Desiccation tolerance in the chlorophyte green alga Ulva compressa: does cell wall architecture contribute to ecological success?

Planta

Volumn 242, Issue 2, 2015, Pages 477-492

  Holzinger, Andreas ^a   Herburger, Klaus ^a   Kaplan, Franziska ^a   Lewis, Louise A ^b  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Cellulose; Imaging PAM; Intertidal zone; Macroalgae; Pectin; Photosynthesis; rbcL phylogeny

Indexed keywords

CHLOROPHYTA; ULVA; ULVA COMPRESSA;

PIGMENT; WATER;

ADAPTATION; CELL WALL; CYTOLOGY; DESICCATION; ELECTRON TRANSPORT; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; METABOLISM; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; ULTRASTRUCTURE; ULVA;

ADAPTATION, PHYSIOLOGICAL; CELL WALL; DESICCATION; ECOLOGICAL AND ENVIRONMENTAL PHENOMENA; ELECTRON TRANSPORT; PHOTOSYNTHESIS; PHYLOGENY; PIGMENTS, BIOLOGICAL; ULVA; WATER;

EID: 84937518527     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2292-6     Document Type: Article

References (83)

1. Abdel-Fattah AF, Edrees M (1972) A study of the polysaccharide content of Ulva lactuca L. Qual Plant Mater Veg 22:15–22
2. Aquino RS, Grativol C, Mourão PAS (2011) Rising from the sea: correlations between sulphated polysaccharides and salinity in plants. PLoS One 6:e18862
3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
4. Bischof K, Kräbs G, Wiencke C, Hanelt D (2002a) Solar ultraviolet radiation affects the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509
5. Bischof K, Peralta G, Kräbs G, Van den Poll WH, Perez-Llorens JL, Breeman AM (2002b) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 379:2411–2421
6. Bliding G (1963) A critical survey of European taxa in Ulvales. Part I. Capsosiphon, Percursaria, Blidingia, Enteromorpha. Obera Bot 8:1–160
7. Blomster J, Maggs CA, Stanhope MJ (1998) Molecular and morphological analysis of Enteromorphaintestinalis and E. compressa (Chlorophyta) in the British isles. J Phycol 34:319–340
8. Bråten T (1975) Observations on the mechanisms of attachment in the green alga UIvamutabilis Föyn. Protoplasma 84:161–173
9. Bråten T, Løvlie A (1968) On the ultrastructure of vegetative and sporulating cells of the multicellular green alga Ulva mutabilis Föyn. Nytt Mag Bot 15:209–219
10. Briand X (1991) Seaweed harvesting in Europe. In: Guiry MD, Blunden G (eds) Seaweed resources in Europe. Wiley, Chichester, pp 259–308
11. Burrows EM (1959) Growth form and environment in Enteromorpha. Bot J Linn Soc 56:204–206
12. Carr H, Björk M (2003) A methodological comparison of photosynthetic oxygen evolution and estimated electron transport rate in tropical Ulva (Chlorophyceae) species under different light and inorganic carbon conditions. J Phycol 39:1125–1131
13. Ciancia M, Alberghina J, Arata PX, Benavides H, Leliaert F, Verbruggen H, Estevez JM (2012) Characterization of cell wall polysaccharides of the coenocytic green seaweed Bryopsis plumosa (Bryopsidaceae, Chlorophyta) from the Argentine coast. J Phycol 48:326–335
14. Contreras-Porcia L, Dennett G, González A, Vergara E, Medina C, Correa JA, Moenne A (2011) Identification of copper-induced genes in the marine alga Ulva compressa (Chlorophyta). Mar Biotechnol 13:544–556
15. Dickson DMJ, Wyn Jones RG, Davenport J (1982) Osmotic adaptation in Ulva lactuca under fluctuating salinity regimes. Planta 155:409–415
16. Domozych DS, Serfis A, Kiemle SN, Gretz MR (2007) The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum. Protoplasma 230:99–115
17. Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WG (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82. doi:10.3389/fpls.2012.00082
18. Estevez JM, Kasuli L, Fernandez PV, Dupree P, Ciancia M (2009) Chemical in situ characterization of macromolecular components of the complex cell walls from the coenocytic green alga Codiumfragile. Glycobiol 18:250–259
19. Franklin LA, Levavasseur G, Osmond CB, Henley WJ, Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186:399–408
20. Gao S, Chen X, Yi Q, Wang G, Pan G, Lin A, Peng G (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS One 5:e8571
21. Gao S, Gu W, Xiong Q, Ge F, Xie X, Li J, Chen W, Pan G, Wang G (2015) Desiccation enhances phosphorylation of PS II and affects the distribution of protein complexes in the thylakoid membrane. Physiol Plant 153:492–502
22. Gao S, Shen S, Wang G, Niu J, Lin A, Pan G (2011) PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol 52:885–893
23. Gao S, Zheng Z, Gu W, Xie X, Huan L, Pan G, Wang G (2014) Photosystem I shows a higher tolerance to sorbitol-induced osmotic stress than photosystem II in the intertidal macro-algae Ulva prolifera (Chlorophyta). Physiol Plant 152:380–388
