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Shade lichens are characterized by rapid relaxation of non-photochemical quenching on transition to darkness

Published online by Cambridge University Press:  13 October 2021

Richard P. Beckett Open the ORCID record for Richard P. Beckett [Opens in a new window] ,
Farida V. Minibayeva Open the ORCID record for Farida V. Minibayeva [Opens in a new window]  and
Kwanele W. G. Mkhize
Richard P. 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, Kazan 420008, Russia
Farida V. Minibayeva
Affiliation:
Kazan Institute of Biochemistry and Biophysics, Federal Research Center ‘Kazan Scientific Center of RAS’, PO Box 30, Kazan 420111, Russia
Kwanele W. G. Mkhize
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa
*
Author for correspondence: Richard P. Beckett. E-mail: rpbeckett@gmail.com
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Abstract

Non-photochemical quenching (NPQ) plays an important role in protecting photosynthetic organisms from photoinhibition by dissipating excess light energy as heat. However, excess NPQ can greatly reduce the quantum yield of photosynthesis at lower light levels. Recently, there has been considerable interest in understanding how plants balance NPQ to ensure optimal productivity in environments in which light levels are rapidly changing. In the present study, chlorophyll fluorescence was used to study the induction and relaxation of non-photochemical quenching (NPQ) in the dark and the induction of photosynthesis in ten species of lichens, five sampled from exposed and five sampled from shaded habitats. Here we show that the main difference between sun and shade lichens is the rate at which NPQ relaxes in the dark, rather than the speed that photosynthesis starts upon illumination. During the first two minutes in the dark, NPQ values in the five sun species declined only by an average of 2%, while by contrast, in shade species the average decline was 40%. For lichens growing in microhabitats where light levels are rapidly changing, rapid relaxation of NPQ may enable their photobionts to use the available light most efficiently.

