Log in

Carbonic anhydrase in relation to higher plants

  • Review
  • Published:
Photosynthetica

Abstract

The review incorporates recent information on carbonic anhydrase (CA, EC: 4.2.1.1) pertaining to types, homology, regulation, purification, in vitro stability, and biological functions with special reference to higher plants. CA, a ubiquitous enzyme in prokaryotes and higher organisms represented by four distinct families, is involved in diverse biological processes, including pH regulation, CO2 transfer, ion exchange, respiration, and photosynthetic CO2 fixation. CA from higher plants traces its origin with prokaryotes and exhibits compartmentalization among their organs, tissues, and cellular organelles commensurate with specific functions. In leaves, CA represents 1βˆ’20 % of total soluble protein and abundance next only to ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) in chloroplast, facilitating CO2 supply to phosphoenol pyruvate carboxylase in C4 and CAM plants and RuBPCO in C3 plants. It confers special significance to CA as an efficient biochemical marker for carbon sequestration and environmental amelioration in the current global warming scenario linked with elevated CO2 concentrations.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adler, L., Brundell, J., Falkering, S.O., Nyman, P.O.: Carbonic anhydrase from Neisseria sicca strain 6021. I Bacterial growth and purification of the enzyme. β€” Biochim. biophys. Acta 284: 298–310, 1972.

    Google ScholarΒ 

  • Aizawa, K., Miyachi, S.: Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. β€” FEMS Microbiol. Rev. 39: 215–233, 1986.

    Google ScholarΒ 

  • Alber, B.B., Ferry, J.G.: A carbonic anhydrase from the archaeon Methanosarcina thermophila. β€” Proc. nat. Acad. Sci. USA 91: 6909–6913, 1994.

    Google ScholarΒ 

  • Alber, B.E., Colangelo, C.M., Dong, J., Stalhandske, C.M., Baird, T.T., Tu, C., Fierk, C.A., Silverman, D.N., Scott, R.A., Ferry, J.G.: Kinetic and spectroscopic characterization of the gamma carbonic anhydrase from the methanoarchaeon Methanosarcina thermophila. β€” Biochemistry 38: 13119–13128, 1999.

    Google ScholarΒ 

  • Atkins, C.A.: Occurrence and some properties of carbonic anhydrate from legume root nodules. β€” Phytochemistry 13: 93–98, 1974.

    Google ScholarΒ 

  • Atkins, C.A., Patterson, B.D., Graham, D.: Plant carbonic anhydrases I. Distribution of types among species. β€” Plant Physiol. 50: 214–217, 1972a.

    Google ScholarΒ 

  • Atkins, C.A., Patterson, B.D., Graham, D.: Plant carbonic anhydrases II. Preparation and some properties of monocotyledon and dicotyledon enzyme types. β€” Plant Physiol. 50: 218–223, 1972b.

    Google ScholarΒ 

  • Badger, M.R., Price, G.D.: Carbonic anhydrase activity associated with the cyanobacterium Synechococcus PCC7942. β€” Plant Physiol. 89: 51–60, 1989.

    Google ScholarΒ 

  • Badger, M.R., Price, G.D.: The role of carbonic anhydrase in photosynthesis. β€” Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 369–392, 1994.

    Google ScholarΒ 

  • Bowen, G.W.: Carbonic anhydrase in marine algae. β€” Plant Physiol. 44: 726–732, 1969.

    Google ScholarΒ 

  • Bradfield, J.R.G.: Plant carbonic anhydrase. β€” Nature 159: 467–468, 1947.

    Google ScholarΒ 

  • Braus-Stromeyer, S.A., Schnappauf, G., Braus, G.H., Gossnet, A.S., Drake, H.L.: Carbonic anhydrase in Acetobacterium woodii and acetogenic bacteria. β€” J. Bacteriol. 179: 7197–7200, 1997.

    Google ScholarΒ 

  • Burnell, J.N.: Immunological study of carbonic anhydrase in C3 and C4 plants using antibodies to maize cytosolic and spinach chloroplastic carbonic anhydrase. β€” Plant Cell Physiol. 31: 423–427, 1990.

    Google ScholarΒ 

  • Burnell, J.N., Hatch, M.D.: Low bundle sheath carbonic anhydrase is apparently essential for effective C4 pathway operation. β€” Plant Physiol. 86: 1252–1256, 1988.

    Google ScholarΒ 

  • Burnell, J.N., Sizuki, I., Sugiyama, T.: Light induction and the effect of nitrogen status upon the activity of carbonic anhydrase in maize leaves. β€” Plant Physiol. 94: 384–387, 1990.

    Google ScholarΒ 

  • Cerfigni, T., Teofani, F., Bassanelli, C.: Effect of CO2 on carbonic anhydrase in Avena sativa and Zea mays. β€” Phytochemistry 10: 2991–2994, 1971.

    Google ScholarΒ 

  • Champagnol, F.: Compt. rend. Acad. Sci. Paris 289: 1273–1275, 1976. [Not read in original.]

    Google ScholarΒ 

  • Chang, C.W.: Carbonic anhydrase of the cotton plant. β€” Phytochemistry 14: 119–121, 1975a.

    Google ScholarΒ 

  • Chang, C.W.: Activation energy for thermal inactivation and Km of carbonic anhydrase from the cotton plant. β€” Plant Sci. Lett. 4: 109–113, 1975b.

    Google ScholarΒ 

  • Chang, C.W.: Carbonic dioxide and senescence in cotton plants. β€” Plant Physiol. 55: 515–519, 1975c.

    Google ScholarΒ 

  • Chen, T.M., Brown, R.H., Black, C.C.: CO2 compensation concentration, rate of photosynthesis, and carbonic anhydrase activity of plants. β€” Weed Sci. 18: 399–403, 1970.

    Google ScholarΒ 

  • Christianson, D.W., Cox, J.D.: Catalysis by metal activated hy-droxide in zinc and manganese metalloenzymes. β€” Annu. Rev. Biochem. 68: 33–57, 1999.

    Google ScholarΒ 

  • Colman, B.: Second International Symposium on inorganic carbon utilization by aquatic photosynthetic organisms. β€” Can. J. Bot. 69: 907–1027, 1991.

    Google ScholarΒ 

  • Cox, H., Me-Lendon, G.L., Lane, T.W., Prince, R.C., Pickering, I.J., George, G.N.: The active site structure of Thalassiosira weissflogii carbonic anhydrase I. β€” Biochemistry 39: 12128–12130, 2000.

    Google ScholarΒ 

  • Earnhardt, J. N., Qian, M., Tu, C., Lakkis, M.M., Bergenhem, N.C., Laipis, P.J., Tashian, R.E., Silverman, D.N.: The catalytic properties of marine carbonic anhydrase VII. β€” Biochemistry 37: 10837–10845, 1998.

    Google ScholarΒ 

  • Edwards, G.E., Mohamed, A.K.: Reduction in carbonic anhydrase activity in zinc deficient leaves of Phaseolus vulgaris L. β€” Crop Sci. 13: 351–354, 1973.

    Google ScholarΒ 

  • Eriksson, M., Karlsson, J., Ramazanov, Z., Gardestrom, P., Samuelsson, G.: Discovery of an algal mitochondrial carbonic anhydrase: molecular cloning and characterization of low CO2 induced polypeptide in Chlamydomonas reinhardtii. β€” Proc. nat. Acad. Sci. USA 93: 12031–12034, 1996.

    Google ScholarΒ 

  • Eriksson, M., Villand, P., Gardestrom, P., Samuelsson, G.: Induction and regulation of expression of a low CO2 induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. β€” Plant Physiol. 116: 637–641, 1998.

    Google ScholarΒ 

  • Everson, R.G.: Carbonic anhydrase and CO2 fixation in isolated chloroplasts. β€” Phytochemistry 9: 25–32, 1970.

    Google ScholarΒ 

  • Everson, R.G., Slack, C.R.: Distribution of carbonic anhydrase in relation to the C4 pathway of photosynthesis. β€” Phytochemistry 7: 581–584, 1968.

    Google ScholarΒ 

  • Fawcett, T.W., Browse, J.A., Volokita, M., Bartlett, S.G.: Spinach carbonic anhydrase primary structure deduced from the sequence of a cDNA clone. β€” J. biol. Chem. 265: 5414–5417, 1990.

    Google ScholarΒ 

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

    Google ScholarΒ 

  • Fukuzawa, H., Fujiwara, S., Yamamoto, Y., Dionisio-Sese, M.L., Miyachi, S.: cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: Regulation by environmental CO2 concentration. β€” Proc. nat. Acad. Sci. USA 87: 4383–4387, 1990.

