Desiccation stress and tolerance in green algae: Consequences for ultrastructure, physiological, and molecular mechanisms

Frontiers in Plant Science

Volumn 4, Issue AUG, 2013, Pages

  Holzinger, Andreas ^a   Karsten, Ulf ^b  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Aeroterrestrial algae; Cell wall; Dehydration; Desiccation tolerance; Osmolyte; Phylogeny of green algae; Soluble carbohydrates; Turgor pressure

Indexed keywords

EID: 84900866870     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00327     Document Type: Review

References (177)

1. Abele, D. (2002). The radical life-giver. Nature 420, 27. doi: 10.1038/420027a
2. Affenzeller, M. J., Darehshouri, A., Andosch, A., Lütz, C., and Lütz-Meindl, U. (2009). Salt stress induced cell death in the unicellular green alga Micrasterias denticulata. J. Exp. Bot. 60, 939-954. doi: 10.1093/jxb/ ern348
3. Agrawal, S. C. (2009). Factors affecting spore germination in algae - review. Folia Microbiol. 54, 273-302. doi: 10.1007/s12223-009-0047-0
4. Agrawal, S. C. (2012). Factors controlling induction of reproduction in green algae - review: the text. Folia Microbiol. 57, 387-407. doi: 10.1007/s12223-012-0147-0
5. Agrawal, S. C., and Singh, V. (2000). Vegetative survival, akinete formation and germination in three blue-green algae and one green alga in relation to light intensity, temperature, heat shock and UV exposure. Folia Microbiol. 45, 439-446. doi: 10.1007/BF028 17618
6. Aigner, S., Remias, D., Karsten, U., and Holzinger, A. (2013). Unusual phenolic compounds contribute to the ecophysiological performance in the purple-colored green alga Zygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high-alpine habitat. J. Phy-col. 49, 648-660. doi: 10.1111/jpy. 12075
7. Allakhverdiev, S. I., Kreslavski, V. D., Klimov, V. V., Los, D. A., Carpen-tier, R., and Mohanty, P. (2008). Heat stress: an overview of molecular responses in photosynthesis. Pho-tosynth. Res. 98, 541-550. doi: 10.1007/s11120-008-9331-0
8. Allakhverdiev, S. I., and Murata, N. (2004). Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Syne-chocystis sp. PCC 6803. Biochim. Biophys. Acta 1657, 23-32. doi: 10.1016/j.bbabio.2004.03.003
9. Alpert, P. (2006). Constraints of tolerance: why are desiccation tolerant organisms so small or rare? J. Exp. Bot. 209, 1575-1584. doi: 10.1242/jeb.02179
10. Austin, J. R. II, Frost, E., Vidi, P. A., Kessler, F., and Staehelin, L.A. (2006). Plastoglobules are lipoprotein sub-compartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18, 1693-1703. doi: 10.1105/tpc.105.039859
11. Azúa-Bustos, A., González-Silva, C., Salas, L., Palma, R. E., and Vicuña, R. (2010). A novel subaerial Dunaliella species growing on cave spiderwebs in the Atacama Desert. Extremophiles 14, 443-452. doi: 10.1007/s00792-010-0322-7
12. Becker, B. (2013). Snowball earth and the split of Streptophyta and Chlorophyta. Trends Plant Sci. 18, 180-183. doi: 10.1016/j.tplants.2012. 09.010
13. Becker, B., and Marin, B. (2009). Streptophyte algae and the origin of embryophytes. Ann. Bot. 103, 999-1004. doi: 10.1093/aob/mcp044
14. Beel, B., Müller, N., Kottke, T., and Mittag, M. (2012). News about cryp-tochrome photoreceptors in algae. Plant Signal. Behav. 8, e22870 doi: 10.4161/psb.22870
15. Bell, R. A. (1993). Cryptoendolithic algae of hot semiarid land and deserts. J. Phycol. 29, 133-139. doi: 10.1111/j.0022-3646.1993.00133.x
16. Belnap, J., and Lange, O. L. (2001). Biological Soil Crusts: Structure, Function and Management. Berlin: Springer.
17. Benson, K. R. (2002). The study of vertical zonation on rocky inter-tidal shores - a historic perspective. Integr. Comp. Biol. 42, 776-779. doi: 10.1093/icb/42.4.776
18. Bertsch, A. (1966). CO2Gaswechsel der Grünalge Apatococcus lobatus. Planta 70, 46-72. doi: 10.1007/ BF00539910
19. Bewley, J. D. (1979). Physiological aspects of desiccation tolerance. Annu. Rev. Plant Physiol. 30, 195-238. doi: 10.1146/annurev.pp.30.060179. 001211
20. Bischof, K., Peralta, G., Kräbs, G., Van den Poll, W. H., Perez-Llorens, J. L., and Breeman, A. M. (2002). Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J. Exp. Bot. 379, 2411-2421. doi: 10.1093/jxb/erf091
21. Bisson, M. A., and Kirst, G. O. (1995). Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 82, 461-471. doi: 10.1007/BF01131597
22. Borowitzka, M. A., Huisman, J. M., and Osborn, A. (1991). Culture of the astaxanthin-producing green alga Haematococcus pluvialis 1. Effects of nutrients on growth and cell type. J. Appl. Phycol. 3, 295-304. doi: 10.1007/BF00026091
23. Brito, J. C., Godinho, R., Martínez-Freiría, F., Pleguezuelos, J. M., Rebelo, H., Santos, X., et al. (2013). Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel. Biol. Rev. Camb. Philos. Soc. doi: 10.1111/brv.12049 [Epub ahead of print].
