Skip to main content

Advertisement

Log in

Photosynthetic and metabolic responses of eelgrass Zostera marina L. to short-term high-temperature exposure

  • Biology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

In recent years, extreme heat events have occurred worldwide and the ocean temperature has been rising, causing stress on the photosynthesis and growth of seagrass. Metabolomics enables detection of metabolic changes under environmental stress. In this study, the photosynthetic physiology and metabolic changes of the eelgrass Zostera marina L. in response to 48 h exposure to 32°C were investigated. The results showed that high temperature induced significant inhibition of photosynthetic efficiency (Δ F / F′m ) (23.9% lower than the control), enhanced respiration (58.3% higher), and decreased carbohydrate decomposition products and tricarboxylic acid (TCA) cycle intermediate products, indicating that the energy supply of the eelgrass may be insufficient at high temperature. In addition, high temperature decreased stearic acid and linoleic acid in eelgrass, suggesting the composition of the membrane system of eelgrass may change at high temperature and implying that high temperature may cause the membrane system to be unstable.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ashraf M, Saeed M M, Qureshi M J. 1994. Tolerance to high temperature in cotton ( Gossypium hirsutum L.) at initial growth stages. Environmental and Experimental Botany, 34 (3): 275–283.

    Article  Google Scholar 

  • Behl R K, Moawad A M, Achtnich W. 1991. Amino acid and protein profile changes in a spring wheat mutant under prolonged heat stress. Annals of Biology, 7: 63–68.

    Google Scholar 

  • Bertelli C M, Unsworth R K F. 2014. Protecting the hand that feeds us: seagrass ( Zostera marina ) serves as commercial juvenile fish habitat. Marine Pollution Bulletin, 83 (2): 425–429.

    Article  Google Scholar 

  • Boström C, Baden S, Bockelmann A C, Dromph K, Fredriksen S, Gustafsson C, Krause–Jensen D, Möller T, Nielsen S L, Olesen B, Olsen J, Pihl L, Rinde E. 2014. Distribution, structure and function of Nordic eelgrass ( Zostera marina ) ecosystems: implications for coastal management and conservation. Aquatic Conservation: Marine and Freshwater Ecosystems, 24 (3): 410–434.

    Article  Google Scholar 

  • Boudouresque C F, Bernard G, Pergent G, Shili A, Verlaque M. 2009. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Botanica Marina, 52 (5): 395–418.

    Article  Google Scholar 

  • Burke M K, Dennison W C, Moore K A. 1996. Non–structural carbohydrate reserves of eelgrass Zostera mar ina. Marine Ecology Progress Series, 137: 195–201.

    Article  Google Scholar 

  • Collier C J, Uthicke S, Waycott M. 2011. Thermal tolerance of two seagrass species at contrasting light levels: implications for future distribution in the Great Barrier Reef. Limnology and Oceanography, 56 (6): 2 200–2 210.

    Article  Google Scholar 

  • Collier C J, Waycott M. 2014. Temperature extremes reduce seagrass growth and induce mortality. Marine Pollution Bulletin, 83 (2): 483–490.

    Article  Google Scholar 

  • Connolly R M, Hindell J S, Gorman D. 2005. Seagrass and epiphytic algae support nutrition of a fisheries species, Sillago schomburgkii, in adjacent intertidal habitats. Marine Ecology Progress Series, 286: 69–79.

    Article  Google Scholar 

  • Dettmer K, Aronov P A, Hammock B D. 2007. Mass spectrometry–based metabolomics. Mass Spectrometry Reviews, 26 (1): 51–78.

    Article  Google Scholar 

  • dos Santos, T B, Budzinski I G F, Marur C J, Petkowicz C L O, Pereira L F P, Vieira L G E. 2011. Expression of three galactinolsynthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant Physiology and Biochemistry, 49 (4): 441–448.

    Article  Google Scholar 

  • Erban A, Schauer N, Fernie A R, Kopka J. 2007. Nonsupervised construction and application of mass spectral and retention time index libraries from time–of–flight gas chromatography–mass spectrometry metabolite profiles. In: Weckwerth W ed. Metabolomics: Methods and Protocols. Humana Press, Clifton County, NJ, USA. 358: p.19–38.

