, Volume 247, Issue 3, pp 705–714 | Cite as

Relationships between water status and photosystem functionality in a chlorolichen and its isolated photobiont

  • Francesco Petruzzellis
  • Tadeja Savi
  • Stefano Bertuzzi
  • Alice Montagner
  • Mauro Tretiach
  • Andrea Nardini
Original Article


Main conclusion

Drought tolerance was greater in the whole lichen than in its isolated photobiont. Cell turgor state has an influence on the functionality of photosynthetic process in lichens.

Irreversible thermodynamics is widely used to describe the water relations of vascular plants. However, poikilohydrous organisms like lichens and aeroterrestrial microalgae have seldom been studied using this approach. Water relations of lichens are generally addressed without separate analysis of the mycobiont and photobiont, and only few studies have correlated changes in photosynthetic efficiency of dehydrating lichens to accurate measurements of their water potential components. We measured water potential isotherms and chlorophyll a fluorescence in the lichen Flavoparmelia caperata harvested in different seasons, as well as in its isolated photobiont, the green alga Trebouxia gelatinosa, either exposed to water stress cycles or fully hydrated. No significant seasonal trends were observed in lichen water relations parameters. Turgor loss point and osmotic potential of the whole thallus were significantly lower than those measured in the photobiont, while differences between the water stressed photobiont and controls were not significant. Dehydration-induced drop of F v/F m was correlated with turgor loss, revealing that the photosynthetic activity of lichens partly depends on their turgor level. We provided one of the first quantitative evidences of the influence that turgor status could exert on the functionality of photosynthetic processes in lichens.


Chlorophyll fluorescence Desiccation tolerance Flavoparmelia caperata Osmotic potential Trebouxia gelatinosa Turgor loss point 


