Establishing research strategies, methodologies and technologies to link genomics and proteomics to seagrass productivity, community metabolism, and ecosystem carbon fluxes
Mazzuca, Silvia; Bjork, M; Beer, Set al.
2013 • In Frontiers in Plant Science, 4 (38), p. 1-19
[en] A complete understanding of the mechanistic basis of marine ecosystem functioning is only possible through integrative and interdisciplinary research.This enables the prediction of change and possibly the mitigation of the consequences of anthropogenic impacts. One major aim of the European Cooperation in Science and Technology (COST) Action ES0609 “Seagrasses productivity. From genes to ecosystem management,” is the calibration and synthesis of various methods and the development of innovative techniques and protocols for studying seagrass ecosystems. During 10 days, 20 researchers representing a range of disciplines (molecular biology, physiology, botany, ecology, oceanography, and underwa- ter acoustics) gathered at The Station de Recherches Sous-marines et Océanographiques (STARESO, Corsica) to study together the nearby Posidonia oceanica meadow. STARESO is located in an oligotrophic area classified as “pristine site” where environmental distur- bances caused by anthropogenic pressure are exceptionally low. The healthy P. oceanica meadow, which grows in front of the research station, colonizes the sea bottom from the surface to 37 m depth. During the study, genomic and proteomic approaches were integrated with ecophysiological and physical approaches with the aim of understanding changes in seagrass productivity and metabolism at different depths and along daily cycles. In this paper we report details on the approaches utilized and we forecast the potential of the data that will come from this synergistic approach not only for P. oceanica but for seagrasses in general.
Establishing research strategies, methodologies and technologies to link genomics and proteomics to seagrass productivity, community metabolism, and ecosystem carbon fluxes
Acunto, S., Rende, F., Cozza, R., and Innocenti, M. (2006). State of health of Posidonia oceanica meadows along the northern Tyrrhenian coast of Calabria, Italy. Biol. Mar. Med. 13, 8-13.
Arnaud-Haond, S., Duarte, C. M., Diaz-Almela, E., Marba, N., Sintes, T., and Serrao, E. A. (2012). Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS ONE 7:30454. doi:10.1371/journal.pone.0030454
Arnaud-Haond, S., Marba, N., Diaz-Almela, E., Serrao, E. A., and Duarte, C. M. (2010). Comparative analysis of stability-genetic diversity in seagrass (Posidonia oceanica) meadows yield unexpected results. Estuar. Coast. 33, 878-888.
Arnaud-Haond, S., Migliaccio, M., Diaz-Almela, E., Teixeira, S., Vliet, M., Alberto, F., et al. (2007). Vicariance patterns in the Mediterranean Sea: East-West cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J. Biogeogr. 34, 963-976.
Arnold, T., Mealey, C., Leahey, H., Whitman Miller, A., Hall-Spencer, J. M., Marco Milazzo, M., et al. (2012). Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE 7:e35107. doi:10.1371/journal.pone.0035107
Bay, D. (1984). A field study of the growth dynamics and productivity of Posidonia oceanica (L.) Delile in Calvi Bay. Aquat. Bot. 20, 43-64.
Beer, S., Axelson, L., and Bjork, M. (2006). Modes of photosynthetic bicarbonate utilization in seagrasses and possible role in the adaptations to specific habitats. Biol. Mar. Med. 1, 3-7.
Beer, S., and Björk, M. (2000). Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry. Aquat. Bot. 66, 69-76.
Beer, S., Vilenkin, B., Weil, A., Veste, M., Susel, L., and Eshel, A. (1998). Measuring photosynthesis in seagrasses by pulse amplitude modulated (PAM) fluorometry. Mar. Ecol. Prog. Ser. 174, 293-300.
Bergmann, N., Winters, G., Rauch, G., Eizaguirre, C., Gu, J., Nelle, P., et al. (2010). Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming. Mol. Ecol. 19, 2870-2883.
Bouck, A., and Vision, T. (2007). The molecular ecologist's guide to expressed sequence tags. Mol. Ecol. 16, 907-924.
