Skip to main content

Halotolerance in Lichens: Symbiotic Coalition Against Salt Stress

  • Chapter
  • First Online:
Ecophysiology and Responses of Plants under Salt Stress

Abstract

Lichens are among the most conspicuous and ubiquitous symbiosis on this planet. They are highly adapted to terrestrial habitats of all climatic zones including the most hostile environments on Earth, such as high altitudes in the Himalayas or the cold deserts of Antarctica. Among the extreme habitats are the littoral (or intertidal) zones of coasts. In this chapter, we present an overview of the current knowledge about the halotolerance mechanisms in lichens. Halotolerant organisms generally accumulate osmotically active solutes to cope with increasing external salinity. In intertidal lichens, mannitol could play an important role in osmoregulation. Epilichenic bacterial colonies may be also involved in limiting lichen nutrient imbalance by producing osmoprotective compounds and storing high ionic concentrations. In addition, the comparison with related inland species suggests that morphological adaptations could also be involved in adaptation to increased salt levels. Maritime species often have strongly conglutinated hyphae and small or no intercellular spaces in their thalli. So far, little genetic information exists about the genes involved in halotolerance and their regulation. Comparison of forthcoming genomic information from lichen fungi with those of other halotolerant fungi will soon help to change the picture and reveal genetic adaptations to saline environments.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adhikary SP (2003) Heat shock proteins in the terrestrial epilithic cyanobacterium Tolypothrix byssoidea. Biol Plant 47:125–128

    CAS  Google Scholar 

  • Ahmadjian V (1993a) The lichen symbiosis. Wiley, New York

    Google Scholar 

  • Ahmadjian V (1993b) The lichen photobiont – what can it tell us about lichen systematic. Bryologist 96:310–313

    Google Scholar 

  • Ahmadjian V (1995) Lichens are more important than you think. BioScience 45:123–124

    Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    PubMed  CAS  Google Scholar 

  • Al-Waibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ 23:139–150

    Google Scholar 

  • An SY, Xiao T, Yokota A (2008) Schumannella luteola gen. nov., sp. nov., a novel genus of the family Microbacteriaceae. J Gen Appl Microbiol 54:253–258

    PubMed  CAS  Google Scholar 

  • An SY, Xiao T, Yokota A (2009) Leifsonia lichenia sp. nov., isolated from lichen in Japan. J Gen Appl Microbiol 55:339–343

    PubMed  CAS  Google Scholar 

  • Andrawis A, Kahn V (1985) Inactivation of mushroom tyrosinase by hydrogen peroxide. Phytochemistry 24:397–405

    CAS  Google Scholar 

  • Arup U (1995) Littoral species of Caloplaca in North America: a summary and key. Bryologist 98:129–140

    Google Scholar 

  • Aubert S, Juge C, Boisson AM, Gout E, Bligny R (2007) Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans in high mountain environments. Planta 226:1287–1297

    PubMed  CAS  Google Scholar 

  • Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microb 77:1309–1314

    CAS  Google Scholar 

  • Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, Irthlingborough

    Google Scholar 

  • Beckett RP, Minibayeva FV (2007) Rapid breakdown of exogenous extracellular hydrogen peroxide by lichens. Physiol Plant 129:588–596

    CAS  Google Scholar 

  • Beckett RP, Minibayeva FV, Vylegzhanina NV, Tolpysheva T (2003) High rates of extracellular superoxide reduction by lichens in the Suborder Peltigerineae correlate with indices of high metabolic activity. Plant Cell Environ 26:1827–1837

    CAS  Google Scholar 

  • Beckett RP, Kranner I, Minibayeva FV (2008) Stress physiology and the symbiosis. In: Nash TH III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 134–151

    Google Scholar 

  • Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Bioch Biophys Acta – Biomembranes 1758:994–1003

    Google Scholar 

  • Bienert GP, Møller ALB, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    PubMed  CAS  Google Scholar 

  • Billi D, Potts M (2002) Life and death of dried prokaryotes. Res Microbiol 153:7–12

    PubMed  CAS  Google Scholar 

  • Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Øvreås L (2011) Microbial metacommunities in the lichen-rock habitat. Environ Microbiol Rep 3:434–442

    Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    PubMed  CAS  Google Scholar 

