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The Complexity of Fungal Vision

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  • Authors: Reinhard Fischer1, Jesus Aguirre2, Alfredo Herrera-Estrella3, Luis M. Corrochano4
  • Editors: Joseph Heitman5, Neil A. R. Gow6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    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]
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  • 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.

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0020-2016
2016-11-18
2020-08-14

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.

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The Complexity of Fungal Vision
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Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2016. The complexity of fungal vision. microbiolspec 4(6): doi:10.1128/microbiolspec.FUNK-0020-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0020-2016.fig1
FIGURE 1
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).
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FIGURE 1

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
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FIGURE 2
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.
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FIGURE 2

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
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FIGURE 3
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).
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FIGURE 3

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
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FIGURE 4
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.
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FIGURE 4

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
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