    Google ScholarΒ 

  • Fukuzawa, H., Suzuki, E., Komukai, Y., Miyachi, S.: A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. β€” Proc. nat. Acad. Sci. USA 89: 4437–4441, 1992.

    Google ScholarΒ 

  • Funke, R.P., Kovar, J.L., Weeks, D.P.: Intracellular carbonic anhydrase is essential to photosynthesis in Chlamydomonas reinhardtii at atmospheric level of CO2. β€” Plant Physiol. 114: 237–244, 1997.

    Google ScholarΒ 

  • Ghoshal, D., Goyal, A.: Carbon concentration mechanism(s) in unicellular green algae and cyanobacteria. β€” J. Plant Biochem. Biotech. 10: 83–90, 2001.

    Google ScholarΒ 

  • Gill, S.R., Fedorka-Cray, P.J., Tweten, R.K., Sleeper, B.P.: Purification and properties of the carbonic anhydrase of Rhodospirillum rubrum. β€” Arch. Microbiol. 138: 113–118, 1984.

    Google ScholarΒ 

  • Giuliano, G., Pichersky, E., Malik, V.S., Timko, M.P., Scolnik, P.A., Cashmore, A.R.: An evolutionary conserved protein binding sequence upstream of a plant light-regulated gene. β€” Proc. nat. Acad. Sci. USA 85: 7089–7093, 1988.

    Google ScholarΒ 

  • Goustiana, L.M., Fournadjievna, S.T., Pesheva, I.S., Kudrev, M.C.: Two forms of carbonic anhydrase in pea roots. β€” Compt. rend. Acad. bulg. Sci. 41: 103–105, 1998.

    Google ScholarΒ 

  • Goyal, A., Shiraiwa, Y., Tolbert, N.E.: External and internal carbonic anhydrases in Dunaliella species. β€” Mar. Biol. 113: 349–355, 1992.

    Google ScholarΒ 

  • Graham, D., Atkins, C.A., Reed, M.L., Patterson, B.D., Smillie, R.M.: Carbonic anhydrase, photosynthesis, and light-induced pH changes. β€” In: Hatch, M.D., Osmond, C.B., Slatyer, R.O. (ed.): Photosynthesis and Photorespiration. Pp. 267–274. John Wiley and Sons, New York β€” London β€” Sydney β€” Toronto 1971.

    Google ScholarΒ 

  • Graham, D., Reed, M.L.: Carbonic anhydrase and the regulation of photosynthesis. β€” Nature-new Biol. 231: 81–83, 1971.

    Google ScholarΒ 

  • Graham, D., Reed, M.L., Patterson, B.D., Hockley, D.G., Dwyer, M.R.: Chemical properties, distribution and physiology of plant and algal carbonic anhydrase. β€” Ann. New York Acad. Sci. 429: 222–237, 1984.

    Google ScholarΒ 

  • Green, L.S., Laudenbach, D.E., Grossman, A.R.: Nature of the light-induced H+ efflux and Na+ uptake in cyanobacteria. β€” Plant Physiol. 89: 1220–1225, 1989.

    Google ScholarΒ 

  • Green, P.J., Kay, S.A., Chua, N.H.: Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. β€” EMBO J. 6: 2543–2549, 1987.

    Google ScholarΒ 

  • Gutierrez, M., Huber, S.C., Ku, S.B., Kanai, R., Edwards, G.E.: Intracellular localization of carbon metabolism in mesophyll cells of C4 plants. β€” In: Avron, M. (ed.): Proceedings of the Third International Congress of Photosynthesis. Vol. II. Pp. 1219–1230. Elsevier, Amsterdam β€” Oxford β€” New York 1975.

    Google ScholarΒ 

  • Hatch, M.D., Burnell, J.N.: Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. β€” Plant Physiol. 93: 825–828, 1990.

    Google ScholarΒ 

  • Hewett-Emmett, D., Tashian, R.E.: Functional diversity, conservation and convergence in the evolution of the alpha beta and gamma carbonic anhydrase gene families. β€” Mol. phylogenet. Evol. 5: 52–77, 1996.

    Google ScholarΒ 

  • Hiltonen, T., Bjorkbacka, H., Forsman, C. Clarke, A.K., Samuelsson, G.: Intracellular beta carbonic anhydrase of the unicellular green alga coccomyxa. β€” Plant Physiol. 117: 1341–1349, 1998.