  • Brodo IM, Sloan NA (2004) Lichen zonation on coastal rocks in Gwaii Haanas National Park Reserve, Haida Gwaii (Queen Charlotte Islands), British Columbia. Can Field-Naturalist 117:405–424

    Google Scholar 

  • Büdel B (2011) Cyanobacteria: habitats and species. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance, ecological studies 215. Springer, Berlin, pp 11–21

    Google Scholar 

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

    CAS  Google Scholar 

  • Canh DS, Horák J, Kotyk A, Ríhová L (1975) Transport of acyclic polyols in Saccharomyces cerevisiae. Folia Microbiol 20:320–325

    CAS  Google Scholar 

  • Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495

    PubMed  CAS  Google Scholar 

  • Cardinale M, Vieira de Castro J Jr, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of alphaproteobacteria. FEMS Microbiol Ecol 66:63–71

    PubMed  CAS  Google Scholar 

  • Cardinale M, Grube M, Berg G (2011) Frondihabitans cladoniiphilus sp. nov., an actinobacterium of the family microbacteriaceae isolated from lichen, and emended description of the genus Frondihabitans. Int J Sys Evol Microbiol 61:3033–3038

    CAS  Google Scholar 

  • Cardinale M, Grube M, Castro JV Jr, Müller H, Berg G (2012a) Bacterial taxa associated with the lung lichen Lobaria pulmonaria are differentially shaped by geography and habitat. FEMS Microbiol Lett 329:111–115

    PubMed  CAS  Google Scholar 

  • Cardinale M, Steinova J, Rabensteiner J, Berg G, Grube M (2012b) Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 4:23–28

    Google Scholar 

  • Cheenpracha S, Vidor NB, Yoshida WY, Davies J, Chang LC (2010) Coumabiocins A-F, aminocoumarins from an organic extract of Streptomyces sp. L-4-4. J Nat Prod 73:880–884

    PubMed  CAS  Google Scholar 

  • Chou TS, Chao YY, Kao CH (2012) Involvement of hydrogen peroxide in heat shock- and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. J Plant Physiol 169:478–486

    PubMed  CAS  Google Scholar 

  • Coba de la Peña T, Redondo FJ, Manrique E, Lucas MM, Pueyo JJ (2010) Nitrogen fixation persists under conditions of salt stress in transgenic Medicago trunculata plants expressing a cyanobacterial flavodoxin. Plant Biotechnol J 8:954–965

    PubMed  Google Scholar 

  • Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175

    CAS  Google Scholar 

  • Cortés-Rojo C, Estrada-Villagómez M, Calderón-Cortés E, Clemente-Guerrero M, Mejía-Zepeda R, Boldogh I, Saavedra-Molina A (2011) Electron transport chain dysfunction by H2O2 is linked to increased reactive oxygen species production and iron mobilization by lipoperoxidation: Studies using Saccharomyces cerevisiae mitochondria. J Bioenerg Biomemb:135–147

    Google Scholar 

  • Csonka LN (1989) Physiological and genetic responses of Bacteria to osmotic stress. Microbiol Rev 53:121–147

    PubMed  CAS  Google Scholar 

  • D’Antonio C, Haubensak K (2005) Variation in biotic crusts, shrubs, rainfall and resistance to cheatgrass invasion in the Great Basin. Ecological Society of America 2005, Montréal

    Google Scholar 

  • da Silva Graça MMC (2004) Salt stress response of the extremely halotolerant yeast Candida halophila (syn versatilis) CBS 4019 – Biochemical and physiological studies. Universidade do Minho – Escola de Ciências, Braga

    Google Scholar 

  • Dadheech N (2010) Desiccation tolerance in cyanobacteria. Afr J Microbiol Res 4:1584–1593

    CAS  Google Scholar 

  • Davies J, Wang H, Taylor T, Warabi K, Huang XH, Andersen RJ (2005) Uncialamycin, a new enediyne antibiotic. Org Lett 7:5233–5236

    PubMed  CAS  Google Scholar 

  • De Bary A (1879) Die Erscheinung der Symbiose. Karl J Trübner, Strasbourg

    Google Scholar 

  • Delmail D, Labrousse P (2012) Plant ageing, a counteracting agent to xenobiotic stress. In: Nagata T (ed) Senescence. InTech Publishers, Rijeka, pp 89–106

