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      Transport and Use of Bicarbonate in Plants: Current Knowledge and Challenges Ahead

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          Abstract

          Bicarbonate plays a fundamental role in the cell pH status in all organisms. In autotrophs, HCO 3 − may further contribute to carbon concentration mechanisms (CCM). This is especially relevant in the CO 2-poor habitats of cyanobacteria, aquatic microalgae, and macrophytes. Photosynthesis of terrestrial plants can also benefit from CCM as evidenced by the evolution of C 4 and Crassulacean Acid Metabolism (CAM). The presence of HCO 3 − in all organisms leads to more questions regarding the mechanisms of uptake and membrane transport in these different biological systems. This review aims to provide an overview of the transport and metabolic processes related to HCO 3 − in microalgae, macroalgae, seagrasses, and terrestrial plants. HCO 3 − transport in cyanobacteria and human cells is much better documented and is included for comparison. We further comment on the metabolic roles of HCO 3 − in plants by focusing on the diversity and functions of carbonic anhydrases and PEP carboxylases as well as on the signaling role of CO 2/HCO 3 − in stomatal guard cells. Plant responses to excess soil HCO 3 − is briefly addressed. In conclusion, there are still considerable gaps in our knowledge of HCO 3 − uptake and transport in plants that hamper the development of breeding strategies for both more efficient CCM and better HCO 3 − tolerance in crop plants.

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          CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution.

          Mario Giordano, John Beardall, John Raven (2005)
          The evolution of organisms capable of oxygenic photosynthesis paralleled a long-term reduction in atmospheric CO2 and the increase in O2. Consequently, the competition between O2 and CO2 for the active sites of RUBISCO became more and more restrictive to the rate of photosynthesis. In coping with this situation, many algae and some higher plants acquired mechanisms that use energy to increase the CO2 concentrations (CO2 concentrating mechanisms, CCMs) in the proximity of RUBISCO. A number of CCM variants are now found among the different groups of algae. Modulating the CCMs may be crucial in the energetic and nutritional budgets of a cell, and a multitude of environmental factors can exert regulatory effects on the expression of the CCM components. We discuss the diversity of CCMs, their evolutionary origins, and the role of the environment in CCM modulation.
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            Climate change and ocean acidification effects on seagrasses and marine macroalgae.

            Marguerite Koch, George Bowes, Cliff Ross … (2013)
            Although seagrasses and marine macroalgae (macro-autotrophs) play critical ecological roles in reef, lagoon, coastal and open-water ecosystems, their response to ocean acidification (OA) and climate change is not well understood. In this review, we examine marine macro-autotroph biochemistry and physiology relevant to their response to elevated dissolved inorganic carbon [DIC], carbon dioxide [CO2 ], and lower carbonate [CO3 (2-) ] and pH. We also explore the effects of increasing temperature under climate change and the interactions of elevated temperature and [CO2 ]. Finally, recommendations are made for future research based on this synthesis. A literature review of >100 species revealed that marine macro-autotroph photosynthesis is overwhelmingly C3 (≥ 85%) with most species capable of utilizing HCO3 (-) ; however, most are not saturated at current ocean [DIC]. These results, and the presence of CO2 -only users, lead us to conclude that photosynthetic and growth rates of marine macro-autotrophs are likely to increase under elevated [CO2 ] similar to terrestrial C3 species. In the tropics, many species live close to their thermal limits and will have to up-regulate stress-response systems to tolerate sublethal temperature exposures with climate change, whereas elevated [CO2 ] effects on thermal acclimation are unknown. Fundamental linkages between elevated [CO2 ] and temperature on photorespiration, enzyme systems, carbohydrate production, and calcification dictate the need to consider these two parameters simultaneously. Relevant to calcifiers, elevated [CO2 ] lowers net calcification and this effect is amplified by high temperature. Although the mechanisms are not clear, OA likely disrupts diffusion and transport systems of H(+) and DIC. These fluxes control micro-environments that promote calcification over dissolution and may be more important than CaCO3 mineralogy in predicting macroalgal responses to OA. Calcareous macroalgae are highly vulnerable to OA, and it is likely that fleshy macroalgae will dominate in a higher CO2 ocean; therefore, it is critical to elucidate the research gaps identified in this review. © 2012 Blackwell Publishing Ltd.
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              The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.

              Jeanine Olsen, Pierre Rouzé, Bram Verhelst … (2016)
              Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.
              Article 0 comments Cited 197 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Int J Mol Sci
                Journal ID (iso-abbrev): Int J Mol Sci
                Journal ID (publisher-id): ijms
                Title: International Journal of Molecular Sciences
                Publisher: MDPI
                ISSN (Electronic): 1422-0067
                Publication date (Electronic): 03 May 2018
                Publication date Collection: May 2018
                Volume: 19
                Issue: 5
                Electronic Location Identifier: 1352
                Affiliations
                [1 ]Plant Physiology Lab., Bioscience Faculty, Universidad Autónoma de Barcelona, 08193 Barcelona, Spain; laura.perez.martin@ 123456uab.cat (L.P.); joana.tege@ 123456gmail.com (J.T.); juan.barcelo@ 123456uab.es (J.B.)
                [2 ]Department Biologia. Vegetal, Campus Teatinos, Universidad de Málaga, 29071 Málaga, Spain; ja_fernandez@ 123456uma.es (J.A.F.); lrubio@ 123456uma.es (L.R.)
                Author notes
                [* ]Correspondence: charlotte.poschenrieder@ 123456uab.es ; Tel.: +34-935-812-163
                Author information
                https://orcid.org/0000-0002-3818-0874
                https://orcid.org/0000-0002-3034-8708
                https://orcid.org/0000-0002-7747-2722
                https://orcid.org/0000-0003-3068-2738
                Article
                Publisher ID: ijms-19-01352
                DOI: 10.3390/ijms19051352
                PMC ID: 5983714
                PubMed ID: 29751549
                SO-VID: 3bd0ab88-ec9e-49b0-89aa-2e99423aaf65
                Copyright © © 2018 by the authors.
                License:

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 13 April 2018
                Date accepted : 28 April 2018
                Categories
                Subject: Review

                ScienceOpen disciplines: Molecular biology
                Keywords: bicarbonate,transporter,metabolism,carbonic anhydrase,carboxylases,carbon concentration mechanisms,algae,seagrass,higher land plants,limestone soil
                Data availability:
                ScienceOpen disciplines: Molecular biology
                Keywords: bicarbonate, transporter, metabolism, carbonic anhydrase, carboxylases, carbon concentration mechanisms, algae, seagrass, higher land plants, limestone soil

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