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Low oxygen affects photophysiology and the level of expression of two-carbon metabolism genes in the seagrass Zostera muelleri

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Abstract

Seagrasses are a diverse group of angiosperms that evolved to live in shallow coastal waters, an environment regularly subjected to changes in oxygen, carbon dioxide and irradiance. Zostera muelleri is the dominant species in south-eastern Australia, and is critical for healthy coastal ecosystems. Despite its ecological importance, little is known about the pathways of carbon fixation in Z. muelleri and their regulation in response to environmental changes. In this study, the response of Z. muelleri exposed to control and very low oxygen conditions was investigated by using (i) oxygen microsensors combined with a custom-made flow chamber to measure changes in photosynthesis and respiration, and (ii) reverse transcription quantitative real-time PCR to measure changes in expression levels of key genes involved in C4 metabolism. We found that very low levels of oxygen (i) altered the photophysiology of Z. muelleri, a characteristic of C3 mechanism of carbon assimilation, and (ii) decreased the expression levels of phosphoenolpyruvate carboxylase and carbonic anhydrase. These molecular-physiological results suggest that regulation of the photophysiology of Z. muelleri might involve a close integration between the C3 and C4, or other CO2 concentrating mechanisms metabolic pathways. Overall, this study highlights that the photophysiological response of Z. muelleri to changing oxygen in water is capable of rapid acclimation and the dynamic modulation of pathways should be considered when assessing seagrass primary production.

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References

  • Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of Real-Time Quantitative Reverse Transcription-PCR Data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250. doi:10.1158/0008-5472.can-04-0496

    Article  CAS  PubMed  Google Scholar 

  • Anderson M, Gorley RN, Clarke RK (2008) Permanova+ for primer: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059. doi:10.1093/jxb/err012

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. doi:10.1146/annurev.arplant.59.032607.092759

    Article  CAS  PubMed  Google Scholar 

  • Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: photorespiration and chlororespiration. Photosynthesis in algae. Springer, New York, pp 157–181

  • Beck MW et al (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51:633–641

    Article  Google Scholar 

  • Beer S, Rehnberg J (1997) The acquisition of inorganic carbon by the seagrass Zostera marina. Aquat Bot 56:277–283

    Article  CAS  Google Scholar 

  • Beer S, Wetzel RG (1981) Photosynthetic carbon metabolism in the submerged aquatic angiosperm Scirpus subterminalis. Plant Sci Lett 21:199–207

    Article  CAS  Google Scholar 

  • Beer S, Eshel A, Waisel Y (1977) Carbon metabolism in seagrasses I. The utilization of exogenous inorganic carbon species in photosynthesis. J Exp Bot 28:1180–1189

    Article  CAS  Google Scholar 

  • Beer S, Shomer-Ilan A, Waisel Y (1980) Carbon metabolism in seagrasses II. Patterns of photosynthetic CO2 incorporation. J Exp Bot 31:1019–1026

    Article  CAS  Google Scholar 

  • Beer S, Vilenkin B, Weil A, Veste M, Susel L, Eshel A (1998) Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry. Mar Ecol Prog Ser 174:293–300

    Article  CAS  Google Scholar 

  • Beer S, Larsson C, Poryan O, Axelsson L (2000) Photosynthetic rates of Ulva (Chlorophyta) measured by pulse amplitude modulated (PAM) fluorometry. Eur J Phycol 35:69–74. doi:10.1080/09670260010001735641

    Article  Google Scholar 

  • Beer S, Bjork M, Hellblom F, Axelsson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29:349–354

    Article  CAS  Google Scholar 

  • Benedict CR, Scott JR (1976) Photosynthetic carbon metabolism of a marine grass. Plant Physiol 57:876–880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Björk M, Haglund K, Ramazanov Z, Pedersén M (1993) Inducible mechanisms for HCO3 utilization and repression of photorespiration in protoplasts and thalli of three species of Ulva (Chlorophyta). J Phycol 29:166–173. doi:10.1111/j.0022-3646.1993.00166.x