24. Brown, A. D., and Simpson, J. R. (1972). Water relations of sugar-tolerant yeasts: the role of intracel-lular polyols. J. Gen. Microbiol. 72, 589-591. doi: 10.1099/00221287-72-3-589
25. Büdel, B. (2005). "Microorganisms of biological crusts on soil surface," in Microorganisms in Soils: Roles in Genesis and Functions, Vol. 3, Soil Biology, eds F. Buscot and A. Varma (Heidelberg: Springer), 307-323.
26. Büdel, B. (2011). "Eukaryotic algae," in Plant Desiccation Tolerance, Vol. 215, Ecological Studies, eds U. Lüttge, E. Beck, and D. Bartels (Heidelberg: Springer), 45-63.
27. Buitink, J., Hemmings, M. A., and Hoekstra, F. A. (2002). "Is there a roll for oligosaccharides in seed longevity? An assessment of intracellular glass stability," in Desiccation and Survival in Plants: Drying without Dying, eds M. Black and H. W. Pritchards (Wallingford, Oxon: CABI Publishing), 293-318.
28. Cardon, Z. G., Gray, D. W., and Lewis, L. A. (2008). The green algal underground: evolutionary secrets of desert cells. Bioscience 58, 114-122. doi: 10.1641/B580206
29. Castillo-Monroy, A. P., Maestre, F. T., Delgado-Baquerizo, M., and Gal-lardo, A. (2010). Biological soil crusts modulate nitrogen availability in semi-arid ecosystem: insights from a Mediterranean grassland. Plant Soil 333, 21-34. doi: 10.1007/s11104-009-0276-7
30. Coleman, A. W. (1983). "The role of resting spores and akinetes in chloro-phyte survival," in Survival Strategies of the Algae, ed. G. A. Fryxell (Cambridge: University Press), 1-21.
31. Cooper, K., and Farrant, J. M. (2002). Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J. Exp. Bot. 53, 1805-1813. doi: 10.1093/jxb/ erf028
32. Darehshouri, A., and Lütz-Meindl, U. (2010). H2O2 localization in the green alga Micrasterias after salt and osmotic stress by TEM-coupled electron energy loss spec-troscopy. Protoplasma 239, 49-56. doi: 10.1007/s00709-009-0081-4
33. Darienko, T., Friedl, T., and Pröschold, T. (2009). Desmochloris mollenhaueri - a new terrestrial ulvophycean alga from South-west African soils. (Molecular phylogeny and systemat-ics of terrestrial Ulvophyceae I). Algol. Stud. 129, 25-40. doi: 10.1127/1864-1318/2009/0129-0025
34. Darienko, T., Gustavs, L., Mudimu, O., Menendez, C. R., Schumann, R., Karsten, U., et al. (2010). Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxio-phyceae, Chlorophyta). Eur. J. Phy-col. 45, 79-95. doi: 10.1080/ 09670260903362820
35. Davis, J. S. (1972). Survival records in the algae, and the survival role of certain algal pigments, fats and mucilaginous substances. Biologist 54, 52-93.
36. De Winder, B., Matthijs, H. C. P., and Mur, L. R. (1990). The effect of dehydration and ion stress on carbon dioxide fixation in drought-tolerant phototrophic micro-organisms. FEMS Microbiol. Ecol. 74, 33-38. doi: 10.1111/j.1574-6941.1990.tb01669.x
37. Dilks, T. J. K., and Proctor, M. C. F. (1979). Respiration and water content in bryophytes. New Phy-tol. 82, 97-114. doi: 10.1111/j.1469-8137.1979.tb07564.x
38. Domozych, D. S., Roberts, R., Danyow, C., Flitter, R., Smith, B., and Providence, K. (2003). Plasmol-ysis, Hechtian strand formation, and localized membrane-wall adhesions in the desmid, Closterium acerosum (Chlorophyta). J. Phycol. 39, 1194-1206. doi: 10.1111/j.0022-3646.2003.03-033.x
39. Elbert, W., Weber, B., Burrows, S., Steinkamp, J., Büdel, B., Andreae, M. O., et al. (2012). Contribution of cryptogrammic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5, 459-462. doi: 10.1038/ngeo1486
40. Elster, J., Degma, P., Kovacik, L., Valen-tova, L., Sramkova, K., and Pereira, B. (2008). Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from Antarctic, Arctic and Slovakia. Biologia 63, 839-847. doi: 10.2478/s11756-008-0111-2
