Journal of Applied Phycology

, Volume 20, Issue 5, pp 915–924 | Cite as

Differing patterns of hsp70 gene expression in invasive and native kelp species: evidence for acclimation-induced variation

  • Sarah K. HenkelEmail author
  • Gretchen E. Hofmann


Temperature is one of the primary factors determining the geographic boundaries of seaweeds. Thus, investigations of how seaweeds cope with temperature stress and what affects their ability for range expansion are particularly important when studying invasive species. In physiological ecology, an established index of thermotolerance is the up-regulation of heat shock genes and subsequent synthesis of heat shock proteins (Hsps). The goal of this study was to examine the up-regulation of the hsp70 gene to assess physiological tolerances of the Eastern Pacific invasive kelp, Undaria pinnatifida, as compared to a potentially competing native kelp, Egregia menziesii. Individuals of both species were collected from six known Undaria invasion sites on the west coast of North America and held in the laboratory for 1–2 weeks for acclimation at 10°C. Samples were then heat shocked at 7 temperatures for 1 h. RNA was extracted, reverse transcribed, and amplified in quantitative PCR reactions to determine relative amounts of hsp70 transcript. Results indicate that the native Egregia may be locally adapted to different thermal regimes across latitude, while the invasive Undaria populations exhibit similar expression profiles across latitude but differ by habitat.


Egregia Heat shock Real time PCR Seaweed Temperature Undaria 



This study was funded primarily by an EPA STAR grant S.K.H. Additional funds were obtained from a PISCO grant to G.E.H. The authors wish to acknowledge the following individuals who made this study possible: Steve Lonhart of the Monterey Bay National Marine Sanctuary for identification of Undaria locations in Monterey Harbor, and Harbor Master Steve Pryor for access to Monterey Harbor; Marla Ranelletti for identification of Undaria sites in Santa Barbara Harbor; Rachel Woodfield for identification of Undaria sites in Los Angeles Harbor; Erin Maloney of Moss Landing Marine Laboratories for identification of Undaria sites in San Diego Bay; Kathy Ann Miller of the University of California Berkeley for Undaria collection from Catalina Island; and Eugenio Carpizo of UABC and Elizabeth Hoaglund of UCSB for assistance with Undaria collection from Todos Santos Island in Baja California, Mexico. We appreciate temperature data for Todos Santos Island shared by Julio Palleiro of CICESE. This is contribution number 243 from PISCO, the Partnership for Interdisciplinary Studies of Coastal Oceans funded primarily by the Gordon and Betty Moore Foundation and David and Lucile Packard Foundation.


