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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adhikary SP (2003) Heat shock proteins in the terrestrial epilithic cyanobacterium Tolypothrix byssoidea. Biol Plant 47:125–128
Ahmadjian V (1993a) The lichen symbiosis. Wiley, New York
Ahmadjian V (1993b) The lichen photobiont – what can it tell us about lichen systematic. Bryologist 96:310–313
Ahmadjian V (1995) Lichens are more important than you think. BioScience 45:123–124
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
Al-Waibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ 23:139–150
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
An SY, Xiao T, Yokota A (2009) Leifsonia lichenia sp. nov., isolated from lichen in Japan. J Gen Appl Microbiol 55:339–343
Andrawis A, Kahn V (1985) Inactivation of mushroom tyrosinase by hydrogen peroxide. Phytochemistry 24:397–405
Arup U (1995) Littoral species of Caloplaca in North America: a summary and key. Bryologist 98:129–140
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
Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microb 77:1309–1314
Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, Irthlingborough
Beckett RP, Minibayeva FV (2007) Rapid breakdown of exogenous extracellular hydrogen peroxide by lichens. Physiol Plant 129:588–596
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
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
Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Bioch Biophys Acta – Biomembranes 1758:994–1003
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
Billi D, Potts M (2002) Life and death of dried prokaryotes. Res Microbiol 153:7–12
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
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111
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
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
Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136
Canh DS, Horák J, Kotyk A, Ríhová L (1975) Transport of acyclic polyols in Saccharomyces cerevisiae. Folia Microbiol 20:320–325
Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495
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
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
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
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
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
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
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
Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175
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
Csonka LN (1989) Physiological and genetic responses of Bacteria to osmotic stress. Microbiol Rev 53:121–147
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
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
Dadheech N (2010) Desiccation tolerance in cyanobacteria. Afr J Microbiol Res 4:1584–1593
Davies J, Wang H, Taylor T, Warabi K, Huang XH, Andersen RJ (2005) Uncialamycin, a new enediyne antibiotic. Org Lett 7:5233–5236
De Bary A (1879) Die Erscheinung der Symbiose. Karl J Trübner, Strasbourg
Delmail D, Labrousse P (2012) Plant ageing, a counteracting agent to xenobiotic stress. In: Nagata T (ed) Senescence. InTech Publishers, Rijeka, pp 89–106
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
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
Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 106:119–133
Eisenman HC, Casadevall A (2012) Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol 93:931–940
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280
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
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
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
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
Fletcher A (1973a) The ecology of marine (littoral) lichens on some rocky shores of Anglesey. Lichenologist 5:368–400
Fletcher A (1973b) The ecology of marine (supralittoral) lichens on some rocky shores of Anglesey. Lichenologist 5:401–422
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
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
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
Friedl T, Büdel B (2008) Photobionts. In: Nash TH III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 9–26
Fulda S, Hagemann M (1995) Salt treatment induces accumulation of flavodoxin in the cyanobacterium Synechocystis sp. PCC6803. J Plant Physiol 146:520–536
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
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
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
Gauslaa Y, Solhaug KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126:462–471
Gauslaa Y, Solhaug KA (2004) Photoinhibition in lichens depends on cortical characteristics and hydration. Lichenologist 36:133–143
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
Gilbert O (2000) Lichens. Harper Collins, London
Gilbert O (2001) The lichen flora of coastal saline lagoons in England. Lichenologist 33:409–417
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930
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
Gopalakrishnan M, Kumar AS, Mody K, Jha B (2006) Biosurfactant production by marine bacteria. Nat Acad Sci Lett 29:95–101
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
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
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
Grube M (2010) Die hard: lichens. In: Seckbach J, Grube M (eds) Symbioses and stress: joint ventures in biology. Springer, Dordrecht, pp 509–523
Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85
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
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
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
Gueidan C, Thüs H, Pérez-Ortega S (2011) Phylogenetic position of the brown algae-associated lichenized fungus Verrucaria tavaresiae (Verrucariaceae). Bryologist 114:563–569
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
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
Hawksworth DL (2000) Freshwater and marine lichen-forming fungi. Fungal Div 5:1–7
Healey FP (1973) Characteristics of phosphorus deficiency in Anabaena. J Phycol 9:383–394
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
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
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
Hill DJ, Ahmadjian V (1972) Relationship between carbohydrate movement and the symbiosis in lichens with green algae. Planta 103:267–277
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
Honegger R (1998) The lichen symbiosis – what is so spectacular about it? Lichenologist 30:193–212
Honegger R (2001) The symbiotic phenotype of lichen-forming ascomyces. In: Hock B (ed) The mycota; IX fungal associations. Springer, Berlin, pp 165–188