41. Ettl, H., and Gärtner, G. (1995). Syllabus der Boden, Luftund Flechtenalgen. Stuttgart: Gustav Fischer.
42. Evans, J. H. (1958). The survival of freshwater algae during dry periods. Part I: an investigation of the algae of five small ponds. J. Ecol. 46, 149-168. doi: 10.2307/2256910
43. Evans, R. D., and Johansen, J. R. (1999). Microbiotic crusts and ecosystem processes. Crit. Rev. Plant Sci. 18,183-225. doi: 10.1016/S0735-2689(99)00384-6
44. Feige, G. B., and Kremer, B. P. (1980). Unusual carbohydrate pattern in Trentepohlia species. Phytochemistry 19, 1844-1845. doi: 10.1016/S0031-9422(00)83826-1
45. Fernández-Marín, B., Kranner, I., Sebastián, M. S., Artetxe, U., Laza, J. M., Vilas, J. L., et al. (2013). Evidence for the absence of enzymatic reactions in the glassy state. A case study of xanthophyll cycle pigments in the desiccation-tolerant moss Syntrichia ruralis. J. Exp. Bot. 64, 3033-3043. doi: 10.1093/jxb/ert145
46. Flechtner, V. R. (2007). "North American desert microbiotic soil crust communities: diversity despite challenge," in Algae and Cyanobacte-ria in Extreme Environments, ed. J. Seckbach (Berlin: Springer), 537-551. doi: 10.1007/978-1-4020-6112-7_29
47. Friedl, T. (1997). The evolution of the green algae. Plant Syst. Evol. 11, 87-101. doi: 10.1007/978-3-7091-6542-3_4
48. Friedl, T., and Rybalka, N. (2012). Systematics of the green algae: a brief introduction to the current status. Progr. Bot. 73, 259-280. doi: 10.1007/978-3-642-22746-2_10
49. Friedmann, E. I., Lipkin, Y., and Ocampo-Paus, R. (1967). Desert algae of the Negev (Israel). Phycologia 7, 185-200. doi: 10.2216/i0031-8884-6-4-185.1
50. Fritsch, F. E., and Haines, F. M. (1923). Moisture relation of terrestrial algae. II. The changes during exposure to drought and treatment with hypertonic solutions. Ann. Bot. 37, 683-728.
51. Gaff, D. F., and Oliver, M. (2013). The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct. Plant Biol. 40, 315-328. doi: 10.1071/ FP12321
52. Gao, S., Shen, S., Wang, G., Niu, J., Lin, A., and Pan, G. (2012). PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol. 52, 885-893. doi: 10.1093/pcp/ pcr038
53. Gasulla, F., de Nova, P. G., Esteban-Carrasco, A., Zapata, J. M., Barreno, E., and Guéra, A. (2009). Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxaerici: alternative and classical protective mechanisms. Planta 231, 195-208. doi: 10.1007/s00425-009-1019-y
54. Gasulla, F., Jain, R., Barreno, E., Guéra, A., Balbuena, T. S., Thelen, J. J., et al. (2013a). The response of Aste-rochloris erici (Ahmadjian) Skaloud et Peksa to desiccation: a proteomic approach. Plant Cell Environ. doi: 10.1111/pce.12065 [Epub ahead of print].
55. Gasulla, F., Vom Dorp, K., Dom-brink, I., Zähringer, U., Gisch, N., Dörrmann, P., et al. (2013b). The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J. doi: 10.1111/tpj.12241 [Epub ahead of print].
56. Gechev, T. S., Dinakar, C., Benina, M., Toneva, V., and Bartels, D. (2013). Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol. Life Sci. 70, 689-709. doi: 10.1007/s00018-012-1155-6
57. Genkel, P. A., and Pronina, N. D. (1979). Ecology of Zygnema stellinum Vauch. during desiccation of a shallow body of water. Biol. Bull. Acad. Sci. 6, 504-509.
58. Gerotto, C., and Morosinotto, T. (2013). Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol. Plant. doi: 10.1111/ppl.12070 [Epub ahead of print].
59. Goyal, K., Walton, L. J., and Tunna-cliffe, A. (2005). LEA proteins prevent protein aggregation due to water stress. Biochem. J. 388, 151-157. doi: 10.1042/BJ20041931
60. Graham, L. E., Arancibia-Avila, P., Taylor, W. A., Strother, P. K., and Cook, M. E. (2012). Aeroterrestrial Coleochaete (Strep-tophyta, Coleochaetales) models early plant adaptation to land. Am. J. Bot. 99,130-144. doi: 10.3732/ajb.1100245
61. Gray, D. W., Lewis, L. A., and Cardon, Z. G. (2007). Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ. 30, 1240-1255. doi: 10.1111/j.1365-3040.2007.01704.x
62. Green, T. G. A., Nash T. H. III, and Lange, O. L. (2008). "Physiological ecology of carbon dioxide exchange," in Lichen Biology, ed. T. H. Nash III (Cambridge: University Press), 152-181.
