Skip to main content
SpringerLink
Log in

Stress-Related Changes in the Expression and Activity of Plant Carbonic Anhydrases

  • Review
  • Published:
Planta Aims and scope Submit manuscript

A Correction to this article was published on 02 March 2021

This article has been updated

Abstract

The data on stress-related changes in the expression and activity of plant carbonic anhydrases (CAs) suggest that they are generally upregulated at moderate stress severity. This indicates probable involvement of CAs in adaptation to drought, high salinity, heat, high light, Ci deficit, and excess bicarbonate. The changes in CA levels under cold stress are less studied and generally represented by the downregulation of CAs excepting βCA2. Excess Cd2+ and deficit of Zn2+ specifically reduce CA activity and reduce its synthesis. Probable roles of βCAs in stress adaptation include stomatal closure, ROS scavenging and partial compensation for decreased mesophyll CO2 conductance. βCAs play contrasting roles in pathogen responses, interacting with phytohormone signaling networks. Their role can be either negative or positive, probably depending on the host–pathogen system, pathogen initial titer, and levels of ·NO and ROS. It is still not clear why CAs are suppressed under severe stress levels. It should be noted, that the role of βCAs in the facilitation of CO2 diffusion and their involvement in redox signaling or ROS detoxication are potentially antagonistic, as they are inactivated by oxidation or nitrosylation. Interestingly, some chloroplastic βCAs may be relocated to the cytoplasm under stress conditions, but the physiological meaning of this effect remains to be studied.

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

Similar content being viewed by others

Change history

Abbreviations

CA:

Carbonic anhydrase

CCM:

Carbon concentrating mechanism

Ci:

Inorganic carbon

GFP:

Green fluorescent protein

SA:

Salicylic acid

ABA:

Abscisic acid

JA:

Jasmonic acid

References

  • Ahsan N, Donnart T, Nouri M-Z, Komatsu S (2010) Tissue-specific defense and thermo-adaptive mechanisms of soybean seedlings under heat stress revealed by proteomic approach. J Proteome Res 9(8):4189–4204

    Article  CAS  PubMed  Google Scholar 

  • Alterio V, Langella E, Viparelli F, Vullo D et al (2012) Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. Biochimie 94(5):1232–1241

    Article  CAS  PubMed  Google Scholar 

  • Asencio CI, Cedeno-Maldonado A (1978) Effects of cadmium on carbonic anhydrase and activities dependent on electron transport of isolated chloroplasts. Journal of Agriculture of University of Puerto Rico 63(2):195–201

    Google Scholar 

  • Aslam M, Sinha VB, Singh RK, Anandhan S et al (2010) Isolation of cold stress-responsive genes from Lepidium latifolium by suppressive subtraction hybridization. Acta Physiol Plant 32(1):205–210

    Article  CAS  Google Scholar 

  • Azeem A, Wu Y, Xing D, Javed Q et al (2017) Photosynthetic response of two okra cultivars under salt stress and re-watering. Journal of Plant Interactions 12(1):67–77

    Article  CAS  Google Scholar 

  • Badger M (2003) The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynth Res 77:83–94

    Article  CAS  PubMed  Google Scholar 

  • Bar-Akiva A, Lavon R (1969) Carbonic anhydrase activity as an indicator of zinc deficiency in citrus leaves. Journal of Horticultural Science 44(4):359–362

    Article  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24(1):23–58

    Article  CAS  Google Scholar 

  • Behal RH, Lin M, Back S, Oliver DJ (2002) Role of acetyl-coenzyme A synthetase in leaves of Arabidopsis thaliana. Arch Biochem Biophys 402:259–267

    Article  CAS  PubMed  Google Scholar 

  • Benlloch R, Shevela D, Hainzl T, Grundström C et al (2015) Crystal structure and functional characterization of photosystem II-associated carbonic anhydrase CAH3 in Chlamydomonas reinhardtii. Plant Physiol 167(3):950–962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berghuijs HNC, Yin X, Ho QT, Retta MA et al (2017) Localization of (photo)respiration and CO2 re-assimilation in tomato leaves investigated with a reaction-diffusion model. PLoS ONE 12(9):e0183746