  1. Ahmadjian V (1973) Methods of isolation and culturing lichen symbionts and thalli. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 653–659CrossRefGoogle Scholar
  2. Alam MA, Gauslaa Y, Solhaug KA (2015) Soluble carbohydrates and relative growth rates in chloro-, cyano- and cephalolichens: effects of temperature and nocturnal hydration. New Phytol 208:750–762CrossRefPubMedGoogle Scholar
  3. Aranda I, Gil L, Pardos J (1996) Seasonal water relations of three broadleaved species (Fagus sylvatica L., Quercus petraea (Mattuschka) Liebl. and Quercus pyrenaica Willd.) in a mixed stand in the centre of the Iberian Peninsula. For Ecol Manag 84:219–229CrossRefGoogle Scholar
  4. Barták M, Trnková K, Hansen ES (2015) Effect of dehydration on spectral reflectance and photosynthetic efficiency in Umbilicaria arctica and U. hyperborea. Biol Plant 59:357–365CrossRefGoogle Scholar
  5. Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405CrossRefPubMedGoogle Scholar
  6. Bartlett MK, Zhang Y, Kreidler N, Sun S, Ardy R, Cao K, Sack L (2014) Global analysis of plasticity in turgor loss point, a key drought tolerance trait. Ecol Lett 17:1580–1590CrossRefPubMedGoogle Scholar
  7. Baruffo L, Tretiach M (2008) Seasonal variation of F o, F m, and F v/F m in an epiphytic population of the lichen Punctelia subrudecta (Nyl.) Krog. Lichenologist 39:555–565CrossRefGoogle Scholar
  8. Beckett RP (1995) Some aspects of the water relations of lichens from habitats of contrasting water status studied using thermocouple psychrometry. Ann Bot 76:211–217CrossRefGoogle Scholar
  9. Beckett RP (1996) Some aspects of the water relations of the lichen Parmotrema tinctorum measured using thermocouple psychrometry. Lichenologist 28:257–266Google Scholar
  10. Bidussi M, Gauslaa Y, Solhaug KA (2013) Prolonging the hydration and active metabolism from light periods into nights substantially enhances lichen growth. Planta 237:1359–1366CrossRefPubMedGoogle Scholar
  11. Binks O, Meir P, Rowland L, da Costa ACL, Vasconcelos SS, de Oliveira AAR, Ferreira L, Christoffersen B, Nardini A, Mencuccini M (2016) Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytol 211:477–488CrossRefPubMedPubMedCentralGoogle Scholar
  12. Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504CrossRefPubMedGoogle Scholar
  13. Candotto Carniel F, Gerdol M, Montagner A, Banchi E, De Moro G, Manfrin C, Muggia L, Pallavicini A, Tretiach M (2016) New features of desiccation tolerance in the lichen photobiont Trebouxia gelatinosa are revealed by a transcriptomic approach. Plant Mol Biol 91:319–339CrossRefGoogle Scholar
  14. Casolo V, Tomasella M, De Col V, Braidot E, Savi T, Nardini A (2015) Water relations of an invasive halophyte (Spartina patens): osmoregulation and ionic effects on xylem hydraulics. Funct Plant Biol 42:264–273Google Scholar
  15. Centeno DC, Hell AF, Braga MR, del Campo EM, Casano LM (2016) Contrasting strategies used by lichen microalgae to cope with desiccation–rehydration stress revealed by metabolite profiling and cell wall analysis. Environ Microbiol 18:1546–1560CrossRefPubMedGoogle Scholar
  16. Cosgrove DJ (1981) Analysis of the dynamic and steady-state responses of growth rate and turgor pressure to changes in cell parameters. Plant Physiol 68:1439–1446CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326CrossRefPubMedGoogle Scholar
  18. Coxson DS (1991) Impendance measurement of thallus moisture content in lichens. Lichenologist 23:74–84CrossRefGoogle Scholar
  19. Ding Y, Zhang Y, Zheng QS, Tyree MT (2014) Pressure–volume curves: revisiting the impact of negative turgor during cell collapse by literature review and simulations of cell micromechanics. New Phytol 203:378–387CrossRefPubMedGoogle Scholar
  20. Domaschke S, Vivas M, Sancho LG, Printzen C (2013) Ecophysiology and genetic structure of polar versus temperate populations of the lichen Cetraria aculeata. Oecologia 173:699–709CrossRefPubMedGoogle Scholar
  21. Dudley SA, Lechowicz MJ (1987) Losses of polyol through leaching in subarctic lichens. Plant Physiol 83:813–815CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fanjul L, Rosher PH (1984) Effects of water stress on internal water relations of apple leaves. Physiol Plant 46:109–114Google Scholar
  23. Gasulla F, de Nova PG, 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
  24. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  25. Green TGA, Lange OL, Cowan IR (1994) Ecophysiology of lichen photosynthesis: the role of water status and thallus diffusion resistances. Cryptogam Bot 4:166–178Google Scholar
  26. Gupta AS, Berkowitz GA (1987) Osmotic adjustment, symplast volume, and nonstomatally mediated water stress inhibition of photosynthesis in wheat. Plant Physiol 85:1040–1047CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hájek J, Barták M, Dubová J (2006) Inhibition of photosynthetic processes in foliose lichens induced by temperature and osmotic stress. Biol Plant 50:624–634CrossRefGoogle Scholar