    Book  Google Scholar 

  • Gao Y, Fang J, Du M, Fang J, Jiang W, Jiang Z. 2017. Response of the eelgrass ( Zostera marina L.) to the combined effects of high temperatures and the herbicide, atrazine. Aquatic Botany, 142: 41–47.

    Article  Google Scholar 

  • Gu J, Weber K, Klemp E, Winters G, Franssen S U, Wienpahl I, Huylmans A K, Zecher K, Reusch T B H, Bornberg–Bauer E, Weber A P M. 2012. Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness. Integrative Biology, 4 (5): 480–493.

    Article  Google Scholar 

  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha D K. 2008. Metabolomics of temperature stress. Physiologia Plantarum, 132 (2): 220–235.

    Google Scholar 

  • Hasegawa N, Hori M, Mukai H. 2008. Seasonal changes in eelgrass functions: current velocity reduction, prevention of sediment resuspension, and controlof sediment–water column nutrient flux in relation to eelgrass dynamics. Hydrobiologia, 596 (1): 387–399.

    Article  Google Scholar 

  • Heck Jr K L, Hays G, Orth R J. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series, 253: 123–136.

    Article  Google Scholar 

  • Jordà G, Marbà N, Duarte C M. 2012. Mediterranean seagrass vulnerable to regional climate warming. Nature Climate Change, 2 (11): 821–824.

    Article  Google Scholar 

  • Joshi V, Joung J G, Fei Z J, Jander G. 2010. Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids, 39 (4): 933–947.

    Article  Google Scholar 

  • Kaplan F, Kopka J, Haskell D W, Zhao W, Schiller K C, Gatzke N, Sung D Y, Guy C L. 2004. Exploring the temperaturestress metabolome of Arabidopsis. Plant Physiology, 136 (4): 4 159–4 168.

    Article  Google Scholar 

  • Kim J B, Lee W C, Lee K S, Park J I. 2013. Growth dynamics of eelgrass, Zostera marina, in the intertidal zone of Seomjin Estuary, Korea. Ocean Science Journal, 48 (3): 239–250.

    Article  Google Scholar 

  • Larkindale J, Huang B R. 2004. Changes of lipid composition and saturation level in leaves and roots for heat–stressed and heat–acclimated creeping bentgrass ( Agrostis stolonifera ). Environmental and Experimental Botany, 51 (1): 57–67.

    Article  Google Scholar 

  • Lee K S, Park S R, Kim Y K. 2007. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. Journal of Experimental Marine Biology and Ecology, 350 (1–2): 144–175.

    Article  Google Scholar 

  • Lepoint G, Cox A S, Dauby P, Poulicek M, Gobert S. 2006. Food sources of two detritivore amphipods associated with the seagrass Posidonia oceanica leaf litter. Marine Biology Research, 2 (5): 355–365.

    Article  Google Scholar 

  • Liu X, Yang J H, Li B, Yang X M, Meng Q W. 2010. Antisense expression of tomato chloroplast omega–3 fatty acid desaturase gene ( LeFAD7 ) enhances the tomato hightemperature tolerance through reductions of trienoic fatty acids and alterations of physiological parameters. Photosynthetica, 48 (1): 59–66.

    Article  Google Scholar 

  • Marbà N, Duarte C M. 2010. Mediterranean warming triggers seagrass ( Posidonia oceanica ) shoot mortality. Global Change Biology, 16 (8): 2 366–2 375.

    Article  Google Scholar 

  • Marcum K B. 1998. Cell membrane thermostability and whole–plant heat tolerance of Kentucky bluegrass. Crop Science, 38 (5): 1 214–1 218.

    Article  Google Scholar 

  • Marsh Jr J A, Dennison W C, Alberte R S. 1986. Effects of temperature on photosynthesis and respiration in eelgrass ( Zostera marina L.). Journal of Experiment al Marine Biology and Ecology, 101 (3): 257–267.

