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Chapter 20 : The Complexity of Fungal Vision

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Abstract:

Sunlight, harvested by photosynthetic organisms (plants, algae, and some bacteria) and used to synthesize energy-rich molecules (sugars) from carbon dioxide and water, provides the energy required to sustain life on Earth. In addition, sunlight properties such as intensity, duration, polarization, and spectral composition are used as sources of information ( ). Indeed, all forms of life are continuously obtaining and decoding information from their environment. In fungi sunlight, ranging from ultraviolet (UV) to infrared wavelengths, regulates a diversity of biological processes including circadian rhythms, morphogenesis, tropism, and synthesis of pigments, among others (reviewed in reference ). UV light can be harmful, since DNA modification products of photochemical reactions may be transmitted to the next generation as a mutation. Visible light appears not only to provide early warning of the presence of impending UV radiation and further damage, but also seems to contribute to the capacity of these organisms to deal with abiotic stress in general ( ). Thus, the ability of most fungi to perceive and respond to light has very likely contributed to their survival and fitness.

Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2017. The Complexity of Fungal Vision, p 441-461. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0020-2016
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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).

Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2017. The Complexity of Fungal Vision, p 441-461. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. 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.

Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2017. The Complexity of Fungal Vision, p 441-461. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. 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).

Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2017. The Complexity of Fungal Vision, p 441-461. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. 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.

Citation: Fischer R, Aguirre J, Herrera-Estrella A, Corrochano L. 2017. The Complexity of Fungal Vision, p 441-461. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0020-2016
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