  28. Honegger R (1993) Developmental biology of lichens. New Phytol 125:659–677CrossRefGoogle Scholar
  29. Honegger R (2006) Water relations in lichens. In: Gadd G, Watkinson SC, Dyer PS (eds) Fungi in the environment. Cambridge University Press, Cambridge, pp 185–200Google Scholar
  30. Jensen M, Chakir S, Feige GB (1999) Osmotic and atmospheric dehydration effects in the lichens Hypogymnia physoides, Lobaria pulmonaria and Peltigera aphthosa: an in vivo study of the chlorophyll fluorescence induction. Photosynthetica 37:393–404CrossRefGoogle Scholar
  31. Jonsson Čabrajić AV, Lidén M, Lundmark T, Ottosson-Löfvenius M, Palmqvist K (2010) Modelling hydration and photosystem II activation in relation to in situ rain and humidity patterns: a tool to compare performance of rare and generalist epiphytic lichens. Plant Cell Environ 33:840–850Google Scholar
  32. Jonsson AV, Moen J, Palmqvist K (2008) Predicting lichen hydration using biophysical models. Oecologia 156:259–273CrossRefPubMedGoogle Scholar
  33. Kaiser WM (1982) Correlation between changes in photosynthetic activity and changes in total protoplast volume in leaf tissue from hygro-, meso- and xerophytes under osmotic stress. Planta 154:538–545CrossRefPubMedGoogle Scholar
  34. Kappen L, Sommerkorn M, Schroeter B (1995) Carbon acquisition and water relations of lichens in polar regions—potentials and limitations. Lichenologist 27:531–545Google Scholar
  35. Kershaw KA, Macfarlane JD (1980) Physiological–environmental interactions in lichens. New Phytol 84:687–702CrossRefGoogle Scholar
  36. 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
  37. Kosugi M, Shizuma R, Moriyama Y, Koike H, Fukunaga Y, Takeuchi A, Uesugi K, Suzuki Y, Imura S, Kudoh S, Miyazawa A, Kashino Y, Satoh K (2014) Ideal osmotic spaces for chlorobionts or cyanobionts are differentially realized by lichenized fungi. Plant Physiol 166:337–348CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334CrossRefGoogle Scholar
  39. 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 102:3141–3146CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lajos K, Mayr S, Buchner O, Blaas K, Holzinger A (2016) A new microscopic method to analyse desiccation-induced volume changes in aeroterrestrial green algae. J Microsc 263:192–199CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lange OL, Green TGA, Ziegler H (1988) Water status related photosynthesis and carbon isotope discrimination in species of the lichen genus Pseudocyphellaria with green or blue-green photobionts and in photosymbiodemes. Oecologia 75:494–501CrossRefPubMedGoogle Scholar
  42. Lange OL, Pfanz H, Kilian E, Meyer A (1990) Effect of low water potential on photosynthesis in intact lichens and their liberated algal components. Planta 182:467–472CrossRefPubMedGoogle Scholar
  43. Lange OL, Büdel B, Heber U, Meyer A, Zellner H, Green TGA (1993) Temperate rain forest lichens in New Zealand: high thallus water content can severely limit photosynthetic CO2 exchange. Oecologia 95:303–313CrossRefPubMedGoogle Scholar
  44. Larcher W (2003) Water Relations. In: Larcher W (ed) Physiological plant ecology—ecophysiology and stress. Springer, Berlin, pp 231–286CrossRefGoogle Scholar
  45. Larson DW (1981) Differential wetting in some lichens and mosses: the role of morphology. Bryologist 84:1–15CrossRefGoogle Scholar
  46. Lenz TI, Wright IJ, Westoby M (2006) Interrelations among pressure–volume curve traits across species and water availability gradients. Physiol Plant 127:423–433CrossRefGoogle Scholar
  47. Lidén M, Jonsson Čabrajič AV, Ottoson-Löfvenius M, Palmqvist K, Lundmark T (2010) Species-specific activation time-lags can explain habitat restrictions in hydrophilic lichens. Plant Cell Environ 33:851–862PubMedGoogle Scholar
  48. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059CrossRefPubMedPubMedCentralGoogle Scholar
  49. McEvoy M, Gauslaa Y, Solhaug KA (2007) 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 175:271–282CrossRefPubMedGoogle Scholar
  50. Nardini A, Salleo S, Trifilò P, Lo Gullo MA (2003) Water relations and hydraulic characteristics of three woody species co-occurring in the same habitat. Ann For Sci 60:297–305CrossRefGoogle Scholar
  51. Nardini A, Marchetto A, Tretiach M (2013) Water relation parameters of six Peltigera species correlate with their habitat preferences. Fungal Ecol 6:397–407CrossRefGoogle Scholar
  52. Nash TH, Lange OL (1988) Responses of lichens to salinity: concentration and time-course relationships and variability among Californian species. New Phytol 109:361–367CrossRefGoogle Scholar
  53. Nash TH, Reiner A, Demmig-Adams B, Kilian E, Kaiser WM, Lange OL (1990) The effect of atmospheric desiccation and osmotic water stress on photosynthesis and dark respiration of lichens. New Phytol 116:269–276CrossRefGoogle Scholar
  54. Oliver MJ, Bewley JD (1997) Desiccation-tolerance of plant tissues: a mechanistic overview. Hortic Rev 18:171–217Google Scholar