  1. Aguilar-Rosas R, Aguilar-Rosas LE, Avila-Serrano G, Marcos-Ramírez R (2004) First record of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta) on the Pacific coast of Mexico. Bot Mar 47:255–258CrossRefGoogle Scholar
  2. Ambrose RF, Nelson BV (1982) Inhibition of giant kelp recruitment by an introduced brown alga. Bot Mar 25:265–267Google Scholar
  3. Arrontes J (2002) Mechanisms of range expansion in the intertidal brown alga Fucus serratus in northern Spain. Mar Biol 141:1059–1067CrossRefGoogle Scholar
  4. Barton NH (1989) Founder effect speciation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, Mass., pp 229–256Google Scholar
  5. Barua D, Downs CA, Heckathorn SA (2003) Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Funct Plant Biol 30:1071–1079CrossRefGoogle Scholar
  6. Battershill C, Miller K, Cole R (1998) The Understorey of Marine Invasions. Seafood NZ 6:31–33Google Scholar
  7. Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc B 26:211–252Google Scholar
  8. Breeman AM (1988) Relative importance of temperature and other factors in determining geographic boundaries of seaweeds: experimental and phenological evidence. Helgo Meer 42:199–241CrossRefGoogle Scholar
  9. Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar Ecol Progr Ser 277:61–78CrossRefGoogle Scholar
  10. Buckley BA, Hofmann GE (2002) Thermal acclimation changes DNA-binding activity of heat shock factor 1 (HSF1) in the goby Gillichthys mirabilis: implications for plasticity in the heat shock response in natural populations. J Exp Bio 205:3231–3240Google Scholar
  11. Buckley BA, Hofmann GE (2004) Seasonal patterns and in vitro kinetics of HSF1 activation and Hsp70 mRNA production in the goby, Gillichthys mirabilis. Physiol Biochem Zool 77:570–581PubMedCrossRefGoogle Scholar
  12. Buckley BA, Owen ME, Hofmann GE (2001) Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J Exp Bio 204:3571–3579Google Scholar
  13. Casas G, Scrosati R, Piriz ML (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Inv 6:411–416CrossRefGoogle Scholar
  14. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116CrossRefGoogle Scholar
  15. Downs CA, Heckthorn SA, Bryan JK, Coleman JS (1998) The methionine-rich low-molecular-weight chloroplast heat-shock protein: evolutionary conservation and accumulation in relation to thermotolerance. Am J Bot 85:175–183CrossRefGoogle Scholar
  16. Fangue NA, Hofmeister M, Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872PubMedCrossRefGoogle Scholar
  17. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  18. Floc’h JY, Pajot R, Wallentinus I (1991) The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. J Conseil 47:379–390Google Scholar
  19. Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia 39:547–553CrossRefGoogle Scholar
  20. Gacia E, Rodriguez-Prieto C, Delgado O, Ballesteros E (1996) Seasonal light and temperature responses of Caulerpa taxifolia from the northwestern Mediterranean. Aquat Bot 53:215–225CrossRefGoogle Scholar
  21. Gillespie RD, Meinesz A, Critchley AT (1997) Growth responses of Caulerpa taxifolia (Ulvophyceae, Chlorophyta) from the South African aquarist trade. A potential invasive of South African coastal waters. S Afr J Bot 63:480–483Google Scholar
  22. Halpin PM, Sorte CJ, Hofmann GE, Menge BA (2002) Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Integr Comp Biol 42:815–824CrossRefGoogle Scholar
  23. Hamdoun AM, Cheney DP, Cherr GN (2003) Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific Oyster (Crassostrea gigas): Implications for thermal limits and induction of thermal tolerance. Biol Bull 205:160–169PubMedCrossRefGoogle Scholar
  24. Harris LG, Tyrrell MC (2001) Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol Inv 3:9–21CrossRefGoogle Scholar
  25. Hay CH, Luckens PA (1987) The Asian Kelp Undaria pinnatifida (Phaeophyta, Laminariales) found in a New Zealand harbor. NZ J Bot 25:329–332Google Scholar
  26. Hay CH, Villouta E (1993) Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Bot Mar 36:461–476CrossRefGoogle Scholar
  27. Heckathorn SA, Poeller GJ, Coleman JS, Hallberg RL (1996) Nitrogen availability alters patterns of accumulation of heat stress-induced proteins in plants. Oecologia 105:413–418CrossRefGoogle Scholar
  28. Helmuth B (2002) How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Int Comp Biol 42:837–845CrossRefGoogle Scholar
  29. Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384PubMedCrossRefGoogle Scholar
  30. Hochachka PW, Somero GN (2002) Biochemical Adaptation. Oxford University Press, New YorkGoogle Scholar
  31. Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889–900Google Scholar
  32. Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures-Seasonal changes in levels of ubiquitin conjugates and Hsp70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518PubMedGoogle Scholar
  33. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392–4397PubMedCrossRefGoogle Scholar
  34. Howarth CJ (1991) Molecular responses of plants to an increased incidence of heat-shock. Plant Cell Environ 14:831–841CrossRefGoogle Scholar
  35. Ireland HE, Harding SJ, Bonwick GA, Jones M, Smith CJ, Williams JHH (2004) Evaluation of heat shock protein 70 as a biomarker of environmental stress in Fucus serratus and Lemna minor. Biomarkers 9:139–155CrossRefGoogle Scholar
  36. Kimpel JA, Key JL (1985) Heat-shock in plants. Trends Biochem Sci 10:353–357CrossRefGoogle Scholar
  37. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larve. Cell Stress Chaperon 2:60–71CrossRefGoogle Scholar
  38. Krebs RA, Holbrook SH (2001) Reduced enzyme activity following Hsp70 overexpression in Drosophila melanogaster. Biochem Genet 39:73–82PubMedCrossRefGoogle Scholar
  39. Lewis S, May S, Donkin ME, Depledge MH (1998) The influence of copper and heatshock on the physiology and cellular stress response of Enteromorpha intestinalis. Mar Environ Res 46:421–424CrossRefGoogle Scholar
  40. Li R, Brawley SH (2004) Improved survival under heat stress in intertidal embryos (Fucus spp.) simultaneously exposed to hypersalinity and the effect of parental thermal history. Mar Biol 144:205–213CrossRefGoogle Scholar
