Advertisement

Marine Biology

, Volume 149, Issue 1, pp 97–106 | Cite as

Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta)

  • M. Kakinuma
  • D. A. Coury
  • Y. Kuno
  • S. Itoh
  • Y. Kozawa
  • E. Inagaki
  • Y. Yoshiura
  • H. Amano
Mini-Review

Abstract

Like other organisms in the marine ecosystem, macroalgae are subjected to intense environmental stresses, particularly in the intertidal zone. The green seaweed Ulva inhabits rocky intertidal zones worldwide, suggesting that this alga may be a good model system for studying environmental stress responses in marine plants. Here, we review the physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa. In response to high-temperature stress, the amount of photosynthetic pigments, major free amino acids (AA), and total carbon and nitrogen in U. pertusa increase. Changes in chemical components due to high-temperature stress are consistent with morphological changes in thalli subjected to high temperature and suggest that high-temperature stress mainly affects nitrogen metabolism. Isozyme assays show that the alga expresses a glutamate dehydrogenase isozyme in response to high-temperature stress, and that its expression was regulated at the mRNA transcription level. Chemical component changes due to salinity stress indicate a possibility that the low- and high-salinity conditions affect photosynthesis and carbon and nitrogen metabolism, respectively. In particular, it was observed that thalli exposed to hypersaline conditions rapidly accumulate the organic osmolyte proline, suggesting that free proline accumulation is an important tolerance mechanism in this alga for adapting to hypersaline conditions. Finally, we discuss future directions for the molecular analysis of environmental stress in U. pertusa.

Keywords

Salinity Stress Photosynthetic Pigment Ulva Ammonia Assimilation Total Carbon Content 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This study was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports, and Culture of Japan. We thank Dr. M. Maegawa of the Faculty of Bioresources, Mie University, Japan, and Dr. T. Morita of the Marine Productivity Division of National Research Institute of Fisheries Science, Japan, for help with the experiments.

