Skip to main content

Advertisement

SpringerLink
Log in

Carbonic anhydrase: a key regulatory and detoxifying enzyme for Karst plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Karstification is a rapid process during which calcidic stones/limestones undergo dissolution with the consequence of a desertification of karst regions. A slow-down of those dissolution processes of Ca-carbonate can be approached by a reforestation program using karst-resistant plants that can resist alkaline pH and higher bicarbonate (HCO3 −) concentrations in the soil. Carbonic anhydrases (CA) are enzymes that mediate a rapid and reversible interconversion of CO2 and HCO3 −. In the present study, the steady-state expression of a CA gene, encoding for the plant carbonic anhydrase from the parsley Petroselinum crispum, is monitored. The studies were primarily been performed during germination of the seeds up to the 12/14-day-old embryos. The CA cDNA was cloned. Quantitative polymerase chain reaction (qPCR) analysis revealed that the gene expression level of the P. crispum CA is strongly and significantly affected at more alkaline pH in the growth medium (pH 8.3). This abolishing effect is counteracted both by addition of HCO3 − and by addition of polyphosphate (polyP) to the culture medium. In response to polyP, the increased pH in the vacuoles of the growing plants is normalized. The effect of polyP let us to propose that this polymer acts as a buffer system that facilitates the adjustment of the pH in the cytoplasm. In addition, it is proposed that polyP has the potential to act, especially in the karst, as a fertilizer that allows the karstic plants to cope with the adverse pH and HCO3 − condition in the soil.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

CA:

Carbonic anhydrases

polyP:

Polyphosphate

qPCR:

Quantitative polymerase chain reaction

V-ATPase:

Vacuolar H+-ATPase

V-PPase:

Vacuolar H+-pyrophosphatase

References

  • Alvarez BV, Quon AL, Mullen J, Casey JR (2013) Quantification of carbonic anhydrase gene expression in ventricle of hypertrophic and failing human heart. BMC Cardiovasc Disord 13:2. doi:10.1186/1471-2261-13-2

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Armstrong JM, Myers DV, Verpoorte JA, Edsall JT (1966) Purification and properties of human erythrocyte carbonic anhydrase. J Biol Chem 241:5137–5149

    CAS  PubMed  Google Scholar 

  • Atkins CA, Patterson BD, Graham D (1972) Plant carbonic anhydrases. II. Preparation and some properties of monocotyledon and dicotyledon enzyme types. Plant Physiol 50:218–223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45:369–392

    Article  CAS  Google Scholar 

  • Bezlaj F (ed) (1982) Etimološki slovar slovenskega jezika. Slovenska akademija znanosti in umetnosti, Ljubljana, vol 2, pp 82–82

  • Bonacci O (ed) (2010) Sustainability of the Karst environment. Dinaric Karst and other Karst regions. In: International Interdisciplinary Scientific Conference, Plitvice Lakes, Croatia, 23–26 September 2009. UNESCO Proceedings, Paris, IHP-VII, Series on GW No 2

  • Britto D, Kronzucker H (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409

    Article  CAS  Google Scholar 

  • Casamayor EO, Llirós M, Picazo A, Barberá A, Borrego CM, Camacho A (2012) Contribution of deep dark fixation processes to overall CO2 incorporation and large vertical changes of microbial populations in stratified karstic lakes. Aquat Sci 74:61–75

    Article  CAS  Google Scholar 

  • Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT (2000) Current protocols in protein science. Wiley, Chichester, pp 2.0.1–2.8.17

    Google Scholar 

  • Compton S, Jones CG (1985) Mechanism of dye response and interference in the Bradford protein assay. Anal Biochem 151:369–374

    Article  CAS  PubMed  Google Scholar 

  • Cotzur D, Bara I (2006) The expression pattern of two carbonic anhydrase genes in different organs of Lotus japonicas L. Ann ‘‘Alexandru Ioan Cuza’’ Univ; Sect II a 7:121–126

    Google Scholar 

  • Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT, Moore B, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of Earth as a system. Science 290:291–296

    Article  CAS  PubMed  Google Scholar 

  • Ferreira FJ, Guo C, Coleman JR (2008) Reduction of plastid-localized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship. Plant Physiol 147:585–594

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fett JP, Coleman JR (1994) Characterization and expression of two cDNAs encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiol 105:707–713

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Flemetakis E, Dimou M, Cotzur D, Aivalakis G, Efrose RC, Kenoutis C, Udvardi M, Katinakis P (2003) A Lotus japonicus beta-type carbonic anhydrase gene expression pattern suggests distinct physiological roles during nodule development. Biochim Biophys Acta 1628:186–194

