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Improved photoprotection in melanized lichens is a result of fungal solar radiation screening rather than photobiont acclimation

Published online by Cambridge University Press:  04 November 2019

Richard Peter BECKETT ,
Knut Asbjørn SOLHAUG ,
Yngvar GAUSLAA Open the ORCID record for Yngvar GAUSLAA [Opens in a new window]  and
Farida MINIBAYEVA
Richard Peter BECKETT
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa; and OpenLab ‘Biomarker’, Kazan Federal University, Kazan 420008, Republic of Tatarstan, Russia. Email: rpbeckett@gmail.com
Knut Asbjørn SOLHAUG
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway.
Yngvar GAUSLAA
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway.
Farida MINIBAYEVA
Affiliation:
Kazan Institute of Biochemistry and Biophysics, Federal Research Center ‘Kazan Scientific Center of RAS’, P.O. Box 30, Kazan 420111, Russia. Email: minibayeva@kibb.knc.ru
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Abstract

Some lichenized ascomycetes synthesize melanic pigments in their upper cortices when exposed to ultraviolet light and high solar radiation. Our previous work showed that melanized chloro- and cyanolichens from both high light and more shaded habitats were less photoinhibited than pale ones during controlled exposure to high light. However, protection from high light might not necessarily be the consequence of just sun-screening by melanins in upper cortices. An inherent problem with earlier experiments was that the photobionts of melanized thalli might have received more light than those beneath pale cortices. The photobionts may therefore have possessed other light-induced tolerance mechanisms that gave protection from photoinhibition. Here, we aimed to test directly the inherent tolerance of lichen photobionts to photoinhibition. The method involved removing the lower cortices and medullas of three lichen species, Cetraria islandica, Crocodia aurata and Lobaria pulmonaria, and exposing the photobionts to light from below. Results confirmed that most of the improvement in tolerance to photoinhibition in melanized lichens derives from fungal melanization in the upper cortex. However, in C. islandica, the most heavily melanized species, algae from melanized thalli possessed a significantly higher tolerance to photoinhibition than those from pale thalli, suggesting that photobionts can also adapt themselves to high light.

Keywords

acclimationchlorophyll fluorescencedesiccationlichensmelaninphotoinhibitionUV-B
Type
Articles
Information
The Lichenologist , Volume 51 , Issue 5 , September 2019 , pp. 483 - 491
Copyright
Copyright © British Lichen Society 2019 

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References

Adams, W. W. III, Demmig-Adams, B. & Lange, O. L. (1993) Carotenoid composition and metabolism in green and blue-green algal lichens in the field. Oecologia 94: 576–584.Google Scholar
Foyer, C. H. (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environmental and Experimental Botany 154: 134–142.Google Scholar
Gauslaa, Y. & Coxson, D. (2011) Interspecific and intraspecific variations in water storage in epiphytic old forest foliose lichens. Botany 89: 787–798.Google Scholar
Gauslaa, Y. & Solhaug, K. A. (2000) High-light-intensity damage to the foliose lichen Lobaria pulmonaria within a natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32: 271–289.Google Scholar
Gauslaa, Y. & Solhaug, K. A. (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126: 462–471.Google Scholar
Gururani, M. A., Venkatesh, J. & Tran, L. S. P. (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Molecular Plant 8: 1304–1320.Google Scholar
Jairus, K., Lõhmus, A. & Lõhmus, P. (2009) Lichen acclimatization on retention trees: a conservation physiology lesson. Journal of Applied Ecology 46: 930–936.Google Scholar
Leisner, J. M. R., Green, T. G. A. & Lange, O. L. (1997) Photobiont activity of a temperate crustose lichen: long-term chlorophyll fluorescence and CO2 exchange measurements in the field. Symbiosis 23: 165–182.Google Scholar
Mafole, T. C., Solhaug, K. A., Minibayeva, F. V. & Beckett, R. P. (2019 a) Tolerance to photoinhibition within a lichen species is higher in melanised thalli. Photosynthetica 57: 96–102.Google Scholar
Mafole, T. C., Solhaug, K. A., Minibayeva, F. V. & Beckett, R. P. (2019 b) Occurrence and possible roles of melanic pigments in lichenized ascomycetes. Fungal Biology (in press). https://doi.org/10.1016/j.fbr.2018.10.002.Google Scholar
McEvoy, M., Gauslaa, Y. & Solhaug, K. A. (2007) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytologist 175: 271–282.Google Scholar
Míguez, F., Fernández-Marín, B., Becerril, J.-M. & García-Plazaola, J. I. (2017) Diversity of winter photoinhibitory responses: a case study in co-occurring lichens, mosses, herbs and woody plants from subalpine environments. Physiologia Plantarum 160: 282–296.Google Scholar
Nath, K., Jajoo, A., Poudyal, R. S., Timilsina, R., Park, Y. S., Aro, E. M., Nam, H. G. & Lee, C. H. (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Letters 587: 3372–3381.Google Scholar
Onuț-Brännström, I., Benjamin, M., Scofield, D. G., Heiðmarsson, S., Andersson, M. G. I., Lindström, E. S. & Johannesson, H. (2018) Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing. Scientific Reports 8: 4406.Google Scholar
Phinney, N. H., Gauslaa, Y. & Solhaug, K. A. (2019) Why chartreuse? The pigment vulpinic acid screens blue light in the lichen Letharia vulpina. Planta 249: 709–718.Google Scholar
Pospíšil, P. (2016) Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Frontiers in Plant Science 7: 1950. https://doi.org/10.3389/fpls.2016.01950Google Scholar
Škaloud, P., Friedl, T., Hallmann, C., Beck, A. & Dal Grande, F. (2016) Taxonomic revision and species delimitation of coccoid green algae currently assigned to the genus Dictyochloropsis (Trebouxiophyceae, Chlorophyta). Journal of Phycology 52: 599–617.Google Scholar
Solhaug, K. A. (2018) Low-light recovery effects on assessment of photoinhibition with chlorophyll fluorescence in lichens. Lichenologist 50: 139–145.Google Scholar
Solhaug, K. A. & Gauslaa, Y. (2012) Secondary lichen compounds as protection against excess solar radiation and herbivores. Progress in Botany 73: 283–304.Google Scholar
Solhaug, K. A., Gauslaa, Y., Nybakken, L. & Bilger, W. (2003) UV-induction of sun-screening pigments in lichens. New Phytologist 158: 91–100.Google Scholar
Solhaug, K. A., Larsson, P. & Gauslaa, Y. (2010) Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 213: 1003–1011.Google Scholar
Solovchenko, A. E., Chivkunova, O. B., Merzlyak, M. N. & Reshetnikova, I. V. (2001) A spectrophotometric analysis of pigments in apples. Russian Journal of Plant Physiology 48: 693–700.Google Scholar
Spribille, T., Tuovinen, V., Resl, P., Vanderpool, D., Wolinski, H., Aime, M. C., Schneider, K., Stabentheiner, E., Toome-Heller, M., Thor, G., et al. (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353: 488–492.Google Scholar
Thell, A. & Moberg, R. (2011) Nordic Lichen Flora. Volume 4. Parmeliaceae. Uppsala: Museum of Evolution.Google Scholar
Verhoven, A., García-Plazaola, J. I. & Fernández-Marín, B. (2018) Shared mechanisms of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature. Environmental and Experimental Botany 154: 66–79.Google Scholar