    Article  PubMed  PubMed Central  Google Scholar 

  • Blanco-Rivero A, Shutova T, Román MJ, Villarejo A et al (2012) Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS ONE 7(11):e49063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyd RA, Gandin A, Cousins AB (2015) Temperature response of C4 photosynthesis: Biochemical analysis of Rubisco, phosphoenolpyruvate carboxylase and carbonic anhydrase in Setaria viridis. Plant Physiol 169:1850–1861

    CAS  PubMed  PubMed Central  Google Scholar 

  • Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2: Intracellular CO2 reassimilation. Plant, Cell Environ 36(1):200–212

    Article  CAS  Google Scholar 

  • Caruso G, Cavaliere C, Foglia P, Gubbiotti R et al (2009) Analysis of drought responsive proteins in wheat (Triticum durum) by 2D-PAGE and MALDI-TOF mass spectrometry. Plant Sci 177(6):570–576

    Article  CAS  Google Scholar 

  • Caruso G, Cavaliere C, Guarino C, Gubbiotti R et al (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Analytical and Bioanalytical Chemistry 391(1):381–390

  • Carvallo MA, Pino M-T, Jeknić Z, Zou C et al (2011) A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 62(11):3807–3819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaki M, Carreras A, López-Jaramillo J, Begara-Morales JC et al (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide 29:30–33

    Article  CAS  PubMed  Google Scholar 

  • Chen I-H, Tsai AY, Huang Y-P, Wu I-F et al (2017) Nuclear-encoded plastidal carbonic anhydrase is involved in replication of Bamboo mosaic virus RNA in Nicotiana benthamiana. Frontiers in Microbiology 8:2046

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Gallie DR (2015) Ethylene regulates energy-dependent non-photochemical quenching in Arabidopsis through repression of the xanthophyll cycle. PLoS ONE 10(12):e0144209

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng S-F, Huang Y-P, Wu Z-R, Hu C-C et al (2010) Identification of differentially expressed genes induced by Bamboo mosaic virus infection in Nicotiana benthamiana by cDNA-amplified fragment length polymorphism. BMC Plant Biol 10(1):286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman JR, Grossman AR (1984) Biosynthesis of carbonic anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc Natl Acad Sci 81(19):6049–6053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins RM, Afzal M, Ward DA, Prescott MC et al (2010) Differential proteomic analysis of Arabidopsis thaliana genotypes exhibiting resistance or susceptibility to the insect herbivore. Plutella xylostella PLoS ONE 5(4):e10103

    Article  PubMed  Google Scholar 

  • Dąbrowska-Bronk J, Komar DN, Rusaczonek A, Kozłowska-Makulska A et al (2016) β-carbonic anhydrases and carbonic ions uptake positively influence Arabidopsis photosynthesis, oxidative stress tolerance and growth in light dependent manner. J Plant Physiol 203:44–54

    Article  PubMed  Google Scholar 

  • Das A, Eldakak M, Paudel B, Kim D-W et al (2016) Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. Biomed Res Int 2016:6021047

    Article  CAS  Google Scholar 

  • De Simone G, Di Fiore A, Capasso C, Supuran CT (2015) The zinc coordination pattern in the η-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett 25(7):1385–1389

    Article  PubMed  Google Scholar 

  • DiMario RJ, Clayton H, Mukherjee A, Ludwig M et al (2017) Plant carbonic anhydrases: Structures, locations, evolution, and physiological roles. Molecular Plant 10(1):30–46

    Article  CAS  PubMed  Google Scholar 

  • DiMario RJ, Machingura MC, Waldrop GL, Moroney JV (2018) The many types of carbonic anhydrases in photosynthetic organisms. Plant Sci 268:11–17