    Google Scholar 

  • Delmail D, Buzier R, Simon S, Hourdin P, Botineau M, Labrousse P (2011) HPLC method for the analysis of α-tocopherol from Myriophyllum alterniflorum. Chem Nat Compd 47:679–680

    CAS  Google Scholar 

  • dos Santos Freire MBG, Lira-Cadete L, de Farias ARB, Kuklinsky-Sobral J, dos Santos KCF (2010) Isolation of Atriplex nummularia-associated halotolerant bacteria and bioprospecting by nitrogen fixing bacteria in saline-sodic soil. 19th World Congress of Soil Science – Soil Solutions for a Changing World, Brisbane

    Google Scholar 

  • Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 106:119–133

    CAS  Google Scholar 

  • Eisenman HC, Casadevall A (2012) Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol 93:931–940

    PubMed  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    PubMed  CAS  Google Scholar 

  • Fabian M, Skultety L, Brunel C, Palmer G (2001) The cyanide stimulated dissociation of chloride from the catalytic center of oxidized oxidase. Biochemistry 40:6061–6069

    PubMed  CAS  Google Scholar 

  • Feller G, Bussy O, Houssier C, Gerday C (1996) Structural and functional aspects of chloride binding to Alteromonas haloplanctis alpha-amylase. J Biol Chem 271:23836–23841

    PubMed  CAS  Google Scholar 

  • Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637

    PubMed  CAS  Google Scholar 

  • Fernández E, Reyes A, Hidalgo ME, Quilhot W (1998) Photoprotector capacity of lichen metabolites assessed through the inhibition of the 8-methoxypsoralen photobinding to protein. J Photochem Photobiol B 42:195–201

    PubMed  Google Scholar 

  • Fletcher A (1973a) The ecology of marine (littoral) lichens on some rocky shores of Anglesey. Lichenologist 5:368–400

    Google Scholar 

  • Fletcher A (1973b) The ecology of marine (supralittoral) lichens on some rocky shores of Anglesey. Lichenologist 5:401–422

    Google Scholar 

  • Fletcher A (1976) Nutritional aspects of marine and maritime lichen ecology. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, New York, pp 359–384

    Google Scholar 

  • Fornazier RF, Ferreira RR, Vitória AP, Molina SMG, Lea PJ, Azevedo RA (2002) Effects of cadmium on antioxidant enzyme activities in sugar cane. Biol Plant 45:91–97

    CAS  Google Scholar 

  • Frechilla S, Lasa B, Ibarretxe L, Lamsfus C, Aparicio Trejo P (2001) Pea response to saline stress is affected by the source of nitrogen nutrition (ammonium or nitrate). Plant Growth Regul 35:171–179

    CAS  Google Scholar 

  • Friedl T, Büdel B (2008) Photobionts. In: Nash TH III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 9–26

    Google Scholar 

  • Fulda S, Hagemann M (1995) Salt treatment induces accumulation of flavodoxin in the cyanobacterium Synechocystis sp. PCC6803. J Plant Physiol 146:520–536

    CAS  Google Scholar 

  • García-Molina F, Hiner ANP, Fenoll LG, Rodríguez-Lopez JN, García-Ruiz PA, García-Cánovas F, Tudela J (2005) Mushroom tyrosinase: catalase activity, inhibition, and suicide inactivation. J Agric Food Chem 53:3702–3709

    PubMed  Google Scholar 

  • Gasulla F, Gomez De Nova P, Esteban-Carrasco A, Zapat 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 231:195–208

    PubMed  CAS  Google Scholar 

  • Gauslaa Y, Solhaug KA (1999) High-light damage in air-dry thalli of the old forest lichen Lobaria pulmonaria – interactions of irradiance, exposure duration and high temperature. J Exp Bot 50:697–705

    CAS  Google Scholar 

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

    Google Scholar 

  • Gauslaa Y, Solhaug KA (2004) Photoinhibition in lichens depends on cortical characteristics and hydration. Lichenologist 36:133–143

    Google Scholar 

  • Gauslaa Y, Ustvedt EM (2003) Is parietin a UV-B or a blue-light screening pigment in the lichen Xanthoria parietina? Photoch Photobio Sci 2:424–432

    CAS  Google Scholar 

  • Gilbert O (2000) Lichens. Harper Collins, London

    Google Scholar 

  • Gilbert O (2001) The lichen flora of coastal saline lagoons in England. Lichenologist 33:409–417