  55. Pellegrini E, Bertuzzi S, Candotto Carniel F, Lorenzini G, Nali C, Tretiach M (2014) Ozone tolerance in lichens: a possible explanation from biochemical to physiological level using Flavoparmelia caperata as test organism. J Plant Physiol 171:1514–1523CrossRefPubMedGoogle Scholar
  56. Piccotto M, Bidussi M, Tretiach M (2011) Effects of the urban environmental conditions on the chlorophyll a fluorescence emission in transplants of three ecologically distinct lichens. Env Exp Bot 73:102–107CrossRefGoogle Scholar
  57. Proctor MCF (2010) Recovery rates of chlorophyll-fluorescence parameters in desiccation tolerant plants: fitted logistic curves as a versatile and robust source of comparative data. Plant Growth Regul 62:233–240CrossRefGoogle Scholar
  58. Proctor MCF, Tuba Z (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytol 156:327–349CrossRefGoogle Scholar
  59. Rundel PW (1982) The role of morphology in the water relations of desert lichens. J Hattori Bot Lab 53:315–320Google Scholar
  60. Saito T, Terashima I (2004) Reversible decreases in the bulk elastic modulus of mature leaves of deciduous Quercus species subjected to two drought treatments. Plant Cell Environ 27:863–875CrossRefGoogle Scholar
  61. Sancho LG, de la Torre R, Horneck G, Ascaso C, de los Rios A, Pintado A, Werzchos J, Schuster M (2007) Lichens survive in space: results from the 2005 LICHENS experiment. Astrobiology 7:443–454CrossRefPubMedGoogle Scholar
  62. Savi T, Marin M, Luglio J, Petruzzellis F, Mayr S, Nardini A (2016) Leaf hydraulic vulnerability protects stem functionality under drought stress in Salvia officinalis. Funct Plant Biol 43:370–379CrossRefGoogle Scholar
  63. Scheidegger C, Schroeter B, Frey B (1995) Structural and functional processes during water vapour uptake and desiccation in selected lichens with green algal photobionts. Planta 197:399–409CrossRefGoogle Scholar
  64. Schlensog M, Green TGA, Schroeter B (2013) Life form and water source interact to determine active time and environment in cryptogams: an example from the maritime Antarctic. Oecologia 173:59–72CrossRefPubMedGoogle Scholar
  65. Schulte PJ (1992) The units of currency for plant water status. Plant Cell Environ 15:7–10CrossRefGoogle Scholar
  66. Smith D, Molesworth S (1973) Lichen physiology XIII. Effects of rewetting dry lichens. New Phytol 72:525–533CrossRefGoogle Scholar
  67. Tretiach M, Pecchiari M (1995) Gas exchange rates and chlorophyll content of epi- and endolithic lichens from the Trieste Karst. New Phytol 130:585–592CrossRefGoogle Scholar
  68. Tretiach M, Crisafulli P, Virgilio D, Baruffo L, Jensen M (2003) Seasonal variation of photoinhibition in an epiphytic population of the lichen Parmelia sulcata Taylor. Bibl Lichenol 86:313–327Google Scholar
  69. Tretiach M, Adamo P, Bargagli R, Baruffo L, Carletti L, Crisafulli P, Giordano S, Modenesi P, Orlando S, Pittao E (2007) Lichen and moss bags as monitoring devices in urban areas. Part I: influence of exposure on sample vitality. Environ Pollut 146:380–391CrossRefPubMedGoogle Scholar
  70. Tretiach M, Bertuzzi S, Salvadori O (2010) Chlorophyll a fluorescence as a practical tool for checking the effects of biocide treatments on endolithic lichens. Int Biodeterior Biodegrad 64:452–460CrossRefGoogle Scholar
  71. Tretiach M, Pavanetto S, Pittao E, Sanità di Toppi L, Piccotto M (2012) Water availability modifies tolerance to photo-oxidative pollutants in transplants of the lichen Flavoparmelia caperata. Oecologia 168:589–599CrossRefPubMedGoogle Scholar
  72. Tretiach M, Bertuzzi S, Candotto Carniel F, Virgilio D (2013) Seasonal acclimation in the epiphytic lichen Parmelia sulcata is influenced by change in photobiont population density. Oecologia 173:649–663CrossRefPubMedGoogle Scholar
  73. Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:266–282CrossRefGoogle Scholar
  74. Váczi P, Barták M (2006) Photosynthesis of lichen symbiotic alga Trebouxia erici as affected by irradiance and osmotic stress. Biol Plant 50:257–264CrossRefGoogle Scholar
  75. Vráblíková H, McEvoy M, Solhaug KA, Barták M, Gauslaa Y (2006) Annual variation in photoacclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. J Photochem Photobiol B Biol 83:151–162CrossRefGoogle Scholar
  76. Wu L, Lan S, Zhang D, Hu C (2013) Functional reactivation of photosystem II in lichen soil crusts after long-term desiccation. Plant Soil 369:177–186CrossRefGoogle Scholar
  77. Yamamoto Y, Kinoshita Y, Yoshimura I (2002) Photobiont culturing. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring. Springer, Berlin, pp 34–42Google Scholar
  78. Zhang L, Li Y, Liu J (2016) Complete inactivation of photosynthetic activity during desiccation and rapid recovery by rehydration in the aerial microalga Trentepohlia jolithus. Plant Biol 18:1058–1061CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Life SciencesUniversity of TriesteTriesteItaly

Personalised recommendations