    Article  CAS  PubMed  Google Scholar 

  • Ford DC, Williams P (2007) Karst hydrogeology and geomorphology. Wiley, Chichester

    Book  Google Scholar 

  • Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S (1990) Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87:9779–9783

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214

    Article  CAS  PubMed  Google Scholar 

  • Gout E, Bligny R, Douce R (1992) Regulation of intracellular pH values in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. J Biol Chem 267:13903–13909

    CAS  PubMed  Google Scholar 

  • Grennan AK (2008) Phosphate accumulation in plants: signaling. Plant Physiol 148:3–5

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guern J, Mathieu Y, Pean M, Pasquier C, Beloeil J-C, Lallemand J-Y (1986) Cytoplasmic pH regulation in Acer pseudoplatanus cells. I. A 31P NMR description of acid load effects. Plant Physiol 82:840–845

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guern J, Mathieu Y, Kurkdjian A, Manigault P, Manigault J, Gillet B, Beloeil JC, Lallemand JY (1989) Regulation of vacuolar pH of plant cells: II. A P NMR study of the modifications of vacuolar pH in isolated vacuoles induced by proton pumping and cation/H exchanges. Plant Physiol 89:27–36

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haglund K, Ramazanov Z, Mtolera M, Pedersén M (1992) Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L. and Laminaria saccharina (L.) Lamour (Phaeophyta). Planta 188:1–6

    Article  CAS  PubMed  Google Scholar 

  • Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5:50–77

    Article  CAS  PubMed  Google Scholar 

  • Hopkins WG, Hüner NPA (2004) Introduction to plant physiology, 3rd edn. Wiley, New York

    Google Scholar 

  • Kandegedara A, Rorabacher DB (1999) Noncomplexing tertiary amines as ‘better’ buffers covering the range of pH 3–11. Temperature dependence of their acid dissociation constants. Anal Chem 71:3140–3144

    Article  CAS  PubMed  Google Scholar 

  • Krasko A, Schröder HC, Batel R, Grebenjuk VA, Steffen R, Müller IM, Müller WEG (2002) Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA Cell Biol 21:67–80

    Article  CAS  PubMed  Google Scholar 

  • Krebs M, Beyhl D, Görlich E, Al-Rasheid KAS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107:3251–3256

    Article  CAS  PubMed  Google Scholar 

  • Kresic N, Papic P (1990) Specific chemical composition of karst groundwater in the Ophiolite Belt of the Yugoslav Inner Dinarides: a case for covered karst. Environ Geol Water Sci 15:131–135

    Article  Google Scholar 

  • Li Q, Müller WEG (2012) Determination method of carbonic anhydrase in plants. Patent application (05-09-2012) No. YR-JJHF-2012-414

  • Li W, Liu LP, Zhou PP, Cao L, Yu LJ, Jiang SY (2011) Calcite precipitation induced by bacteria and bacterially produced carbonic anhydrase. Curr Sci 100:502–508

    CAS  Google Scholar 

  • Lian B, Yuan DX, Liu ZH (2011) Effect of microbes on karstification in karst ecosystems. Chin Sci Bull 56:3743–3747

    Article  CAS  Google Scholar 

  • Liebig J (1840) Die organische Chemie in ihrer Anwendung auf Agricultur und Physiologie. F Vieweg, Braunschweig, pp 1–352

    Google Scholar 

  • Liu Z, You S, Li Q, Zhang M (2002) Hydrochemical and isotopic characteristics of tufa in the Baishuitai scenic area of Yunnan and their implications for paleoenvironmental reconstruction. Quat Sci (Chinese) 22:459–467

    Google Scholar 

  • Liu Z, Sun H, Baoying L, Xiangling L, Wenbing Y, Cheng Z (2010) Wet-dry seasonal variations of hydrochemistry and carbonate precipitation rates in a travertine-depositing canal at Baishuitai, Yunnan, SW China: implications for the formation of biannual laminae in travertine and for climatic reconstruction. Chem Geol 273:258–266

    Article  CAS  Google Scholar 

  • Ludwig M, Burnell JN (1995) Molecular comparison of carbonic anhydrase from Flaveria species demonstrating different photosynthetic pathways. Plant Mol Biol 29:353–365

    Article  CAS  PubMed  Google Scholar 

  • Majeau N, Arnoldo MA, Coleman JR (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol Biol 25:377–385