Bouderesque, C. F., and Meinesz, A. (1982). Découverte de l'herbier de Posidonie. Cahiers du Parc National de Port-Cros 4, 1-79.
Boudouresque, C. F., Bernard, G., Bonhomme, P., Charbonnel, E., Diviacco, G., Meinesz, A., et al. (2006). Préservation et Conservation des Herbiers à Posidonia oceanica. Monaco: Ramonge pub. 1-202 ISBN 2-905540-30-3
Boudouresque, C. F., Bernard, G., Pergent, G., Shili, A., and Verlaque, M. (2009). Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot. Mar. 52, 395-418.
Champenois, W., and Borges, A. V. (2012). Seasonal and inter-annual variations of community metabolism rates of a Posidonia oceanica seagrass meadow. Limnol. Oceanogr. 57, 347-361.
Dauby, P., and Poulicek, M. (1995). Methods for removing epiphytes from seagrasses: SEM observations on treated leaves. Aquat. Bot. 52, 217-228.
D'Esposito, D., Orsini, L., and Procaccini, G. (in press). Development of 51 novel EST-linked microsatellites in the Mediterranean seagrass Posidonia oceanica. Mar. Ecol. Resour.
Duarte, C. M. (1999). Seagrass ecology at the turn of the millennium: challenges for the new century. Aquat. Bot.65, 7-20.
Ehlers, A., Worm, B., and Reusch, T. B. H. (2008). Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar. Ecol. Prog. Ser. 355, 1-7.
Ferro, M., Brugiere, S., Salvi, D., Seigneurin-Biery, D., Court, M., Moyet, L., et al. (2010). AT_CHLORO: a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteomics 9, 1063-1084.
Filadoro, D. (2007). Protein Biomarkers in Posidonia oceanica Acclimated to Low Light Regime. Ph.D. thesis, Doctorate Research Program in Plant Biology, University of Calabria XX Cycle, Italy.
Finiguerra, A., Spadafora, A., Filadoro, D., and Mazzuca, S. (2010). Surface-activated chemical ionization time-of-flight mass spectrometry and labeling-free approach: two powerful tools for the analysis of complex plant functional proteome profiles. Rapid Commun. Mass Spectrom. 24, 1155-1160.
Franssen, S. U., Gu, J., Bergmann, N., Winters, G., Klostermeier, U. C., Rosenstiel, P., et al. (2011). Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proc. Natl. Acad. Sci. U.S.A. 108, 19276-19281.
Gobert, S., Defawe, O., Lepoint, G., Demoulin, V., and Bouquegneau, J. M. (2001). Anthesis effects on Posidonia oceanica (L.) Delile phenology. Hydrobiologia 455, 121-125.
Gobert, S., Cambridge, M. L., Velimirov, B., Pergent, G., Lepoint, G., Bouquegneau, J. M., et al. (2006). "Biology ofPosidonia, " in Seagrasses: Biology, Ecology and Conservation, eds A. W. D. Larkum, R. J. Orth, and C. M. Duarte (Berlin: Springer Verlag), 387-408.
Gobert, S., Laumont, N., and Bouquegneau, J. M. (2002). Posidonia oceanica meadow: a low nutrient high chlorophyll (LNHC) system? BMC Ecol. 2:9. doi:10.1186/1472-6785-2-9
Gobert, S., Lejeune, P., Chery, A., Boissery, P., Sartoretto, S., Andral, B., et al. (2012). "Assessment of the ecological status of Posidonia oceanica meadow with a "Non Destructive Shoot Method": NDSM, " in Proceedings of the Mediterranean Seagrass Workshop Essaouira, Morocco.
Gobert, S., Sartoretto, S., Rico-Raimondino, V., Andral, A., Chery, B., Lejeune, P., et al. (2009). Assessment of the ecological status of Mediterranean French coastal waters as required by the water framework directive using thePosidonia oceanica rapid easy index: PREI. Mar. Pollut. Bull. 58, 727-733.
Gobert, S. M., Kyramarios, G., Lepoint, C., Pergent-Martini, G., and Bouquegneau, J. M. (2003a). Variations at different spatial scales of Posidonia oceanica (L.) Delile beds; effects on the physico-chemical parameters of the sediment. Oceanol. Acta 26, 199-207.
Gobert, S. O., Defawe, G., Lepoint, V., Demoulin, V., and Bouquegneau, J. M. (2003b). Anthesis effects on Posidonia oceanica (L.) Delile phenology. Hydrobiologia 455, 121-125.
Gu, J., Weber, K., Klemp, E., Winters, G., Franssen, S. U., Wienpahl, I., et al. (2012). Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness. Integr. Biol. (Camb.) 4, 480-493.
Hall-Spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S. M., et al. (2008). Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96-99.
Heber, U., Bligny, R., Streb, P., and Douce, R. (1995). Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight. Bot. Acta. 109, 307-315.
Hemminga, M. A., and Duarte, C. M. (2000). Seagrass Ecology. Cambridge: Cambridge University Press.
Hermand, J. P. (2003). "Acoustic remote sensing of photosynthetic activity, " in Seagrass Beds, Scaling Methods in Aquatic Ecology. Measurement, Analysis, Simulation, eds L. Seuront and P. G. Strutton (Boca Raton, FL: CRC Press LLC), 65-96.
Hermand, J.-P., and Alberotanza, L. (2000). "A novel acoustic tomography experiment in the lagoon of Venice, " inLa Ricerca Scientifica per Venezia. Il Progetto Sistema Lagunare Veneziano. Modellistica del Sistema Lagunare. Studio di Impatto Ambientale, vol. II, part 1.4 (Padova: Atti dell' Istituto Veneto di Science, Lettere ed Arti), 199-222.
Invers, O., Romero, J., and Pérez, M. (1997). Effects of pH on seagrass photosynthesis: a laboratory and field assessment. Aquat. Bot. 59, 185-194.
Jiang, C. Z., and Rodermel, S. R. (1995). Regulation of photosynthesis during leaf development in RbcS antisense DNA mutants of tobacco. Plant Physiol. 107, 215-224.
Kraemer, G. P., Mazzella, L., and Alberte, R. S. (1997). Nitrogen assimilation and partitioning in the Mediterranean seagrass Posidonia oceanica. Mar. Ecol. 18, 175-188.
Lepoint, G., Havelange, S., Gobert, S., and Bouquegneau, J. M. (1999). Fauna v.s. flora contribution to the leaf epiphytes biomass in a Posidonia oceanica seagrass bed (Revellata Bay, Corsica). Hydrobiologia 394, 63-67.
Lepoint, G., Jacquemart, J., Bouquegneau, J. M., Demoulin, V., and Gobert, S. (2007). Field measurments of inorganic nitrogen uptake by different epifloral components colonising the seagrass Posidonia oceanica(Monocotyledon, Posidoniaceae). J. Phycol. 43, 208-218.
Lepoint, G., Millet, S., Dauby, P., Gobert, S. J. M., and Bouquegneau, J. M. (2002). An annual nitrogen budget of the seagrass Posidonia oceanica as determined by in situ uptake experiments. J. Sea Res. 48, 173-179.
Lipkin, Y., Beer, S., Best, E. P. H., Karesalo, T., and Salonen, K. (1986). Primary production of macrophytes. Terminology, approaches and a comparison of methods. Aquat. Bot. 26, 129-142.
Macreadie, P. I., Hindell, J. S., Keough, M. J., Jenkins, G. P., and Connolly, R. M. (2010). Resource distribution influences positive edge effects in a seagrass fish. Ecology 91, 2013-2021.
