Log in

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

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 47:255–258

    Article  Google Scholar 

  • Ambrose RF, Nelson BV (1982) Inhibition of giant kelp recruitment by an introduced brown alga. Bot Mar 25:265–267

    Google Scholar 

  • Arrontes J (2002) Mechanisms of range expansion in the intertidal brown alga Fucus serratus in northern Spain. Mar Biol 141:1059–1067

    Article  Google Scholar 

  • Barton NH (1989) Founder effect speciation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, Mass., pp 229–256

    Google Scholar 

  • 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 30:1071–1079

    Article  CAS  Google Scholar 

  • Battershill C, Miller K, Cole R (1998) The Understorey of Marine Invasions. Seafood NZ 6:31–33

    Google Scholar 

  • Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc B 26:211–252

    Google Scholar 

  • Breeman AM (1988) Relative importance of temperature and other factors in determining geographic boundaries of seaweeds: experimental and phenological evidence. Helgo Meer 42:199–241

    Article  Google Scholar 

  • 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 277:61–78

    Article  Google Scholar 

  • 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 205:3231–3240

    CAS  Google Scholar 

  • 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 77:570–581

    Article  PubMed  CAS  Google Scholar 

  • 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 204:3571–3579

    CAS  Google Scholar 

  • 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 6:411–416

    Article  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • 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 85:175–183

    Article  CAS  Google Scholar 

  • 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 209:2859–2872

    Article  PubMed  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  PubMed  CAS  Google Scholar 

  • 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 47:379–390

    Google Scholar 

  • 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 39:547–553

    Article  Google Scholar 

  • Gacia E, Rodriguez-Prieto C, Delgado O, Ballesteros E (1996) Seasonal light and temperature responses of Caulerpa taxifolia from the northwestern Mediterranean. Aquat Bot 53:215–225

    Article  Google Scholar 

  • 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 63:480–483

    Google Scholar 

  • 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 42:815–824

    Article  CAS  Google Scholar 

  • 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 205:160–169

    Article  PubMed  CAS  Google Scholar 

  • Harris LG, Tyrrell MC (2001) Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol Inv 3:9–21

    Article  Google Scholar 

  • Hay CH, Luckens PA (1987) The Asian Kelp Undaria pinnatifida (Phaeophyta, Laminariales) found in a New Zealand harbor. NZ J Bot 25:329–332

    Google Scholar 

  • Hay CH, Villouta E (1993) Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Bot Mar 36:461–476

    Article  Google Scholar 

  • Heckathorn SA, Poeller GJ, Coleman JS, Hallberg RL (1996) Nitrogen availability alters patterns of accumulation of heat stress-induced proteins in plants. Oecologia 105:413–418

    Article  Google Scholar 

  • Helmuth B (2002) How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Int Comp Biol 42:837–845

    Article  Google Scholar 

  • Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384

    Article  PubMed  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical Adaptation. Oxford University Press, New York

    Google Scholar 

  • Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889–900

    CAS  Google Scholar 

  • 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 198:1509–1518

    PubMed  CAS  Google Scholar 

  • Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392–4397

    Article  PubMed  CAS  Google Scholar 

  • Howarth CJ (1991) Molecular responses of plants to an increased incidence of heat-shock. Plant Cell Environ 14:831–841

    Article  CAS  Google Scholar 

  • 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 9:139–155

    Article  CAS  Google Scholar 

  • Kimpel JA, Key JL (1985) Heat-shock in plants. Trends Biochem Sci 10:353–357

    Article  CAS  Google Scholar 

  • Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larve. Cell Stress Chaperon 2:60–71

    Article  CAS  Google Scholar 

  • Krebs RA, Holbrook SH (2001) Reduced enzyme activity following Hsp70 overexpression in Drosophila melanogaster. Biochem Genet 39:73–82

    Article  PubMed  CAS  Google Scholar 

  • 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 46:421–424

    Article  CAS  Google Scholar 

  • 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 144:205–213

    Article  Google Scholar 

  • 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 143:435–446

    Article  CAS  Google Scholar 

  • Lüning K, Freshwater W (1988) Temperature tolerance of northeast Pacific marine algae. J Phycol 24:310–315

    Google Scholar 

  • Lüning K, Guiry MD, Masuda M (1987) Upper temperature tolerance of North Atlantic and North Pacific geographical isolates of Chondrus crispus (Rhodophyta). Helgo Meer 41:297–306

    Article  Google Scholar 

  • 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 30:1–11

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • 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 327:134–143

    Article  CAS  Google Scholar 

  • Pelham HR (1982) A regulatory upstream promoter element in the Drosophila hsp70 heat-shock gene. Cell 30:517–528

    Article  PubMed  CAS  Google Scholar 

  • 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 315–328

    Google Scholar 

  • Peters AF, Breeman AM (1992) Temperature responses of disjunct temperate brown-algae indicate long-distance dispersal of microthalli across the tropics. J Phycol 28:428–438

    Article  Google Scholar 

  • 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 217–268

    Google Scholar 

  • 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 33:622–630

    Article  Google Scholar 

  • Sanchez I, Fernandez C, Arrontes J (2005) Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Pheophyta). J Phycol 41:942–949

    Article  Google Scholar 

  • 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 22:465–471

    PubMed  Google Scholar 

  • 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 28:277–292

    Article  Google Scholar 

  • 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 179:179–193

    Article  CAS  Google Scholar 

  • Shi Y, Mosser DD, Morimoto RI (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12:654–666

    Article  PubMed  CAS  Google Scholar 

  • 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 4:333–338

    Article  Google Scholar 

  • 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 99:15479–15500

    Article  CAS  Google Scholar 

  • 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 268:69–80

    Article  Google Scholar 

  • Tomanek L (2002) The heat-shock response: Its variation, regulation and ecological importance in intertidal gastropods (genus Tegula). Int Comp Biol 42:797–807

    Article  CAS  Google Scholar 

  • 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 202:2925–2936

    PubMed  Google Scholar 

  • 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 73:249–256

    Article  CAS  Google Scholar 

  • 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 520:1–6

    Article  CAS  Google Scholar 

  • Underwood AJ (1997) Ecological Experiments: Their Logical Design and Interpretation using Analysis of Variance. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 45:687–695

    Article  Google Scholar 

  • 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 55:223–230

    Article  Google Scholar 

  • Vayda ME, Yuan M-L (1994) The heat shock response of an antarctic alga is evident at 5°C. Plant Mol Biol 24:229–233

    Article  PubMed  CAS  Google Scholar 

  • Verlaque M (1994) Inventaire des plantes introduites en Méditerraneé: origine et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23

    Google Scholar 

  • 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 29:159–171

    Article  CAS  Google Scholar 

  • 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 38:437–441

    Google Scholar 

  • 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 102:5432–5437

    Article  PubMed  CAS  Google Scholar 

  • Walker DI, Kendrick GA (1998) Threats to macroalgal diversity: marine habitat destruction and fragmentation, pollution, and introduced species. Bot Mar 41:105–112

    Article  Google Scholar 

  • Westwood JT, Clos J, Wu C (1991) Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353:822–827

    Article  PubMed  CAS  Google Scholar 

  • Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sarah K. Henkel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Henkel, S.K., Hofmann, G.E. Differing patterns of hsp70 gene expression in invasive and native kelp species: evidence for acclimation-induced variation. J Appl Phycol 20, 915–924 (2008). https://doi.org/10.1007/s10811-007-9275-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-007-9275-3

Keywords

Navigation