    Article  CAS  PubMed  Google Scholar 

  • Mathieu Y, Guern J, Kurkdjian A, Manigault P, Manigault J, Zielinska T, Gillet B, Beloeil JC, Lallemand JY (1989) Regulation of vacuolar pH of plant cells I. Isolation and properties of vacuoles suitable for 31P-NMR studies. Plant Physiol 89:19–26

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McBeath TM, Lombi E, McLaughlin MJ, Bünemann EK (2007) Polyphosphate-fertilizer solution stability with time, temperature, and pH. J Plant Nutr Soil Sci 170:387–391

    Article  CAS  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24:141–153

    Article  CAS  Google Scholar 

  • Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109:133–149

    Article  CAS  PubMed  Google Scholar 

  • Müller WEG, Kasueske M, Wang XH, Schröder HC, Wang Y, Pisignano D, Wiens M (2009) Luciferase a light source for the silica-based optical waveguides (spicules) in the demosponge Suberites domuncula. Cell Mol Life Sci 66:537–552

    Article  PubMed  Google Scholar 

  • Müller WEG, Wang X, Schröder HC, Korzhev M, Grebenjuk VA, Markl JS, Jochum KP, Pisignano D, Wiens M (2010) A cryptochrome-based photosensory system in the siliceous sponge Suberites domuncula (Demospongiae). FEBS J 277:1182–1201

    Article  PubMed  Google Scholar 

  • Müller WEG, Wang XH, Diehl-Seifert B, Kropf K, Schloßmacher U, Lieberwirth I, Glasser G, Wiens M, Schröder HC (2011) Inorganic polymeric phosphate/polyphosphate as an inducer of alkaline phosphatase and a modulator of intracellular Ca2+ level in osteoblasts (SaOS-2 cells) in vitro. Acta Biomater 7:2661–2671

    Article  PubMed  Google Scholar 

  • Müller WEG, Wang XH, Grebenjuk VA, Korzhev M, Wiens M, Schloßmacher U, Schröder HC (2012a) Nocturnin in the demosponge Suberites domuncula: a potential circadian clock protein controlling glycogenin synthesis in sponges. Biochem J 448:233–242

    Article  PubMed  Google Scholar 

  • Müller WEG, Wang XH, Grebenjuk VA, Korzhev M, Wiens M, Schloßmacher U, Schröder HC (2012b) Common genetic denominators for Ca++-based skeleton in Metazoa: role of osteoclast-stimulating factor and of carbonic anhydrase in a calcareous sponge. PLoS One 7:e34617. doi:10.1371/journal.pone.0034617

    Article  PubMed Central  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc Natl Acad Sci USA 110:1767–1772

    Google Scholar 

  • Pick U, Weiss M (1991) Polyphosphate hydrolysis within acidic vacuoles in response to amine-induced alkaline stress in the halotolerant alga Dunaliella salina. Plant Physiol 97:1234–1240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price GD, von Caemmerer S, Evans JR, Yu J-W, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A, Badger MR (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340

    Article  CAS  Google Scholar 

  • Radmer R, Ollinger O (1980) Light-driven uptake of oxygen, carbon dioxide, and bicarbonate by the green alga Scenedesmus. Plant Physiol 65:723–729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rao NN, Gómez-García MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78:605–647

    Article  CAS  PubMed  Google Scholar 

  • Roberts JKM, Ray PM, Wade-Jardetzky N, Jardetzky O (1980) Estimation of cytoplasmic and vacuolar pH in higher plant cells by 31P NMR. Nature 283:870–872

    Article  CAS  Google Scholar 

  • Sachs L (1984) Angewandte Statistik. Springer, Berlin, p 242

    Book  Google Scholar 

  • Tanz SK, Tetu SG, Vella NG, Ludwig M (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. Plant Physiol 150:1515–1529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsuzuki M, Miyachi S, Edwards GE (1985) Localization of carbonic anhydrase in mesophyll cells of terrestrial C3 plants in relation to CO2 assimilation. Plant Cell Physiol 26:881–891

    CAS  Google Scholar 

  • Vandemoortele JL, Billard JP, Boucaud J, Gaspar Th (1996) Micropropagation of parsley through axillary shoot proliferation. Plant Cell Tiss Org 44:25–30

    Article  CAS  Google Scholar 

  • Verpoorte JA, Mehta S, Edsall JT (1967) Esterase activities of human carbonic anhydrases B and C. J Biol Chem 242:4221–4229

    CAS  PubMed  Google Scholar 

  • Walworth JL (2009) Soil fertility basics. Crop production and soil management series—University of Alaska; FGV-00242A

