, Volume 231, Issue 6, pp 1335–1342 | Cite as

Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria

  • B. Fernández-Marín
  • J. M. Becerril
  • J. I. García-Plazaola
Original Article


Desiccation-tolerance ability in photosynthetic organisms is largely based on a battery of photoprotective mechanisms. Xanthophyll cycle operation induced by desiccation in the absence of light has been previously proven in the desiccation-tolerant fern Ceterach officinarum. To understand the physiological function of xanthophyll cycle induction in darkness and its implication in the desiccation tolerance in more detail, we studied its triggering factors and its photochemical effects in the lichen Lobaria pulmonaria. We found that both the drying rate and the degree of desiccation play a crucial role in the violaxanthin de-epoxidase activation. De-epoxidation of violaxanthin to zeaxanthin (Z) occurs when the tissue has lost most of its water and only after slow dehydration, suggesting that a minimum period of time is required for the enzyme activity induction. Fluorescence analysis showed that Z, synthesised during tissue dehydration in the absence of light, prevents photoinhibition when rewatered tissues are illuminated. This is probably due to Z implication in both non-photochemical quenching and/or antioxidative responses.


Darkness Desiccation Lobaria Non-photochemical quenching (NPQ) Xanthophyll cycle Zeaxanthin 











Minimum chlorophyll fluorescence yield


Maximum chlorophyll fluorescence yield


Variable chlorophyll fluorescence


Maximum quantum yield of the PS II




Non-photochemical quenching


Photon flux density




Relative humidity


Reactive oxygen species


Relative water content




Violaxanthin de-epoxidase






Zeaxanthin epoxidase



We are very grateful to Jane Edwards for linguistic consultation of the manuscript. B.F.M. received a fellowship from the Basque Government. This research was supported by research BFU 2007-62637 from the Ministry of Education and Science of Spain and research project UPV/EHU-GV IT-299-07.