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

    CAS  Google Scholar 

  • González I, Ayuso-Sacido A, Anderson A, Genilloud O (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 54:401–415

    PubMed  Google Scholar 

  • Gopalakrishnan M, Kumar AS, Mody K, Jha B (2006) Biosurfactant production by marine bacteria. Nat Acad Sci Lett 29:95–101

    CAS  Google Scholar 

  • Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255

    PubMed  CAS  Google Scholar 

  • Green TGA, Sancho LG, Pintado A (2011) Ecophysiology of Desiccation/Rehydration Cycles in Mosses and Lichens. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance, ecological studies 215. Springer, Berlin, pp 89–120

    Google Scholar 

  • Green TGA, Brabyn L, Beard C, Sancho LG (2012) Extremely low lichen growth rates in Taylor Valley, Dry Valleys, continental Antarctica. Polar Biol 35:535–541

    Google Scholar 

  • Grube M (2010) Die hard: lichens. In: Seckbach J, Grube M (eds) Symbioses and stress: joint ventures in biology. Springer, Dordrecht, pp 509–523

    Google Scholar 

  • Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85

    Google Scholar 

  • Grube M, Blaha J (2005) Halotolerance and lichen symbioses. In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Dordrecht, pp 471–488

    Google Scholar 

  • Grube M, Muggia L (2010) Identifying algal symbionts in lichen symbioses. In: Nimis PL, Lebbe RV (eds) Tools for identifying biodiversity: progress and problems. Proceedings of the International Congress (Museum National d’Histoire Naturelle), Paris, pp 295–299

    Google Scholar 

  • Grube M, Cardinale M, Vieira de Castro J Jr, Müller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. Intern Soc Microbial Ecol 3:1105–1115

    Google Scholar 

  • Gueidan C, Thüs H, Pérez-Ortega S (2011) Phylogenetic position of the brown algae-associated lichenized fungus Verrucaria tavaresiae (Verrucariaceae). Bryologist 114:563–569

    Google Scholar 

  • Hagemann M, Effmert U, Kerstan T, Schoor A, Erdmann N (2001) Biochemical characterization of glucosylglycerol-phosphate synthase of Synechocystis sp. strain PCC 6803: comparison of crude, purified, and recombinant enzymes. Curr Microbiol 43:278–283

    PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 51:463–499

    CAS  Google Scholar 

  • Hawksworth DL (2000) Freshwater and marine lichen-forming fungi. Fungal Div 5:1–7

    Google Scholar 

  • Healey FP (1973) Characteristics of phosphorus deficiency in Anabaena. J Phycol 9:383–394

    CAS  Google Scholar 

  • Heber U, Bilger W, Turk R, Lange OL (2010) Photoprotection of reaction centres in photosynthetic organisms: mechanisms of thermal energy dissipation in dessicated thalli of the lichen Lobaria pulmonaria. New Phytol 185:459–470

    PubMed  CAS  Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara coralline: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    PubMed  CAS  Google Scholar 

  • Hidalgo ME, Fernández E, Ponce M, Rubio C, Quilhot W (2002) Photophysical, photochemical, and thermodynamic properties of shikimic acid derivatives: calycin and rhizocarpic acid (lichens). J Photochem Photobiol B 66:213–217

    PubMed  CAS  Google Scholar 

  • Hill DJ, Ahmadjian V (1972) Relationship between carbohydrate movement and the symbiosis in lichens with green algae. Planta 103:267–277

    CAS  Google Scholar 

  • Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2011) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161

    PubMed  Google Scholar 

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

    Google Scholar 

  • Honegger R (2001) The symbiotic phenotype of lichen-forming ascomyces. In: Hock B (ed) The mycota; IX fungal associations. Springer, Berlin, pp 165–188

    Google Scholar 

  • Incharoensakdi A, Takabe T (1988) Determination of intracellular chloride ion concentration in a halotolerant cyanobacterium Aphanothece halophytica. Plant Cell Physiol 29:1073–1075

    CAS  Google Scholar 

  • Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274

    PubMed  CAS  Google Scholar 

  • Johnson AM (2007) Food abundance and energetic carrying capacity for wintering waterfowl on the Great Salt Lake wetlands. Oregon State University, Corvallis