24. Gasulla F, Jain R, Barreno E, Guéra A, Balbuena TS, Thelen JJ, Oliver MJ (2013) The response of Asterochloriserici (Ahmadjian) Skaloud et Peksa to desiccation: a proteomic approach. Plant Cell Environ 36:1363–1378
25. 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
26. Herburger K, Lewis LA, Holzinger A (2015) Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation. Protoplasma 252:571–589
27. Hernández I, Peralta G, Pérez-Lloréns JL, Vergara JJ, Niell FX (1997) Biomass and dynamics of growth of Ulva species in almones River estuary. J Phycol 33:764–772
28. Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological, and molecular mechanisms. Front Plant Sci 4:327. doi:10.3389/fpls.2013.00327
29. Holzinger A, Lütz C, Karsten U (2011) Desiccation stress causes structural and ultra-structural alterations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust. J Phycol 47:591–602
30. Holzinger A, Roleda M, Lütz C (2009) The vegetative arctic green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838
31. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
32. Kaplan F, Lewis LA, Herburger K, Holzinger A (2013) Osmotic stress in the Arctic and Antarctic green alga Zygnema sp. (Zygnemtales, Streptophyta): effects on photosynthesis and ultrastructure. Micron 44:317–330
33. Kaplan F, Lewis LA, Wastian J, Holzinger A (2012) Plasmolysis effects and osmotic potential of two phylogenetically distinct alpine strains of Klebsormidium (Streptophyta). Protoplasma 249:789–804
34. Karsten U, Herburger K, Holzinger A (2014) Dehydration, temperature and light tolerance in members of the aeroterrestrial green algal genus Interfilum (Streptophyta) from biogeographically different temperate soils. J Phycol 50:804–816
35. Karsten U, Holzinger A (2012) Light, temperature and desiccation effects on photosynthetic activity and drought-induced ultrastructural changes in the green alga Klebsormidiumdissectum (Streptophyta) from a high alpine soil crust. Microb Ecol 63:51–63
36. Karsten U, Holzinger A (2014) Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodivers Conserv 23:1845–1858
37. Kirkendale L, Saunders GW, Winberg P (2013) A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J Phycol 49:69–81
38. Kirst GO (1990) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 41:21–53
39. Kosugi M, Shizuma R, Moriyama Y, Koike H, Fukunaga Y, Takeuchi A, Uesugi K, Suzuki Y, Imura S, Kudoh S, Miyazawa A, Kashino Y, Satoh K (2014) Ideal osmotic spaces for chlorobionts or cyanobionts are differentially realized by lichenized fungi. Plant Physiol 166:337–348
40. Kranner I, Birtic F (2005) A modulation role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740
41. Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Nat Acad Sci USA 102:3141–3146
42. Krishnamurthy KV (1999) Methods in cell wall cytochemistry. CRC Press, Boca Raton, p 318
43. Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112
44. Lahaye M, Ray B (1996) Cell-wall polysaccharides from the marine green alga Ulva “rigida” (Ulvales, Chlorophyta)—NMR analysis of ulvan oligosaccharides. Carbohyd Res 22:161–173
45. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1766–1774
46. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46
47. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry (CPFA). John Wiley and Sons, New York, pp F4.3.1–F4.3.8
48. Longstaff BJ, Kildea T, Runcie JW, Cheshire A, DennisonWC Hurd C, Kana T, Raven JA, Larkum WD (2002) An in situ study of photosynthetic oxygen exchange and electron transport rate in marine macroalga Ulva lactuca (Chlorophyta). Photosynth Res 74:281–293
49. McArthur D, Moss B (1977) The ultrastructure of cell walls in Enteromorphaintestinalis (L.) Link. Br Phycol J 12:359–368
50. McArthur D, Moss B (1978) Ultrastructural studies of vegetative cells, mitosis and cell division in Enteromorphaintestinalis (L.) Link. Br Phycol J 13:255–267
51. McManus HA, Lewis LA (2011) Molecular phylogenetic relationships in the freshwater family Hydrodictyaceae (Sphaeropleales, Chlorophyceae) with an emphasis on Pediastrum duplex. J Phycol 47:152–163
52. Messyasz B, Czerwik J, Marcinkowska Uher B, Rybak A, Szendzina L, Pikosz M (2013) Ulva flexuosa subsp. pilifera (Chlorophyta, Ulvophyceae) from the Wielkopolska region (West Poland): a new observation on the ultrastructure of vegetative cells. Oceanol Hydrobiol Stud 42:209–215
