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Adaptions of photosynthesis in sun and shade in populations of some Afromontane lichens

Published online by Cambridge University Press:  29 November 2022

Kwanele Goodman Wandile Mkhize ,
Farida Minibayeva  and
Richard Peter Beckett Open the ORCID record for Richard Peter Beckett [Opens in a new window]
Kwanele Goodman Wandile Mkhize
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa
Farida Minibayeva
Affiliation:
Kazan Institute of Biochemistry and Biophysics, Federal Research Center ‘Kazan Scientific Center of RAS’, P.O. Box 261, Kazan 420111, Russia
Richard Peter Beckett*
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa Open Lab ‘Biomarker’, Kazan (Volga Region) Federal University, Kremlevskaya str. 18, 420008 Kazan, Russia
*
Author for correspondence: Richard Peter Beckett. E-mail: rpbeckett@gmail.com
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Abstract

Photosynthetic organisms have evolved a great variety of mechanisms to optimize their use of sunlight. Some of the clearest examples of adaptations can be seen by comparing photosynthesis in different species and in different individuals of the same species that grow under high and low light levels. While the adaptations of sun and shade higher plants have been relatively well studied, much less information is available on the photobionts of lichenized Ascomycetes. An important adaptation that can protect photosynthetic organisms from the potentially harmful effects of excess light is non-photochemical quenching (NPQ); NPQ can dissipate unused light energy as heat. Here we used chlorophyll fluorescence to compare the induction and relaxation of NPQ and the induction of electron transport (rETR) in collections of the same lichen species from exposed and from more shaded locations. All species have trebouxioid photobionts and normally grow in more exposed microhabitats but can also be readily collected from more shaded locations. Shade forms display generally higher NPQ, presumably to protect lichens from occasional rapid increases in light that occur during sunflecks. Furthermore, the NPQ of shade forms relaxes quickly when light levels are reduced, presumably to ensure efficient photosynthesis after a sunfleck has passed. The maximal relative electron transport rate is lower in shade than sun collections, probably reflecting a downregulation of photosynthetic capacity to reduce energy costs. We also compared collections of pale and melanized thalli from three species of shade lichens with Symbiochloris as their photobiont. Interestingly, NPQ in melanized thalli from slightly more exposed microhabitats induced and relaxed in a way that resembled shade rather than sun forms of the trebouxioid lichens. This might suggest that in some locations melanization induced during a temporary period of high light may be excessive and could potentially reduce photosynthesis later in the growing season. Taken together, the results suggest that lichen photobionts can flexibly adjust the amount and type of NPQ, and their levels of rETR in response to light availability.

Keywords

chlorophyll fluorescencephotoprotectionphotosynthesissunfleckxanthophyll cycle
Type
Standard Paper
Information
The Lichenologist , Volume 54 , Special Issue 5: African Lichenology , September 2022 , pp. 319 - 329
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the British Lichen Society