    Google Scholar 

  • Keddy PA (2007) Positive interactions: mutualism, commensalism, and symbiosis. In: Keddy PA (ed) Plant and vegetation: origins, processes, consequences. Cambridge University Press, Cambridge, pp 336–402

    Google Scholar 

  • Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330

    PubMed  CAS  Google Scholar 

  • Killham K, Firestone MK (1984) Salt stress control of intracellular solutes in Streptomycetes indigenous to saline soils. Appl Environ Microb 47:301–306

    CAS  Google Scholar 

  • Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562

    PubMed  Google Scholar 

  • Kneip C, Lockhart P, Voß C, Maier UG (2007) Nitrogen fixation in eukaryotes – New models for symbiosis. BMC Evol Biol 7:55

    PubMed  Google Scholar 

  • Koag MC, Fenton RD, Wilkens S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol 131:309–316

    PubMed  CAS  Google Scholar 

  • Kogej T, Wheeler MH, Lanišnik Rižner T, Gunde-Cimerman N (2004) Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiol Lett 232:203–209

    PubMed  CAS  Google Scholar 

  • Kohlmeyer J, Kohlmeyer E (1979) Marine mycology. The higher fungi. Academic Press, New York

    Google Scholar 

  • Kohlmeyer J, Volkmann-Kohlmeyer B (1988) Halographis (Opegraphales), a new endolithic lichenoid from corals and snails. Can J Bot 66:1138–1141

    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

    PubMed  CAS  Google Scholar 

  • Kotlova ER, Sinyutina NF (2005) Changes in the content of individual lipid classes of a lichen Peltigera aphthosa during dehydration and subsequent rehydration. Russ J Plant Physiol 52:35–42

    CAS  Google Scholar 

  • Kranner I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 154:451–460

    CAS  Google Scholar 

  • Kranner I, Lutzoni F (1999) Evolutionary consequences of transition to a lichen symbiotic state and physiological adaptation to oxidative damage associated with poikilohydry. In: Lerner HR (ed) Plant response to environmental stress: from phytohormones to genome reorganization. Dekker, New York, pp 591–628

    Google Scholar 

  • Kranner I, Zorn M, Turk B, Wornik S, Beckett RP, Batic F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytologist 160:167–176

    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. P Natl Acad Sci USA 102:3141–3146

    CAS  Google Scholar 

  • Kranner I, Beckett R, Hochman A, Nash TH III (2008) Desiccation tolerance in lichen: a review. Bryologist 111:576–593

    Google Scholar 

  • Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246

    PubMed  CAS  Google Scholar 

  • Künzler K, Eichenberger W (1997) Betaine lipids and zwitterionic phospholipids in plants and fungi. Phytochemistry 46:883–892

    PubMed  Google Scholar 

  • Lagadic L, Caquet T, Amiard JC (1997) Biomarqueurs en écotoxicologie : principes et définitions. In: Lagadic L, Caquet T, Amiard JC (eds) Biomarqueurs en écotoxicologie. Masson, Paris, pp. 1–10

    Google Scholar 

  • Lages F, Lucas C (1995) Characterization of a glycerol/H+ symport in the halotolerant yeast Pichia sorbitophila. Yeast 11:111–119

    PubMed  CAS  Google Scholar 

  • Lages F, Lucas C (1997) Contribution to the characterization of glycerol active uptake in Saccharomyces cerevisiae. Bioch Biophys Acta – Bioenergetics 1322:8–18

    CAS  Google Scholar 

  • Lages F, Silva-Graça M, Lucas C (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 145:2577–2585

    PubMed  CAS  Google Scholar 

  • Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142:11–19

    PubMed  Google Scholar 

  • Lewitus AJ, Caron DA (1990) Relative effects of nitrogen or phosphorus depletion and light intensity on the pigmentation, chemical composition, and volume of Pyrenomonas salina (Cryptophyceae). Mar Ecol Prog Ser 61:171–181

    CAS  Google Scholar 

  • Li X, Weinman SA (2002) Chloride channels and hepatocellular function: prospects for molecular identification. Annu Rev Physiol 64:609–633

    PubMed  CAS  Google Scholar 

  • Li Y, Trush MA, Yager JD (1994) DNA damage caused by reactive oxygen species originating from a copper-dependent oxidation of the 2-hydroxy catechol of estradiol. Carcinogenesis 15:1421–1427