63. Guarnieri, M. T., Nag, A., Smolinski, S. L., Darzins, A., Seibert, M., and Pienkos, P. T. (2011). Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and pro-teomic analyses in an unsequenced microalga. PLoS ONE 6:e25851. doi: 10.1371/journal.pone.0025851
64. Gustavs, L., Eggert, A., Michalik, D., and Karsten, U. (2010). Physiological and biochemical responses of aeroterrestrial green algae (Treboux-iophyceae) to osmotic and matric stress. Protoplasma 243, 3-14. doi: 10.1007/s00709-009-0060-9
65. Gustavs, L., Görs, M., and Karsten, U. (2011). Polyols as chemotaxonomic markers to differentiate between aeroterrestrial green algae (Treboux-iophyceae, Chlorophyta). J. Phycol. 47, 533-537. doi: 10.1111/j.1529-8817.2011.00979.x
66. Gustavs, L., Schumann, R., Eggert, A., and Karsten, U. (2009). In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aquat. Microb. Ecol. 55, 95-104. doi: 10.3354/ame01291
67. Hall, J. D., Karol, K. G., McCourt, R. M., and Delwhice, C. F. (2008). Phylogeny of the conjugating green algae based on chloroplast and mitochondrial nucleotide sequence data. J. Phycol. 44, 467-477. doi: 10.1111/j.1529-8817.2008.00485.x
68. Halliwell, B. (1987). Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chem. Phys. Lipids 44, 327-340. doi: 10.1016/0009-3084(87)90056-9
69. Hanelt, D. (1998). Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar. Biol. 131, 361-369. doi: 10.1007/s002270050329
70. Haney, P. J., Badger, J. H., Buldak, G. L., Reich, C. I., Woese, C. R., and Olsen, G. J. (1999). Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococ-cus species. Proc. Natl. Acad. Sci. U.S.A. 96, 3578-3583. doi: 10.1073/pnas.96.7.3578
71. Häubner, N., Schumann, R., and Karsten, U. (2006). Aeroterrestrial algae growing in biofilms on facades - response to temperature and water stress. Microb. Ecol. 51, 285-293. doi: 10.1007/s00248-006-9016-1
72. Holzinger, A. (2009). "Desiccation tolerance in green algae: implications of physiological adaptation and structural requirements," in Algae, Nutrition, Pollution Control and Energy Sources, ed. K. N. Hagen (New York: Nova Science Publishers), 41-56.
73. Holzinger, A., Di Piazza, L., Lütz, C., and Roleda, M. Y. (2011). Sporo-genic and vegetative tissues of Saccharina latissima (Laminariales, Phaeophyceae) exhibit distinctive sensitivity to experimentally enhanced ultraviolet radiation: photosynthetically active radiation ratio. Phycol. Res. 59, 221-235. doi: 10.1111/j.1440-1835. 2011.00620.x
74. Holzinger, A., Karsten, U., Lütz, C., and Wiencke, C. (2006). Ultrastructure and photosynthesis in the supralit-toral green macroalga Prasiola crispa (Lightfoot) Kützing from Spitsbergen (Norway) under UV exposure. Phy-cologia 45, 168-177. doi: 10.2216/ 05-20.1
75. Holzinger, A., and Lütz, C. (2006). Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37, 190-207. doi: 10.1016/j.micron.2005.10.015
76. Holzinger, A., Lütz, C., and Karsten, U. (2011). Desiccation stress causes structural and ultra-structural alter ations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Strepto-phyta) isolated from an alpine soil crust. J. Phycol. 47, 591-602. doi: 10.1111/j.1529-8817. 2011.00980.x
77. Holzinger, A., Lütz, C., Karsten, U., and Wiencke, C. (2004). The effect of ultraviolet radiation on ultra-structure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Arctic waters. Plant Biol. 6, 568-577. doi: 10.1055/s-2004-821003
78. Holzinger, A., Roleda, M. Y., and Lütz, C. (2009). The vegetative arctic green alga Zygnema is insensitive to experimental UV exposure. Micron 40, 831-838. doi: 10.1016/j.micron.2009.06.008
79. Holzinger, A., Tschaikner, A., and Remias, D. (2010). Cytoarchitecture of the desiccation-tolerant green alga Zygogonium ericetorum. Protoplasma 243, 15-24. doi: 10.1007/s00709-009-0048-5
80. Honjoh, K., Matsumoto, H., Shimizu, H., Ooyama, K., Tanaka, K., Oda, Y., et al. (2000). Cryopro-tective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci. Biotechnol. Biochem. 64, 1656-1663. doi: 10.1271/bbb.64.1656
81. Hoppert, M., Reimer, R., Kemmling, A., Schröder, A., Günzl, B., and Heinken, T. (2004). Structure and reactivity of a biological soil crust from axeric sandy soil in central Europe. Geomicrobiol. J. 21, 183-191. doi: 10.1080/01490450490275433
82. Jacob, A., Wiencke, C., Lehmann, H., and Kirst, G. O. (1992). Physiology and ultrastructure in the green alga Prasiola crispa from Antarctica. Bot. Mar. 35, 297-303. doi: 10.1515/botm.1992.35.4.297
83. Jobson, R. W., and Qui, Y.-L. (2011). Amino acid compositional shifts during streptophyte transitions to terrestrial habitats. J. Mol. Evol. 72, 204-214. doi: 10.1007/s00239-010-9416-1
84. Kanervo, E., Mäenpää, P., and Aro, E.-M. (1993). D1 protein degradation and psbA transcript levels in Synechocystis PCC 6803 during photoinhibition in vivo. J. Plant Physiol. 142, 669-675. doi: 10.1016/S0176-1617(11)80900-4
85. Kaplan, F., Lewis, L. A., Herburger, K., and Holzinger, A. (2013). Osmotic stress in the arctic and antarctic green alga Zygnema sp. (Zygnematales, Streptophyta): effects on photosynthesis and ultrastruc-ture. Micron 44, 317-330. doi: 10.1016/j.micron.2012.08.004
86. Kaplan, F., Lewis, L. A., Wastian, J., and Holzinger, A. (2012). Plasmol-ysis effects and osmotic potential of two phylogenetically distinct alpine strains of Klebsormidium (Strepto-phyta). Protoplasma 249, 789-804. doi: 10.1007/s00709-011-0324-z
87. Kappen, L., Lange, O. L., Schulze, E. D., Evenari, M., and Buschbom, U. (1979). Ecophysiological investigations on lichens of the Negev desert. Flora 168, 85-108. doi: 10.1007/BF00751603
88. Karsten, U. (2012). "Seaweed acclimation to salinity and desiccation stress," in Seaweed cophysiology and Ecology, Vol. 219, Ecological Studies, eds C. Wiencke and K. Bischof (Berlin: Springer), 87-107.