    Article  CAS  PubMed  Google Scholar 

  • DiMario RJ, Quebedeaux JC, Longstreth DJ, Dassanayake M et al (2016) The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2. Plant Physiol 171(1):280–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dionisio-Sese ML, Fukuzawa H, Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 94:1103–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreyer A, Schackmann A, Kriznik A, Chibani K et al (2020) Thiol redox regulation of plant β-carbonic anhydrase. Biomolecules 10(8):1125

    Article  CAS  PubMed Central  Google Scholar 

  • Dutilleul C, Driscoll S, Cornic G, De Paepe R et al (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131(1):264–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engineer CB, Ghassemian M, Anderson JC, Peck SC et al (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513(7517):246–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson M, Karlsson J, Ramazanov Z, Gardestrom P et al (1996) Discovery of an algal mitochondrial carbonic anhydrase: Molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci 93(21):12031–12034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson M, Villand P, Gardeström P, Samuelsson G (1998) Induction and regulation of expression of a low-CO2 -induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 116(2):637–641

    Article  Google Scholar 

  • Escudero-Almanza DJ, Ojeda-Barrios DL, Hernández-Rodríguez OA, Sánchez Chávez E et al (2012) Carbonic anhydrase and zinc in plant physiology. Chilean Journal of Agricultural Research 72(1):140–146

    Article  Google Scholar 

  • Evers D, Legay S, Lamoureux D, Hausman JF et al (2012) Towards a synthetic view of potato cold and salt stress response by transcriptomic and proteomic analyses. Plant Mol Biol 78(4–5):503–514

    Article  CAS  PubMed  Google Scholar 

  • Everson RG, Slack CR (1968) Distribution of carbonic anhydrase in relation to the C4 pathway of photosynthesis. Phytochemistry 7(4):581–584

    Article  CAS  Google Scholar 

  • Fabre N, Reiter IM, Becuwe-Linka N, Genty B et al (2007) Characterization and expression analysis of genes encoding α and β carbonic anhydrases in Arabidopsis. Plant, Cell Environ 30(5):617–629

    Article  CAS  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(2):585–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrio JP, Pou A, Florez-Sarasa I, Gessler A et al (2012) The Péclet effect on leaf water enrichment correlates with leaf hydraulic conductance and mesophyll conductance for CO2: Oxygen isotopes, leaf hydraulics and mesophyll. Plant, Cell Environ 35(3):611–625

    Article  CAS  Google Scholar 

  • Fisher M, Gokhman I, Pick U, Zamir A (1996) A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 271(30):17718–17723

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Barbour MM, Brendel O, Cabrera HM et al (2012) Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis. Plant Sci 193–194:70–84

    Article  PubMed  Google Scholar 

  • Flexas J, Barón M, Bota J, Ducruet J-M et al (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri×V. rupestris). Journal of Experimental Botany 60(8):2361–2377

  • Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2017) The effects of pharmacological carbonic anhydrase suppression on defence responses of potato leaves to Phytophthora infestans. Journal of Plant Science and Phytopathology 1(1):011–025

    Article  Google Scholar 

  • Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2017) The multifunctional face of plant carbonic anhydrase. Plant Physiol Biochem 112:362–368

    Article  Google Scholar 

  • Fromm S, Senkler J, Zabaleta E, Peterhänsel C et al (2016) The carbonic anhydrase domain of plant mitochondrial complex I. Physiol Plant 157(3):289–296

    Article  CAS  PubMed  Google Scholar 

  • Rowlett RS (2014) Structure and catalytic mechanism of β-carbonic anhydrases. In: Frost SC and McKenna R (eds) Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications. Springer, Dordrecht, pp 53–76

  • 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 87(24):9779–9783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML et al (1990) cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: Regulation by environmental CO2 concentration. Proc Natl Acad Sci 87(11):4383–4387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galle A, Florez-Sarasa I, Tomas M, Pou A et al (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): Acclimation or limitation? J Exp Bot 60(8):2379–2390

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Zhou Y, Zhu W, Li X et al (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230(5):1033–1046

    Article  CAS  PubMed  Google Scholar 

  • Gee CW, Niyogi KK (2017) The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. Proc Natl Acad Sci 114(17):4537–4542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geilfus C-M (2017) The pH of the apoplast: dynamic factor with functional impact under stress. Molecular Plant 10(11):1371–1386

    Article  CAS  PubMed  Google Scholar 

  • Geng S, Misra BB, de Armas E, Huhman DV et al (2016) Jasmonate-mediated stomatal closure under elevated CO2 revealed by time-resolved metabolomics. Plant J 88(6):947–962

    Article  CAS  PubMed  Google Scholar 

  • Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M et al (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. Journal of Proteomics 94:289–301

    Article  CAS  PubMed  Google Scholar 

  • Gillon JS, Yakir D (2000) Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves. Plant Physiol 123(1):201–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA et al (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47(5):720–734

    Article  CAS  PubMed  Google Scholar 

  • Goyal A, Shiraiwa Y, Husic HD, Tolbert NE (1992) External and internal carbonic anhydrases in Dunaliella species. Mar Biol 113(3):349–355

    Article  CAS  Google Scholar 

  • Gu J-F, Qiu M, Yang J-C (2013) Enhanced tolerance to drought in transgenic rice plants overexpressing C4 photosynthesis enzymes. The Crop Journal 1(2):105–114

    Article  Google Scholar 

  • Gulick PJ, Drouin S, Yu Z, Danyluk J et al (2005) Transcriptome comparison of winter and spring wheat responding to low temperature. Genome 48(5):913–923

    Article  CAS  PubMed  Google Scholar 

  • Guliyev N, Bayramov S, Babayev H (2008) Effect of water deficit on Rubisco and carbonic anhydrase activities in different wheat genotypes. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the Sun, pp 1465–1468

  • Guo W-L, Chen R-G, Gong Z-H, Yin Y-X et al (2013) Suppression subtractive hybridization analysis of genes regulated by application of exogenous abscisic acid in pepper plant (Capsicum annuum L.) leaves under chilling stress. PLoS ONE 8(6):e66667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gӧtz R, Gnann A, Zimmermann FK (1999) Deletion of the carbonic anhydrase-like gene NCE103 of the yeast Saccharomyces cerevisiae causes an oxygen-sensitive growth defect. Yeast 15:855–864

    Article  Google Scholar 

  • Hagemann M, Kaplan A (2020) Is the structure of the CO2-hydrating complex I compatible with the cyanobacterial CO2-concentrating mechanism? Plant Physiol 183(2):460–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han X, Sun N, Xu M, Mi H (2017) Co-ordination of NDH and Cup proteins in CO2 uptake in cyanobacterium Synechocystis sp. PCC 6803. Journal of Experimental Botany 68(14):3869–3877

  • Hang H, Wu Y (2019) Effect of bicarbonate stress on carbonic anhydrase gene expressions from Orychophragmus violaceus and Brassica juncea seedlings. Polish Journal of Environmental Studies 28(3):1135–1143

    Article  Google Scholar 

  • Hanson MR, Hines KM (2018) Stromules: Probing formation and function. Plant Physiol 176(1):128–137

    Article  CAS  PubMed  Google Scholar 

  • Hasan SA, Ali B, Hayat S, Ahmad A (2007) Cadmium-induced changes in the growth and carbonic anhydrase activity of chickpea. Turk J Biol 31:137–140

    CAS  Google Scholar 

  • Hayat S, Hasan SA, Fariduddin Q, Ahmad A (2008) Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. Journal of Plant Interactions 3(4):297–304

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Ahmad A (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Botanica Croatica 72(2):323–335

  • Hayat S, Yadav S, Alyemeni MN, Irfan M et al (2013) Alleviation of salinity stress with sodium nitroprusside in tomato. Int J Veg Sci 19(2):164–176