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References

Alter, P, Dreissen, A, Luo, FL and Matsubara, S (2012) Acclimatory responses of Arabidopsis to fluctuating light environment: comparison of different sunfleck regimes and accessions. Photosynthesis Research 113, 221–237.CrossRefGoogle ScholarPubMed
Beckett, RP, Minibayeva, FV and Mkhize, KWG (2021 a) Shade lichens are characterized by rapid relaxation of non-photochemical quenching on transition to darkness. Lichenologist 53, 409–414.CrossRefGoogle Scholar
Beckett, RP, Minibayeva, FV, Solhaug, KA and Roach, T (2021 b) Photoprotection in lichens: adaptations of photobionts to high light. Lichenologist 53, 21–33.CrossRefGoogle Scholar
Bilger, W, Schreiber, U and Bock, M (1995) Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102, 425–432.CrossRefGoogle ScholarPubMed
Blommaert, L, Chafai, L and Bailleul, B (2021) The fine-tuning of NPQ in diatoms relies on the regulation of both xanthophyll cycle enzymes. Scientific Reports 11, 12750.CrossRefGoogle ScholarPubMed
Demmig-Adams, B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant and Cell Physiology 39, 474–482.CrossRefGoogle Scholar
Demmig-Adams, B, Adams, WW III, Czygan, F-C, Schreiber, U and Lange, OL (1990) Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180, 582–589.CrossRefGoogle ScholarPubMed
Demmig-Adams, B, Stewart, JJ, López-Pozo, M, Polutchko, SK and Adams, WW III (2020) Zeaxanthin, a molecule for photoprotection in many different environments. Molecules 25, 5825.CrossRefGoogle ScholarPubMed
Eilers, PHC and Peeters, JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42, 199–215.CrossRefGoogle Scholar
Fernández-Marín, B, Roach, T, Verhoeven, A and García-Plazaola, JI (2021) Shedding light on the dark side of xanthophyll cycles. New Phytologist 230, 1336–1344.CrossRefGoogle ScholarPubMed
Gauslaa, Y and Goward, T (2020) Melanic pigments and canopy-specific elemental concentration shape growth rates of the lichen Lobaria pulmonaria in unmanaged mixed forest. Fungal Ecology 47, 100984.CrossRefGoogle Scholar
Gilmore, AM (2004) Excess light stress: probing excitation dissipation mechanisms through global analysis of time- and wavelength-resolved chlorophyll a fluorescence. In Papageorgiou, GC and Govindjee, (eds), Chlorophyll a Fluorescence: a Signature of Photosynthesis. Dordrecht: Springer, pp. 555–581.CrossRefGoogle Scholar
Greer, DH (2022) Sunlight and plant production. In Munns R, Schmidt S, Beveridge C and Mathesius U (eds), Plants in Action, 2nd Edition. Australian Society of Plant Scientists. [WWW resource] URL https://www.asps.org.au/plants-in-action-2nd-edition-pdf-filesGoogle Scholar
Griffiths, H and Maxwell, K (1999) In Memory of C. S. Pittendrigh: does exposure in forest canopies relate to photoprotective strategies in epiphytic bromeliads? Functional Ecology 13, 15–23.Google Scholar
Kalaji, MH, Goltsev, VN, Żuk-Golaszewska, K, Zivcak, M and Brestic, M (2017) Chlorophyll Fluorescence. Understanding Crop Performance – Basics and Applications. Boca Raton: CRC Press.CrossRefGoogle Scholar
Kromdijk, J, Glowacka, K, Leonelli, L, Gabilly, ST, Iwai, M, Niyogi, KK and Long, SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857–861.CrossRefGoogle ScholarPubMed
Liu, J, Lu, Y, Hau, W and Last, RL (2019) A new light on photosystem II maintenance in oxygenic photosynthesis. Frontiers in Plant Science 10, 975.CrossRefGoogle ScholarPubMed
MacKenzie, TDB, Król, M, Huner, NPA and Campbell, DA (2002) Seasonal changes in chlorophyll fluorescence quenching and the induction and capacity of the photoprotective xanthophyll cycle in Lobaria pulmonaria. Canadian Journal of Botany 80, 255–261.CrossRefGoogle Scholar
Mathur, S, Jain, L and Jajoo, A (2018) Photosynthetic efficiency in sun and shade plants. Photosynthetica 56, 354–365.CrossRefGoogle Scholar
Mkhize, KGW, Minibayeva, FV and Beckett, RP (2022) Lichen photobionts can be hardened to photoinhibition by pretreatment with light. Acta Physiologiae Plantarum 44, 122.CrossRefGoogle Scholar
Murchie, EH and Ruban, AV (2020) Dynamic non-photochemical quenching in plants: from molecular mechanism to productivity. Plant Journal 101, 885–896.CrossRefGoogle ScholarPubMed
Ndhlovu, NT, Minibayeva, FV and Beckett, RP (2022) Unpigmented lichen substances protect lichens against photoinhibition of photosystem II in both the hydrated and desiccated states. Acta Physiologiae Plantarum 44, 123.CrossRefGoogle Scholar
Nelsen, MP, Leavitt, SD, Heller, K, Muggia, L and Lumbsch, HT (2022) Contrasting patterns of climatic niche divergence in Trebouxia – a clade of lichen-forming algae. Frontiers in Microbiology 13, 791546.CrossRefGoogle ScholarPubMed
Piccotto, M and Tretiach, M (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. Journal of Plant Research 123, 763–775.CrossRefGoogle ScholarPubMed
Proctor, MCF (2003) Comparative ecophysiological measurements on the light responses, water relations and desiccation tolerance of the filmy ferns Hymenophyllum wilsonii Hook. and H. tunbrigense (L.) Smith. Annals of Botany 91, 717–727.CrossRefGoogle Scholar
Proctor, MCF and Smirnoff, N (2015) Photoprotection in bryophytes: rate and extent of dark relaxation of non-photochemical quenching of chlorophyll fluorescence. Journal of Bryology 37, 171–177.CrossRefGoogle Scholar
Rambold, G, Friedl, T and Beck, A (1998) Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101, 392–397.CrossRefGoogle Scholar
Roach, T and Krieger-Liszkay, A (2019) Photosynthetic regulatory mechanisms for efficiency and prevention of photo-oxidative stress. Annual Plant Reviews Online 2, 273–306.CrossRefGoogle Scholar
Solhaug, KA and Gauslaa, Y (2012) Secondary lichen compounds as protection against excess solar radiation and herbivores. Progress in Botany 73, 283–304.Google Scholar
Solhaug, KA, Gauslaa, Y, Nybakken, L and Bilger, W (2003) UV-induction of sun-screening pigments in lichens. New Phytologist 158, 91–100.CrossRefGoogle Scholar
Veres, K, Farkas, E and Csintalan, Z (2020) The bright and shaded side of duneland life: the photosynthetic response of lichens to seasonal changes is species-specific. Mycological Progress 19, 629–641.CrossRefGoogle Scholar
Vráblíková, H, McEvoy, M, Solhaug, KA, Barták, M and Gauslaa, Y (2006) Annual variation in photoacclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. Journal of Photochemistry and Photobiology B: Biology 83, 151–162.CrossRefGoogle Scholar