89. Karsten, U., Barrow, K. D., Nixdorf, O., and King, R. J. (1996). The compatibility of unusual organic osmolytes from mangrove red algae with enzyme activity. Aust. J. Plant Physiol. 23, 577-582. doi: 10.1071/PP9960577
90. Karsten, U., and Holzinger, A. (2012). Light, temperature and desiccation effects on photosynthetic activity and drought-induced ultrastructural changes in the green alga Klebsormid-ium dissectum (Streptophyta) from a high alpine soil crust. Microb. Ecol. 63, 51-63. doi: 10.1007/s00248-011-9924-6
91. Karsten, U., Lütz, C., and Holzinger, A. (2010). Ecophysiological perfor mance of the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Strepto-phyta) isolated from an alpine soil crust with an emphasis on desiccation stress. J. Phycol. 4, 1187-1197. doi: 10.1111/j.1529-8817.2010.00921.x
92. Karsten, U., Schumann, R., and Mostaert, A. (2007). "Aeroterres-trial algae growing on man-made surfaces - what are the secrets of their ecological success?," in Algae and Cyanobacteria in Extreme Environments, ed. J. Seckbach (Berlin: Springer), 583-597.
93. Karsten, U., Wiencke, C., and Kirst, G. O. (1991). The effect of salinity changes upon the physiology of eulittoral green macroalgae from Antarctica and Southern Chile. II. Intracellular inorganic ions and organic compounds. J. Exp. Bot. 245, 1533-1539. doi: 10.1093/jxb/42. 12.1533
94. Kirst, G. O. (1990). Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 21-53. doi: 10.1146/annurev.pp.41. 060190.000321
95. Knowles, E. J., and Castenholz, R. W. (2008). Effect of exogenous extracellular polysaccharides on the desiccation and freezing tolerance of rock-inhabiting pho-totrophic microorganisms. FEMS Microbiol. Ecol. 66, 261-270. doi: 10.1111/j.1574-6941.2008.00568.x
96. Kosugi, M., Miyake, H., Yamakawa, H., Shibata, Y., Miyazawa, A., Sugimura, T., et al. (2013). Arabitol provided by lichenous fungi enhances ability to dissipate excess light energy in a symbiotic green alga under desiccation. Plant Cell Physiol. 54, 1316-1325. doi: 10.1093/pcp/pct079
97. Kranner, I., Beckett, R., Hochman, A., and Nash T. H. III, (2008). Desiccation-tolerance in lichens: a review. Bryologist 111, 576-593. doi: 10.1639/0007-2745-111.4.576
98. Kranner, I., and Birtic, F. (2005). A modulation role for antioxi-dants in desiccation tolerance. Integr. Comp. Biol. 45, 734-740. doi: 10.1093/icb/45.5.734
99. Kranner, I., Cram, W. J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., et al. (2005). Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc. Natl. Acad. Sci. U.S.A. 102, 3141-3146. doi: 10.1073/pnas.0407716102
100. Kranner, I., Zorn, M., Turk, B., Wornik, S., Beckett, R. P., and Batic, F. (2003). Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol. 160, 167-176. doi: 10.1046/j.1469-8137.2003. 00852.x
101. Lange, O. L., Bilger, W., Rimke, S., and Schreiber, U. (1989). Chlorophyll fluorescence of lichens containing green and blue-green algae during hydration by water vapor uptake and by addition of liquid water. Bot. Acta 102, 306-313.
102. Lange, O. L., Green, T. G. A., Melzer, B., Meyer, A., and Zellner, H. (2006). Water relations and CO2 exchange of the terrestrial lichen Teloschistes capensis in the Namib fog desert: measurements during two seasons in the field under controlled conditions. Flora 201, 268-280. doi: 10.1016/j.flora.2005.08.003
103. Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delchiche, C. F., et al. (2012). Phy-logeny and molecular evolution of green algae. Crit. Rev. Plant Sci. 31, 1-46. doi: 10.1080/07352689.2011. 615705
104. Lewis, L. A. (2007). "Chlorophyta on land: independent lineages of green eukaryotes from arid lands," in Algae and Cyanobacteria in extreme Environments, ed. J. Seckbach (Berlin: Springer), 571-582.
105. Lewis, L. A., and Lewis, P. O. (2005). Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Syst. Biol. 54, 936-947. doi: 10.1080/ 10635150500354852
106. Lewis, L.A., and McCourt, R.M. (2004). Green algae and the origin of land plants. Am. J. Bot. 91, 1535-1556. doi: 10.3732/ajb.91.10.1535
107. Lewis, L. A., and Trainor, F. R. (2012). Survival of Protosiphon botry-oides (Chlorophyceae, Chlorophyta) from a Connecticut soil dried for 43 years. Phycologia 51, 662-665. doi: 10.2216/11-108.1
108. Lunch, C. K., LaFountain, A. M., Thomas, S., Frank, H. A., Lewis, L. A., and Cardon, Z. G. (2013). The xanthophyll cycle and NPQ in diverse desert and aquatic green algae. Photosynth. Res. 115, 139-151. doi: 10.1007/s11120-013-9846-x
109. Lüttge, U. (2011). "Cyanobacteria: multiple stresses, desiccation-tolerant photosynthesis and di-nitorgen fixation," in Plant Desiccation Tolerance, Vol. 215, Ecological Studies, eds U. Lüttge, E. Beck, and D. Bartels (Heidelberg: Springer), 23-44.
