016. The Complexity of Fungal Vision. Microbiol Spectrum 4(6):FUNK-0020-2016. doi:10.1128/microbiolspec.FUNK-0020-2016.


1. Casas-Flores S, Herrera-Estrella A. 2016. The bright and dark sides of fungal life, p 41–77. In Druzhinina LS, Kubicek CP (ed), Environmental and Microbial Relationships. Springer, Berlin, Germany. http://dx.doi.org/10.1007/978-3-319-29532-9_3
2. Berrocal-Tito G, Sametz-Baron L, Eichenberg K, Horwitz BA, Herrera-Estrella A. 1999. Rapid blue light regulation of a Trichoderma harzianum photolyase gene. J Biol Chem 274:14288–14294 http://dx.doi.org/10.1074/jbc.274.20.14288.
3. Esquivel-Naranjo EU, García-Esquivel M, Medina-Castellanos E, Correa-Pérez VA, Parra-Arriaga JL, Landeros-Jaime F, Cervantes-Chávez JA, Herrera-Estrella A. 2016. A Trichoderma atroviride stress-activated MAPK pathway integrates stress and light signals. Mol Microbiol 100:860–876 http://dx.doi.org/10.1111/mmi.13355.
4. Yu Z, Armant O, Fischer R. 2016. Fungi use the SakA (HogA) pathway for phytochrome-dependent light signalling. Nat Microbiol 1:16019. http://dx.doi.org/10.1038/nmicrobiol.2016.19.
5. Lamb TM, Goldsmith CS, Bennett L, Finch KE, Bell-Pedersen D. 2011. Direct transcriptional control of a p38 MAPK pathway by the circadian clock in Neurospora crassa. PLoS One 6:e27149. http://dx.doi.org/10.1371/journal.pone.0027149.
6. Payen A. 1843. Extrait d’un rapport adressé à M. Le Maréchal Duc de Dalmatie, Ministre de la guerre, President du Conseil, sur und altération extraordinaire du pain de munition. Ann Chim Phys 9:5–21.
7. Marsh PB, Taylor EE, Bassler LM. 1959. A guide to the literature on certain effects of light on fungi: reproduction, morphology, pigmentation, and phototropic phenomena. Plant Dis Reptr 261(Suppl) :251–312.
8. Horwitz BA, Perlman A, Gressel J. 1990. Induction of Trichoderma sporulation by nanosecond laser pulses: evidence against cryptochrome cycling. Photochem Photobiol 51:99–104 http://dx.doi.org/10.1111/j.1751-1097.1990.tb01689.x.
9. Betina V, Zajacová J. 1978. Inhibition of photo-induced Trichoderma viride conidiation by inhibitors of RNA synthesis. Folia Microbiol (Praha) 23:460–464 http://dx.doi.org/10.1007/BF02885576.
10. Corrochano LM. 2007. Fungal photoreceptors: sensory molecules for fungal development and behaviour. Photochem Photobiol Sci 6:725–736 http://dx.doi.org/10.1039/b702155k.
11. Purschwitz J, Müller S, Kastner C, Fischer R. 2006. Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9:566–571 http://dx.doi.org/10.1016/j.mib.2006.10.011.
12. Herrera-Estrella A, Horwitz BA. 2007. Looking through the eyes of fungi: molecular genetics of photoreception. Mol Microbiol 64:5–15 http://dx.doi.org/10.1111/j.1365-2958.2007.05632.x.
13. Rodriguez-Romero J, Hedtke M, Kastner C, Müller S, Fischer R. 2010. Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64:585–610 http://dx.doi.org/10.1146/annurev.micro.112408.134000. [CrossRef]
14. Bayram O, Braus GH, Fischer R, Rodriguez-Romero J. 2010. Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet Biol 47:900–908 http://dx.doi.org/10.1016/j.fgb.2010.05.008.
15. Dasgupta A, Fuller KK, Dunlap JC, Loros JJ. 2016. Seeing the world differently: variability in the photosensory mechanisms of two model fungi. Environ Microbiol 18:5–20 http://dx.doi.org/10.1111/1462-2920.13055.
16. Fuller KK, Loros JJ, Dunlap JC. 2015. Fungal photobiology: visible light as a signal for stress, space and time. Curr Genet 61:275–288 http://dx.doi.org/10.1007/s00294-014-0451-0.
17. Idnurm A, Verma S, Corrochano LM. 2010. A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol 47:881–892 http://dx.doi.org/10.1016/j.fgb.2010.04.009.
18. Okamoto S, Furuya K, Nozaki S, Aoki K, Niki H. 2013. Synchronous activation of cell division by light or temperature stimuli in the dimorphic yeast Schizosaccharomyces japonicus. Eukaryot Cell 12:1235–1243 http://dx.doi.org/10.1128/EC.00109-13.
19. Bayram O, Biesemann C, Krappmann S, Galland P, Braus GH. 2008. More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol Biol Cell 19:3254–3262 http://dx.doi.org/10.1091/mbc.E08-01-0061.
20. Bejarano ER, Avalos J, Lipson ED, Cerdá-Olmedo E. 1991. Photoinduced accumulation of carotene in Phycomyces. Planta 183:1–9 http://dx.doi.org/10.1007/BF00197560.
21. De Fabo EC, Harding RW, Shropshire W. 1976. Action spectrum between 260 and 800 nanometers for the photoinduction of carotenoid biosynthesis in Neurospora crassa. Plant Physiol 57:440–445 http://dx.doi.org/10.1104/pp.57.3.440.
22. Galland P, Lipson ED. 1985. Modified action spectra of photogeotropic equilibrium in Phycomyces blakesleeanus mutants with defects in genes madA, madB, madC, and madH. Photochem Photobiol 41:331–335 http://dx.doi.org/10.1111/j.1751-1097.1985.tb03493.x.
23. Corrochano LM, Galland P, Lipson ED, Cerdá-Olmedo E. 1988. Photomorphogenesis in Phycomyces: fluence-response curves and action spectra. Planta 174:315–320 http://dx.doi.org/10.1007/BF00959516.
24. Kües U. 2000. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353 http://dx.doi.org/10.1128/MMBR.64.2.316-353.2000.