    Article  Google Scholar 

  • Björk M, Weil A, Semesi S, Beer S (1997) Photosynthetic utilisation of inorganic carbon by seagrasses from Zanzibar, East Africa. Mar Biol 129:363–366

    Article  Google Scholar 

  • Black C, Burris J, Everson R (1976) Influence of oxygen concentration on photosynthesis in marine plants. Funct Plant Biol 3:81–86. doi:10.1071/PP9760081

    CAS  Google Scholar 

  • Blandon A, Zu Ermgassen PS (2014) Quantitative estimate of commercial fish enhancement by seagrass habitat in southern Australia. Estuar Coast Shelf Sci 141:1–8

    Article  Google Scholar 

  • Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden CJ (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158. doi:10.1111/j.1365-2745.2004.00943.x

    Article  CAS  Google Scholar 

  • Borum J, Pedersen O, Kotula L, Fraser MW, Statton J, Colmer TD, Kendrick GA (2016) Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant Cell Environ 39:1240–1250. doi:10.1111/pce.12658

    Article  CAS  PubMed  Google Scholar 

  • Bowes G, Salvucci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34:233–266

    Article  CAS  Google Scholar 

  • Braun HP, Zabaleta E (2007) Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiol Plant 129:114–122

    Article  CAS  Google Scholar 

  • Brodersen KE, Nielsen DA, Ralph PJ, Kühl M (2014) A split flow chamber with artificial sediment to examine the below-ground microenvironment of aquatic macrophytes. Mar Biol 161:2921–2930. doi:10.1007/s00227-014-2542-3

    Article  Google Scholar 

  • Brodersen KE, Lichtenberg M, Paz L-C, Kühl M (2015) Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue. Front Mar Sci 2:58

    Article  Google Scholar 

  • Brodersen KE et al. (2017) Sediment resuspension and deposition on seagrass leaves impedes internal plant aeration and promotes phytotoxic H2S intrusion. Front Plant Sci. doi:10.3389/fpls.2017.00657

    PubMed  PubMed Central  Google Scholar 

  • Buapet P, Björk M (2016) The role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L. Photosynth Res 129:1–11

    Article  Google Scholar 

  • Buapet P, Rasmusson LM, Gullström M, Björk M (2013) Photorespiration and carbon limitation determine productivity in temperate seagrasses. PLoS ONE 8:e83804

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulmer R, Kelly S, Jeffs A (2016) Light requirements of the seagrass, Zostera muelleri, determined by observations at the maximum depth limit in a temperate estuary, New Zealand. N Z J Mar Freshwat Res 50:1–12

    Article  Google Scholar 

  • Bustin SA et al (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Carlson P, Yarbro L, Sargent W, Arnold H (1988) Hypoxic stress in Thalassia testudinum: evidence from diurnal changes in rhizome gas composition. Eos 69:733–746

    Google Scholar 

  • Chartrand KM, Bryant CV, Carter AB, Ralph PJ, Rasheed MA (2016) Light thresholds to prevent dredging impacts on the Great Barrier Reef seagrass, Zostera muelleri ssp. capricorni. Front Mar Sci 3:106

    Article  Google Scholar 

  • Chi S, Wu S, Yu J, Wang X, Tang X, Liu T (2014) Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes. PLoS ONE 9:e110154

    Article  PubMed  PubMed Central  Google Scholar 

  • Chollet R, Vidal J, O’Leary MH (1996) Phosphoenol pyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Biol 47:273–298

    Article  CAS  Google Scholar 

  • Colman B, Norman EG (1997) Serine synthesis in cyanobacteria by a nonphotorespiratory pathway. Physiol Plant 100:133–136

    Article  CAS  Google Scholar 

  • Costanza R et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Del Prete S, Vullo D, Fisher GM, Andrews KT, Poulsen S-A, Capasso C, Supuran CT (2014) Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum—the η-carbonic anhydrases. Bioorg Med Chem Lett 24:4389–4396