110. Lüttge, U., and Büdel, B. (2010). Resurrection kinetics of photosynthesis in desiccation-tolerant terrestrial green algae (Chlorophyta) on tree bark. Plant Biol. 123, 437-444. doi: 10.1111/j.1438-8677.2009. 00249.x
111. McCourt, R. M., Delwiche, C. F., and Karol, K. G. (2004). Charophyte algae and land plant origins. Trends Ecol. Evol. 19, 661-666. doi: 10.1016/j.tree.2004. 09.013
112. McCourt, R. M., Karol, K. G., Bell, J., Helm-Bychowski, K. M., Grajewska, A., Wojciechowski, M. F., et al. (2000). Phylogeny of the conjugating green algae (Zygnemophyceae) based on rbcL sequences. J. Phycol. 36, 747-758. doi: 10.1046/j.1529-8817.2000.99106.x
113. Mikhailyuk, T. I., Sluiman, H. J., Massalski, A., Mudimu, O., Demchenko, E. M., Kondratyuk, S. Y., et al. (2008). New streptophyte green algae from terrestrial habitats and an assessment of the genus Interfilum (Klebsormid-iophyceae, Streptophyta). J. Phycol. 44, 1586-1603. doi: 10.1111/j.1529-8817.2008.00606.x
114. Moore, J. P., Le, N. T., Brandt, W. F., Dri-ouich, A., and Farrant, J. M. (2009). Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci. 14, 110-117. doi: 10.1016/j.tplants.2008.11.007
115. Morison, M. O., and Sheath, R. G. (1985). Responses to desiccation stress by Klebsormidium rivulare (Ulotrichales, Chlorophyta) from a Rhode Island stream. Phycologia 24, 129-145. doi: 10.2216/i0031-8884-24-2-129.1
116. Mulec, J., and Kosi, G. (2009). Lampenflora algae and methods of growth control. J. Cave Karst Stud. 71, 109-115.
117. Mulo, P., Sakurai, I., and Aro, E. M. (2012). Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim. Biophys. Acta 1817, 247-257. doi: 10.1016/j.bbabio.2011.04.011
118. Nagao, M., Matsui, K., and Uemura, M. (2008). Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ. 31, 872-885. doi: 10.1111/j.1365-3040.2008. 01804.x
119. Nagao, M., and Uemura, M. (2012). Sucrose phosphate phosphatase in the green alga Klebsormidium flac-cidum (Streptophyta) lacks an extensive C-terminal domain and differs from that of land plants. Planta 235, 851-861. doi: 10.1007/s00425-011-1550-5
120. Nelsen, M. P., Plata, E. R., Andrew, C. J., Lücking, R., and Lumbsch, H. T. (2011). Phylogenetic diversity of trentepohlian algae associated with lichen-forming fungi. J. Phycol. 47, 282-290. doi: 10.1111/j.1529-8817.2011.00962.x
121. Nienow, J. A. (1996). Ecology of sub-aerial algae. Nova Hedwig. Beih. 112, 537-552.
122. Niyogi, K. K. (1999). Photoprotec-tion revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359. doi: 10.1146/annurev.arplant. 50.1.333
123. Oliver, M. J., and Bewley, J. (1997). Desiccation tolerance of plant tissues: a mechanistic overview. Hortic. Rev. 18, 171-214.
124. Oliver, M. J., Cushman, J. C., and Koster, K. L. (2010)."Dehydration tolerance in plants," in Plant Stress Tolerance, Vol. 639, Methods in Molecular Biology, ed. R. Sunkar (NewYork: Springer), 3-24.
125. Oliver, M. J., Dowd, S. E., Zaragoza, J., Mauget, S. A., and Payton, P. R. (2004). The rehydration tran-scriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5:89. doi: 10.1186/1471-2164-5-89
126. Oliver, M. J., Jain, R., Balbuena, T. S., Agrawal, G., Gasulla, F., and The-len, J. J. (2011). Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochem-istry 72, 1273-1284. doi: 10.1016/j. phytochem.2010.10.020
127. Oliver, M. J., Tuba, Z., and Mish-ler, B. D. (2000). The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 151, 85-100. doi: 10.1023/A:1026550 808557
128. Ong, B., Lim, M., and Wee, Y. (1992). Effects of desiccation and illumination on photosynthesis and pigmentation of an edaphic population of Trentepohlia odorata (Chlorophyta). J. Phycol. 28, 768-772. doi: 10.1111/j.0022-3646.1992. 00768.x
129. Oren, A. (2007). "Diversity of organic osmotic compounds and osmotic adaptation in cyanobacteria and algae," in Algae and Cyanobacteria in Extreme Environments, ed. J. Seck-bach (Berlin: Springer), 639-655.
130. Palmqvist, K., and Sundberg, B. (2002). "Characterising photosynthesis and respiration in freshly isolated or cultured lichen photobionts," in Protocols in Lichenology, (Springer Lab Manuals), 152-181.