25. Lu BC. 1965. The role of light in fructification of the basidiomnycete Cyathus stercoreus. Am J Bot 52:432–437 http://dx.doi.org/10.2307/2440258.
26. Lu BC, Gallo N, Kües U. 2003. White-cap mutants and meiotic apoptosis in the basidiomycete Coprinus cinereus. Fungal Genet Biol 39:82–93 http://dx.doi.org/10.1016/S1087-1845(03)00024-0.
27. Morimoto N, Oda Y. 1973. Effects of light on fruit-body formation in a basidiomycete, Coprinus macrorhizus. Plant Cell Physiol 14:217–225.
28. Kertesz-Chaloupková K, Walser PJ, Granado JD, Aebi M, Kües U. 1998. Blue light overrides repression of asexual sporulation by mating type genes in the basidiomcycete Coprinus cinereus. Fungal Genet Biol 23:95–109 http://dx.doi.org/10.1006/fgbi.1997.1024.
29. Lu YK, Sun KH, Shen WC. 2005. Blue light negatively regulates the sexual filamentation via the Cwc1 and Cwc2 proteins in Cryptococcus neoformans. Mol Microbiol 56:480–491 http://dx.doi.org/10.1111/j.1365-2958.2005.04549.x.
30. Idnurm A, Heitman J. 2005. Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3:e95. http://dx.doi.org/10.1371/journal.pbio.0030095.
31. Tan KK. 1974. Blue-light inhibition of sporulation in Botrytis cinerea. J Gen Microbiol 82:191–200 http://dx.doi.org/10.1099/00221287-82-1-191.
32. Lukens RJ. 1963. Photo-inhibition of sporulation in Alternaria solani. Am J Bot 50:720–724 http://dx.doi.org/10.2307/2440051.
33. Tan KK. 1974. Red-far-red reversible photoreaction in the recovery from blue-light inhibition of sporulation in Botrytis cinerea. J Gen Microbiol 8a:201–202 http://dx.doi.org/10.1099/00221287-82-1-201.
34. Purschwitz J, Müller S, Kastner C, Schöser 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 18:255–259 http://dx.doi.org/10.1016/j.cub.2008.01.061.
35. Mooney JL, Yager LN. 1990. Light is required for conidiation in Aspergillus nidulans. Genes Dev 4:1473–1482 http://dx.doi.org/10.1101/gad.4.9.1473.
36. Chen CL, Kuo HC, Tung SY, Hsu PW, Wang CL, Seibel C, Schmoll M, Chen RS, Wang TF. 2012. Blue light acts as a double-edged sword in regulating sexual development of Hypocrea jecorina ( Trichoderma reesei). PLoS One 7:e44969 http://dx.doi.org/10.1371/journal.pone.0044969.
37. Innocenti FD, Pohl U, Russo VE. 1983. Photoinduction of protoperithecia in Neurospora crassa by blue light. Photochem Photobiol 37:49–51 http://dx.doi.org/10.1111/j.1751-1097.1983.tb04432.x.
38. Oda K, Hasunuma K. 1997. Genetic analysis of signal transduction through light-induced protein phosphorylation in Neurospora crassa perithecia. Mol Gen Genet 256:593–601 http://dx.doi.org/10.1007/s004380050607.
39. Harding RW, Melles S. 1983. Genetic analysis of phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol 72:996–1000 http://dx.doi.org/10.1104/pp.72.4.996.
40. Lauter FR, Marchfelder U, Russo VE, Yamashiro CT, Yatzkan E, Yarden O. 1998. Photoregulation of cot-1, a kinase-encoding gene involved in hyphal growth in Neurospora crassa. Fungal Genet Biol 23:300–310 http://dx.doi.org/10.1006/fgbi.1998.1038.
41. Fuller KK, Ringelberg CS, Loros JJ, Dunlap JC. 2013. The fungal pathogen Aspergillus fumigatus regulates growth, metabolism, and stress resistance in response to light. MBio 4:e00142-13. http://dx.doi.org/10.1128/mBio.00142-13.
42. Röhrig J, Kastner C, Fischer R. 2013. Light inhibits spore germination through phytochrome in Aspergillus nidulans. Curr Genet 59:55–62 http://dx.doi.org/10.1007/s00294-013-0387-9.
43. Chen C, Dickman MB. 2002. Colletotrichum trifolii TB3 kinase, a COT1 homolog, is light inducible and becomes localized in the nucleus during hyphal elongation. Eukaryot Cell 1:626–633 http://dx.doi.org/10.1128/EC.1.4.626-633.2002.
44. Ambra R, Grimaldi B, Zamboni S, Filetici P, Macino G, Ballario P. 2004. Photomorphogenesis in the hypogeous fungus Tuber borchii: isolation and characterization of Tbwc-1, the homologue of the blue-light photoreceptor of Neurospora crassa. Fungal Genet Biol 41:688–697 http://dx.doi.org/10.1016/j.fgb.2004.02.004.
45. Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A. 2004. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 150:3561–3569 http://dx.doi.org/10.1099/mic.0.27346-0.
46. Zalokar M. 1954. Studies on biosynthesis of carotenoids in Neurospora crassa. Arch Biochem Biophys 50:71–80 http://dx.doi.org/10.1016/0003-9861(54)90010-7.
47. Avalos J, Schrott EL. 1990. Photoinduction of carotenoid biosynthesis in Gibberella fujikuroi. FEMS Lett 66:295–298 http://dx.doi.org/10.1111/j.1574-6968.1990.tb04014.x.
48. Calvo AM. 2008. The VeA regulatory system and its role in morphological and chemical development in fungi. Fungal Genet Biol 45:1053–1061 http://dx.doi.org/10.1016/j.fgb.2008.03.014.
49. Atoui A, Kastner C, Larey CM, Thokala R, Etxebeste O, Espeso EA, Fischer R, Calvo AM. 2010. Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet Biol 47:962–972 http://dx.doi.org/10.1016/j.fgb.2010.08.007.
50. 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 http://dx.doi.org/10.1016/bs.adgen.2015.09.003.
51. Hurley J, Loros JJ, Dunlap JC. 2015. Dissecting the mechanisms of the clock in Neurospora. Methods Enzymol 551:29–52 http://dx.doi.org/10.1016/bs.mie.2014.10.009.
52. Baker CL, Loros JJ, Dunlap JC. 2012. The circadian clock of Neurospora crassa. FEMS Microbiol Rev 36:95–110 http://dx.doi.org/10.1111/j.1574-6976.2011.00288.x.
53. Merrow M, Boesl C, Ricken J, Messerschmitt M, Goedel M, Roenneberg T. 2006. Entrainment of the Neurospora circadian clock. Chronobiol Int 23:71–80 http://dx.doi.org/10.1080/07420520500545888.
54. Froehlich AC, Liu Y, Loros JJ, Dunlap JC. 2002. White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297:815–819 http://dx.doi.org/10.1126/science.1073681.
55. 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 297:840–843 http://dx.doi.org/10.1126/science.1072795.
56. Corrochano LM, Garre V. 2010. Photobiology in the Zygomycota: multiple photoreceptor genes for complex responses to light. Fungal Genet Biol 47:893–899 http://dx.doi.org/10.1016/j.fgb.2010.04.007.
57. Saranak J, Foster KW. 1997. Rhodopsin guides fungal phototaxis. Nature 387:465–466 http://dx.doi.org/10.1038/387465a0.
58. 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 24:1234–1240 http://dx.doi.org/10.1016/j.cub.2014.04.009.
59. Ruger-Herreros C, Rodríguez-Romero J, Fernández-Barranco R, Olmedo M, Fischer R, Corrochano LM, Canovas D. 2011. Regulation of conidiation by light in Aspergillus nidulans. Genetics 188:809–822 http://dx.doi.org/10.1534/genetics.111.130096.
60. Sánchez-Arreguín A, Pérez-Martínez AS, Herrera-Estrella A. 2012. 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 http://dx.doi.org/10.1128/EC.05263-11.
61. Bayram Ö, Feussner K, Dumkow M, Herrfurth C, Feussner I, Braus GH. 2016. Changes of global gene expression and secondary metabolite accumulation during light-dependent Aspergillus nidulans development. Fungal Genet Biol 87:30–53 http://dx.doi.org/10.1016/j.fgb.2016.01.004.
62. Wu C, Yang F, Smith KM, Peterson M, Dekhang R, Zhang Y, Zucker J, Bredeweg EL, Mallappa C, Zhou X, Lyubetskaya A, Townsend JP, Galagan JE, Freitag M, Dunlap JC, Bell-Pedersen D, Sachs MS. 2014. Genome-wide characterization of light-regulated genes in Neurospora crassa. G3 (Bethesda) 4:1731–1745 http://dx.doi.org/10.1534/g3.114.012617.
63. Corrochano LM, Galland P. 2016. Photomorphogenesis and gravitropism in fungi, p 235–266. In Wendland J (ed), The Mycota. I. Growth, Differentiation and Sexuality. Springer, Berlin, Germany. http://dx.doi.org/10.1007/978-3-319-25844-7_11
64. García-Esquivel M, Esquivel-Naranjo EU, Hernández-Oñate MA, Ibarra-Laclette E, Herrera-Estrella A. 2016. The Trichoderma atroviride cryptochrome/photolyase genes regulate the expression of blr1-independent genes both in red and blue light. Fungal Biol 120:500–512 http://dx.doi.org/10.1016/j.funbio.2016.01.007.
65. Cetz-Chel JE, Balcázar-López E, Esquivel-Naranjo EU, Herrera-Estrella A. 2016. The Trichoderma atroviride putative transcription factor Blu7 controls light responsiveness and tolerance. BMC Genomics 17:327. http://dx.doi.org/10.1186/s12864-016-2639-9.
66. Corrochano LM, et al. 2016. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr Biol 26:1577–1584.
67. Delbrück M, Shropshire W. 1960. Action and transmission spectra of Phycomyces. Plant Physiol 35:194–204 http://dx.doi.org/10.1104/pp.35.2.194. [CrossRef]
68. Bergman K, Eslava AP, Cerdá-Olmedo E. 1973. Mutants of Phycomyces with abnormal phototropism. Mol Gen Genet 123:1–16 http://dx.doi.org/10.1007/BF00282984.
69. Gressel JB, Hartmann KM. 1968. Morphogenesis in Trichoderma: action spectrum of photoinduced sporulation. Planta 79:271–274 http://dx.doi.org/10.1007/BF00396034.
70. Kumagai T, Oda Y. 1969. An action spectrum for photoinduced sporulation in the fungus Trichoderma viride. Plant Cell Physiol 10:387–392.
71. Otto MK, Jayaram M, Hamilton RM, Delbrück M. 1981. Replacement of riboflavin by an analogue in the blue-light photoreceptor of Phycomyces. Proc Natl Acad Sci USA 78:266–269 http://dx.doi.org/10.1073/pnas.78.1.266.
72. 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 15:1650–1657.
73. Ballario P, Macino G. 1997. White collar proteins: PASsing the light signal in Neurospora crassa. Trends Microbiol 5:458–462 http://dx.doi.org/10.1016/S0966-842X(97)01144-X.
74. 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 15:1833–1838 http://dx.doi.org/10.1016/j.cub.2005.08.061.
75. Schleicher E, Kowalczyk RM, Kay CW, Hegemann P, Bacher A, Fischer M, Bittl R, Richter G, Weber S. 2004. On the reaction mechanism of adduct formation in LOV domains of the plant blue-light receptor phototropin. J Am Chem Soc 126:11067–11076 http://dx.doi.org/10.1021/ja049553q.
76. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506.
77. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, Tag AG, Sancar C, Bredeweg EL, Priest HD, McCormick RF, Thomas TL, Carrington JC, Stajich JE, Bell-Pedersen D, Brunner M, Freitag M. 2010. 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 http://dx.doi.org/10.1128/EC.00154-10.
78. Wang B, Zhou X, Loros JJ, Dunlap JC. 2016. Alternative use of DNA binding domains by the Neurospora white collar complex dictates circadian regulation and light responses. Mol Cell Biol 36:781–793 http://dx.doi.org/10.1128/MCB.00841-15.
79. Silva F, Torres-Martínez S, Garre V. 2006. Distinct white collar-1 genes control specific light responses in Mucor circinelloides. Mol Microbiol 61:1023–1037 http://dx.doi.org/10.1111/j.1365-2958.2006.05291.x.
80. Silva F, Navarro E, Peñaranda A, Murcia-Flores L, Torres-Martínez S, Garre V. 2008. A RING-finger protein regulates carotenogenesis via proteolysis-independent ubiquitylation of a white collar-1-like activator. Mol Microbiol 70:1026–1036.
81. Sanz C, Rodríguez-Romero J, Idnurm A, Christie JM, Heitman J, Corrochano LM, Eslava AP. 2009. Phycomyces MADB interacts with MADA to form the primary photoreceptor complex for fungal phototropism. Proc Natl Acad Sci USA 106:7095–7100 http://dx.doi.org/10.1073/pnas.0900879106.
82. Idnurm A, Rodríguez-Romero J, Corrochano LM, Sanz C, Iturriaga EA, Eslava AP, Heitman J. 2006. The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc Natl Acad Sci USA 103:4546–4551 http://dx.doi.org/10.1073/pnas.0600633103.
83. Larhammar D, Nordström K, Larsson TA. 2009. Evolution of vertebrate rod and cone phototransduction genes. Philos Trans R Soc Lond B Biol Sci 364:2867–2880 http://dx.doi.org/10.1098/rstb.2009.0077.
84. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, Dunlap JC, Crane BR. 2007. Conformational switching in the fungal light sensor Vivid. Science 316:1054–1057 http://dx.doi.org/10.1126/science.1137128.
85. Lokhandwala J, Hopkins HC, Rodriguez-Iglesias A, Dattenböck C, Schmoll M, Zoltowski BD. 2015. Structural biochemistry of a fungal LOV domain photoreceptor reveals an evolutionarily conserved pathway integrating light and oxidative stress. Structure 23:116–125 http://dx.doi.org/10.1016/j.str.2014.10.020.
86. Lokhandwala J, Silverman y de la Vega RI, Hopkins HC, Britton CW, Rodriguez-Iglesias A, Bogomolni R, Schmoll M, Zoltowski BD. 2016. A native threonine coordinates ordered water to tune LOV photocycle kinetics and osmotic stress signaling in Trichoderma reesei ENVOY. J Biol Chem 291:14839–14850.
87. Malzahn E, Ciprianidis S, Káldi K, Schafmeier T, Brunner M. 2010. Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142:762–772 http://dx.doi.org/10.1016/j.cell.2010.08.010.
88. Vaidya AT, Chen CH, Dunlap JC, Loros JJ, Crane BR. 2011. Structure of a light-activated LOV protein dimer that regulates transcription. Sci Signal 4:ra50. http://dx.doi.org/10.1126/scisignal.2001945.
89. Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A, Börner T. 1997. A prokaryotic phytochrome. Nature 386:663 http://dx.doi.org/10.1038/386663a0.
90. Butler WL, Norris KH, Siegelman HW, Hendricks SB. 1959. Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci USA 45:1703–1708 http://dx.doi.org/10.1073/pnas.45.12.1703.
91. Yeh K-C, Wu S-H, Murphy JT, Lagarias JC. 1997. A cyanobacterial phytochrome two-component light sensory system. Science 277:1505–1508 http://dx.doi.org/10.1126/science.277.5331.1505.
92. Fortunato AE, Jaubert M, Enomoto G, Bouly JP, Raniello R, Thaler M, Malviya S, Bernardes JS, Rappaport F, Gentili B, Huysman MJ, Carbone A, Bowler C, d’Alcalà MR, Ikeuchi M, Falciatore A. 2016. Diatom phytochromes reveal the existence of far-red-light-based sensing in the ocean. Plant Cell 28:616–628 http://dx.doi.org/10.1105/tpc.15.00928.
93. Rockwell NC, Duanmu D, Martin SS, Bachy C, Price DC, Bhattacharya D, Worden AZ, Lagarias JC. 2014. Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA 111:3871–3876 http://dx.doi.org/10.1073/pnas.1401871111. (Erratum, http://www.pnas.org/content/112/9/E1051.full.)
94. Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD. 2014. Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proc Natl Acad Sci USA 111:10179–10184 http://dx.doi.org/10.1073/pnas.1403096111.
95. Scheerer P, Michael N, Park JH, Noack S, Förster C, Hammam MA, Inomata K, Choe HW, Lamparter T, Krauss N. 2006. Crystallization and preliminary X-ray crystallographic analysis of the N-terminal photosensory module of phytochrome Agp1, a biliverdin-binding photoreceptor from Agrobacterium tumefaciens. J Struct Biol 153:97–102 http://dx.doi.org/10.1016/j.jsb.2005.11.002.
96. Rockwell NC, Lagarias JC. 2006. The structure of phytochrome: a picture is worth a thousand spectra. Plant Cell 18:4–14 http://dx.doi.org/10.1105/tpc.105.038513.
97. Brandt S, von Stetten D, Günther M, Hildebrandt P, Frankenberg-Dinkel N. 2008. The fungal phytochrome FphA from Aspergillus nidulans. J Biol Chem 283:34605–34614 http://dx.doi.org/10.1074/jbc.M805506200.
98. Njimona I, Yang R, Lamparter T. 2014. Temperature effects on bacterial phytochrome. PLoS One 9:e109794. http://dx.doi.org/10.1371/journal.pone.0109794.
99. Hughes J, Lamparter T. 1999. Prokaryotes and phytochrome. The connection to chromophores and signaling. Plant Physiol 121:1059–1068 http://dx.doi.org/10.1104/pp.121.4.1059.
100. Kooß S, Lamparter T. 2016. Cyanobacterial origin of plant phytochromes. Protoplasma. [Epub ahead of print.] doi:10.1007/s00709-016-0951-5
101. Azuma N, Kanamaru K, Matsushika A, Yamashino T, Mizuno T, Kato M, Kobayashi T. 2007. In vitro analysis of His-Asp phosphorelays in Aspergillus nidulans: the first direct biochemical evidence for the existence of His-Asp phosphotransfer systems in filamentous fungi. Biosci Biotechnol Biochem 71:2493–2502 http://dx.doi.org/10.1271/bbb.70292.
102. 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:e84223. http://dx.doi.org/10.1371/journal.pone.0084223.
