Skip to main content
SpringerLink
Log in

Photosynthesis measurements on the upper and lower side of the thallus of the foliose lichen Nephroma arcticum (L.) Torss

  • Original article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The measurements of chlorophyll fluorescence play an important role in studies of lichen physiology. Usually, for foliose lichens fluorescence kinetics is recorded from the upper thalline side often exhibiting green color reflecting the presence of photosynthetic pigments. The lower side of such lichens is grey, dark-brown or black. At the first time, we evaluated photosynthetic activity distribution by chlorophyll fluorescence analysis on both lower and upper thallus sides for the foliose lichen Nephroma arcticum. We have demonstrated that photosynthesis proceeds not only on the green-colored upper side, but also on the gray lower side of the curled growing edges of the thallus lobes. These sides were differed in terms of PSII photochemical quantum yield, activity of non-regulatory dissipation and non-photochemical quenching of excited chlorophyll states (NPQ). Upper side was characterized by higher maximal PSII efficiency, whereas the lower one of the curled edges was characterized by higher actual photochemical quantum yield during actinic light acclimation. NPQ was higher on the upper surface, whereas, on the lower side (of the curled edges) non-regulatory dissipation was predominant. In terms of photosynthetic activity measurements, these results show, that actinic and measuring light reached the layer of phycobiont despite its shielding by mycobiont hyphae. On the melanized lower side in the basal thalline zone attached to the substratum photosynthesis was not detected. Lower side demonstrated higher level of light scattering in the reflectance spectra. We believe that different photoprotective mechanisms against high light are crucial on the upper and lower sides: NPQ on the upper surface, and light scattering and shielding by mycobiont on the lower side. Possible biological role of photosynthesis on the lower side is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

a. u.:

Arbitrary units of chlorophyll fluorescence intensity

BRI:

Browning reflectance index

CF:

Chlorophyll fluorescence

ETC:

Electron transport chain

F J :

The value of CF intensity at inflection J

Fm:

Peak value of the CF intensity

Fo:

Fluorescence intensity in the origin point of the curve

Fv:

Variable fluorescence

Mo:

Normalized initial slope of OJIP curve

N(Q A):

QA turnover number

NDVI:

Normalized Difference Vegetation Index

PAR:

Photosynthetic active radiation

PS II:

Photosystem II

QA :

Primary PS II quinone acceptor

PRI:

Photochemical Reflectance Index

R Red, R NIR :

Total reflectance in the red and near infrared bands of the spectrum, respectively

R(λ):

Reflectance at the wavelength λ

RC:

Reaction center

Sm, Ss:

Normalized area between the OJIP curve and the horizontal line F(t) = Fm in the case of multiple and single QA turnover number, respectively

SR:

Simple ratio

VJ :

Relative height of O-J-step of OJIP curve

φ Do :

Quantum yield of thermal dissipation

φ Eo :

Quantum yield of electron transport

φ Po :

Maximal photosystem II (PSII) photochemical quantum yield of the dark-adapted thalli

Ψ0 :

The probability of electron transport beyond QA

References

  • Ahmadjian V, Jacobs JB (1981) Relationship between fungus and alga in the lichen Cladonia cristatella Tuck. Nature 289.5794:169

    Article  Google Scholar 

  • Ametrano CG, Muggia L, Grube M (2019) Extremotolerant black fungi from rocks and lichens. In: Tiquia-Arashiro SM, Grube M (eds) Fungi in extreme environments: ecological role and biotechnological significance. Springer, Cham, pp 119–143

    Chapter  Google Scholar 

  • Barták M (2014) Lichen photosynthesis. Scaling from the cellular to the organism level. In: Hohmann-Marriott MF (ed) The structural basis of biological energy generation. Springer, New York, pp 379–400

    Chapter  Google Scholar 

  • Barták M, Hájek J, Gloser J (2000) Heterogeneity of chlorophyll fluorescence over thalli of several foliose macrolichens exposed to adverse environmental factors: interspecific differences as related to thallus hydration and high irradiance. Photosynthetica 38(4):531–537

    Article  Google Scholar 

  • Barták M, Gloser J, Hájek J (2005) Visualized photosynthetic characteristics of the lichen Xanthoria elegans related to daily courses of light, temperature and hydration: a field study from Galindez Island, maritime Antarctica. Lichenologist 37(5):433–443