    Google ScholarΒ 

  • Houghton, R.A.: The future role of tropical forests in affecting the carbon dioxide concentration of the atmosphere. β€” Ambio 19: 204–209, 1990.

    Google ScholarΒ 

  • Husic, H.D., Marcus, C.A.: Identification of intracellular carbonic anhydrase in Chlamydomonas reinhardtii with a carbonic anhydrase directed photoaffinity label. β€” Plant Physiol. 105: 133–139, 1994.

    Google ScholarΒ 

  • Imamura, M., Tsuzuki, M., Hogetsu, D., Miyachi, S.: Role of carbonic anhydrase in algal photosynthesis. β€” In: Akoyunoglou, G. (ed.): Photosynthesis. Vol. IV. Pp. 471–482. Balaban International Science Services, Philadelphia 1981.

    Google ScholarΒ 

  • Jiang, W., Gupta, D.: Structure of the carbonic anhydrase vi (CA-6) genes evidence for two distinct groups with in the alpha-CA gene family. β€” Biochem. J. 344: 385–390, 1999.

    Google ScholarΒ 

  • Kachru, R.B., Anderson, L.E.: Chloroplast and cytoplasmic enzymes. V. Pea-leaf carbonic anhydrases. β€” Planta 118: 235–240, 1974.

    Google ScholarΒ 

  • Kamo, T., Shimogawara, K., Fukuzawa, H., Muto, S., Miyachi, S.: Subunit constitution of carbonic anhydrate from Chlamydomonas reinhardtii. β€” Eur. J. Biochem. 192: 557–562, 1990.

    Google ScholarΒ 

  • Karlsson, J., Clarke, A.K., Chen, Z.Y., Hugghins, S.Y., Park, Y.I., Husic, D., Moroney, J.V., Samuelsson, G.: A novel alpha type carbonic anhydrase associated with thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. β€” EMBO J. 17: 1208–1216, 1998.

    Google ScholarΒ 

  • Karlsson, J., Hiltonen, T., Husic, D., Ramazanov, Z., Samuelsson, G.: Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. β€” Plant Physiol. 109: 533–539, 1995.

    Google ScholarΒ 

  • Khan, N.A.: Variation in carbonic anhydrase activity and its relationship with photosynthesis and dry mass of mustard. β€” Photosynthetica 30: 317–320, 1994.

    Google ScholarΒ 

  • Kim, H.J., Bracey, M.H., Barlett, S.G.: Nucleotide sequence of a gene encoding carbonic anhydrase in Arabidopsis thaliana. β€” Plant Physiol. 105: 449, 1994.

    Google ScholarΒ 

  • Kimber, M.S., Pai, E.F.: The active site architecture of Pisum sativum beta carbonic anhydrase is a mirror image of that of alpha carbonic anhydrases. β€” EMBO J. 19:1407–1418, 2000.

    Google ScholarΒ 

  • Kisiel, W., Graf, G. Purification and characterization of carbonic anhydrase from Pisum sativum. β€” Phytochemistry 11: 113–117, 1972.

    Google ScholarΒ 

  • Kisker, C., Schindelin, H., Alber, B.E., Ferry, J.G., Rees, D.C.: A left hand Ξ² helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila. β€” EMBO J. 15: 2323–2330, 1996.

    Google ScholarΒ 

  • Kositsin, A.V., Khalidova, G.B.: [Electrophoretic properties of carbonic anhydrase from tomato chloroplasts.]. β€” Fiziol. Rast. 21: 1178–1181, 1974. [In Russ.; not read in original.]

    Google ScholarΒ 

  • Ku, S.B., Edwards, G.E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. IV. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. β€” Z. Pflanzenphysiol. 77: 16–32, 1975.

    Google ScholarΒ 

  • Lane, T.W., Morel, F.M.: A biological function for cadmium in marine diatoms. β€” Proc. nat. Acad. Sci. USA 97: 4627–4631, 2000.

    Google ScholarΒ 

  • Lee, J.G., Morel, F.M.M.: Replacement of Zn by cadmium in marine phytoplankton. β€” Mar. Ecol. Progr. Ser. 127: 305–309, 1995.

    Google ScholarΒ 

  • Lee, J.G., Morel, F.M.M.: In vivo substitution of Zn by cobalt (II) substituted carbonic anhydrase II of the exchange of oxygen-18 between CO2 and H2O. β€” Biochemistry 24: 5881–5887, 1996.