103. 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:e02148-15. http://dx.doi.org/10.1128/mBio.02148-15.
104. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M. 2011. The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364 http://dx.doi.org/10.1146/annurev-arplant-042110-103759.
105. Liu H, Liu B, Zhao C, Pepper M, Lin C. 2011. The action mechanisms of plant cryptochromes. Trends Plant Sci 16:684–691 http://dx.doi.org/10.1016/j.tplants.2011.09.002.
106. Froehlich AC, Chen CH, Belden WJ, Madeti C, Roenneberg T, Merrow M, Loros JJ, Dunlap JC. 2010. Genetic and molecular characterization of a cryptochrome from the filamentous fungus Neurospora crassa. Eukaryot Cell 9:738–750 http://dx.doi.org/10.1128/EC.00380-09.
107. Olmedo M, Ruger-Herreros C, Luque EM, Corrochano LM. 2010. 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 http://dx.doi.org/10.1016/j.fgb.2009.11.004.
108. Nsa IY, Karunarathna N, Liu X, Huang H, Boetteger B, Bell-Pedersen D. 2015. A novel cryptochrome-dependent oscillator in Neurospora crassa. Genetics 199:233–245 http://dx.doi.org/10.1534/genetics.114.169441. [CrossRef]
109. Castrillo M, García-Martínez J, Avalos J. 2013. Light-dependent functions of the Fusarium fujikuroi CryD DASH cryptochrome in development and secondary metabolism. Appl Environ Microbiol 79:2777–2788 http://dx.doi.org/10.1128/AEM.03110-12.
110. Veluchamy S, Rollins JA. 2008. A CRY-DASH-type photolyase/cryptochrome from Sclerotinia sclerotiorum mediates minor UV-A-specific effects on development. Fungal Genet Biol 45:1265–1276 http://dx.doi.org/10.1016/j.fgb.2008.06.004.
111. Guzmán-Moreno J, Flores-Martínez A, Brieba LG, Herrera-Estrella A. 2014. The Trichoderma reesei Cry1 protein is a member of the cryptochrome/photolyase family with 6-4 photoproduct repair activity. PLoS One 9:e100625. http://dx.doi.org/10.1371/journal.pone.0100625.
112. Campuzano V, Galland P, Alvarez MI, Eslava AP. 1996. Blue-light receptor requirement for gravitropism, autochemotropism and ethylene response in Phycomyces. Photochem Photobiol 63:686–694 http://dx.doi.org/10.1111/j.1751-1097.1996.tb05674.x.
113. Tagua VG, Pausch M, Eckel M, Gutiérrez G, Miralles-Durán A, Sanz C, Eslava AP, Pokorny R, Corrochano LM, Batschauer A. 2015. Fungal cryptochrome with DNA repair activity reveals an early stage in cryptochrome evolution. Proc Natl Acad Sci USA 112:15130–15135 http://dx.doi.org/10.1073/pnas.1514637112.
114. Sharma AK, Spudich JL, Doolittle WF. 2006. Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 14:463–469 http://dx.doi.org/10.1016/j.tim.2006.09.006.
115. Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H. 2014. Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 114:126–163 http://dx.doi.org/10.1021/cr4003769.
116. Spudich JL. 2006. The multitalented microbial sensory rhodopsins. Trends Microbiol 14:480–487 http://dx.doi.org/10.1016/j.tim.2006.09.005.
117. Brown LS, Dioumaev AK, Lanyi JK, Spudich EN, Spudich JL. 2001. Photochemical reaction cycle and proton transfers in Neurospora rhodopsin. J Biol Chem 276:32495–32505 http://dx.doi.org/10.1074/jbc.M102652200.
118. Bergo V, Spudich EN, Spudich JL, Rothschild KJ. 2002. A Fourier transform infrared study of Neurospora rhodopsin: similarities with archaeal rhodopsins. Photochem Photobiol 76:341–349 http://dx.doi.org/10.1562/0031-8655(2002)076<0341:AFTISO>2.0.CO;2.
119. Furutani Y, Bezerra AGJ Jr, Waschuk S, Sumii M, Brown LS, Kandori H. 2004. FTIR spectroscopy of the K photointermediate of Neurospora rhodopsin: structural changes of the retinal, protein, and water molecules after photoisomerization. Biochemistry 43:9636–9646 http://dx.doi.org/10.1021/bi049158c.
120. Bieszke JA, Braun EL, Bean LE, Kang S, Natvig DO, Borkovich KA. 1999. 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 http://dx.doi.org/10.1073/pnas.96.14.8034.
121. Bieszke JA, Spudich EN, Scott KL, Borkovich KA, Spudich JL. 1999. A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38:14138–14145 http://dx.doi.org/10.1021/bi9916170.
122. Bieszke JA, Li L, Borkovich KA. 2007. The fungal opsin gene nop-1 is negatively-regulated by a component of the blue light sensing pathway and influences conidiation-specific gene expression in Neurospora crassa. Curr Genet 52:149–157 http://dx.doi.org/10.1007/s00294-007-0148-8.
123. Idnurm A, Howlett BJ. 2001. Characterization of an opsin gene from the ascomycete Leptosphaeria maculans. Genome 44:167–171 http://dx.doi.org/10.1139/g00-113.
124. Waschuk SA, Bezerra AGJ Jr, Shi L, Brown LS. 2005. Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci USA 102:6879–6883 http://dx.doi.org/10.1073/pnas.0409659102.
125. Prado MM, Prado-Cabrero A, Fernández-Martín R, Avalos J. 2004. A gene of the opsin family in the carotenoid gene cluster of Fusarium fujikuroi. Curr Genet 46:47–58 http://dx.doi.org/10.1007/s00294-004-0508-6.
126. García-Martínez J, Brunk M, Avalos J, Terpitz U. 2015. The CarO rhodopsin of the fungus Fusarium fujikuroi is a light-driven proton pump that retards spore germination. Sci Rep 5:7798 http://dx.doi.org/10.1038/srep07798.
127. Estrada AF, Avalos J. 2009. Regulation and targeted mutation of opsA, coding for the NOP-1 opsin orthologue in Fusarium fujikuroi. J Mol Biol 387:59–73 http://dx.doi.org/10.1016/j.jmb.2009.01.057.