Keywords

chlorophyll fluorescencephotoprotectionphotosynthesissunfleckxanthophyll cycle
Type
Standard Paper
Information
The Lichenologist , Volume 53 , Issue 5 , September 2021 , pp. 409 - 414
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Copyright
Copyright © The Author(s), 2021. 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, 221–237.10.1007/s11120-012-9757-2CrossRefGoogle ScholarPubMed
Armbruster, U, Carrillo, LR, Venema, K, Pavlovic, L, Schmidtmann, E, Kornfeld, A, Jahns, P, Berry, JA, Kramer, DM and Jonikas, MC (2014) Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nature Communications 5, 5439.10.1038/ncomms6439CrossRefGoogle ScholarPubMed
Armbruster, U, Leonelli, L, Correa Galvis, V, Strand, D, Quinn, EH, Jonikas, MC and Niyogi, KK (2016) Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light. Plant and Cell Physiology 57, 1557–1567.Google ScholarPubMed
Beckett, RP, Minibayeva, FV, Solhaug, KA and Roach, T (2021) Photoprotection in lichens: adaptations of photobionts to high light. Lichenologist 53, 21–33.10.1017/S0024282920000535CrossRefGoogle 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, 425–432.10.1007/BF00341354CrossRefGoogle ScholarPubMed
Caliandro, R, Nagel, KA, Kastenholz, B, Bassi, R, Li, ZR, Niyogi, KK, Pogson, BJ, Schurr, U and Matsubara, S (2013) Effects of altered α- and β-branch carotenoid biosynthesis on photoprotection and whole-plant acclimation of Arabidopsis to photo-oxidative stress. Plant Cell and Environment 36, 438–453.10.1111/j.1365-3040.2012.02586.xCrossRefGoogle ScholarPubMed
Correa Galvis, V, Strand, DD, Messer, M, Thiele, W, Bethmann, S, Hübner, D, Uflewski, M, Kaiser, E, Siemiatkowska, B, Morris, BA, et al. (2020) H+ transport by K+ EXCHANGE ANTIPORTER3 promotes photosynthesis and growth in chloroplast ATP synthase mutants. Plant Physiology 182, 2126–2142.10.1104/pp.19.01561CrossRefGoogle Scholar
Cruz, JA, Savage, LJ, Zegarac, R, Hall, CC, Satoh-Cruz, M, Davis, GA, Kovac, WK, Chen, J and Kramer, DM (2016) Dynamic environmental photosynthetic imaging reveals emergent phenotypes. Cell Systems 2, 365–377.10.1016/j.cels.2016.06.001CrossRefGoogle ScholarPubMed
Demmig-Adams, B, Stewart, JJ, López-Pozo, M, Polutchko, SK and Adams, WW (2020) Zeaxanthin, a molecule for photoprotection in many different environments. Molecules 25, 5825.10.3390/molecules25245825CrossRefGoogle ScholarPubMed
Derks, AK and Bruce, D (2018) Rapid regulation of excitation energy in two pennate diatoms from contrasting light climates. Photosynthesis Research 138, 149–165.10.1007/s11120-018-0558-0CrossRefGoogle ScholarPubMed
Dietz, S, Büdel, B, Lange, OL and Bilger, W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibliotheca Lichenologica 75, 171–182.Google Scholar
Eilers, PHC and Peeters, JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42, 199–215.10.1016/0304-3800(88)90057-9CrossRefGoogle Scholar
Fisher, NL, Campbell, DA, Hughes, DJ, Kuzhiumparambil, U, Halsey, KH, Ralph, PJ and Suggett, DJ (2020) Divergence of photosynthetic strategies amongst marine diatoms. PLoS ONE 15, e0244252.10.1371/journal.pone.0244252CrossRefGoogle ScholarPubMed
Green, TGA, Büdel, B, Meyer, A, Zellner, H and Lange, OL (1997) Temperate rainforest lichens in New Zealand: light response of photosynthesis. New Zealand Journal of Botany 35, 493–504.10.1080/0028825X.1987.10410173CrossRefGoogle Scholar
Greer, DH (2021) Sunlight and plant production. In Munns, R, Schmidt, S, Beveridge, C and Mathesius, U (eds), Plants in Action, 2nd Edn. Australian Society of Plant Scientists. [WWW document] URL https://asps.org.au/plants-in-action-2nd-edition-pdf-filesGoogle Scholar
Kaiser, E, Correa Galvis, V and Armbruster, U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast's perspective. Biochemical Journal 476, 2725–2741.10.1042/BCJ20190134CrossRefGoogle ScholarPubMed
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, 857–861.10.1126/science.aai8878CrossRefGoogle ScholarPubMed
Kubasek, J, Hajek, T and Glime, J (2014) Bryophyte photosynthesis in sunflecks: greater relative induction rate than in tracheophytes. Journal of Bryology 36, 110–117.10.1179/1743282014Y.0000000096CrossRefGoogle Scholar
Lakatos, M, Rascher, U and Büdel, B (2006) Functional characteristics of corticolous lichens in the understory of a tropical lowland rain forest. New Phytologist 172, 679–695.10.1111/j.1469-8137.2006.01871.xCrossRefGoogle ScholarPubMed
Morales, A and Kaiser, E (2020) Photosynthetic acclimation to fluctuating irradiance in plants. Frontiers in Plant Science 11, 268.10.3389/fpls.2020.00268CrossRefGoogle ScholarPubMed
Murchie, EH and Ruban, AV (2020) Dynamic non-photochemical quenching in plants: from molecular mechanism to productivity. Plant Journal 101, 885–896.10.1111/tpj.14601CrossRefGoogle Scholar
Nelsen, MP, Leavitt, SD, Heller, K, Muggia, L and Lumbsch, HT (2021) Macroecological diversification and convergence in a clade of keystone symbionts. FEMS Microbiology Ecology 97, fiab072.10.1093/femsec/fiab072CrossRefGoogle Scholar
Pallardy, SG (2008) Physiology of Woody Plants, 3rd Edn. Elsevier: Amsterdam.Google Scholar
Piccotto, M and Tretiach, M (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. Journal of Plant Research 123, 763–775.10.1007/s10265-010-0329-2CrossRefGoogle ScholarPubMed
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, 171–177.10.1179/1743282015Y.0000000001CrossRefGoogle Scholar
Roach, T and Krieger-Liszkay, A (2019) Photosynthetic regulatory mechanisms for efficiency and prevention of photo-oxidative stress. Annual Plant Reviews Online 2, 273–306.10.1002/9781119312994.apr0666CrossRefGoogle Scholar