    Article  Google Scholar 

  • Massa S I, Arnaud–Haond S, Pearson G A, Serrão E A. 2009. Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in Southern Europe (Ria Formosa, Portugal). Hydrobiolog ia 619 (1): 195–201.

    Article  Google Scholar 

  • Micheli F, Bishop M J, Peterson C H, Rivera J. 2008. Alteration of seagrass species composition and function over two decades. Ecological Monographs, 78 (2): 225–244.

    Article  Google Scholar 

  • Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K. 2000. Trienoic fatty acids and plant tolerance of high temperature. Science, 287 (5452): 476–479.

    Article  Google Scholar 

  • Nambara E, Kawaide H, Kamiya Y, Naito S. 1998. Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA–dependent and ABA–independent accumulation of free amino acids during dehydration. Plant and Cell Physiology, 39 (8): 853–858.

    Article  Google Scholar 

  • Paulsen G M. 1994. High temperature responses of crop plants. In: Boote K J, Bennett J M, Sinclair T R, Paulsen G M eds. Physiology and Determination of Crop Yield. ASA, CSSA, SSSA, Madison, WI. p.365–389.

  • Pedersen O, Colmer T D, Borum J, Zavala–Perez A, Kendrick G A. 2016. Heat stress of two tropical seagrass species during low tides–impact on underwater net photosynthesis, dark respiration and diel in situ internal aeration. New Phytologist, 210 (4): 1 207–1 218.

    Article  Google Scholar 

  • Peterson T C, Heim Jr R R, Hirsch R, Kaiser D P, Brooks H, Diffenbaugh N S, Dole R M, Giovannettone J P, Guirguis K, Karl T R, Katz R W, Kunkel K, Lettenmaier D, McCabe G J, Paciorek C J, Ryberg K R, Schubert S, Silva V B S, Stewart B C, Vecchia A V, Villarini G, Vose R S, Walsh J, Wehner M, Wolock D, Wolter K, Woodhouse C A, Wuebbles D. 2013. Monitoring and understanding changes in heat waves, cold waves, floods, and droughts in the United States: state of knowledge. Bulletin of the American Meteorological Society, 94 (6): 821–834.

    Article  Google Scholar 

  • Ralph P J, Tomasko D, Moore K, Seddon S, Macinnis–Ng C M O. 2007. Human impacts on seagrasses: eutrophication, sedimentation, and contamination. In: Larkum A W D, Orth R J, Duarte C M eds. SEAGRASSES: Biology, Ecology and Conservation. Springer, Dordrecht, Netherlands. p.567–593.

  • Rasheed M A, Dew K R, McKenzie L J, Coles R G, Kerville S P, Campbell S J. 2008. Productivity, carbon assimilation and intra–annual change in tropical reef platform seagrass communities of the Torres Strait, north–eastern Australia. Continental Shelf Research, 28 (16): 2 292–2 303.

    Article  Google Scholar 

  • Rasheed M A, Unsworth R K F. 2011. Long–term climateassociated dynamics of a tropical seagrass meadow: implications for the future. Marine Ecology Progress Series, 422: 93–103.

    Article  Google Scholar 

  • Reusch T B H, Ehlers A, Hämmerli A, Worm B. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America, 102 (8): 2826–2831.

    Article  Google Scholar 

  • Ribeiro P R, Fernandez L G, De Castro R D, Ligterink W, Hilhorst H W. 2014. Physiological and biochemical responses of Ricinus communis seedlings to different temperatures: a metabolomics approach. BMC Plant Biology, 14: 223.

    Article  Google Scholar 

  • Savchenko G E, Klyuchareva E A, Abramchik L M, Serdyuchenko E V. 2002. Effect of periodic heat shock on the inner membrane system of etioplasts. Russ ian Journal of Plant Physiology, 49 (3): 349–359.

    Article  Google Scholar 

  • Seifert G J, Roberts K. 2007. The biology of arabinogalactan proteins. Annual Review of Plant Biology, 58: 137–161.

    Article  Google Scholar 

  • Shin H, Cho K H, Oh Y S. 2002. Zostera geojeensis, a new species of seagrass from Korea. Algae, 17 (2): 71–74.