131. Pichrtová, M., Remias, D., Lewis, L. A., and Holzinger, A. (2013). Changes in phenolic compounds and cellular ultrastructure of arctic and Antarctic strains of Zygnema (Zygnematales, Streptophyta) after exposuretoexperimentally enhanced UV to PAR ratio. Microb. Ecol. 65, 68-83. doi: 10.1007/s00248-012-0096-9
132. Piercy, A. (1917). The structure and mode of life of a form of Hormid-ium flaccidum, A. Braun. Ann. Bot. 31, 513-537.
133. Potts, M. (1994). Desiccation tolerance in prokaryotes. Microbiol. Rev. 58, 755-805.
134. Potts, M. (2001). Desiccation tolerance: a simple process? Trends Microbiol. 9, 553-559. doi: 10.1016/S0966-842X(01)02231-4
135. Potts, M., Slaughter, S. M., Hunneke, F.-U., Garst, J. F., and Helm, R. F. (2005). Desiccation tolerance of prokaryotes: application of principles to human cells. Integr. Comp. Biol. 45, 800-809. doi: 10.1093/icb/45.5.800
136. Pressel, S., and Duckett, J. G. (2010). Cytological insights into the desiccation biology of a model system: moss protonema. New Phytol. 185, 944-963. doi: 10.1111/j.1469-8137.2009.03148.x
137. Pressel, S., Duckett, J. G., Ligrone, R., and Proctor, M. C. F. (2009). Effects of de-and rehydration in desiccation tolerant liverworts: a cytologi-cal and physiological study. Int. J. Plant Sci. 170, 182-199. doi: 10.1086/ 595285
138. Proctor, M. C. F. (2000). The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecol. 151, 41-49. doi: 10.1023/A: 1026517920852
139. Proctor, M. C. F., Ligrone, R., and Duckett, J. G. (2007). Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann. Bot. 99, 75-93. doi: 10.1093/aob/mcl246
140. Proctor, M. C. F., and Smirnoff, N. (2000). Rapid recovery of photosystems on rewetting desiccation tolerant mosses: chlorophyll fluorescence and inhibitor experiments. J. Exp. Bot. 51, 1695-1704. doi: 10.1093/jexbot/51.351.1695
141. Ratnakumar, S., and Tunnacliffe, A. (2006). Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast. FEMS Yeast Res. 6, 902-913. doi: 10.1111/j.1567-1364. 2006.00066.x
142. Remias, D., Holzinger, A., Aigner, S., and Lütz, C. (2012). Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Strep-tophyta), causing brown ice on glaciers in Svalbard (high arctic). Polar Biol. 35, 899-908. doi: 10.1007/s00300-011-1135-6
143. Remias, D., Holzinger, A., and Lütz, C. (2009). Ultrastructure and physiological characterization of the ice alga Mesotaenium berggrenii (Zygnemaphyceae, Chlorophyta) from glaciers in the European Alps. Phycologia 48, 302-312. doi: 10.2216/ 08-13.1
144. Remias, D., and Lütz, C. (2005). Photosynthesis, pigments and ultra-structure of the alpine snow alga Chlamydomonas nivalis. Eur. J. Phy-col. 40, 259-268. doi: 10.1080/ 09670260500202148
145. Remias, D., and Lütz, C. (2007). Characterisation of esterified secondary carotenoids and of their isomers in green algae: a HPLC approach. Algol. Stud. 124, 85-94. doi: 10.1127/1864-1318/2007/0124-0085
146. Reynolds, R., Belnap, J., Reheis, M., Lamothe, P., and Luiszer, F. (2001). Aeolian dust in Colorado Plateau soils: nutrient inputs and recent change in source. Proc. Natl. Acad. Sci. U.S.A. 98, 7123-7127. doi: 10.1073/pnas.121094298
147. Rindi, F. (2011). "Terrestrial green algae: systematics, biogeography and expected responses to climate change," in Climate Change, Ecology and Systematics, eds T. R. Hodkinson, M. B. Jones, S. Waldren, and J. Parnell (Cambridge: Cambridge University Press), 201-230. doi: 10.1017/CBO978051197 4540.010
148. Rindi, F., and Guiry, M. D. (2004). Composition and spatial variability of terrestrial algal assemblages occurring at the bases of urban walls in Europe. Phycologia 43, 225-235. doi: 10.2216/i0031-8884-43-3-225.1
149. Rindi, F., Guiry, M. D., Barbiero, R. P., and Cinelli, F. (1999). The marine and terrestrial Prasiolales (Chloro-phyta) of Galway City Ireland: a morphological and ecological study. J. Phycol. 35, 469-482. doi: 10.1046/j.1529-8817.1999.35 30469.x
150. Rindi, F., Guiry, M. D., and López-Bautista, J. M. (2008). Distribution, morphology, and phylogeny of Klebsormidium (Kleb-sormidiales, Charophyceae) in urban environments in Europe. J. Phycol. 44, 1529-1540. doi: 10.1111/j.1529-8817.2008.00593.x
151. Rindi, F., Mikhailyuk, T. I., Sluiman, H. J., Friedl, T., and López-Bautista, J. M. (2011). Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Strepto-phyta). Mol. Phylogenet. Evol. 58, 218-231. doi: 10.1016/j.ympev.2010. 11.030
152. Roberts, M. F. (2005). Organic compatible solutes of halotoler-ant and halophilic microorganisms. Saline Syst. 1, 5. doi: 10.1186/1746-1448-1-5
153. Rodriguez, M. C. S., Edsgärd, D., Sarfraz, H. S., Alquezar, D., Ras-mussen, M., Gilbert, T., et al. (2010). Transcriptomes of the desiccation tolerant resurrection plant Craterostigma plantagineum. Plant J. 63, 212-228. doi: 10.1111/j.1365-313X.2010.04243.x
154. Santarius, K. A. (1973). The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance. Planta 113, 105-114. doi: 10.1007/BF00388196
155. Scheibe, R., and Beck, E. (2011). "Drought, desiccation, and oxidative stress," in Plant Desiccation Tolerance, Vol. 215, Ecological Studies, eds U. Lüttge, E. Beck, and D. Bartels (Heidelberg: Springer), 209-232.