128. Linden H, Macino G. 1997. White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J 16:98–109 http://dx.doi.org/10.1093/emboj/16.1.98.
129. Lewis ZA, Correa A, Schwerdtfeger C, Link KL, Xie X, Gomer RH, Thomas T, Ebbole DJ, Bell-Pedersen D. 2002. Overexpression of White Collar-1 (WC-1) activates circadian clock-associated genes, but is not sufficient to induce most light-regulated gene expression in Neurospora crassa. Mol Microbiol 45:917–931 http://dx.doi.org/10.1046/j.1365-2958.2002.03074.x.
130. He Q, Liu Y. 2005. Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation. Genes Dev 19:2888–2899 http://dx.doi.org/10.1101/gad.1369605.
131. Schafmeier T, Káldi K, Diernfellner A, Mohr C, Brunner M. 2006. Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator. Genes Dev 20:297–306 http://dx.doi.org/10.1101/gad.360906.
132. Talora C, Franchi L, Linden H, Ballario P, Macino G. 1999. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J 18:4961–4968 http://dx.doi.org/10.1093/emboj/18.18.4961.
133. Froehlich AC, Loros JJ, Dunlap JC. 2003. Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc Natl Acad Sci USA 100:5914–5919 http://dx.doi.org/10.1073/pnas.1030057100.
134. Brenna A, Grimaldi B, Filetici P, Ballario P. 2012. 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 http://dx.doi.org/10.1091/mbc.E12-02-0142.
135. Grimaldi B, Coiro P, Filetici P, Berge E, Dobosy JR, Freitag M, Selker EU, Ballario P. 2006. The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol Biol Cell 17:4576–4583 http://dx.doi.org/10.1091/mbc.E06-03-0232.
136. Ruesch CE, Ramakrishnan M, Park J, Li N, Chong HS, Zaman R, Joska TM, Belden WJ. 2014. The histone H3 lysine 9 methyltransferase DIM-5 modifies chromatin at frequency and represses light-activated gene expression. G3 (Bethesda) 5:93–101.
137. 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 28:1029–1042 http://dx.doi.org/10.1038/emboj.2009.54.
138. Castellanos F, Schmoll M, Martínez P, Tisch D, Kubicek CP, Herrera-Estrella A, Esquivel-Naranjo EU. 2010. Crucial factors of the light perception machinery and their impact on growth and cellulase gene transcription in Trichoderma reesei. Fungal Genet Biol 47:468–476 http://dx.doi.org/10.1016/j.fgb.2010.02.001.
139. Schwerdtfeger C, Linden H. 2001. Blue light adaptation and desensitization of light signal transduction in Neurospora crassa. Mol Microbiol 39:1080–1087 http://dx.doi.org/10.1046/j.1365-2958.2001.02306.x.
140. Chen CH, DeMay BS, Gladfelter AS, Dunlap JC, Loros JJ. 2010. Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proc Natl Acad Sci USA 107:16715–16720 http://dx.doi.org/10.1073/pnas.1011190107.
141. Hunt SM, Thompson S, Elvin M, Heintzen C. 2010. 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 http://dx.doi.org/10.1073/pnas.1009474107.
142. Gin E, Diernfellner AC, Brunner M, Höfer T. 2013. The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation. Mol Syst Biol 9:667 http://dx.doi.org/10.1038/msb.2013.24.
143. Sancar G, Sancar C, Brügger B, Ha N, Sachsenheimer T, Gin E, Wdowik S, Lohmann I, Wieland F, Höfer T, Diernfellner A, Brunner M. 2011. A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora. Mol Cell 44:687–697 http://dx.doi.org/10.1016/j.molcel.2011.10.019.
144. Ruger-Herreros C, Gil-Sánchez MM, Sancar G, Brunner M, Corrochano LM. 2014. 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. http://dx.doi.org/10.1371/journal.pone.0095069.
145. Rodríguez-Romero J, Corrochano LM. 2006. Regulation by blue light and heat shock of gene transcription in the fungus Phycomyces: proteins required for photoinduction and mechanism for adaptation to light. Mol Microbiol 61:1049–1059 http://dx.doi.org/10.1111/j.1365-2958.2006.05293.x.
146. Berrocal-Tito GM, Rosales-Saavedra T, Herrera-Estrella A, Horwitz BA. 2000. Characterization of blue-light and developmental regulation of the photolyase gene phr1 in Trichoderma harzianum. Photochem Photobiol 71:662–668 http://dx.doi.org/10.1562/0031-8655(2000)071<0662:COBLAD>2.0.CO;2.
147. Casas-Flores S, Rios-Momberg M, Rosales-Saavedra T, Martínez-Hernández P, Olmedo-Monfil V, Herrera-Estrella A. 2006. Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot Cell 5:499–506 http://dx.doi.org/10.1128/EC.5.3.499-506.2006.
148. Berrocal-Tito GM, Esquivel-Naranjo EU, Horwitz BA, Herrera-Estrella A. 2007. Trichoderma atroviride PHR1, a fungal photolyase responsible for DNA repair, autoregulates its own photoinduction. Eukaryot Cell 6:1682–1692 http://dx.doi.org/10.1128/EC.00208-06.
149. Bluhm BH, Dunkle LD. 2008. PHL1 of Cercospora zeae-maydis encodes a member of the photolyase/cryptochrome family involved in UV protection and fungal development. Fungal Genet Biol 45:1364–1372 http://dx.doi.org/10.1016/j.fgb.2008.07.005.
150. Hedtke M, Rauscher S, Röhrig J, Rodríguez-Romero J, Yu Z, Fischer R. 2015. 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 http://dx.doi.org/10.1111/mmi.13062.
151. Bayram O, Braus GH. 2012. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36:1–24 http://dx.doi.org/10.1111/j.1574-6976.2011.00285.x.
152. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH. 2008. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506 http://dx.doi.org/10.1126/science.1155888.
153. Bayram O, Krappmann S, Seiler S, Vogt N, Braus GH. 2008. Neurospora crassa ve-1 affects asexual conidiation. Fungal Genet Biol 45:127–138 http://dx.doi.org/10.1016/j.fgb.2007.06.001.