    Article  Google Scholar 

  • Barták M, Solhaug KA, Vráblíková H, Gauslaa Y (2006) Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. Oecologia 149(4):553–560

    Article  PubMed  Google Scholar 

  • Barták M, Trnková K, Hansen ES, Hazdrová J, Skácelová K, Hájek J, Forbelská M (2015) Effect of dehydration on spectral reflectance and photosynthetic efficiency in Umbilicaria arctica and U. hyperborea. Biol Plant 59:357–365

    Article  CAS  Google Scholar 

  • Baruffo L, Piccotto M, Tretiach M (2008) Intrathalline variation of chlorophyll a fluorescence emission in the epiphytic lichen Flavoparmelia caperata. Bryologist 111(3):455–462

    Article  Google Scholar 

  • Bokhorst S, Tømmervik H, Callaghan TV, Phoenix GK, Bjerke JW (2012) Vegetation recovery following extreme winter warming events in the sub-Arctic estimated using NDVI from remote sensing and handheld passive proximal sensors. Environ Exp Bot 81:18–25

    Article  Google Scholar 

  • Büdel B, Scheidegger C (2008) Thallus morphology and anatomy. In: Nash TH (ed) Lichen biology. Cambrige University Press, Cambridge, pp 40–68

    Chapter  Google Scholar 

  • Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44(12):1115–1136

    Article  CAS  Google Scholar 

  • Chekanov K, Feoktistov A, Lobakova E (2017) Spatial organization of the three-component lichen Peltigera aphthosa in functional terms. Physiol Plant 160:328–338

    Article  CAS  PubMed  Google Scholar 

  • Chivkunova OB, Solovchenko AE, Sokolova SG, Merzlyak MN, Reshetnikova IV, Gitelson AA (2001) Reflectance spectral features and detection of superficial scald-induced browning in storing apple fruit. J Russ Phytopathol Soc 2:73–77

    Google Scholar 

  • Conti S, Hazdrová J, Hájek J, Očenášová P, Barták M, Skácelová K, Adamo P (2014) Comparative analysis of heterogeneity of primary photosynthetic processes within fruticose lichen thalli: preliminary study of interspecific differences. Czech Polar Reports 4(2):149–157

    Article  Google Scholar 

  • Demmig-Adams B, Adams Iii WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Biol 43(1):599–626

    Article  CAS  Google Scholar 

  • Fortuna L, Baracchini E, Adami G, Tretiach M (2017) Melanization affects the content of selected elements in parmelioid lichens. J Chem Ecol 43(11):1086–1096

    Article  CAS  PubMed  Google Scholar 

  • Gamon JA, Huemmrich KF, Stone RS, Tweedie CE (2013) Spatial and temporal variation in primary productivity (NDVI) of coastal Alaskan tundra: decreased vegetation growth following earlier snowmelt. Remote Sens Environ 129:144–153

    Article  Google Scholar 

  • Garty J, Weissman L, Tamir O, Beer S, Cohen Y, Karnieli A, Orlovsky L (2000) Comparison of five physiological parameters to assess the vitality of the lichen Ramalina lacera exposed to air pollution. Physiol Plant 109(4):410–418

    Article  CAS  Google Scholar 

  • Gauslaa Y, Solhaug KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126(4):462–471

    Article  PubMed  Google Scholar 

  • Gessler NN, Egorova AS, Belozerskaya TA (2014) Melanin pigments of fungi under extreme environmental conditions. Appl Biochem Microbiol 50(2):105–113

    Article  CAS  Google Scholar 

  • Gloser J, Gloser V (2007) Changes in spectral reflectance of a foliar lichen Umbilicaria hirsuta during desiccation. Biol Plant 51(2):395–398

    Article  Google Scholar 

  • Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63(6):869–893

    Article  CAS  Google Scholar 

  • Hájek J, Barták M, Dubová J (2006) Inhibition of photosynthetic processes in foliose lichens induced by temperature and osmotic stress. Biol Plant 50(4):624–634

    Article  Google Scholar 

  • Hájek J, Barták M, Hazdrová J, Forbelská M (2016) Sensitivity of photosynthetic processes to freezing temperature in extremophilic lichens evaluated by linear cooling and chlorophyll fluorescence. Cryobiology 73(3):329–334

    Article  PubMed  CAS  Google Scholar 

  • Honegger R (2008) Morphogenesis. In: Nash TH (ed) Lichen biology. Cambrige University Press, Cambridge, pp 69–93