    Article  Google Scholar 

  • Short F T, Polidoro B, Livingstone S R, Carpenter K E, Bandeira S, Bujang J S, Calumpong H P, Carruthers T J B, Coles R G, Dennison W C, Erftemeijer P L A, Fortes M D, Freeman A S, Jagtap T G, Kamal A H M, Kendrick G A, Kenworthy W J, La Nafie Y A, Nasution I M, Orth R J, Prathep A, Sanciangco J C, van Tussenbroek B, Vergara S G, Waycott M, Zieman J C. 2011. Extinction risk assessment of the world’s seagrass species. Biological Conservation, 144 (7): 1 961–1 971.

    Article  Google Scholar 

  • Short F T, Wyllie–Echeverria S. 1996. Natural and humaninduced disturbance of seagrasses. Environmental Conservation, 23 (1): 17–27.

    Article  Google Scholar 

  • Simon–Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde J A. 2006. Stress–induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biologia Plantarum, 50 (4): 793–796.

    Article  Google Scholar 

  • Sohn S O, Back K. 2007. Transgenic rice tolerant to high temperature with elevated contents of dienoic fatty acids. Biologia Plantarum, 51 (2): 340–342.

    Article  Google Scholar 

  • Thangaradjou T, Nobi E P, Dilipan E, Sivakumar K, Susila S. 2010. Heavy metal enrichment in seagrasses of Andaman Islands and its implication to the health of the coastal ecosystem. India n Journal of Marine Sciences, 39 (1): 85–91.

    Google Scholar 

  • Triba M N, Le Moyec L, Amathieu R, Goossens C, Bouchemal N, Nahon P, Rutledge D N, Savarin P. 2015. PLS/OPLS models in metabolomics: the impact of permutation of dataset rows on the K–fold cross–validation quality parameters. Molecular BioSystems, 11 (1): 13–19.

    Article  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad M R. 2007. Heat tolerance in plants: an overview. Environmental and Experimental Botany, 61 (3): 199–223.

    Article  Google Scholar 

  • Waycott M, Duarte C M, Carruthers T J B, Orth R J, Dennison W C, Olyarnik S, Calladine A, Fourqurean J W, Heck Jr K L, Hughes A R, Kendrick G A, Kenworthy W J, Short F T, Williams S L, Paine R T. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106 (30): 12 377–12 381.

    Article  Google Scholar 

  • Waycott M, McKenzie L, Mellors J E, Ellison J C, Sheaves M T, Collier C, Schwarz A M, Webb A, Johnson J E, Payri C E. 2011. Vulnerability of mangroves, seagrasses and intertidal flats in the tropical Pacific to climate change. In: Bell J D, Johnson J E, Hobday A J eds. Vulnerability of Tropical Pacific Fisheries and Aquaculture to Climate Change. Secretariat of the Pacific Community, Noumea, New Caledonia. p.297–368.

  • Xu Y, Du H M, Huang B R. 2013. Identification of metabolites associated with superior heat tolerance in thermal bentgrass through metabolic profiling. Crop Science, 53 (4): 1 626–1 635.

    Article  Google Scholar 

  • Yamakawa H, Hakata M. 2010. Atlas of rice grain fillingrelated metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant and Cell Physiology, 51 (5): 795–809.

    Article  Google Scholar 

  • Zimmerman R C, Smith R D, Alberte R S. 1989. Thermal acclimation and whole–plant carbon balance in Zostera marina L. (eelgrass). Journal of Experimental Marine Biology and Ecology, 130 (2): 93–109.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianguang Fang.

Additional information

Supported by the National Natural Science Foundation of China (Nos. 41306117, 41676147, U1405234) and the International Science & Technology Cooperation Program of China (No. 2016YFE0112600)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Y., Jiang, Z., Du, M. et al. Photosynthetic and metabolic responses of eelgrass Zostera marina L. to short-term high-temperature exposure. J. Ocean. Limnol. 37, 199–209 (2019). https://doi.org/10.1007/s00343-019-7319-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-7319-6

Keyword

Navigation