154. Ahmed YL, Gerke J, Park HS, Bayram Ö, Neumann P, Ni M, Dickmanns A, Kim SC, Yu JH, Braus GH, Ficner R. 2013. The velvet family of fungal regulators contains a DNA-binding domain structurally similar to NF-κB. PLoS Biol 11:e1001750. http://dx.doi.org/10.1371/journal.pbio.1001750. [Erratum, 12:e1001849.]
155. Purschwitz J, Müller 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 Genet Genomics 281:35–42 http://dx.doi.org/10.1007/s00438-008-0390-x.
156. Rauscher S, Pacher S, Hedtke M, Kniemeyer O, Fischer R. 2016. A phosphorylation code of the Aspergillus nidulans global regulator VelvetA (VeA) determines specific functions. Mol Microbiol 99:909–924 http://dx.doi.org/10.1111/mmi.13275.
157. Lara-Rojas F, Sánchez O, Kawasaki L, Aguirre J. 2011. Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol Microbiol 80:436–454 http://dx.doi.org/10.1111/j.1365-2958.2011.07581.x.
158. Qiu L, Wang JJ, Chu ZJ, Ying SH, Feng MG. 2014. 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 http://dx.doi.org/10.1111/1462-2920.12486.
159. Rockwell NC, Su Y-S, Lagarias JC. 2006. Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858 http://dx.doi.org/10.1146/annurev.arplant.56.032604.144208.
160. Tan KK. 1975. Interaction of near-ultraviolet, blue, red, and far-red light in sporulation of Botrytis cinerea. Trans Br Mycol Soc 64:215–222 http://dx.doi.org/10.1016/S0007-1536(75)80105-7.
161. Casas-Flores S, Rios-Momberg M, Rosales-Saavedra T, Martínez-Hernández P, Olmedo-Monfil V, Herrera-Estrella A. 2006. Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot Cell 5:499–506 http://dx.doi.org/10.1128/EC.5.3.499-506.2006.
162. Olmedo M, Ruger-Herreros C, Luque EM, Corrochano LM. 2010. 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 http://dx.doi.org/10.1016/j.fgb.2009.11.004.
163. Posas F, Takekawa M, Saito H. 1998. Signal transduction by MAP kinase cascades in budding yeast. Curr Opin Microbiol 1:175–182 http://dx.doi.org/10.1016/S1369-5274(98)80008-8.
164. Vitalini MW, de Paula RM, Goldsmith CS, Jones CA, Borkovich KA, Bell-Pedersen D. 2007. Circadian rhythmicity mediated by temporal regulation of the activity of p38 MAPK. Proc Natl Acad Sci USA 104:18223–18228 http://dx.doi.org/10.1073/pnas.0704900104.
165. Vargas-Pérez I, Sánchez O, Kawasaki L, Georgellis D, Aguirre J. 2007. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryot Cell 6:1570–1583 http://dx.doi.org/10.1128/EC.00085-07.
166. Banno S, Noguchi R, Yamashita K, Fukumori F, Kimura M, Yamaguchi I, Fujimura M. 2007. Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in Neurospora crassa. Curr Genet 51:197–208 http://dx.doi.org/10.1007/s00294-006-0116-8.
167. Yamashita K, Shiozawa A, Watanabe S, Fukumori F, Kimura M, Fujimura M. 2008. ATF-1 transcription factor regulates the expression of ccg-1 and cat-1 genes in response to fludioxonil under OS-2 MAP kinase in Neurospora crassa. Fungal Genet Biol 45:1562–1569 http://dx.doi.org/10.1016/j.fgb.2008.09.012.
168. Lamb TM, Finch KE, Bell-Pedersen D. 2012. The Neurospora crassa OS MAPK pathway-activated transcription factor ASL-1 contributes to circadian rhythms in pathway responsive clock-controlled genes. Fungal Genet Biol 49:180–188 http://dx.doi.org/10.1016/j.fgb.2011.12.006.
169. Shiozaki K, Russell P. 1995. Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature 378:739–743 http://dx.doi.org/10.1038/378739a0.
170. Kawasaki L, Sánchez O, Shiozaki K, Aguirre J. 2002. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45:1153–1163 http://dx.doi.org/10.1046/j.1365-2958.2002.03087.x.
171. Nguyen AN, Shiozaki K. 1999. Heat-shock-induced activation of stress MAP kinase is regulated by threonine- and tyrosine-specific phosphatases. Genes Dev 13:1653–1663 http://dx.doi.org/10.1101/gad.13.13.1653.
172. Hartmuth S, Petersen J. 2009. Fission yeast Tor1 functions as part of TORC1 to control mitotic entry through the stress MAPK pathway following nutrient stress. J Cell Sci 122:1737–1746 http://dx.doi.org/10.1242/jcs.049387.
173. Han KH, Prade RA. 2002. Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol Microbiol 43:1065–1078 http://dx.doi.org/10.1046/j.1365-2958.2002.02774.x.
174. Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K. 2005. Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol 56:1246–1261 http://dx.doi.org/10.1111/j.1365-2958.2005.04605.x.
175. Hagiwara D, Asano Y, Marui J, Yoshimi A, Mizuno T, Abe K. 2009. Transcriptional profiling for Aspergillusnidulans HogA MAPK signaling pathway in response to fludioxonil and osmotic stress. Fungal Genet Biol 46:868–878 http://dx.doi.org/10.1016/j.fgb.2009.07.003.
176. Jaimes-Arroyo R, Lara-Rojas F, Bayram Ö, Valerius O, Braus GH, Aguirre J. 2015. The SrkA kinase is part of the SakA mitogen-activated protein kinase interactome and regulates stress responses and development in Aspergillus nidulans. Eukaryot Cell 14:495–510 http://dx.doi.org/10.1128/EC.00277-14.
177. Idnurm A, Bahn YS. 2016. Fungal physiology: red light plugs into MAPK pathway. Nat Microbiol 1:16052. http://dx.doi.org/10.1038/nmicrobiol.2016.52.
178. Belden WJ, Loros JJ, Dunlap JC. 2007. Execution of the circadian negative feedback loop in Neurospora requires the ATP-dependent chromatin-remodeling enzyme CLOCKSWITCH. Mol Cell 25:587–600 http://dx.doi.org/10.1016/j.molcel.2007.01.010.