    PubMed  CAS  Google Scholar 

  • Li B, Xie CH, Yokota A (2007) Nocardioides exalbidus sp. nov., a novel actinomycete isolated from lichen in Izu-Oshima Island, Japan. Actinomycetologica 21:22–26

    Google Scholar 

  • Liao DI, Basarab GS, Gatenby AA, Valent B, Jordan DB (2001) Structures of trihydroxynaphthalene reductase-fungicide complexes: implications for structure-based design and catalysis. Structure 9:19–27

    PubMed  CAS  Google Scholar 

  • Liba CM, Ferrara FIS, Manfio GP, Fantinatti-Garboggini F, Albuquerque RC, Pavan C, Ramos PL, Moreira-Filho CA, Barbosa HR (2006) Nitrogen-fixing chemo-organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J Appl Microbiol 101:1076–1086

    PubMed  CAS  Google Scholar 

  • Lucas C, da Costa M, van Uden N (1990) Osmoregulatory active sodium-glycerol co-transport in the halotolerant yeast Debaryomyces hansenii. Yeast 6:187–191

    CAS  Google Scholar 

  • Lüttge U (2011) Cyanobacteria: multiple stresses, desiccation-tolerant photosynthesis and di-nitrogen fixation. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance, ecological studies 215. Springer, Berlin, pp 23–43

    Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    PubMed  CAS  Google Scholar 

  • Makkonen S, Hurri RSK, Hyvärinen M (2007) Differential responses of lichen symbionts to enhanced nitrogen and phosphorus availability: an experiment with Cladina stellaris. Ann Bot 99:877–884

    PubMed  CAS  Google Scholar 

  • Mao X, Olman V, Stuart R, Paulsen IT, Palenik B, Xu Y (2010) Computational prediction of the osmoregulation network in Synechococcus sp. WH8102. BMC Genomics 11:291

    Google Scholar 

  • Maphangwa KW, Musil CF, Raitt L, Zedda L (2012) Differential interception and evaporation of fog, dew and water vapour and elemental accumulation by lichens explain their relative abundance in a coastal desert. J Arid Environ 82:71–80

    Google Scholar 

  • Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83

    PubMed  CAS  Google Scholar 

  • Matias D, Zurbriggen MD, Tognetti VB, Fillat MF, Hajirezae MR, Valle EM, Carrillo N (2008) Combating stress with flavodoxin: a promising route for crop improvement. Trends Biotechnol 26:531–537

    Google Scholar 

  • Matos P, Cardoso-Vilhena J, Figueira R, Sousa AJ (2011) Effects of salinity stress on cellular location of elements and photosynthesis in Ramalina canariensis Steiner. Lichenologist 43:155–164

    Google Scholar 

  • Matthes-Sears U, Nash TH III, Larson DW (1987) Salt loading does not control CO2 exchange in Ramalina menziesii Tayl. New Phytol 106:59–69

    CAS  Google Scholar 

  • Miyasaka NRS, Thuler DS, Floh EIS, Handro W, Toledo MBD, Gagioti SM, Barbosa HR (2003) During stationary phase, Beijerinckia derxii shows nitrogenase activity concomitant with the release and accumulation of nitrogenated substances. Microbiol Res 158:309–315

    PubMed  CAS  Google Scholar 

  • Moe RL (1997) Verrucaria tavaresiae sp. nov., a marine lichen with a brown algal photobiont. Bull Californ Lichen Soc 4:7–11

    Google Scholar 

  • Morbach S, Krämer R (2002) Body shaping under water stress: osmosensing and osmoregulation of solute transport in Bacteria. ChemBioChem 3:384–397

    PubMed  CAS  Google Scholar 

  • Morrison M, Schonbaum GR (1976) Peroxidase-catalyzed halogenation. Annu Rev Biochem 45:861–888

    PubMed  CAS  Google Scholar 

  • Motohashi K, Takagi M, Yamamura H, Hayakawa M, Shin-Ya K (2010) A new angucycline and a new butenolide isolated from lichen-derived Streptomyces spp. J Antibiot 63:545–548

    PubMed  CAS  Google Scholar 

  • Muggia L, Zellnig G, Rabensteiner J, Grube M (2010) Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51:149–160