156. Schreiber, U., and Bilger, W. (1993). Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Progr. Bot. 54, 151-173. doi: 10.1007/978-3-642-78020-2_8
157. Sharma, N., Rai, A., Singh, S., and Brown, R. (2007). Airborne algae: their present status and relevance. J. Phycol. 43, 615-627. doi: 10.1111/j.1529-8817.2007. 00373.x
158. Singh, R. N. (1941). On some phases in the life history of the terrestrial alga, Fritschiella tuberosa Iyeng. and its autecology. New Phytol. 40, 170-182. doi: 10.1111/j.1469-8137.1941.tb07041.x
159. Škaloud, P., and Rindi, F. (2013). Ecological differentiation of cryptic species within an asexual pro-tist morphospecies: a case study of filamentous green alga Klebsormid-ium (Streptophyta). J. Eukar. Micro-biol. 60, 350-362. doi: 10.1111/jeu. 12040
160. Sørensen, I., Pettolino, F. A., Bacic, A., Ralph, J., Lu, F., O'Neill, M. A., etal. (2011). The charo-phycean green algae provide insights into the early origins of plant cell walls. Plant J. 68, 201-211. doi: 10.1111/j.1365-313X.2011. 04686.x
161. Stabenau, H., and Winkler, U. (2005). Glycolate metabolism in green algae. Physiol. Plant. 123, 235-245. doi: 10.1111/j.1399-3054.2005. 00442.x
162. Stancheva, R., Hall, J. D., and Sheath, R. G. (2012). Systematics of the genus Zygnema (Zygne-matophyceae, Charophyta) from Californian watersheds. J. Phycol. 48, 409-422. doi: 10.1111/j.1529-8817.2012.01127.x
163. Starr, R. C. (1955). Zygospore germination in Cosmarium botrytis var. subtumidum. Am. J. Bot. 42, 577-581. doi: 10.2307/2485314
164. Sundberg, B., Ekblad, A., Näsholm, T., and Palmqvist, K. (1999). Lichen respiration in relation to active time, temperature, nitrogen and ergos-terol concentrations. Funct. Ecol. 13, 119-125. doi: 10.1046/j.1365-2435.1999.00295.x
165. Takahashi, S., and Murata, N. (2008). How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13, 178-182. doi: 10.1016/j.tplants.2008. 01.005
166. Timme, R. E., Bachvaroff, T. R., and Delwiche, C. F. (2012). Broad phy-logenomic sampling and the sister lineage of land plants. PLoS ONE 7:e29696. doi: 10.1371/journal.pone. 0029696
167. Timme, R. E., and Delwiche, C. F. (2010). Uncovering the evolutionary origin of plant molecular pro cesses: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol. 10:96. doi: 10.1186/ 1471-2229-10-96
168. Trainor, F. R., and Gladych, R. (1995). Survival of algae in a desiccated soil: a 35-year study. Phycologia 34, 191-192. doi: 10.2216/i0031-8884-34-3-191.1
169. Weissman, L., Garty, J., and Hochman, A. (2005). Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration. Appl. Environ. Microbiol. 71, 6508-6514. doi: 10.1128/AEM.71.11.6508-6514.2005
170. Wieners, P. C., Mudimu, O., and Bil-ger, W. (2012). Desiccation-induced non-radiative dissipation in isolated green lichen algae. Photosynth Res. 113, 239-247. doi: 10.1007/s11120-012-9771-4
171. Wise, M. J., and Tunnacliffe, A. (2004). POPP the question: what do LEA proteins do? Trends Plant Sci. 9, 747-757. doi: 10.1016/j.tplants.2003. 10.012
172. Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A. J., Philippe, H., Melko-nian, M., et al. (2011). Origin of land plants: do conjugating green algae hold the key? BMC Evol. Biol. 11:104. doi: 10.1186/1471-2148-11-104
173. Wood, A. J. (2007). The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts and mosses. Bryologist 110, 163-177. doi: 10.1639/0007-2745 (2007)110[163:IENFIB]2.0.CO;2
174. Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830. doi: 10.1242/jeb.01730
175. Ytterberg, A. J., Peltier, J. B., and van Wijk, K. J. (2006). Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol. 140, 984-997. doi: 10.1104/pp.105.076083
176. Zhao, M., and Running, S. W. (2010). Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940-943. doi: 10.1126/science.1192666
177. Zou, D. H., Gao, K. S., Xia, J. R., Xu, Z. G., Zhang X., and Liu, S. X. (2007). Responses of dark respiration in the light to desiccation and temperature in the intertidal macroalga, Ulva lactuca (Chloro-phyta) during emersion. Phycolo-gia 46, 363-370. doi: 10.2216/06-98.1