179. Stoll DA, Link S, Kulling S, Geisen R, Schmidt-Heydt M. 2014. Comparative proteome analysis of Penicillium verrucosum grown under light of short wavelength shows an induction of stress-related proteins associated with modified mycotoxin biosynthesis. Int J Food Microbiol 175:20–29 http://dx.doi.org/10.1016/j.ijfoodmicro.2014.01.010.
180. Hirayama J, Cho S, Sassone-Corsi P. 2007. Circadian control by the reduction/oxidation pathway: catalase represses light-dependent clock gene expression in the zebrafish. Proc Natl Acad Sci USA 104:15747–15752 http://dx.doi.org/10.1073/pnas.0705614104.
181. Hansberg W, Aguirre J. 1990. Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J Theor Biol 142:201–221 http://dx.doi.org/10.1016/S0022-5193(05)80222-X.

Article metrics loading...



Life, as we know it, would not be possible without light. Light is not only a primary source of energy, but also an important source of information for many organisms. To sense light, only a few photoreceptor systems have developed during evolution. They are all based on an organic molecule with conjugated double bonds that allows energy transfer from visible (or UV) light to its cognate protein to translate the primary physical photoresponse to cell-biological actions. The three main classes of receptors are flavin-based blue-light, retinal-based green-light (such as rhodopsin), and linear tetrapyrrole-based red-light sensors. Light not only controls the behavior of motile organisms, but is also important for many sessile microorganisms including fungi. In fungi, light controls developmental decisions and physiological adaptations as well as the circadian clock. Although all major classes of photoreceptors are found in fungi, a good level of understanding of the signaling processes at the molecular level is limited to some model fungi. However, current knowledge suggests a complex interplay between light perception systems, which goes far beyond the simple sensing of light and dark. In this article we focus on recent results in several fungi, which suggest a strong link between light-sensing and stress-activated mitogen-activated protein kinases.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...



Image of FIGURE 1

Click to view


Phenomena of fungal responses to light. Light has a large impact on fungal morphology and physiology. The pictures of were provided by Shanta Subba and Ursula Kües (University of Göttingen).

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0020-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view


Schemes of the photoreceptor proteins and their presence in , , and . The figure shows the set of photoreceptors and a comparison of the presence of homologous genes in other model fungi, including the LOV-domain photoreceptors WC-1 and VIVID (VVD) together with WC-2, the protein that interacts with WC-1 to form the WC complex. Other photoreceptors identified in the genome are a rhodopsin (NOP-1), a cryptochrome (CRY), and two phytochromes (PHY-1 and PHY-2). LOV-domain photoreceptors contain the flavin chromophore-binding domain (LOV) and may also contain the protein-interaction domains (PAS) and the Zn finger domain. Rhodopsins contain the retinal-binding domain. Cryptochromes contain the FAD chromophore-binding domain and the domain for binding the antenna cofactor. Phytochromes contain an amino-terminal sensory domain and a carboxy-terminal output domain. The sensory domain involved in binding the bilin chromophore is composed of three domains (PAS, GAF, and PHY). The output domain is composed of the histidine kinase domain (HK), the ATPase domain found in ATP binding proteins, and the response-regulator domain (RR) that is likely involved in relaying the light signal to other proteins. The number indicates the presence and number of photoreceptor protein encoding genes in the genomes of (A.n.), (T.a.), and (P.b.). The * indicates that the protein is present but lacks the critical lysine residue required for retinal binding.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0020-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view


Model for WCC-dependent light signaling in . A simplified model for the activation of transcription by light and photoadaptation. Light reception by the FAD chromophore of WC-1 should trigger the formation of a flavin-cysteinyl adduct, causing a conformational change that leads to WCC dimerization, chromatin remodeling through the histone acetyltransferase NGF-1, and the activation of gene transcription. The modified histones are shown by stars at the site of promoter binding. Light exposure stimulates the transcription of , , and other light-induced genes. Newly synthesized VVD competes with the light-activated WC-1 and disrupts the formation of WCC dimers, reducing WCC binding to the promoter. The WCC bound to VVD is not transcriptionally active, and it results in the attenuation of the response to light. Different fractions of the light-activated WCC are stabilized by FRQ (not shown) and transiently phosphorylated (black dots) and partially degraded, probably through an interaction with the protein kinase C (PKC) and other kinases and phosphates, some of them not yet identified (not shown).

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0020-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view


Phytochrome functions in light regulation in and the link of light and stress sensing in (A) and (B). There is good evidence that the light signal is perceived by FphA in the cytoplasm and transmitted into the nucleus by activating the SakA stress signal pathway. SakA becomes phosphorylated, shuttles into the nucleus, and activates the transcription factor AtfA. (modified after 177) Light signaling also involves chromatin remodeling of the promoters of light-regulated genes such as or . It was shown that the acetylation level of lysine 9 of histone H3 increases upon illumination, that LreA interacts with the acetyltransferease GcnE and the histone deacetylase HdaA, that deletion of the SAGA/Ada complex component AdaB causes reduction, whereas deletion of causes induction of the photoinduction, and that changes of lysine 9 in histone H3 phenocopy the phenotypes of or deletion strains. VeA is always bound to the or promoter, whereas LreA leaves the promoter upon illumination. Hence, LreA could keep GcnE inactive and stimulate HdaA in the dark. The situation would be reversed after illumination, and the acetylation level of the lysine residue 9 of histone H3 would increase. There is evidence that GcnE is further activated through FphA. Lysine 9 acetylation was dependent on FphA, but an interaction between the two proteins was only shown by split YFP and could not be verified by Co-IP. The arrows indicate protein interactions verified by different methods. It should be noted that the current models rely solely on the results obtained with two light-regulated genes, and . The link between light and stress regulation in . In a quick response light causes phosphorylation of the MAPK Tmk3, which requires the MAPKK Pbs2. Nevertheless, it is still unclear where the WCC is linked to the Tmk3 MAPK pathway. At the promoter of a set of light-regulated genes the WCC could interact either with Tmk3 or with a not-yet-identified AtfA ortholog. Light also stimulates the transcription of the gene, giving rise to higher levels of Tmk3, which may aid in keeping a sustained response.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0020-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error