    Google Scholar 

  • Nash TH III, Lange OL (1988) Responses of lichens to salinity: concentration and time-course relationships and variability among Californian species. New Phytol 109:361–367

    Google Scholar 

  • Okanenko A, Tarand N, Kosyk O (2011) Sulfurcontaining plant lipids. АВЕГА, Kiev

    Google Scholar 

  • Øvstedal DO, Tønsberg T, Elvebakk A (2009) The lichen flora of Svalbard. Sommerfeltia 33:1–393

    Google Scholar 

  • Ozenda P, Clauzade G (1970) Les lichens: étude biologique et flore illustrée. Masson, Paris

    Google Scholar 

  • Paramesha S, Vijay R, Bekal M, Kumari S, Pushpalatha KC (2011) A study on lipid peroxidation and total antioxidant status in diabetes with and without hypertension. Res J Pharm Biol Chem Sci 2:329–334

    Google Scholar 

  • Parent C, Capelli N, Dat J (2008) Formes réactives de l’oxygène, stress et mort cellulaire chez les plantes. CR Biol 331:255–261

    CAS  Google Scholar 

  • Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant Soil 239:123–132

    CAS  Google Scholar 

  • Potts M, Slaughter SM, Hunneke FU, Garst JF, Helm RF (2005) Desiccation tolerance of Prokaryotes: application of principles to human cells. Integr Comp Biol 45:800–809

    PubMed  CAS  Google Scholar 

  • Rai V, Tiwari SP, Rai AK (2001) Effect of NaCl on nitrogen fixation of unadapted and NaCl-adapted Azolla pinnataAnabaena azollae. Aquat Bot 71:109–117

    CAS  Google Scholar 

  • Raikou V, Protopapa E, Kefala V (2011) Photo-protection from marine organisms. Rev Clin Pharmacol Pharmacokinet 25:131–136

    CAS  Google Scholar 

  • Rancan F, Rosan S, Boehm K, Fernández E, Hidalgo ME, Quihot W, Rubio C, Boehm F, Piazena H, Oltmanns U (2002) Protection against UVB irradiation by natural filters extracted from lichens. J Photochem Photobiol B 68:133–139

    PubMed  CAS  Google Scholar 

  • Rodríguez-Navarro A (2000) Potassium transport in fungi and plants. Bioch Biophys Acta 1469:1–30

    Google Scholar 

  • Rorat T (2006) Plant dehydrins – tissue location, structure and function. Cell Mol Biol Lett 11:536–556

    PubMed  CAS  Google Scholar 

  • Roullier C, Chollet-Krugler M, Van de Weghe P, Lohezic-Le Devehat F, Boustie J (2010) A novel aryl-hydrazide from the marine lichen Lichina pygmaea: isolation, synthesis of derivatives, and cytotoxicity assays. Bioorg Med Chem Lett 20:4582–4586

    PubMed  CAS  Google Scholar 

  • Roullier C, Chollet-Krugler M, Pferschy-Wenzig EM, Maillard A, Rechberger GN, Legouin-Gargadennec B, Bauer R, Boustie J (2011) Characterization and identification of mycosporine-like compounds in cyanolichens. Isolation of mycosporine hydroxyglutamicol from Nephroma laevigatum Ach. Phytochemistry 72:1348–1357

    PubMed  CAS  Google Scholar 

  • Rundel PW (1974) Water relations and morphological variation in Ramalina menziesii Tayl. Bryologist 77:23–32

    Google Scholar 

  • Sanders WB, Moe RL, Ascaso C (2004) The intertidal marine lichen formed by the pyrenomycete fungus Verrucaria tavaresiae (Ascomycotina) and the brown alga Petroderma maculiforme (Phaeophyceae): thallus organization and symbiont interaction. Am J Bot 91:511–522

    PubMed  Google Scholar 

  • Schaich KM (2005) Lipid oxidation: theoretical aspects. In: Shahidi F (ed) Bailey’s industrial oil and fat products. Wiley, Hoboken, pp 269–355

    Google Scholar 

  • Schneider T, Schmid E, De Castro Jr JV, Cardinale M, Eberl L, Grube M, Berg G, Riedel K (2011) Structure and function of the symbiosis partners of the lung lichen (Lobaria pulmonaria L. Hoffm.) analyzed by metaproteomics. Proteomics 11:2752–2756