Incharoensakdi A, Takabe T (1988) Determination of intracellular chloride ion concentration in a halotolerant cyanobacterium Aphanothece halophytica. Plant Cell Physiol 29:1073–1075
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
Johnson AM (2007) Food abundance and energetic carrying capacity for wintering waterfowl on the Great Salt Lake wetlands. Oregon State University, Corvallis
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
Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330
Killham K, Firestone MK (1984) Salt stress control of intracellular solutes in Streptomycetes indigenous to saline soils. Appl Environ Microb 47:301–306
Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562
Kneip C, Lockhart P, Voß C, Maier UG (2007) Nitrogen fixation in eukaryotes – New models for symbiosis. BMC Evol Biol 7:55
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
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
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology. The higher fungi. Academic Press, New York
Kohlmeyer J, Volkmann-Kohlmeyer B (1988) Halographis (Opegraphales), a new endolithic lichenoid from corals and snails. Can J Bot 66:1138–1141
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
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
Kranner I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 154:451–460
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
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
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
Kranner I, Beckett R, Hochman A, Nash TH III (2008) Desiccation tolerance in lichen: a review. Bryologist 111:576–593
Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246
Künzler K, Eichenberger W (1997) Betaine lipids and zwitterionic phospholipids in plants and fungi. Phytochemistry 46:883–892
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
Lages F, Lucas C (1995) Characterization of a glycerol/H+ symport in the halotolerant yeast Pichia sorbitophila. Yeast 11:111–119
Lages F, Lucas C (1997) Contribution to the characterization of glycerol active uptake in Saccharomyces cerevisiae. Bioch Biophys Acta – Bioenergetics 1322:8–18
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
Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142:11–19
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
Li X, Weinman SA (2002) Chloride channels and hepatocellular function: prospects for molecular identification. Annu Rev Physiol 64:609–633
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
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
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
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
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
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
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
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
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
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
Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83
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
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
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
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
Moe RL (1997) Verrucaria tavaresiae sp. nov., a marine lichen with a brown algal photobiont. Bull Californ Lichen Soc 4:7–11
Morbach S, Krämer R (2002) Body shaping under water stress: osmosensing and osmoregulation of solute transport in Bacteria. ChemBioChem 3:384–397
Morrison M, Schonbaum GR (1976) Peroxidase-catalyzed halogenation. Annu Rev Biochem 45:861–888
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
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
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
Okanenko A, Tarand N, Kosyk O (2011) Sulfurcontaining plant lipids. АВЕГА, Kiev
Øvstedal DO, Tønsberg T, Elvebakk A (2009) The lichen flora of Svalbard. Sommerfeltia 33:1–393
Ozenda P, Clauzade G (1970) Les lichens: étude biologique et flore illustrée. Masson, Paris
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
Parent C, Capelli N, Dat J (2008) Formes réactives de l’oxygène, stress et mort cellulaire chez les plantes. CR Biol 331:255–261
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
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
Rai V, Tiwari SP, Rai AK (2001) Effect of NaCl on nitrogen fixation of unadapted and NaCl-adapted Azolla pinnata–Anabaena azollae. Aquat Bot 71:109–117
Raikou V, Protopapa E, Kefala V (2011) Photo-protection from marine organisms. Rev Clin Pharmacol Pharmacokinet 25:131–136
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
Rodríguez-Navarro A (2000) Potassium transport in fungi and plants. Bioch Biophys Acta 1469:1–30
Rorat T (2006) Plant dehydrins – tissue location, structure and function. Cell Mol Biol Lett 11:536–556
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
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
Rundel PW (1974) Water relations and morphological variation in Ramalina menziesii Tayl. Bryologist 77:23–32
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
Schaich KM (2005) Lipid oxidation: theoretical aspects. In: Shahidi F (ed) Bailey’s industrial oil and fat products. Wiley, Hoboken, pp 269–355
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
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
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
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
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
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 127:27–58
Smith VR, Gremmen NJM (2001) Photosynthesis in a sub-Antarctic shore-zone lichen. New Phytol 149:291–299
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
Solhaug KA, Gauslaa Y (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108:412–418
Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV-Induction of sun-screening pigments in lichens. New Phytol 158:91–100
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
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
Thompson JE, Legge RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105:317–344
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
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
Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) CRC handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 39–92
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
Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544
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
Yocum CF (2008) The calcium and chloride requirements of the O2 evolving complex. Coord Chem Rev 252:296–305
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-1-4614-4747-4_4
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-4746-7
Online ISBN: 978-1-4614-4747-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)