    Article  PubMed  Google Scholar 

  • Downton W, Bishop D, Larkum AWD, Osmond C (1976) Oxygen inhibition of photosynthetic oxygen evolution in marine plants. Funct Plant Biol 3:73–79

    Google Scholar 

  • Drechsler Z, Beer S (1991) Utilization of inorganic carbon by Ulva lactuca. Plant Physiol 97:1439–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Figueroa FL, Jerez CG, Korbee N (2013) Use of in vivo chlorophyll fluorescence to estimate photosynthetic activity and biomass productivity in microalgae grown in different culture systems. Lat Am J Aquat Res 41:801–819. doi:10.3856/vol41-issue5-fulltext-1

    Article  Google Scholar 

  • Fourqurean JW et al (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–509

    Article  CAS  Google Scholar 

  • Greiner JT, McGlathery KJ, Gunnell J, McKee BA (2013) Seagrass restoration enhances “blue carbon” sequestration in coastal waters. PloS one 8:e72469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greve TM, Borum J, Pedersen O (2003) Meristematic oxygen variability in eelgrass (Zostera marina). Limnol Oceanogr 48:210–216. doi:10.4319/lo.2003.48.1.0210

    Article  Google Scholar 

  • Harlin MM (1995) Changes in major plant groups following nutrient enrichment. Eutrophic Shallow Estuaries and Lagoons CRC Press, Inc, Boca Raton, pp 173–187

    Google Scholar 

  • Hellblom F, Axelsson L (2003) External HCO3 dehydration maintained by acid zones in the plasma membrane is an important component of the photosynthetic carbon uptake in Ruppia cirrhosa. Photosynth Res 77:173–181

    Article  CAS  PubMed  Google Scholar 

  • Hellblom F, Beer S, Björk M, Axelsson L (2001) A buffer sensitive inorganic carbon utilisation system in Zostera marina. Aquat Bot 69:55–62

    Article  CAS  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Invers O, Zimmerman RC, Alberte RS, Perez M, Romero J (2001) Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. J Exp Mar Biol Ecol 265:203–217

    Article  CAS  Google Scholar 

  • Jiménez C, Niell FX, Algarra P (1987) Photosynthetic adaptation of Zostera noltii Hornem. Aquat Bot 29:217–226

    Article  Google Scholar 

  • Jørgensen BB, Revsbech NP (1985) Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol Oceanogr 30:111–122. doi:10.4319/lo.1985.30.1.0111

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biol 19:103–132

    Article  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  CAS  PubMed  Google Scholar 

  • Kühl M, Cohen Y, Dalsgaard T, Jørgensen B, Revsbech NP (1995) The microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Article  Google Scholar 

  • Larkum A, den Hartog C (1989) Evolution and biogeography of seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses, 1 edn. Elsevier Pub Co, Amsterdam, pp 112–156

    Google Scholar 

  • Larkum A, Davey P, Kuo J, Ralph P, Raven J (2017) Carbon-concentrating mechanisms in seagrasses. J Exp Bot 68:3773–3784. doi:10.1093/jxb/erx206

    Article  PubMed  Google Scholar 

  • Larsson C, Lennart A, Ryberg H, Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur J Phycol 32:49–54. doi:10.1080/09541449710001719365

    Article  Google Scholar 

  • Lee H et al. (2016) The genome of a southern hemisphere seagrass species (Zostera muelleri). Plant Physiol 172:272–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22:443–463

    Article  Google Scholar 

  • Lichtenberg M, Kühl M (2015) Pronounced gradients of light, photosynthesis and O2 consumption in the tissue of the brown alga Fucus serratus. New Phytol 207:559–569. doi:10.1111/nph.13396

    Article  CAS  PubMed  Google Scholar 

  • Long MH, McGlathery KJ, Zieman JC, Berg P (2008) The role of organic acid exudates in liberating phosphorus from seagrass-vegetated carbonate sediments. Limnol Oceanogr 53:2616–2626. doi:10.4319/lo.2008.53.6.2616