    Google ScholarΒ 

  • Liljas, A., Laurberg, M.: A wheel invented three times: The molecular structures of the three carbonic anhydrases. β€” EMBO Rep. 1: 16–17, 2000.

    Google ScholarΒ 

  • Majeau, N., Arnoldo, M.A., Coleman, J.R.: Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. β€” Plant mol. Biol. 25: 377–385, 1994.

    Google ScholarΒ 

  • Majeau, N., Coleman, J.R.: Isolation and characterization of a cDNA coding for pea chloroplastic carbonic anhydrase. β€” Plant Physiol. 95: 264–268, 1991.

    Google ScholarΒ 

  • Majeau, N., Coleman, J.R.: Nucleotide sequence of a complementary DNA encoding tobacco chloroplastic carbonic anhydrase. β€” Plant Physiol. 100: 1077–1078, 1992.

    Google ScholarΒ 

  • Majeau, N., Coleman, J.R.: Correlation of carbonic anhydrase and ribulose-1,5 bisphosphate carboxylase/oxygenase expression in pea. β€” Plant Physiol. 104: 1393–1399, 1994.

    Google ScholarΒ 

  • Meldrum, N.N., Roughton, F.J.W.: Carbonic anhydrase: its properties. β€” J. Physiol. 80: 113–142, 1933.

    Google ScholarΒ 

  • Millikan, C.R.: Relative effects of zinc and copper deficiencies on lucerne and subterranean clover. β€” Aust. J. biol. Sci. 6: 164–177, 1953.

    Google ScholarΒ 

  • Mitsahashi, S., Mizushima, T., Yamashita, E., Yamamoto, M., Kumasaka, T., Moriyama, H., Miyachi, S., Tsukihra, T.: X-ray structure of beta carbonic anhydrase from the red alga Porphyridium purpureum reveals a novel catalytic site for CO2 hydration. β€” J. biol. Chem. 275: 5521–5526, 2000.

    Google ScholarΒ 

  • Morel, F.M.M., Reinfelder, J.R., Roberts, S.B., Chamberlain, C.P., Lee, J.G., Yee, D.: Zinc and carbon co-limitation of marine phytoplankton. β€” Nature 369: 740–742, 1994.

    Google ScholarΒ 

  • Moroney, J.V., Bartlett, S.G., Samuelsson, G.: Carbonic anhydrases in plants and algae. β€” Plant Cell Environ. 24: 141–153, 2001.

    Google ScholarΒ 

  • Moroney, J.V., Kitayama, M., Togasaki, R.K., Tolbert, N.E.: Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii. β€” Plant Physiol. 83: 460–463, 1987.

    Google ScholarΒ 

  • Moroney, J.V., Somanchi, A.: How do algae concentrate CO2 increase the efficiency of photosynthetic carbon fixation? β€” Plant Physiol. 119: 9–16, 1999.

    Google ScholarΒ 

  • Mount, S.M.: A catalogue of splice junction sequences. β€” Nucleic Acids Res. 10: 459–472, 1982.

    Google ScholarΒ 

  • Nimer, N.A., Iglesias-Rodriguez, M.D., Merrett, M.J.: Bicarbonate utilization by marine phytoplankton species. β€” J. Phycol. 33: 625–631, 1997.

    Google ScholarΒ 

  • Nishimura, M., Graham, D., Akazawa, T.: Isolation of intact chloroplasts and other cell organelles from spinach leaf protoplasts. β€” Plant Physiol. 58: 309–314, 1976.

    Google ScholarΒ 

  • Okabe, K., Yang, S.-Y., Tsuzuki, M., Miyachi, S.: Carbonic anhydrase: its content in spinach leaves and its taxonomic diversity studied with anti-spinach leaf carbonic anhydrase anti-body. β€” Plant Sci. Lett. 33: 145–153, 1984.

    Google ScholarΒ 

  • Okazaki, M., Yoshida, T., Feruya, K.: The effects of light on carbonic anhydrases in the etiolated leaves of Phaseolus vulgaris and in intact chloroplasts from spinach. β€” Bull. Tokyo Gakugei Univ., Ser. IV 28: 199–206, 1976.