    Chapter  Google Scholar 

  • Honegger R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In: Hock B (ed) Fungal associations, the mycota IX, 2nd edn. Springer, Berlin, pp 287–339

    Chapter  Google Scholar 

  • Jensen M, Siebke K (1997) Technical report. fluorescence imaging of lichens in the macro scale. Symbiosis 23:183–196

    Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122(2):121–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A et al (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38(4):102

    Article  CAS  Google Scholar 

  • Kuusinen N, Juola J, Karki B, Stenroos S, Rautiainen M (2020) A spectral analysis of common boreal ground lichen species. Remote Sens Environ 247:111955

    Article  PubMed  PubMed Central  Google Scholar 

  • Lange OL, Green TA, Reichenberger H (1999) The response of lichen photosynthesis to external CO2 concentration and its interaction with thallus water-status. J Plant Physiol 154(2):157–166

    Article  CAS  Google Scholar 

  • Lange OL, Green TA, Heber U (2001) Hydration-dependent photosynthetic production of lichens: what do laboratory studies tell us about field performance? J Exp Bot 52(363):2033–2042

    Article  CAS  PubMed  Google Scholar 

  • Lange OL, Green TA, Melzer B, Meyer A, Zellner H (2006) Water relations and CO2 exchange of the terrestrial lichen Teloschistes capensis in the Namib fog desert: measurements during two seasons in the field and under controlled conditions. Flora-Morphol Distrib Funct Ecol Plants 201(4):268–280

    Article  Google Scholar 

  • Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30

    Article  PubMed  Google Scholar 

  • Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147

    Article  PubMed  CAS  Google Scholar 

  • Mafole T (2017) Melanisation of lichens: the composition of melanin and the role of ultraviolet light (uv) in peltigeralean and non-peltigeralean Lichens (Doctoral dissertation)

  • Mafole TC, Chiang C, Solhaug KA, Beckett RP (2017) Melanisation in the old forest lichen Lobaria pulmonaria reduces the efficiency of photosynthesis. Fungal Ecol 29:103–110

    Article  Google Scholar 

  • Mafole TC, Solhaug KA, Minibayeva FV, Beckett RP (2019a) Tolerance to photoinhibition within a lichen species is higher in melanised thalli. Photosynthetica 57(1):96–102

    Article  CAS  Google Scholar 

  • Mafole TC, Solhaug KA, Minibayeva FV, Beckett RP (2019b) Occurrence and possible roles of melanic pigments in lichenized ascomycetes. Fungal Biol Rev 33(3–4):159–165

    Article  Google Scholar 

  • Maksimov EG, Schmitt FJ, Tsoraev GV, Ryabova AV, Friedrich T, Paschenko VZ (2014) Fluorescence quenching in the lichen Peltigera aphthosa due to desiccation. Plant Physiol Biochem 81:67–73

    Article  CAS  PubMed  Google Scholar 

  • Matee LP, Beckett RP, Solhaug KA, Minibayeva FV (2016) Characterization and role of tyrosinases in the lichen Lobaria pulmonaria (L.) Hoffm. Lichenologist 48(4):311–322

    Article  Google Scholar 

  • McEvoy M, Gauslaa Y, Solhaug KA (2007a) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytol 175(2):271–282

    Article  CAS  PubMed  Google Scholar 

  • McEvoy M, Solhaug KA, Gauslaa Y (2007b) Solar radiation screening in usnic acid-containing cortices of the lichen Nephroma arcticum. Symbiosis 43:143–150

    Google Scholar 

  • McLean J, Purvis OW, Williamson BJ, Bailey EH (1998) Role for lichen melanins in uranium remediation. Nature 391(6668):649

    Article  CAS  Google Scholar 

  • Palharini KMZ, Vitorino LC, Menino GCDO, Bessa LA (2020) Edge effects reflect the impact of the agricultural matrix on the corticolous lichens found in fragments of Cerrado Savanna in Central Brazil. Sustainability 12(17):7149

    Article  Google Scholar 

  • Parr CS, Wilson MN et al (2014) The encyclopedia of life v2: providing global access to knowledge about life on earth. Biodivers Data J 2:e1079

    Article  Google Scholar 

  • Peñuelas J, Filella I (1998) Visible and near-infrared reflectance techniques for diagnosing plant physiological status. Trends Plant Sci 3(4):151–156

