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Chapter 28 : Light Sensing

Authors: Luis M. Corrochano1, Javier Avalos2
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Affiliations: 1: Departamento de Genética, Facultad de Biología, Universidad de Sevilla, E-41012 Sevilla, Spain; 2: Departamento de Genética, Facultad de Biología, Universidad de Sevilla, E-41012 Sevilla, Spain
Content Type: Monograph
Publication Year: 2010

Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis

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Abstract:

This chapter summarizes the current knowledge of the mechanism of light sensing in fungi, including a description of fungal photoreceptors and their mechanism of action, and describes the fungal responses that are mediated by these photoreceptors. Blue-light responses in include the induction of sporulation, sexual development, synthesis of mycelial carotenoids, and the regulation of the circadian clock; all of these responses require the products of the -1 and -2 genes. WC- 1 and WC-2 interact through their PAS domains to form a WC complex that binds the promoter of light-inducible genes. In order to understand the molecular mechanism of light-dependent gene regulation, most research has focused on the behavior and activity of the WC complex during and after exposure to light. Light transduction seems to be reduced to a minimum in and other fungi using WC-type photoreceptors. The regulation by light of fungal development (photomorphogenesis) can be measured precisely, allowing the determination of useful parameters, such as thresholds. The carotenoid pathways in filamentous fungi coincide in the first steps, namely, the formation of the colorless phytoene from the condensation of two geranylgeranyl pyrophosphate (GGPP) molecules, a reaction catalyzed by phytoene synthase. Fungal photobiology provides a unique opportunity to investigate the effect of light on a wide group of microbial eukaryotes without the complexities related to photosynthesis and other energy-oriented light perception mechanisms.

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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Light Sensing
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Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
/content/10.1128/9781555816636.ch28.ch28fig01
FIGURE 1
Photoreceptor proteins in . Shown are the LOV-domain photoreceptors WC-1 and VIVID (VVD) together with WC-2, the protein that interacts with WC-1 to form the photoresponsive 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, and the response regulator domain (REC), which is likely involved in relaying the light signal to other proteins. The identity and the position of the domains were predicted using the SMART database (http://smart.embl-heidelberg.de/) ( ) and the Conserved Domain Database (http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) ( ).
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FIGURE 1

Photoreceptor proteins in . Shown are the LOV-domain photoreceptors WC-1 and VIVID (VVD) together with WC-2, the protein that interacts with WC-1 to form the photoresponsive 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, and the response regulator domain (REC), which is likely involved in relaying the light signal to other proteins. The identity and the position of the domains were predicted using the SMART database (http://smart.embl-heidelberg.de/) ( ) and the Conserved Domain Database (http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) ( ).

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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/content/10.1128/9781555816636.ch28.ch28fig02
FIGURE 2
A simplified model for the photoactivation of gene expression by the WC complex. The model shows the WC complex with proteins WC-1 and WC-2, and the promoter and ORF of a light-responsive gene. The proteins that interact with the WC complex in the dark (FRQ, RNA helicase FRH, and PKC) are not shown for simplicity. Light reception at the FAD chromophore of WC-1 triggers the formation of a flavin-cysteinyl adduct causing a conformational change that leads to WC complex aggregation and promoter binding, chromatin remodeling (not shown), and the activation of gene transcription. Gene photoactivation is transient. After further light exposure, WC-1 is phosphorylated (black dots) leading to exclusion of the WC complex from the promoter and termination of gene transcription. The protein VIVID (VVD) is required for the transient gene photoactivation, but the mechanism is not known. The excluded WC complex is dephosphorylated and partially degraded, probably through interaction with PKC. The stability, activity, and nuclear localization of the WC complex are controlled by PKA, but the details of this regulation are not known. After a certain period in the dark the WC complex, probably with the addition of newly synthesized WC-1 and WC-2, is ready for gene photoactivation again. Kinases and phosphatases responsible for the light-dependent phosphorylation of WC-1 have not been identified and are not shown.
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Image of FIGURE 2
FIGURE 2