    Google ScholarΒ 

  • Pesheva, I., Kodama, M., Dionisio-Sese, M.L., Miyachi, S.: Changes in photosynthetic characteristics induced by transferring air-grown cells of Chlorococcum littorale to high-CO2 conditions. β€” Plant Cell Physiol. 35: 379–387, 1994.

    Google ScholarΒ 

  • Pocker, Y., Ng, J.S.Y.: Plant carbonic anhydrase: Properties and carbon dioxide hydration kinetics. β€” Biochemistry 12: 5127–5134, 1973.

    Google ScholarΒ 

  • Pocker, Y., Sarkanen, S.: Carbonic anhydrase structure, catalytic versatility and inhibition. β€” Adv. Enzymol. 47: 149–274, 1978.

    Google ScholarΒ 

  • Poincelot, R.P.: Intracellular distribution of carbonic anhydrase in spinach leaves. β€” Biochim. biophys. Acta 258: 637–642, 1972.

    Google ScholarΒ 

  • Polson, D.E.: A Physiologic-Genetic Study of the Differential Response of Navy Beans (Phaseolus vulgaris L.) to Zinc. β€” Ph. D. Thesis. Michigan State University, No. 68-11,082, 1968.

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

    Google ScholarΒ 

  • Price, N.M., Morel, F.M.M.: Cadmium and cobalt substitution for zinc in a marine diatom. β€” Nature 344: 658–660, 1990.

    Google ScholarΒ 

  • Raines, C.A., Horsnell, P.R., Holder, C., Lloyed, J.C.: Arabidopsis thaliana carbonic anhydrase: cDNA sequence and effect of CO2 on mRNA levels. β€” Plant mol. Biol. 20: 1143–1148, 1992.

    Google ScholarΒ 

  • Randall, P.J., Bauma, D.: Zinc deficiency, carbonic anhydrase and photosynthesis in leaves of spinach. β€” Plant Physiol. 52: 229–232, 1973.

    Google ScholarΒ 

  • Rathnam, C.K.M., Das, V.S.R.: Aspartate-type C-4 photosynthetic carbon metabolism in leaves of Eleusine coracana GAERTN. β€” Z. Pflanzenphysiol. 74: 377–393, 1975.

    Google ScholarΒ 

  • Reed, M.L.: Intracellular location of carbonic dehydratase (carbonic anhydrase) in leaf tissue. β€” Plant Physiol. 63: 216–217, 1979.

    Google ScholarΒ 

  • Reed, M.L., Graham, D.: Carbonic anhydrase in plants: distribution, properties and possible physiological roles. β€” Progr. Phytochem. 7: 47–49, 1981.

    Google ScholarΒ 

  • Roberts, S.B., Lane, T.W., Morel, F.M.M.: Carbonic anhydrase in the marine diatom Thalassiosira weissflogii. β€” J. Phycol. 33: 845–850, 1997.

    Google ScholarΒ 

  • Rossi, C.A., Cherst, A., Cortivo, M.: Studies on carbonic anhydrase from spinach leaves: Isolation and properties. β€” In: Forster, R.E., Edsall, J.T., Otis, A.B., Haughton, F.J.W. (ed.): CO2: Chemical, Biochemical and Physiological Aspects. Pp. 131–138. NASA, Washington 1969.

    Google ScholarΒ 

  • Sasaki, H., Hirose, T., Watanabe, Y., Ohsugi, R.: Carbonic anhydrase activity and CO2 transfer resistance in Zn-deficient rice leaves. β€” Plant Physiol. 118: 929–934, 1998.

    Google ScholarΒ 

  • Smith, K.S., Ferry, J.G.: Prokaryotic carbonic anhydrases. β€” FEMS Microbiol. Rev. 24: 335–366, 2000.

    Google ScholarΒ 

  • Smith, K.S.. Jakubzick, C., Whittam, T.S., Ferry, J.G.: Carbonic anhydrase: is an ancient enzyme widespread in prokaryotes. β€” Proc. nat. Acad. Sci. USA 96: 15184–15189, 1999.

    Google ScholarΒ 

  • Stemler, A.J.: The case for chloroplast thylakoid carbonic anhydrase. β€” Physiol. Plant. 99: 348–353, 1997.

    Google ScholarΒ 

  • Strop, P., Smith, K.S., Iverson, T.M., Ferry, J.G., Rees, D.C.: Crystal structure of the β€œcab” type beta class carbonic anhydrase from the archaeon Methanobacterium thermoautotrophicum. β€” J. biol. Chem. 276: 10299–10305, 2001.