Massa, A. N., Childs, K. L., Lin, H., Bryan, G. J., Giuliano, G., and Buell, C. R. (2011). The transcriptome of the reference potato genome Solanum tuberosum Group Phureja Clone DM1-3 516R44. PLoS ONE 6:e26801. doi:10.1371/journal.pone.0026801
Mazzuca, S., Filadoro, D., Vannini, C., Marsoni, M., Cozza, R., Bracale, M., et al. (2009). Seagrass light acclimation: 2-DE protein analysis in Posidonia leaves grown in chronic low light conditions. J. Exp. Mar. Biol. Ecol. 374, 113-122.
Medwin, H., and Clay, C. S. (1998). Fundamentals of Acoustical Oceanography. Boston: Academic Press.
Migliaccio, M., De Martino, F., Silvestre, F., and Procaccini, G. (2005). Meadow-scale genetic structure in Posidonia oceanica L. (Delile). Mar. Ecol. Prog. Ser. 304, 55-65.
Modigh, M., Lorenti, M., and Mazzella, L. (1998). Carbon assimilation in Posidonia oceanica: 714 biotic determinants. Bot. Mar. 41, 249-256.
Odum, H. T. (1956). Primary production in flowing waters. Limnol. Oceanogr. 1, 102-117.
Oetjen, K., Ferber, S., Dankert, I., and Resuch, T. B. H. (2010). New evidence for habitat-specific selection in Wadden Sea Zostera marina populations revealed by genome scanning using SNP and microsatellite markers. Mar. Biol. 157, 81-89.
Oetjen, K., and Reusch, T. B. H. (2007). Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol. Ecol. 16, 5156-5157.
Pasqualini, V., Pergent-Martini, C., Clabaut, P., and Pergent, G. (1998). Mapping of Posidonia oceanica using aerial photographs and side-scan sonar: application of the islands of Corsica (France). Estuar. Coast. Shelf Sci. 47, 359-367.
Pergent, G., Bazairi, H., Bianchi, C. N., Boudouresque, C. F., Buia, M. C., Clabaut, P., et al. (2012). Mediterranean Seagrass Meadows: Resilience and Contribution to Climate Change Mitigation, A Short Summary/Les herbiers de Magnoliophytes marines de Méditerranée: Résilience et Contribution à L'atténuation des Changements Climatiques, Résumé. Gland, Switzerland and Málaga. Spain: IUCN.
Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36. doi:10.1093/nar/30.9.e36
Platt, T., Gallegos, C. L., and Harrison, W. G. (1980). Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38, 687-701.
Procaccini, G., Beer, S., Björk, M., Olsen, J., Mazzuca, S., and Santos, R. (2012). Seagrass ecophysiology meets ecological genomics: are we ready? Mar. Ecol. 33, 522-527.
Procaccini, G., Dattolo, E., Innocenti, A. M., Mazzuca, S., Cavallini Natali, A. L., Gu, J., et al. (2010). Differential gene expression profiling under different light conditions in Posidonia oceanica (L.) Delile by SSH analysis. Rapp. Comm. Int. Mer Médit. 39, 641-642.
Procaccini, G., Olsen, J. L., and Reusch, T. B. H. (2007). Contribution of genetics and genomics to seagrass biology and conservation. J. Exp. Mar. Biol. Ecol. 350, 234-259.
Quick, W. P., Schurr, U., Fichtner, K., Schulze, E. D., Rodermel, S. R., Bogorad, L., et al. (1991). The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant J. 1, 51-58.
Reusch, T. B. H., Veron, A., Preuss, C., Weiner, J., Wissler, L., Beck, A., et al. (2008). Comparative analysis of expressed sequence Tag (EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar. Biotechnol. (N.Y.) 10, 297-309.
Reusch, T. B. H., and Wood, T. E. (2007). Molecular ecology of global change. Mol. Ecol. 16, 3973-3992.
Ruggiero, M. V., Turk, R., and Procaccini, G. (2002). Genetic identity and homozygosity of North Adriatic populations in Posidonia oceanica: an ancient post-glacial clone? Conserv. Genet. 3, 71-74.
Runcie, J. W., Paulo, D., Santos, R., Sharon, Y., Beer, S., and Silva, J. (2009). Photosynthetic responses of Halophila stipulacea to a light gradient: I-in situ energy partitioning of non-photochemical quenching. Aquat. Biol. 7, 143-152.