References

  1. Amano H, Mizobata Y, Maegawa M, Rogerson A (1998) Production of d-cysteinolic acid, a platelet anti-aggregating amino acid, from clone cultured reproductively sterile Ulva pertusa (Ulvales, Chlorophyta). In: Menasveta P, Tanticharoen M (eds) Proceedings of the 2nd Asia-Pacific marine biotechnology conference and 3rd Asia-Pacific conference on algal biotechnology. National Center for Genetic Engineering and Biotechnology, Bangkok, pp 97–102Google Scholar
  2. Bascomb NF, Schmidt RR (1987) Purification and partial kinetic and physical characterization of two chloroplast-localized NADP-specific glutamate dehydrogenase isozymes and their preferential accumulation in Chlorella sorokiniana cells cultured at low or high ammonium levels. Plant Physiol 83:75–84CrossRefGoogle Scholar
  3. Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222CrossRefGoogle Scholar
  4. Brown MT (1987) Effects of desiccation on photosynthesis of intertidal algae from a Southern New Zealand shore. Bot Mar 30:121–127CrossRefGoogle Scholar
  5. Cammaerts D, Jacobs M (1985) A study of the role of glutamate dehydrogenase in the nitrogen metabolism of Arabidopsis thaliana. Planta 163:517–526CrossRefGoogle Scholar
  6. Chapman ARO (1986) Population and community ecology of seaweeds. Adv Mar Biol 23:1–161Google Scholar
  7. Cock JM, Kim KD, Miller PW, Huston RG, Schmidt RR (1991) Restriction enzyme analysis and cloning of high molecular weight genomic DNA isolate from Chlorella sorokiniana (Chlorophyta). Plant Mol Biol 17:1023–1044CrossRefGoogle Scholar
  8. Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211CrossRefGoogle Scholar
  9. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223CrossRefGoogle Scholar
  10. Edwards DM, Reed RH, Chudek JA, Foster R, Steward WDP (1987) Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Mar Biol 95:583–592CrossRefGoogle Scholar
  11. Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-regulated signal stansduction. J Exp Bot 50:413–434Google Scholar
  12. Haxen PG, Lewis OAM (1981) Nitrate assimilation in the marine kelp Macrocystis anguatifolia (Phaeophyceae). Bot Mar 24:631–635Google Scholar
  13. Hurd CL, Dring MJ (1991) Desiccation and phosphate uptake by intertidal fucoid algae in relation to zonation. Br Phycol J 26:327–333CrossRefGoogle Scholar
  14. Inokuchi R, Itagaki T, Wiskich JT, Nakayama K, Okada M (1997) An NADP-glutamate dehydrogenase from the green alga Bryopsis maxima: purification and properties. Plant Cell Physiol 38:327–335CrossRefGoogle Scholar
  15. Inokuchi R, Motojima K, Yagi Y, Nakayama K, Okada M (1999) Bryopsis maxima (Chlorophyta) glutamate dehydrogenase: multiple genes and isozymes. J Phycol 35:1013–1024CrossRefGoogle Scholar
  16. Ito T, Kito K, Adati N, Mitsui Y, Hagiwara H, Sasaki Y (1994) Fluorescent differential display: arbitrarily primed RT-PCR fingerprinting on an automated DNA sequencer. FEBS Lett 351:231–236CrossRefGoogle Scholar
  17. Joy KW (1988) Ammonia, glutamate and asparagine: a carbon-nitrogen interface. Can J Bot 66:2103–2109CrossRefGoogle Scholar
  18. Kakinuma M, Shibahara N, Ikeda H, Maegawa M, Amano H (2001a) Thermal stress responses of a sterile mutant of Ulva pertusa (Chlorophyta). Fish Sci 67:287–294CrossRefGoogle Scholar
  19. Kakinuma M, Kozawa Y, Itoh S, Amano H (2001b) cDNA cloning of two types of glutamate dehydrogenase from a reproductively sterile mutant of Ulva pertusa (Chlorophyta) grown under different thermal conditions. Fish Sci 67:380–382CrossRefGoogle Scholar
  20. Kakinuma M, Kuno Y, Amano H (2004a) Salinity stress responses of a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Fish Sci 70:1177–1179CrossRefGoogle Scholar
  21. Kakinuma M, Coury DA, Inagaki E, Itoh S, Yoshiura Y, Amano H (2004b) Isolation and characterization of a single-copy actin gene from a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Gene 334:145–155CrossRefGoogle Scholar
  22. Kavi Kishor PB, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394CrossRefGoogle Scholar
  23. Kirst GO (1990) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 40:21–53CrossRefGoogle Scholar
  24. Kiyosue T, Toshiba Y, Yamaguchi-Shinozuka K, Shinozuka K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335CrossRefGoogle Scholar
  25. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress. Plant Physiol 130:2129–2141CrossRefGoogle Scholar
  26. Kúbler JE, Davison IR (1993) High temperature tolerance of photosynthesis in the red alga Chondrus crispus. Mar Biol 117:327–335CrossRefGoogle Scholar
  27. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev Plant Physiol Plant Mol Biol 47:569–593CrossRefGoogle Scholar
  28. Liu CH, Shih MC, Lee TM (2000) Free proline levels in Ulva (Chlorophyta) in response to hypersalinity: elevated NaCl in seawater versus concentrated seawater. J Phycol 36:118–119CrossRefGoogle Scholar
  29. Lobban CS (1985) Seashore communities. In: Lobban CS, Harrison PJ, Duncan MJ (eds) The physiological ecology of seawater. Cambridge University Press, Cambridge, pp 154–187Google Scholar
  30. Loulakakis CA, Roubelakis-Angelakis KA, Kanellis AK (1994) Regulation of glutamate dehydrogenase and glutamine synthetase in avocado fruit during development and ripening. Plant Physiol 106:217–222CrossRefGoogle Scholar
  31. Lüning K (1984) Temperature tolerance and biogeography of seaweeds: the marine algal flora of Helgoland, North Sea, as an example. Helgolander Meeresun 38:305–317CrossRefGoogle Scholar
  32. Maegawa M, Sugiyama A (1995) Relationship between heat tolerance and the vertical distribution of intertidal algae. Suisanzoshoku 43:429–435Google Scholar
  33. Melo-Oliveira R, Oliveira IC, Coruzzi GM (1996) Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Proc Natl Acad Sci USA 93:4718–4723CrossRefGoogle Scholar
  34. Miernyk JA (1999) Protein folding in the plant cell. Plant Physiol 121:695–703CrossRefGoogle Scholar