  1. Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS, Smith SD (2002) Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species in the Mojave Desert. Plant Cell Environ 25:95–103CrossRefGoogle Scholar
  2. Barták M, Solhaug A, Vrablikova H, Gauslaa (2006) Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. Oecology 149:553–560CrossRefGoogle Scholar
  3. Bukhov NG, Kopecky J, Pfündel EE, Klughammer C, Heber U (2001) A few molecules of zeaxanthin per reaction centre of photosystem II permit effective thermal dissipation of light energy in photosystem II of a poikilohydric moss. Planta 212:739–748CrossRefPubMedGoogle Scholar
  4. Casper C, Eickmeier WG, Osmond B (1993) Changes of fluorescence and xanthophyll pigments during dehydration in the resurrection plant Selaginella lepidophylla in low and medium light intensities. Oecologia 94:528–533CrossRefGoogle Scholar
  5. Chakir S, Jensen M (1999) How does Lobaria pulmonaria regulate photosystem II during progressive desiccation and osmotic water stress? A chlorophyll fluorescence study at room temperature and at 77 K. Physiol Plant 105:257–265CrossRefGoogle Scholar
  6. Cooper K, Farrant JM (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J Exp Bot 53:1805–1813CrossRefPubMedGoogle Scholar
  7. Demmig-Adams B, Adams WW III (1996) The role of xanthopyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26CrossRefGoogle Scholar
  8. Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21CrossRefPubMedGoogle Scholar
  9. 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 166:1734–1744CrossRefPubMedGoogle Scholar
  10. García-Plazaola JI, Becerril JM (1999) A rapid HPLC method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 10:307–313CrossRefGoogle Scholar
  11. García-Plazaola JI, Becerril JM (2001) Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Aust J Plant Phys 28:225–232Google Scholar
  12. Gasulla F, Gómez de Nova P, Esteban-Carrasco A, Zapata JM, Barreno E, Guéra A (2009) Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231:195–208CrossRefPubMedGoogle Scholar
  13. Gauslaa Y, Solhaug KA (2000) High-light-intensity damage to the foliose lichen Lobaria pulmonaria within natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32:271–289CrossRefGoogle Scholar
  14. Gauslaaa Y, Lie M, Solhaug KA, Ohlson M (2006) Growth and ecophysiological acclimation of the foliose lichen Lobaria pulmonaria in forest with contrasting light climates. Oecologia 147:406–416CrossRefGoogle Scholar
  15. Goss R, Opitz C, Lepetit B, Wilhelm C (2008) The synthesis of NPQ-effective zeaxanthin depends on the presence of a transmembrane proton gradient and a slightly basic stromal side of the thylakoid membrane. Planta 228:999–1009CrossRefPubMedGoogle Scholar
  16. Hájek J, Barták M, Dubová J (2006) Inhibition of photosynthetic processes in foliose lichens induced by temperature and osmotic stress. Biol Plant 56:624–634CrossRefGoogle Scholar
  17. Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–150CrossRefGoogle Scholar
  18. Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from oxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767CrossRefPubMedGoogle Scholar
  19. Heber U, Lange OL, Shuvalov VA (2006) Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. J Exp Bot 57:1211–1223CrossRefPubMedGoogle Scholar
  20. Heber U, Bilger W, Türk R, Lange OL (2010) Photoprotection of reaction centres in photosynthetic organisms: mechanisms of thermal energy dissipation in desiccated thalli of the lichen Lobaria pulmonaria. New Phytol 185:459–470CrossRefPubMedGoogle Scholar
  21. Jensen M, Chakir S, Feige GB (1999) Osmotic and atmospheric dehydration effects in the lichens Hypogymnia physodes, Lobaria pulmonaria, and Peltigera aphthosa: an in vivo study of the chlorophyll fluorescence induction. Photosynthetica 37:393–404CrossRefGoogle Scholar
  22. 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 50:879–888CrossRefPubMedGoogle Scholar
  23. Kranner I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 154:451–460CrossRefGoogle Scholar
  24. Kranner I, Birtic S (2005) A modulating role for antioxidant in desiccation tolerance. Integr Comp Biol 45:734–740CrossRefGoogle Scholar
  25. Kranner I, Zorn M, Turk B, Wornik S, Backett RP, Patic F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol 160:167–176CrossRefGoogle Scholar
  26. 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 102:3141–3146CrossRefPubMedGoogle Scholar
  27. Kranner I, Beckett R, Hochman A, Nash TH (2008) Desiccation tolerance in lichens: a review. Bryologist 11:576–593CrossRefGoogle Scholar
  28. Latowski D, Kerlund HE, Strzaka K (2004) Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 43:4417–4420CrossRefPubMedGoogle Scholar
  29. Mackenzie TDB, MacDonald, Dubois LA, Campbell (2001) Seasonal changes in temperature and light drive acclimation of photosynthetic physiology and macromolecular content in Lobaria pulmonaria. Planta 214:57–66CrossRefPubMedGoogle Scholar
  30. Minibayeva F, Beckett RP (2001) High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation. New Phytol 152:333–341CrossRefGoogle Scholar
  31. Müller P, Li X-P, Niyogi K (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedGoogle Scholar
  32. Nabe H, Funabiki R, Kashino Y, Koike H, Satoh K (2007) Responses to desiccation stress in bryophytes and important role of dithiothreitol-insensitive non-photochemical quenching against photoinhibition in dehydrated states. Plant Cell Physiol 48:1548–1557CrossRefPubMedGoogle Scholar
  33. Palmqvist K (2000) Carbon economy in lichens. New Phytol 148:11–36CrossRefGoogle Scholar
  34. Proctor MCF, Tuba Z (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytol 156:327–349CrossRefGoogle Scholar
  35. Schofield SC, Campbell DA, Funk C, MacKenzie TB (2003) Changes in macromolecular allocation in nondividing algal symbionts allow for photosynthetic acclimation in the lichen Lobaria pulmonaria. New Phytol 159:709–718CrossRefGoogle Scholar
  36. Stepigova J, Gauslaa Y, Cempirkova-Vrablikova H, Solhaug KA (2008) Irradiance prior to and during desiccation improves the tolerance to excess irradiance in the desiccated state of the old forest lichen Lobaria pulmonaria. Photosynthetica 46:286–290CrossRefGoogle Scholar
  37. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms regulation and adaptation. Taylor and Francis, UK, pp 445–483Google Scholar
  38. Sun WQ, Leopold AC (1997) Cytoplasmic vitrification and survival of anhydrobiotic organisms. Comp Biochem Physiol 117:327–333CrossRefGoogle Scholar
  39. Wendell QS (2002) Methods for the study of water relations under desiccation stress. In: Black M, Pritchard HW (eds) Desiccation and survival in plants. Drying without dying. CABI Publishing, UK, pp 47–93Google Scholar
  40. Yamamoto HY, Komite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim Biophys Acta 267:538–543CrossRefPubMedGoogle Scholar
  41. Zeliou K, Manetas Y, Petropoulou Y (2009) Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. J Exp Bot 60:3031–3042CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • B. Fernández-Marín
    • 1
  • J. M. Becerril
    • 1
  • J. I. García-Plazaola
    • 1
  1. 1.Departamento de Biología Vegetal y EcologíaUniversidad del País VascoBilbaoSpain

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