Runcie, J. W., and Riddle, M. J. (2012). Estimating primary productivity of marine macroalgae in East Antarctica using in situ fluorometry. Eur. J. Phycol. 47, 449-460.
Ruocco, M., Brunet, C., Lorenti, M., Lauritano, C., D'Esposito, D., Riccio, M., et al. (2012). Posidonia oceanicaphotoadaptation to the depth gradient. Biol. Mar. Med. 19, 63-64.
Schulze, W. X., and Usadel, B. (2010). Quantitation in mass-spectrometry-based proteomics. Annu. Rev. Plant Biol.61, 491-516.
Serra, I. A., Innocenti, A. M., Di Maida, G., Calvo, S., Migliaccio, M., Zambianchi, E., et al. (2010). Genetic structure in the Mediterranean seagrass Posidonia oceanica: disentangling past vicariance events from contemporary patterns of gene flow. Mol. Ecol. 19, 557-568.
Serra, I. A., Lauritano, C., Dattolo, E., Puoti, A., Nicastro, S., Innocenti, A. M., et al. (2012). Reference genes assessment for the seagrass Posidonia oceanica in different salinity, pH and light conditions. Mar. Biol. 159, 1269-1282.
Serra, I. A., and Mazzuca, S. (2011). "Posidonia oceanica: from ecological status to genetic and proteomic resources", in Seagrass: Ecology, Uses and Threats, ed. R. S. Pirog (New York: Nova Science Publishers), 71-116.
Spadafora, A., Filadoro, D., Mazzuca, S., Bracale, M., Marsoni, M., Cardilio, M., et al. (2008). 2-DE polypeptide mapping of Posidonia oceanica leaves, a molecular tool for marine environment studies. Plant Biosyst. 142, 213-218.
The Royal Society. (2005). Ocean Acidification due to Increasing Atmospheric Carbon Dioxide. Policy Document 12/05. London: The Royal Society.
Tomasello, A., Di Maida, G., Calvo, S., Pirrotta, M., Borra, M., and Procaccini, G. (2009). Seagrass meadows at the extreme of environmental tolerance: the case of P. oceanica in a semi-enclosed coastal lagoon. Mar. Ecol. 30, 288-300.
Van der Ben, D. (1971). Les epiphytes des feuilles de P. oceanica (L.) Delile sur les côtes françaises de la Méditerranée. Mem. Inst. R. Sci. Nat. Belg. 168, 1-101.
Vogel, C., and Marcotte, E. M. (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227-232.
Webb, W. L., Newron, M., and Starr, D. (1974). Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17, 281-291.
Wilson, C. J., Wilson, P. S., Greene, C. A., and Dunton, K. H. (2012). Seagrass meadows provide an acoustic refuge for estuarine fish. Mar. Biol. 159, 2311-2322.
Wilson, O. B. (1988). An Introduction to the Theory and Design of Underwater Transducers. Los Altos, CA: Peninsula Publishing.
Winters, G., Nelle, P., Fricke, B., Rauch, G., and Reusch, T. B. H. (2011). Effects of a simulated heat wave on photophysiology and gene expression of high-and low-latitude populations of Zostera marina. Marine Ecology Progress Series 435, 83-95.
Wissler, L., Codoñer, F. M., Reusch, T. B. H., Olsen, J. L., Procaccini, G., and Bornberg-Bauer, E. (2011). Back to the Sea twice: identifying candidate plant genes for molecular evolution to marine life. BMC Evol. Biol. 11:8. doi:10.1186/1471-2148-11-8
Wissler, L., Dattolo, E., Moore, A. D., Olsen, J. L., Migliaccio, M., Bornberg-Bauer, E., et al. (2009). Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs. Database doi:10.1093/database/bap009
Zhang, W. B., and Wang, L. (2009). Label-free quantitative proteome analysis of skeletal tissues under mechanical load. J. Cell. Biochem. 108, 600-611.