  • Wang L (2011) China checklist of higher plants. 2009-05-25

  • Wang XH, Schröder HC, Wiens M, Ushijima H, Müller WEG (2012a) Bio-silica and bio-polyphosphate: applications in biomedicine (bone formation). Curr Opin Biotechnol 23:570–578

    Article  CAS  PubMed  Google Scholar 

  • Wang XH, Schröder HC, Wiens M, Schloßmacher U, Müller WEG (2012b) Biosilica: molecular biology, biochemistry and function in demosponges as well as its applied aspects for tissue engineering. In: Becerro MA, Uriz MJ, Maldonado M, Turon X (eds) Adv Marine Biol—Adv Sponge Sci: Physiol Chem Microb Divers Biotechnol 62:231–271

  • Wegner LH, Zimmermann U (2004) Bicarbonate-induced alkalinization of the xylem sap in intact maize seedlings as measured in situ with a novel xylem pH probe. Plant Physiol 136:3469–3477

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wightman S, Higgins S (2011) Sinkhole management for agricultural producers. Cooperative Extension Service, University of Kentucky, Lexington, pp 1–4

    Google Scholar 

  • Wingate L, Ogée J, Cuntz M, Genty B, Reiter I, Seibt U, Yakir D, Maseyk K, Pendall EG, Barbour MM, Mortazav B, Burlett R, Peylin P, Miller J, Mencuccini M, Shim JH, Hunti J, Grace J (2009) The impact of soil microorganisms on the global budget of δ18O in atmospheric CO2. Proc Natl Acad Sci USA 29:22411–22415

    Article  Google Scholar 

  • Woolhouse HW (1966) The effect of bicarbonate on the uptake of iron in four related grasses. New Phytol 65:372–375

    Article  CAS  Google Scholar 

  • Yan J, Li J, Ye Q, Li K (2012) Concentrations and exports of solutes from surface runoff in Houzhai Karst Basin, southwest China. Chem Geol 304–305:1–9

    Article  Google Scholar 

  • Zhang C, Wang J, Pu J, Yan J (2012) Bicarbonate daily variations in a Karst river: the carbon sink effect of subaquatic vegetation photosynthesis. Acta Geol Sinica 86:973–979

    Article  CAS  Google Scholar 

Download references

Acknowledgments

W.E.G. M. is a holder of an ERC Advanced Investigator Grant (No. 268476 BIOSILICA). This work was supported by grants from the Deutsche Forschungsgemeinschaft (Schr 277/10-2), the European Commission (“BIOMINTEC”: No. 215507; Industry-Academia Partnerships and Pathways “CoreShell”: No. 286059; “SPECIAL”: No. 266033; “MarBioTec*EU-CN*”: No. 268476; and “BlueGenics”: No. 311848) and the International Human Frontier Science Program.

Author information

Authors and Affiliations

  1. ERC Advanced Investigator Grant Research Group, University Medical Center, Institute for Physiological Chemistry, Johannes Gutenberg University Mainz, Duesbergweg 6, 55128, Mainz, Germany

    Werner E. G. Müller, Li Qiang, Heinz C. Schröder, Natalie Hönig, Vlad A. Grebenjuk & Xiaohong Wang

  2. CAGS, Institute of Karst Geology, No. 50, Qixing Road, Guilin, Guangxi, China

    Li Qiang & Daoxian Yuan

  3. Section of Biochemistry, Department of Experimental Medicine, Università degli Studi di Genova, Viale Benedetto XV 1, 16132, Genoa, Italy

    Francesca Mussino

  4. DISTAV, Università degli Studi di Genova, Corso Europa 26, 16132, Genoa, Italy

    Marco Giovine

Authors
  1. Werner E. G. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li Qiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heinz C. Schröder
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Natalie Hönig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daoxian Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vlad A. Grebenjuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Francesca Mussino
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marco Giovine
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaohong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Werner E. G. Müller or Xiaohong Wang.

Additional information

A research contribution of the “German-Chinese Center for Bio-inspired Materials”.

Gene deposited: The carbonic anhydrase sequence from Petroselinum crispum (PCCA) has been deposited (EMBL/GenBank) under the accession number HF937210.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Müller, W.E.G., Qiang, L., Schröder, H.C. et al. Carbonic anhydrase: a key regulatory and detoxifying enzyme for Karst plants. Planta 239, 213–229 (2014). https://doi.org/10.1007/s00425-013-1981-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1981-2

Keywords

Search

Navigation