    Article  CAS  Google Scholar 

  • Martin V et al (2009) Recombinant plant gamma carbonic anhydrase homotrimers bind inorganic carbon. FEBS Lett 583:3425–3430. doi:10.1016/j.febslet.2009.09.055

    Article  CAS  PubMed  Google Scholar 

  • Mass T, Genin A, Shavit U, Grinstein M, Tchernov D (2010) Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. Proc Natl Acad Sci USA 107:2527–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLeod E et al (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560. doi:10.1890/110004

    Article  Google Scholar 

  • Millhouse J, Strother S (1986a) The effect of pH on the inorganic carbon source for photosynthesis in the seagrass Zostera muelleri Irmisch ex Aschers. Aquat Bot 24:199–209

    Article  CAS  Google Scholar 

  • Millhouse J, Strother S (1986b) Salt-stimulated bicarbonate-dependent photosynthesis in the marine angiosperm Zostera muelleri. J Exp Bot 37:965–976

    Article  CAS  Google Scholar 

  • Olsen JL et al (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331–335

    Article  CAS  PubMed  Google Scholar 

  • Papenbrock J (2012) Highlights in seagrasses’ phylogeny, physiology, and metabolism: what makes them special? ISRN Bot. doi:10.5402/2012/103892

    Google Scholar 

  • Pedersen O, Colmer TD, Borum J, Zavala-Perez A, Kendrick GA (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 Phytol 210:1207–1218. doi:10.1111/nph.13900

    Article  CAS  PubMed  Google Scholar 

  • Penhale PA, Wetzel RG (1983) Structural and functional adaptations of eelgrass (Zostera marina L.) to the anaerobic sediment environment. Can J Bot 61:1421–1428

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45–e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierrot D, Lewis E, Wallace D (2006) MS Excel program developed for CO2 system calculations: ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge

    Google Scholar 

  • Pregnall A, Smith R, Kursar TA, Alberte R (1984) Metabolic adaptation of Zostera marina (eelgrass) to diurnal periods of root anoxia. Mar Biol 83:141–147

    Article  CAS  Google Scholar 

  • Procaccini G, Olsen JL, Reusch TB (2007) Contribution of genetics and genomics to seagrass biology and conservation. J Exp Mar Biol Ecol 350:234–259

    Article  CAS  Google Scholar 

  • Radonić A, Thulke S, Mackay IM, Landt O, Siegert W, Nitsche A (2004) Guideline to reference gene selection for quantitative real-time PCR. Biochem Biophys Res Commun 313:856–862

    Article  PubMed  Google Scholar 

  • Ralph P, Durako MJ, Enriquez S, Collier C, Doblin M (2007) Impact of light limitation on seagrasses. J Exp Mar Biol Ecol 350:176–193

    Article  Google Scholar 

  • Raven JA (1984) Energetics and transport in aquatic plants. A.R. Liss, New York

    Google Scholar 

  • Raven JA (2014) Speedy small stomata? J Exp Bot 65:1415–1424. doi:10.1093/jxb/eru032

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Beardall J (2016) The ins and outs of CO2. J Exp Bot 67:1–13. doi:10.1093/jxb/erv451

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of isotopes of carbon in plants. New Phytol 116:505–529

    Article  CAS  Google Scholar 

  • Roberts DG, Moriarty DJW (1987) Lacunal gas discharge as a measure of productivity in the seagrasses Zostera capricorni, Cymodocea serrulata and Syringodium isoetifolium. Aquat Bot 28:143–160. doi:10.1016/0304-3770(87)90036-2

    Article  Google Scholar 

  • Sánchez R, Cejudo FJ (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132:949–957