53. Micalef H, Gayral P (1972) Quelques aspects de l’infrastructure des cellules vegetatives et des cellules reproductrices d’ Ulva lactuca (L.). J Microscopie 13:417–428
54. Moore JP, Nguema-Ona EE, Vicré-Gibouin M, Sørensen I, Willats WGT, Driouich A, Farrant JM (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237:739–754
55. Mou S, Zhang X, Dong M, Fan X, Xu J, Gao S, Xu D, Wang W, Ye N (2013) Photoprotection in the green tidal alga Ulva prolifera: role of LHCSR and PsbS proteins in response to high light stress. Plant Biol 15:1033–1039
56. Percival E (1979) The polysaccharides of green, red, and brown seaweeds: their basic structure, biosynthesis and function. Br Phycol J 14:103–117
57. Pichrtová M, Hajek T, Elster J (2014a) Osmotic stress and recovery in field populations of Zygnema sp. (Zygnematophyceae, Streptophyta) on Svalbard (High Arctic) subjected to natural desiccation. FEMS Microbiol Ecol 89:270–280
58. Pichrtová M, Kulichová J, Holzinger A (2014b) Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats. PLoS One 9:e113137
59. Posada D (2008) jModelTest: Phylogenetic model averaging. Mol Biol Evol 25:1253–1256
60. Rambaut A, Drummond A (2003) Tracer: MCMC trace analysis tool. University of Oxford, Oxford
61. Rautenberger R, Bischof K (2006) Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions. Polar Biol 29:988–996
62. Ray B (2006) Polysaccharides from Enteromorphacompressa: isolation, purification and structural features. Carbohyd Polym 66:408–416
63. Reed RH, Russel G (1978) Salinity fluctuations and their influence on “bottle brush” morphogenesis in Enteromorphaintestinalis (L.) Link. Br Phycol J 13:149–153
64. Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362
65. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180
66. Schweiger HG, Dehm P, Berger S (1977) Culture conditions for Acetabularia. In: Woodcock CLF (ed) Progress in Acetabularia research. Academic Press, New York, pp 319–330
67. Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88
68. Smith CM, Berry JA (1986) Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with differing distributional limits. Oecologia 70:6–12
69. Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertl W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48:1433–1447
70. Stancheva R, Hall JD, Herburger K, Lewis LA, McCourt RM, Sheath RG, Holzinger A (2014) Phylogenetic position of Zygogoniumericetorum (Zygnematophyceae, Charophyta) from a high alpine habitat and ultrastructural characterization of unusual aplanospores. J Phycol 50:790–803
71. Sung MS, Hsu YT, Hsu YT, Wu TM, Lee TM (2009) Hypersalinity and hydrogen peroxide upregulation of gene expression of antioxidant enzymes in Ulva fasciata against oxidative stress. Mar Biotech 11:199–209
72. Swofford DL (2002) Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland
73. Veccia FD, Marzocchi M, Maistro S, Moro I (2012) Morphophysiological effects of cadmium on two Ulva species. Algol Stud 138:13–25
74. Walsby AE (1997) Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol 136:189–209
75. Wang C, Yu R, Zhou M (2011) Acute toxicity of live and decomposing green alga Ulva (Enteromorpha) prolifera to abalone Haliotisdiscus hannai. Chinese J Oceanol Limnol 23:541–546
76. West KR, Pitman MG (1967) Ionic relations and ultrastructure in Ulva lactuca. Aust J Biol Sci 20:901–914
77. Wijesekara I, Pangestuti R, Kim SK (2011) Biological activities and potential health benefits of sulphated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21
78. Wolf MA, Sciuto K, Andreoli C, Moro I (2012) Ulva (Chlorophyta, Ulvales) biodiversity in the north Adriatic Sea (Mediterranean, Italy): cryptic species and new introductions. J Phycol 48:1510–1521
79. Xia J, Li Y, Zou D (2004) Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aquat Bot 80:129–137
80. Xie X, Gao S, Gu W, Pan G, Wang G (2013) Desiccation induces accumulation of antheraxanthin and zeaxanthin in intertidal macro-alga Ulva pertusa (Chlorophyta). PLoS One 8:e72929
81. Yaicha H, Garnaa H, Besbesa S, Paquotb M, Bleckerc C, Attiaa H (2011) Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem 128:895–901
82. Zhang X, Ye N, Liang C, Mou S, Fan Y, Xu J, Xu D, Zhuang Z (2012) De novo sequencing and analysis of the Ulva linza transcriptome to discover putative mechanisms associated with its successful colonization of coastal ecosystems. BMC Genom 13:565
83. Zou DH, Gao KS, Xia JR, Xu ZG, Zhang X, Liu SX (2007) Responses of dark respiration in the light to desiccation and temperature in the intertidal macroalga, Ulva lactuca (Chlorophyta) during emersion. Phycologia 46:363–370