  35. Migita S (1985) The sterile mutant of Ulva pertusa Kjellman from Oumra Bay. Bull Fac Fish Nagasaki Univ 57:33–37Google Scholar
  36. Muñouz-Blanco J, Moyano E, Cárdenas J (1989) Glutamate dehydrogenase isozymes of Chlamydomonas reinhardtii. FEMS Microbiol Lett 61:315–318CrossRefGoogle Scholar
  37. Murase N, Maegawa M, Matsui T, Ohgai T, Katayama N, Saitoh M, Yokohama Y (1993) Growth and photosynthesis temperature characteristics of the sterile Ulva pertusa. Nippon Suisan Gakkaishi 60:625–630CrossRefGoogle Scholar
  38. Murthy MS, Rao AS, Reddy ER (1986) Dynamics of nitrate reductase activity in two intertidal algae under desiccation. Bot Mar 24:471–474Google Scholar
  39. Murthy MS, Rao AS, Faldu PJ (1988) Invertase and total amylase activities in Ulva lactuca from different tidal levels, under desiccation. Bot Mar 31:53–56Google Scholar
  40. Murthy MS, Sharma CLNS (1989) Peroxidase activity in Ulva lactuca under desiccation. Bot Mar 32:511–513Google Scholar
  41. Norton TA (1986) The zonation of seaweeds on rocky shores. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Columbia University Press, New York, pp 7–21Google Scholar
  42. Nuccio ML, Rhodes D, McNeil SD, Hanson AD (1999) Metabolic engineering of plants for osmotic stress resistance. Curr Opin Plant Biol 2:128–134CrossRefGoogle Scholar
  43. Oask A (1994) Primary nitrogen assimilation in higher plants and its regulation. Can J Bot 72:739–750CrossRefGoogle Scholar
  44. Osteryoung KW, Vierling E (1994) Dynamics of small heat shock protein distribution within the chloroplasts of higher plants. J Biol Chem 269:28676–28682PubMedGoogle Scholar
  45. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Culture and collection of algae. Proceedings of U.S.–Japan conference in Hakone. Japanese Society of Plant Physiologists, Tokyo, pp 63–75Google Scholar
  46. Quadir A, Harrison PJ, DeWreede RE (1979) The effects of emergence and submergence on the photosynthesis and respiration of marine macrophytes. Phycologia 18:83–88CrossRefGoogle Scholar
  47. Rhodes D, Brunk DG, Magalhaes RJ (1989) Assimilation of ammonia by glutamate dehydrogenase? In: Poulton JE, Romeo JT, Conn EE (eds) Plant nitrogen metabolism, vol 5. Plenum, New York, pp 191–206CrossRefGoogle Scholar
  48. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  49. Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR (1991) The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiol 95:509–516CrossRefGoogle Scholar
  50. Rosana MO, Oliveira IC, Coruzzi GM (1996) Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Proc Natl Acad Sci USA 93:4718–4723CrossRefGoogle Scholar
  51. Sachs MM, Ho THD (1986) Alteration of gene expression during environmental stress in plants. Ann Rev Plant Physiol 37:363–376CrossRefGoogle Scholar
  52. Sakakibara H, Fujii K, Sugiyama T(1995) Isolation and characterization of a cDNA that encodes maize glutamate dehydrogenase. Plant Cell Physiol 36:789–797CrossRefGoogle Scholar
  53. Sato M, Sato Y, Tsuchiya Y (1984) Glutamate dehydrogenase of Porphyra yezoensis. Hydrobiologoa 116/117:584–587CrossRefGoogle Scholar
  54. Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164:151–162CrossRefGoogle Scholar
  55. Shaw CR, Prasad R (1970). Starch gel electrophoresis of enzymes: a compilation of recipes. Biochem Genet 4:297–320CrossRefGoogle Scholar
  56. Sieciechowicz KA, Joy KW, Ireland RJ (1988) The metabolism of asparagine in plants. Phytochem 27:663–671CrossRefGoogle Scholar
  57. Singh RP (1995) Ammonia assimilation. In: Srivastava HS, Singh RP (eds) Nitrogen nutrition in higher plants. Associated Publishing, New Delhi, pp 189–202Google Scholar
  58. Smith CM, Berry JA (1986) Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with different distributional limits. Oecologia 70:6–12CrossRefGoogle Scholar
  59. Srivastava HS, Singh RP (1987) Role and regulation of L-glutamate dehydrogenase activity in higher plants. Phytochem 26:597–610CrossRefGoogle Scholar
  60. Stewart GR, Mann AF, Fentem PA (1980) Enzymes of glutamate formation: glutamate dehydrogenasse, glutamine synthetase and glutamate synthase. In: Miflin BJ (ed) The biochemistry of plants, vol 5. Academic, New York, pp 271–327CrossRefGoogle Scholar
  61. Syntichaki KM, Loulakakis KA, Roubelakis-Angelakis KA (1996) The amino-acid sequence similarity of plant glutamate dehydrogenase to the extremophilic archaeal enzyme conforms to its stress-related function. Gene 168:87–92CrossRefGoogle Scholar
  62. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508–510CrossRefGoogle Scholar
  63. Thomas TE, Turpin DH (1980) Desiccation enhanced nutrient uptake rates in the intertidal alga Fucus distichus. Bot Mar 23:479–481Google Scholar
  64. Turano FJ, Thakkar SS, Fang T, Weisemann JM (1997) Characterization and expression of NAD(H)-dependent glutamate dehydrogenase genes in Arabidopsis. Plant Physiol 113:1329–1341CrossRefGoogle Scholar
  65. Ueda A, Kanechi M, Uno Y, Inagaki N (2003) Photosynthetic limitations of a halophyte sea aster (Aster tripolium L.) under water stress and NaCl stress. J Plant Res 116:65–70PubMedGoogle Scholar
  66. Withholm JM (1972) The use of fluoresce in diacetate and phemosafranine for determining viability of cultured plant cells. Stain Technol 47:189–194CrossRefGoogle Scholar
  67. Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102CrossRefGoogle Scholar
  68. Zehr PJ, Falkowski PG (1988) Pathway of ammonium assimilattion in a marine diatom determined with the radiotracer 13N. J Phycol 24:588–591Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • M. Kakinuma
    • 1
  • D. A. Coury
    • 1
  • Y. Kuno
    • 1
  • S. Itoh
    • 1
  • Y. Kozawa
    • 1
  • E. Inagaki
    • 1
  • Y. Yoshiura
    • 2
  • H. Amano
    • 1
  1. 1.Laboratory of Marine Biochemistry, Faculty of BioresourcesMie UniversityTsu, MieJapan
  2. 2.Division of Aquatic Animal HealthNational Research Institute of AquacultureTamaki, MieJapan

Personalised recommendations