    Article  PubMed  PubMed Central  Google Scholar 

  • Schliep M, Pernice M, Sinutok S, Bryant C, York P, Rasheed M, Ralph P (2015) Evaluation of reference genes for RT-qPCR studies in the seagrass Zostera muelleri exposed to light limitation. Sci Rep 5:17051. doi:10.1038/srep17051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwarz AM (2004) Contribution of photosynthetic gains during tidal emersion to production of Zostera capricorni in a North Island, New Zealand estuary. N Z J Mar Freshwat Res 38:809–818

    Article  Google Scholar 

  • Short FT et al (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144:1961–1971. doi:10.1016/j.biocon.2011.04.010

    Article  Google Scholar 

  • Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56:1200–1212. doi:10.4319/lo.2011.56.4.1200

    Article  CAS  Google Scholar 

  • Sinutok S, Hill R, Doblin MA, Kühl M, Ralph PJ (2012) Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming. Coral Reefs 31:1201–1213. doi:10.1007/s00338-012-0952-6

    Article  Google Scholar 

  • Sinutok S, Hill R, Kühl M, Doblin MA, Ralph PJ (2014) Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis. Mar Biol 161:2143–2154. doi:10.1007/s00227-014-2494-7

    Article  CAS  Google Scholar 

  • Smith RD, Dennison WC, Alberte RS (1984) Role of seagrass photosynthesis in root aerobic processes. Plant Physiol 74:1055–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spilling K, Titelman J, Greve TM, Kühl M (2010) Microsensor measurements of the external and internal microenvironment of Fucus vesiculosus (Phaeophyceae). J Phycol 46:1350–1355. doi:10.1111/j.1529-8817.2010.00894.x

    Article  Google Scholar 

  • Staehr PA, Borum J (2011) Seasonal acclimation in metabolism reduces light requirements of eelgrass (Zostera marina). J Exp Mar Biol Ecol 407:139–146

    Article  Google Scholar 

  • Tripp BC, Smith K, Ferry JG (2001) Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618. doi:10.1074/jbc.R100045200

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115–e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1

    Article  Google Scholar 

  • Vogel S (1994) Life in moving fluids: the physical biology of flow. Princeton University Press, Princeton

    Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543–546

    Article  CAS  PubMed  Google Scholar 

  • Waghmode A, Joshi G (1983) Significance of phosphoglycolate phosphatase and 3-phosphoglycerate phosphatase in photosynthetic carbon assimilation in some marine plants (Ceriops, Lumnitzera, Aegiceras, Aeluropus, Halophila). Photosynthetica 17:193–197

    CAS  Google Scholar 

  • Wang F, Liu R, Wu G, Lang C, Chen J, Shi C (2012) Specific downregulation of the bacterial-type PEPC gene by artificial microRNA improves salt tolerance in Arabidopsis. Plant Mol Biol Report 30:1080–1087

    Article  CAS  Google Scholar 

  • Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra. Oecologia 17:281–291

    Article  PubMed  Google Scholar 

  • Zeebe RE, Wolf-Gladrow DA (2001) CO2 in seawater: equilibrium, kinetics, isotopes, vol 65. Gulf Professional Publishing, Houston

    Google Scholar 

  • Zimmerman RC, Kohrs DG, Steller DL, Alberte RS (1997) Impacts of CO2 enrichment on productivity and light requirements of eelgrass. Plant Physiol 115:599–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank UTS and C3 for strategic research support as well as Dr Audrey Commault, Dr Sutinee Sinutok and Paul Brooks for technical assistance. We also like to thank the editor and two anonymous reviewers for their comments which contributed in improving the quality of this article. The University of Dundee is a registered Scottish charity, No. 015096.

Funding

This study was funded by an Australian Research Council Linkage Grant (LP11020045), Climate Change Cluster Honours Scholarship, University of Technology Sydney (MK) and the Augustinus Foundation (KEB).

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Kim, M., Brodersen, K.E., Szabó, M. et al. Low oxygen affects photophysiology and the level of expression of two-carbon metabolism genes in the seagrass Zostera muelleri . Photosynth Res 136, 147–160 (2018). https://doi.org/10.1007/s11120-017-0452-1

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