A simplified model for the photoactivation of gene expression by the WC complex. The model shows the WC complex with proteins WC-1 and WC-2, and the promoter and ORF of a light-responsive gene. The proteins that interact with the WC complex in the dark (FRQ, RNA helicase FRH, and PKC) are not shown for simplicity. Light reception at the FAD chromophore of WC-1 triggers the formation of a flavin-cysteinyl adduct causing a conformational change that leads to WC complex aggregation and promoter binding, chromatin remodeling (not shown), and the activation of gene transcription. Gene photoactivation is transient. After further light exposure, WC-1 is phosphorylated (black dots) leading to exclusion of the WC complex from the promoter and termination of gene transcription. The protein VIVID (VVD) is required for the transient gene photoactivation, but the mechanism is not known. The excluded WC complex is dephosphorylated and partially degraded, probably through interaction with PKC. The stability, activity, and nuclear localization of the WC complex are controlled by PKA, but the details of this regulation are not known. After a certain period in the dark the WC complex, probably with the addition of newly synthesized WC-1 and WC-2, is ready for gene photoactivation again. Kinases and phosphatases responsible for the light-dependent phosphorylation of WC-1 have not been identified and are not shown.

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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FIGURE 3
Photomorphogenesis in : light inhibition of microphore initiation and development in . Microphores are short sporangiophores, 1 to 2 mm in length, containing a dark ball on top (sporangia) with matured spores. The fungus was grown under continuous light or in the dark. Microphores appeared only in the mycelial surface of cultures kept in the dark. Photographs by L. M. Corrochano.
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Image of FIGURE 3
FIGURE 3

Photomorphogenesis in : light inhibition of microphore initiation and development in . Microphores are short sporangiophores, 1 to 2 mm in length, containing a dark ball on top (sporangia) with matured spores. The fungus was grown under continuous light or in the dark. Microphores appeared only in the mycelial surface of cultures kept in the dark. Photographs by L. M. Corrochano.

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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FIGURE 4
Inhibition of microphorogenesis, stimulation of macrophorogenesis, and stimulation of β-carotene accumulation by blue-light pulses. Standard dark cultures, 2 days old, received pulses of blue light of the fluence given in the abscissa. The number of microphores (m) and the dry weight of macrophores (M) were determined 2 days later and given relative to the values found in dark cultures. β-Carotene content was estimated from the absorbance at 452 nm in mycelial samples 12 h after the end of blue-light illumination. The continuous lines represent computer-fitted algebraic expressions ( ).
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Image of FIGURE 4
FIGURE 4

Inhibition of microphorogenesis, stimulation of macrophorogenesis, and stimulation of β-carotene accumulation by blue-light pulses. Standard dark cultures, 2 days old, received pulses of blue light of the fluence given in the abscissa. The number of microphores (m) and the dry weight of macrophores (M) were determined 2 days later and given relative to the values found in dark cultures. β-Carotene content was estimated from the absorbance at 452 nm in mycelial samples 12 h after the end of blue-light illumination. The continuous lines represent computer-fitted algebraic expressions ( ).

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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FIGURE 5
Carotenoid biosynthetic pathways in , and . The reactions and genes encoding the responsible enzymes for each species are indicated following the code shown in the box. In contrast to other carotenogenic species, phytoene synthesis from GGPP and cyclization reactions are achieved in fungi by a bifunctional protein, encoded here by the gene , or . All the genes displayed are regulated by light except has not been investigated. Trisporic acids are apocarotenoid-derived sexual hormones synthesized from β-carotene in zygomycetes.
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Image of FIGURE 5
FIGURE 5

Carotenoid biosynthetic pathways in , and . The reactions and genes encoding the responsible enzymes for each species are indicated following the code shown in the box. In contrast to other carotenogenic species, phytoene synthesis from GGPP and cyclization reactions are achieved in fungi by a bifunctional protein, encoded here by the gene , or . All the genes displayed are regulated by light except has not been investigated. Trisporic acids are apocarotenoid-derived sexual hormones synthesized from β-carotene in zygomycetes.

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
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Tables

Light Sensing
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Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28
/content/10.1128/9781555816636.ch28.ch28tab01
TABLE 1
Effects of light on fungi
Generic image for table
TABLE 1

Effects of light on fungi

Citation: Corrochano L, Avalos J. 2010. Light Sensing, p 417-441. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch28

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