Cite this paper:
GAO Yaping, JIANG Zengjie, DU Meirong, FANG Jinghui, JIANG Weiwei, FANG Jianguang. Photosynthetic and metabolic responses of eelgrass Zostera marina L. to short-term high-temperature exposure[J]. Journal of Oceanology and Limnology, 2019, 37(1): 199-209

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

GAO Yaping1,3, JIANG Zengjie2,4, DU Meirong2,4, FANG Jinghui2, JIANG Weiwei1,3, FANG Jianguang2,4
1 Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research;Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
3 University of Chinese Academy of Sciences, Beijing 100049, China;
4 Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
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℃ were investigated. The results showed that high temperature induced significant inhibition of photosynthetic efficiency (ΔF/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.
Key words:    high temperature|eelgrass|photosynthetic response|metabolome   
Received: 2017-11-07   Revised: 2018-01-04
Tools
PDF (727 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by GAO Yaping
Articles by JIANG Zengjie
Articles by DU Meirong
Articles by FANG Jinghui
Articles by JIANG Weiwei
Articles by FANG Jianguang
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.
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.
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.
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.
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.
Burke M K, Dennison W C, Moore K A. 1996. Non-structural carbohydrate reserves of eelgrass Zostera marina. Marine Ecology Progress Series, 137:195-201.
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.
Collier C J, Waycott M. 2014. Temperature extremes reduce seagrass growth and induce mortality. Marine Pollution Bulletin, 83(2):483-490.
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.
Dettmer K, Aronov P A, Hammock B D. 2007. Mass spectrometry-based metabolomics. Mass Spectrometry Reviews, 26(1):51-78.
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 galactinol synthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant Physiology and Biochemistry, 49(4):441-448.
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.
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.
Gu J, Weber K, Klemp E, Winters G, Franssen S U, Wienpahl I, Huylmans A K, Zecher K, Reusch T B H, BornbergBauer 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.
Guy C, Kaplan F, Kopka J, Selbig J, Hincha D K. 2008.Metabolomics of temperature stress. Physiologia Plantarum, 132(2):220-235.
Hasegawa N, Hori M, Mukai H. 2008. Seasonal changes in eelgrass functions:current velocity reduction, prevention of sediment resuspension, and control of sediment-water column nutrient flux in relation to eelgrass dynamics.Hydrobiologia, 596(1):387-399.
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.
Jordà G, Marbà N, Duarte C M. 2012. Mediterranean seagrass vulnerable to regional climate warming. Nature Climate Change, 2(11):821-824.
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.
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.
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.
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.
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.
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.
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.
Marbà N, Duarte C M. 2010. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology, 16(8):2 366-2 375.
Marcum K B. 1998. Cell membrane thermostability and whole-plant heat tolerance of Kentucky bluegrass. Crop Science, 38(5):1 214-1 218.
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 Experimental Marine Biology and Ecology, 101(3):257-267.
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). Hydrobiologia 619(1):195-201.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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. Russian Journal of Plant Physiology, 49(3):349-359.
Seifert G J, Roberts K. 2007. The biology of arabinogalactan proteins. Annual Review of Plant Biology, 58:137-161.
Shin H, Cho K H, Oh Y S. 2002. Zostera geojeensis, a new species of seagrass from Korea. Algae, 17(2):71-74.
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.
Short F T, Wyllie-Echeverria S. 1996. Natural and humaninduced disturbance of seagrasses. Environmental Conservation, 23(1):17-27.
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.
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.
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. Indian Journal of Marine Sciences, 39(1):85-91.
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.
Wahid A, Gelani S, Ashraf M, Foolad M R. 2007. Heat tolerance in plants:an overview. Environmental and Experimental Botany, 61(3):199-223.
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.
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.
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.
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.
Copyright © Haiyang Xuebao