    Google ScholarΒ 

  • Sultemeyer, D., Klughammer, B., Badger, M., Price, G.D.: Fast induction of high affinity HCO3 transport in cyanobacteria. β€” Plant Physiol. 116: 183–192, 1998.

    Google ScholarΒ 

  • Tashian, R.F.: The carbonic anhydrase: Widening perspectives on their evolution, expression and function. β€” Bioassays 10: 186–192, 1989.

    Google ScholarΒ 

  • Tobin, A.J.: Carbonic anhydrase from parsley leaves. β€” J. biol. Chem. 245: 2656–2666, 1970.

    Google ScholarΒ 

  • Tripp, B.C., Smith, K., Ferry, J.G.: Carbonic anhydrase: New insights for an ancient enzyme. β€” J. biol. Chem. 276: 48615–48618, 2001.

    Google ScholarΒ 

  • Tsuzuki, M., Miyachi, S.: The function of carbonic anhydrase in aquatic photosynthesis. β€” Aquat. Bot. 34: 85–104, 1989.

    Google ScholarΒ 

  • Tsuzuki, M., Miyachi, S., Edwards, G.E.: Localization of carbonic anhydrase in mesophyll cells of terrestrial C3 plants in relation to CO2 assimilation. β€” Plant Cell Physiol. 26: 881–891, 1985.

    Google ScholarΒ 

  • Tsuzuki, M., Muto, S., Miyachi, S.: Role of carbonic anhydrase in photosynthesis of higher plants: a possible limiting step in CO2 transport. β€” In: Akoyunoglu, G. (ed.): Photosynthesis. Vol. IV. Pp. 483–492. Balaban International Science Services, Philadelphia 1981.

    Google ScholarΒ 

  • Tu, C.K., Silverman, D.N.: Catalysis by cobalt (II) substituted carbonic anhydrase II of the exchange of oxygen-18 between CO2 and H2O. β€” Biochemistry 24: 5881–5887, 1985.

    Google ScholarΒ 

  • Veith, F.P., Blankeship, L.C.: Carbonic anhydrase in bacteria. β€” Nature 197: 76–77, 1963.

    Google ScholarΒ 

  • Walk, R.-A., Metzner, H.: Reinigung und Charakterisierung von Chloroplasten-Carbonat-Dehydratase (Isoenzym I) aus BlΓ€ttern von Lactuca sativa. β€” Hoppe-Seyler's Z. physiol. Chem. 356: 1733–1741, 1975.

    Google ScholarΒ 

  • Waygood, E.R.: Carbonic anhydrase (Plant and animal). β€” In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 2. Pp. 836–846. Academic Press, New York 1955.

    Google ScholarΒ 

  • Waygood, E.R., Clendenning, K.A.: Carbonic anhydrase in green plants. β€” Can. J. Res. 28: 673–689, 1950.

    Google ScholarΒ 

  • Werdan, K.H., Heldt, W., Gelley, G.: Accumulation of bicarbonate in intact chloroplasts following a pH gradient. β€” Biochim. biophys. Acta 288: 430–441, 1972.

    Google ScholarΒ 

  • Wood, J.G., Sibly, P.M.: Carbonic anhydrase activity in plants in relation to zinc content. β€” Aust. J. sci. Res. B 5: 244–255, 1952.

    Google ScholarΒ 

  • Woodwell, G.M.: The carbon dioxide question. β€” Sci. American 283(1): 34–43, 1978.

    Google ScholarΒ 

  • Yagawa, Y., Shiraiwa, Y., Miyachi, S.: Carbonic anhydrase from the blue green alga (cyanobacterium) Anabaena variabilis. β€” Plant Cell Physiol. 25: 775–783, 1984.

    Google ScholarΒ 

  • Yee, D., Morel, F.M.M.: In vivo substitution of zinc by cobalt in carbonic anhydrase of a marine diatom. β€” Limnol. Oceanogr. 41: 575–577, 1996.

    Google ScholarΒ 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. A. Ansari.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tiwari, A., Kumar, P., Singh, S. et al. Carbonic anhydrase in relation to higher plants. Photosynthetica 43, 1–11 (2005). https://doi.org/10.1007/s11099-005-1011-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-005-1011-0

Additional key words

Navigation