  41. Lund SG, Ruberte MR, Hofmann GE (2006) Turning up the heat: The effects of thermal acclimation on the kinetics of hsp70 gene expression in the eurythermal goby, Gillichthys mirabilis. Comp Biochem Physiol A 143:435–446CrossRefGoogle Scholar
  42. Lüning K, Freshwater W (1988) Temperature tolerance of northeast Pacific marine algae. J Phycol 24:310–315Google Scholar
  43. Lüning K, Guiry MD, Masuda M (1987) Upper temperature tolerance of North Atlantic and North Pacific geographical isolates of Chondrus crispus (Rhodophyta). Helgo Meer 41:297–306CrossRefGoogle Scholar
  44. Manitašević S, Dunderski J, Matic G, Tucic B (2007) Seasonal variation in heat shock proteins Hsp70 and Hsp90 expression in an exposed and a shaded habitat of Iris pumila. Plant Cell Environ 30:1–11PubMedCrossRefGoogle Scholar
  45. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  46. Osovitz CO, Hofmann GE (2005) Thermal history-dependent expression of the hsp70 gene in purple sea urchins: Biogeographic patterns and the effect of temperature acclimation. J Exp Mar Biol Ecol 327:134–143CrossRefGoogle Scholar
  47. Pelham HR (1982) A regulatory upstream promoter element in the Drosophila hsp70 heat-shock gene. Cell 30:517–528PubMedCrossRefGoogle Scholar
  48. Perez R, Durand P, Kaas R, Barbaroux O, Barbier V, Vinot C, Bourgeay-Causse M, Leclercq M, Moigne JY (1988) Undaria pinnatifida on the French coasts. Cultivation method; biochemical composition of the sporophyte and the gametophyte. In: Staedler T, Mollion J, Verdus MC, Karamanos Y, Morvan H, Chiristiaen D (eds) Algal biotechnology. Elsevier, London, pp 315–328Google Scholar
  49. Peters AF, Breeman AM (1992) Temperature responses of disjunct temperate brown-algae indicate long-distance dispersal of microthalli across the tropics. J Phycol 28:428–438CrossRefGoogle Scholar
  50. Ribera MA, Boudouresque CF (1995) Introduced marine plants with special reference to macroalgae: mechanisms and impact. In: Round FE, Chapman DJ (ed) Progress in phycological research. Biopress, Bristol, pp 217–268Google Scholar
  51. Sagarin RD, Somero GN (2006) Complex patterns of expression of heat-shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytilus californianus and snail Nucella ostrina. J Biogeogr 33:622–630CrossRefGoogle Scholar
  52. Sanchez I, Fernandez C, Arrontes J (2005) Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Pheophyta). J Phycol 41:942–949CrossRefGoogle Scholar
  53. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM et al (2007) Ecological and evolutionary insights from species invasions. TREE 22:465–471PubMedGoogle Scholar
  54. Seymour RJ, Tegner MJ, Dayton PK, Parnell PE (1989) Storm wave induced mortality of giant kelp, Macrocystis pyrifera, in southern California. Estuar Coast Shelf Sci 28:277–292CrossRefGoogle Scholar
  55. Sharp VA, Miller D, Bythell JC, Brown BE (1994) Expression of low molecular weight HSP70 related polypeptides from the symbiotic sea anemone Anemonia viridis Forskall in response to heatshock. J Exp Mar Biol Ecol 179:179–193CrossRefGoogle Scholar
  56. Shi Y, Mosser DD, Morimoto RI (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12:654–666PubMedCrossRefGoogle Scholar
  57. Silva PC, Woodfield RA, Cohen AN, Harris LH, Goddard JHR (2002) First report of the Asian kelp Undaria pinnatifida in the northeastern Pacific Ocean. Biol Inv 4:333–338CrossRefGoogle Scholar
  58. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15479–15500CrossRefGoogle Scholar
  59. Thornber CS, Kinlan BP, Graham MH, Stachowicz JJ (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Mar Ecol Prog Ser 268:69–80CrossRefGoogle Scholar
  60. Tomanek L (2002) The heat-shock response: Its variation, regulation and ecological importance in intertidal gastropods (genus Tegula). Int Comp Biol 42:797–807CrossRefGoogle Scholar
  61. Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: Implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936PubMedGoogle Scholar
  62. Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (Genus Tegula) from different tidal heights. Physol Biochem Zool 73:249–256CrossRefGoogle Scholar
  63. Torres AI, Gil MN, Esteves JL (2004) Nutrient uptake rates by the alien alga Undaria pinnatifida (Pheophyta) (Nuevo Gulf, Patagonia, Argentina) when exposed to diluted sewage effluent. Hydrobiologia 520:1–6CrossRefGoogle Scholar
  64. Underwood AJ (1997) Ecological Experiments: Their Logical Design and Interpretation using Analysis of Variance. Cambridge University Press, CambridgeGoogle Scholar
  65. Uwai S, Nelson W, Neill K, Wang WD, Aguilar-Rosas LE, Boo SM, Kitayama T, Kawai H (2006) Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes - origins and succession of introduced populations. Phycologia 45:687–695CrossRefGoogle Scholar
  66. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Mar Freshw Res 55:223–230CrossRefGoogle Scholar
  67. Vayda ME, Yuan M-L (1994) The heat shock response of an antarctic alga is evident at 5°C. Plant Mol Biol 24:229–233PubMedCrossRefGoogle Scholar
  68. Verlaque M (1994) Inventaire des plantes introduites en Méditerraneé: origine et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23Google Scholar
  69. Viant MR, Werner I, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2003) Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol Biochem 29:159–171CrossRefGoogle Scholar
  70. Viejo RM, Arrontes J, Andrew NL (1995) An experimental evaluation of the effect of wave action on the distribution of Sargassum muticum in northern Spain. Bot Mar 38:437–441Google Scholar
  71. Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437PubMedCrossRefGoogle Scholar
  72. Walker DI, Kendrick GA (1998) Threats to macroalgal diversity: marine habitat destruction and fragmentation, pollution, and introduced species. Bot Mar 41:105–112CrossRefGoogle Scholar
  73. Westwood JT, Clos J, Wu C (1991) Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353:822–827PubMedCrossRefGoogle Scholar
  74. Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Ecology, Evolution, and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations