Skip to main content

Advertisement

SpringerLink
Log in

Multiple dissipation components of excess light energy in dry lichen revealed by ultrafast fluorescence study at 5 K

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

A time-resolved fluorescence study of living lichen thalli at 5 K was conducted to clarify the dynamics and mechanism of the effective dissipation of excess light energy taking place in lichen under extreme drought conditions. The decay-associated spectra obtained from the experiment at 5 K were characterized by a drastically sharpened spectral band which could not be resolved by experiments at higher temperatures. The present results indicated the existence of two distinct dissipation components of excess light energy in desiccated lichen; one is characterized as rapid fluorescence decay with a time constant of 27 ps in the far-red region that was absent in wet lichen thalli, and the other is recognized as accelerated fluorescence decay in the 685–700 nm spectral region. The former energy-dissipation component with extremely high quenching efficiency is most probably ascribed to the emergence of a rapid quenching state in the peripheral-antenna system of photosystem II (PS II) on desiccation. This is an extremely effective protection mechanism of PS II under desiccation, which lichens have developed to survive in the severely desiccated environments. The latter, which is less efficient at 5 K, might have a supplementary role and take place either in the core antenna of PS II or aggregated peripheral antenna of PS II.

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
Fig. 5

Similar content being viewed by others

References

  • Adams III WW, Demmigadams B, Lange OL (1993) Carotenoid composition and metabolism in green and blue-green-algal lichens in the field. Oecologia 94:576–584

    Google Scholar 

  • Ahmadjian V (1993) The lichen symbiosis. Springer, Berlin

    Google Scholar 

  • Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

    Article  PubMed  CAS  Google Scholar 

  • Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180

    Article  PubMed  CAS  Google Scholar 

  • Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties. FEBS Lett 134:231–234

    Article  CAS  Google Scholar 

  • Davis MS, Forman A, Fajer J (1979) Ligated chlorophyll cation radicals: their function in photosystem II of plant photosynthesis. Proc Natl Acad Sci USA 76:4170–4174

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams III WW (2000) Photosynthesis: harvesting sunlight safely. Nature 403:371–374

    Google Scholar 

  • Fernández-Marín B, Balaguer L, Esteban R, Becerril JM, García-Plazaola JI (2009) Dark induction of the photoprotective xanthophyll cycle in response to dehydration. J Plant Physiol 166:1734–1744

    Article  PubMed  Google Scholar 

  • Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Unraveling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria. Planta 231:1335–1342

    Article  PubMed  Google Scholar 

  • Groot ML, Peterman EJG, van Stokkum IHM, Dekker JP, van Grondelle R (1995) Triplet and fluorescing states of the CP47 antenna complex of photosystem II studied as a function of temperature. Biophys J 68:281–290

    Article  PubMed  CAS  Google Scholar 

  • Groot ML, Frese RN, de Weerd FL, Bromek K, Pettersson A, Peterman EJG, van Stokkum IHM, van Grondelle R, Dekker JP (1999) Spectroscopic properties of the CP43 core antenna protein of photosystem II. Biophys J 77:3328–3340

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B (1984) Chloroplast metabolism. Clarendon Press, Oxford

    Google Scholar 

  • Hirai M, Yamakawa R, Nishio J, Yamaji T, Kashino Y, Koike H, Satoh K (2004) Deactivation of photosynthetic activities is triggered by loss of a small amount of water in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol 45:872–878

    Article  PubMed  CAS  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    Article  PubMed  CAS  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436

    Article  PubMed  CAS  Google Scholar 

  • Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Phys 42:553–578

    Article  CAS  Google Scholar 

  • Honegger R (1998) The lichen symbiosis—what is so spectacular about it? Lichenologist 30:193–212

    Google Scholar 

  • Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079

    Article  PubMed  CAS  Google Scholar 

  • Koenig F, Schmidt M (1995) Gloeobacter violaceus—investigation of an unusual photosynthetic apparatus. Absence of the long wavelength emission of photosystem I in 77 K fluorescence spectra. Physiol Plant 94:621–628

    Article  CAS  Google Scholar 

  • Komura M, Shibata Y, Itoh S (2006) A new fluorescence band F689 in photosystem II revealed by picosecond analysis at 4–77 K: function of two terminal energy sinks F689 and F695 in PS II. Biochim Biophys Acta 1757:1657–1668

    Article  PubMed  CAS  Google Scholar 

  • Komura M, Yamagishi A, Shibata Y, Iwasaki I, Itoh S (2010) Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy. Biochim Biophys Acta Bioenerg 1797:331–338

    Article  CAS  Google Scholar 

  • Kosugi M, Arita M, Shizuma R, Moriyama Y, Kashino Y, Koike H, Satoh K (2009) Responses to desiccation stress in lichens are different from those in their photobionts. Plant Cell Physiol 50:879–888

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci USA 102:3141–3146

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874

    Article  PubMed  CAS  Google Scholar 

  • Ma YZ, Holt NE, Li XP, Niyogi KK, Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100:4377–4382

    Article  PubMed  CAS  Google Scholar 

  • Millbank JW, Kershaw KA (1969) Nitrogen metabolism in lichens.1. Nitrogen fixation in cephalodia of Peltigera aphthosa. New Phytol 68:721–729

    Article  CAS  Google Scholar 

  • Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett 582:3625–3631

    Article  PubMed  CAS  Google Scholar 

  • Müller MG, Lambrev P, Reus M, Wientjes E, Croce R, Holzwarth AR (2010) Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. Chemphyschem 11:1289–1296

    Article  PubMed  Google Scholar 

  • Mullineaux CW, Pascal AA, Horton P, Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHCII chlorophyll-protein complex: a time-resolved fluorescence study. Biochim Biophys Acta 1141:23–28

    Article  CAS  Google Scholar 

  • Munne-Bosch S (2005) The role of alpha-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    Article  PubMed  CAS  Google Scholar 

  • Neupane B, Dang NC, Acharya K, Reppert M, Zazubovich V, Picorel R, Seibert M, Jankowiak R (2010) Insight into the electronic structure of the CP47 antenna protein complex of photosystem II: hole burning and fluorescence study. J Am Chem Soc 132:4214–4229

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta Bioenerg 1757:742–749

    Article  CAS  Google Scholar 

  • Palmqvist K (2000) Carbon economy in lichens. New Phytol 148:11–36

    Article  CAS  Google Scholar 

  • Pieper J, Irrgang KD, Ratsep M, Schrotter T, Voigt J, Small GJ, Renger G (1999) Effects of aggregation on trimeric light-harvesting complex II of green plants: a hole-burning study. J Phys Chem A 103:2422–2428

    Article  CAS  Google Scholar 

  • Ruban AV, Dekker JP, Horton P, van Grondelle R (1995) Temperature-dependence of chlorophyll fluorescence from the light-harvesting complex II of higher-plants. Photochem Photobiol 61:216–221

    Article  CAS  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    Article  PubMed  CAS  Google Scholar 

  • Scheidegger C, Schroeter B, Frey B (1995) Structural and functional processes during water vapor uptake and desiccation in selected lichens with green algal photobionts. Planta 197:399–409

    Article  CAS  Google Scholar 

  • Schweitzer RH, Melkozernov AN, Blankenship RE, Brudvig GW (1998) Time-resolved fluorescence measurements of photosystem II: the effect of quenching by oxidized chlorophyll Z. J Phys Chem B 102:8320–8326

    Article  CAS  Google Scholar 

  • Shibata Y, Yamagishi A, Kawamoto S, Noji T, Itoh S (2010) Kinetically distinct three red chlorophylls in photosystem I of Thermosynechococcus elongatus revealed by femtosecond time-resolved fluorescence spectroscopy at 15 K. J Phys Chem B 114:2954–2963

    Article  PubMed  CAS  Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • van Dorssen RJ, Breton J, Plijter JJ, Satoh K, van Gorkom HJ, Amesz J (1987) Spectroscopic properties of the reaction center and of the 47 kda chlorophyll protein of photosystem II. Biochim Biophys Acta 893:267–274

    Article  CAS  Google Scholar 

  • Veerman J, Vasil’ev S, Paton GD, Ramanauskas J, Bruce D (2007) Photoprotection in the lichen Parmelia sulcata: the origins of desiccation-induced fluorescence quenching. Plant Physiol 145:997–1005

    Article  PubMed  CAS  Google Scholar 

  • Yamagishi A, Ikeda Y, Komura M, Koike H, Satoh K, Itoh S, Shibata Y (2010) Shallow sink in an antenna pigment system of photosystem I of a marine centric diatom, Chaetoceros gracilis, revealed by ultrafast fluorescence spectroscopy at 17 K. J Phys Chem B 114:9031–9038

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by Grants-in-Aid for Scientific Research (No. 17750010), the 21st COE program for “the origin of the universe and matter” from the Japanese Ministry of Education, Science, Sports, and Culture (MEXT), and the Japan Society for the Promotion of Science (JSPS). We thank Dr. Yoshikazu Yamamoto (Faculty of Bioresource Sciences, Akita Prefectural University) for the phylogenic determination of the lichen samples.

Author information

Author notes

  1. Makiko Kosugi

    Present address: National Institute of Polar Research, 10-3 Midori-cho, Tachikawa, Tokyo, 190-8518, Japan

  2. Yutaka Shibata

    Present address: Department of Chemistry, Graduate School of Science, Tohoku University, Aramaki aza Aoba, Aoba-ku, Sendai, 980-8578, Japan

Authors and Affiliations

  1. Division of Material Science (Physics), Graduate School of Science, Nagoya University, Nagoya, 464-8602, Japan

    Hirohisa Miyake, Masayuki Komura, Shigeru Itoh & Yutaka Shibata

  2. Graduate School of Life Science, University of Hyogo, Harima Science Garden City, Hyogo, 678-1297, Japan

    Makiko Kosugi, Yasuhiro Kashino & Kazuhiko Satoh

Authors
  1. Hirohisa Miyake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayuki Komura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shigeru Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Makiko Kosugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasuhiro Kashino
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kazuhiko Satoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yutaka Shibata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yutaka Shibata.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 419 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miyake, H., Komura, M., Itoh, S. et al. Multiple dissipation components of excess light energy in dry lichen revealed by ultrafast fluorescence study at 5 K. Photosynth Res 110, 39–48 (2011). https://doi.org/10.1007/s11120-011-9691-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-011-9691-8

Keywords

Search

Navigation