    Article  Google Scholar 

  • Plonka PM, Grabacka M (2006) Melanin synthesis in microorganisms – biotechnological and medical aspects. Acta Biochim Pol 53:429443. https://doi.org/10.18388/abp.2006_3314

    Article  Google Scholar 

  • Rao DN, LeBlanc F (1965) A possible role of atranorin in the lichen thallus. Bryologist 68(3):284–289

    Article  CAS  Google Scholar 

  • Rassabina AE, Gurjanov OP, Beckett RP, Minibayeva FV (2020) Melanin from the Lichens Cetraria islandica and Pseudevernia furfuracea: structural features and physicochemical properties. Biochem Mosc 85:623–628

    Article  CAS  Google Scholar 

  • Raynolds MK, Walker DA, Verbyla D, Munger CA (2013) Patterns of change within a tundra landscape: 22-year Landsat NDVI trends in an area of the northern foothills of the Brooks Range, Alaska. Arct Antarct Alp Res 45(2):249–260

    Article  Google Scholar 

  • Rikkinen J (2015) Cyanolichens. Biodivers Conserv 24(4):973–993

    Article  Google Scholar 

  • Solhaug KA, Larsson P, Gauslaa Y (2010) Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 231(5):1003–1011

    Article  CAS  PubMed  Google Scholar 

  • Sotille ME, Bremer UF, Vieira G, Velho LF, Petsch C, Simões JC (2020) Evaluation of UAV and satellite-derived NDVI to map maritime Antarctic vegetation. Appl Geogr 125:102322

    Article  Google Scholar 

  • Stirbet A, Riznichenko GY, RubinGovindjee AB (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochem Mosc 79(4):291–323

    Article  CAS  Google Scholar 

  • Stocker-Wörgötter E (2001) Experimental lichenology and microbiology of lichens: culture experiments, secondary chemistry of cultured mycobionts, resynthesis, and thallus morphogenesis. Bryologist 104(4):576–581

    Article  Google Scholar 

  • Strasser RJ, Stirbet AD (2001) Estimation of the energetic connectivity of PS II centres in plants using the fluorescence rise O-J–I–P: Fitting of experimental data to three different PS II models. Math Comput Simul 56(4):451–462

    Article  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a Fluorescence. Springer, Dordrecht, pp 321–362

  • Thomson JW (1972) Distribution patterns of American Arctic lichens. Can J Bot 50(5):1135–1156

    Article  Google Scholar 

  • Urbanavichyus GP (2011) Specific features of lichen diversity of Russia. Izvestiya Rossiiskoi Akademii Nauk Series Geography 1:66–87

    Google Scholar 

  • Valladares F, Sancho LG, Ascaso C (1996) Functional analysis of the intrathalline and intracellular chlorophyll concentrations in the lichen family Umbilicariaceae. Ann Bot 78(4):471–477

    Article  CAS  Google Scholar 

  • Wu L, Zhang G, Lan S, Zhang D, Hu C (2014) Longitudinal photosynthetic gradient in crust lichens’ thalli. Microb Ecol 67(4):888–896

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Microscopic studies were conducted using equipment of the Center of Microscopy of White Sea Biological Station of Moscow State University. The research was performed on the base of the «Research-and-production complex for study, preservation and practical use of cell cultures and organs of higher plants and microalgae» and financially supported by the Government of Russian Federation through Megagrant project no. 075-15-2019-1882.

Author information

Authors and Affiliations

  1. Department of Bioengineering, Faculty of Biology, Lomonosov Moscow State University, 1/12, Moscow, Russia, 119234

    Konstantin Chekanov & Elena Lobakova

  2. Centre for Humanities Research and Technology, National Research Nuclear University MEPhi, Kashirskoe highway, 31, Moscow, Russia, 115409

    Konstantin Chekanov

Authors
  1. Konstantin Chekanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Lobakova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KC—manuscript preparation; CF measurements; spectroscopy; data interpretation. EL—manuscript preparation; experiment design; project administration.

Corresponding author

Correspondence to Konstantin Chekanov.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chekanov, K., Lobakova, E. Photosynthesis measurements on the upper and lower side of the thallus of the foliose lichen Nephroma arcticum (L.) Torss. Photosynth Res 149, 289–301 (2021). https://doi.org/10.1007/s11120-021-00860-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-021-00860-0

Keywords

Search

Navigation