    PubMed  CAS  Google Scholar 

  • Schweikardt T, Olivares C, Solano F, Jaenicke E, García-Borrón JC, Decker H (2007) A three-dimensional model of mammalian tyrosinase active site accounting for loss of function mutations. Pigment Cell Res 20:394–401

    PubMed  CAS  Google Scholar 

  • Sekmen AH, Turkan I, Tanyolac ZO, Ozfidan C, Dinc A (2012) Different antioxidant defense responses to salt stress during germination and vegetative stages of endemic halophyte Gypsophila oblanceolata Bark. Environ Exp Bot 77:63–76

    CAS  Google Scholar 

  • Serrano R, Mulet JM, Rios G, Marquez JA, de Larriona IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft MRR, Montesinos C (1999) A glimpse of the mechanism of ion homeostasis during salt stress. J Exp Bot 50:1023–1036

    CAS  Google Scholar 

  • Sibaja-Cordero JA, Troncoso JS (2011) Upper and lower limits of rocky shore organisms at different spatial scales and wave exposure (Islas CÍES, NW Spain). Thalassas 27:81–100

    Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 127:27–58

    Google Scholar 

  • Smith VR, Gremmen NJM (2001) Photosynthesis in a sub-Antarctic shore-zone lichen. New Phytol 149:291–299

    Google Scholar 

  • Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (2009) The lichens of Great Britain and Ireland. The British Lichen Society, London

    Google Scholar 

  • Solhaug KA, Gauslaa Y (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108:412–418

    Google Scholar 

  • Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV-Induction of sun-screening pigments in lichens. New Phytol 158:91–100

    CAS  Google Scholar 

  • Soriani FM, Kress MR, Fagundes de Gouvêa P, Malavazi I, Savoldi M, Gallmetzer A, Strauss J, Goldman MH, Goldman GH (2009) Functional characterization of the Aspergillus nidulans methionine sulfoxide reductases (msrA and msrB). Fungal Genet Biol 46:410–417

    PubMed  CAS  Google Scholar 

  • Takahagi T, Yamamoto Y, Kinoshita Y, Takeshita S, Yamada T (2002) Inhibitory effects of sodium chloride on induction of tissue cultures of lichens of Ramalina species. Plant Biotechnol 19:53–55

    CAS  Google Scholar 

  • Thompson JE, Legge RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105:317–344

    CAS  Google Scholar 

  • Thuler DS, Floh EIS, Handro W, Barbosa HR (2003) Beijerinckia derxii releases plant growth regulators and amino acids in synthetic media independent of nitrogenase activity. J Appl Microbiol 95:799–806

    Google Scholar 

  • Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ (1999) A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181:6469–6477

    PubMed  CAS  Google Scholar 

  • Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) CRC handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 39–92

    Google Scholar 

  • Van Zyl PJ, Prior BA, Kilian SG (1991) Regulation of glycerol metabolism in Zygosaccharomyces rouxii in response to osmotic stress. Appl Microbiol Biot 36:369–374

    Google Scholar 

  • Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544

    PubMed  CAS  Google Scholar 

  • Williams DE, Davies J, Patrick BO, Bottriell H, Tarling T, Roberge M, Andersen RJ (2008) Cladoniamides A-G, tryptophan-derived alkaloids produced in culture by Streptomyces uncialis. Org Lett 10:3501–3504

    PubMed  CAS  Google Scholar 

  • Yocum CF (2008) The calcium and chloride requirements of the O2 evolving complex. Coord Chem Rev 252:296–305

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Université de Rennes 1, the Université Européenne de Bretagne, the Ministère de l’Enseignement supérieur et de la Recherche, the Institut National des Sciences Appliquées de Rennes and the UMR CNRS 6226 SCR. The authors sincerely thank Dr. Frédéric Barrière and Dr. Marie-Laurence Abasq-Paofai for technical support, Dr. Françoise Lohézic-Le Dévéhat and Friardi Ismed for providing SEM photography, and Dr. Béatrice Legouin-Gargadennec for valuable discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Delmail .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Delmail, D. et al. (2013). Halotolerance in Lichens: Symbiotic Coalition Against Salt Stress. In: Ahmad, P., Azooz, M., Prasad, M. (eds) Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4747-4_4

Download citation

Publish with us

Policies and ethics