    Article  Google Scholar 

  • Hoang CV, Chapman KD (2002) Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves. Plant Physiol 128(4):1417–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoang CV, Chapman KD (2002) Regulation of carbonic anhydrase gene expression in cotyledons of cotton (Gossypium hirsutum L.) seedlings during post-germinative growth. Plant Mol Biol 49:449–458

    Article  CAS  PubMed  Google Scholar 

  • Hopkinson BM, Dupont CL, Matsuda Y (2016) The physiology and genetics of CO2 concentrating mechanisms in model diatoms. Curr Opin Plant Biol 31:51–57

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Rappel W-J, Occhipinti R, Ries A et al (2015) Distinct cellular locations of carbonic anhydrases mediate carbon dioxide control of stomatal movements. Plant Physiol 169(2):1168–1178

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang J, Li Z, Biener G, Xiong E et al (2017) Carbonic anhydrases function in anther cell differentiation downstream of the receptor-like kinase EMS1. Plant Cell 29(6):1335–1356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang W, Han S, Jiang H, Gu S et al (2020) External α-carbonic anhydrase and solute carrier 4 (SLC4) are required for HCO3- uptake in a freshwater angiosperm. J Exp Bot 71(19):6004–6014

    Article  CAS  PubMed  Google Scholar 

  • Iverson TM, Alber BE, Kisker C, Ferry JG et al (2000) A closer look at the active site of γ-class carbonic anhydrases: High-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. Biochemistry 39(31):9222–9231

    Article  CAS  PubMed  Google Scholar 

  • Jensen EL, Clement R, Kosta A, Maberly SC et al (2019) A new widespread subclass of carbonic anhydrase in marine phytoplankton. The ISME Journal 13(8):2094–2106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang C, Tholen D, Xu JM, Xin C et al (2014) Increased expression of mitochondria-localized carbonic anhydrase activity resulted in an increased biomass accumulation in Arabidopsis thaliana. J Plant Biol 57(6):366–374

    Article  CAS  Google Scholar 

  • Jin S, Sun J, Wunder T, Tang D et al (2016) Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases. Proc Natl Acad Sci 113(51):14716–14721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaul T, Reddy PS, Mahanty S, Thirulogachandar V et al (2011) Biochemical and molecular characterization of stress-induced β-carbonic anhydrase from a C4 plant, Pennisetum glaucum. J Plant Physiol 168(6):601–610

    Article  CAS  PubMed  Google Scholar 

  • Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36(2):141–154

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA, Melnicki MR (2016) Assembly, function and evolution of cyanobacterial carboxysomes. Curr Opin Plant Biol 31:66–75

    Article  CAS  PubMed  Google Scholar 

  • Khan NA, Singh S, Anjum NA, Nazar R (2008) Cadmium effects on carbonic anhydrase, photosynthesis, dry mass and antioxidative enzymes in wheat (Triticum aestivum) under low and sufficient zinc. J Plant Interact 3(1):31–37

    Article  CAS  Google Scholar 

  • Kieffer P, Dommes J, Hoffmann L, Hausman J-F et al (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8(12):2514–2530

    Article  CAS  PubMed  Google Scholar 

  • Kieffer P, Planchon S, Oufir M, Ziebel J et al (2009) Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J Proteome Res 8(1):400–417

    Article  CAS  PubMed  Google Scholar 

  • Kikutani S, Nakajima K, Nagasato C, Tsuji Y et al (2016) Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci 113(35):9828–9833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimber MS (2014) Carboxysomal carbonic anhydrases. In: Frost SC and McKenna R (eds) Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications. Springer, Dordrecht, pp 89–103

  • Kimber MS, Pai EF (2000) The active site architecture of Pisum sativum β-carbonic anhydrase is a mirror image of that of α-carbonic anhydrases. EMBO J 19(7):1407–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klimenko O, Pernis M, Danchenko M, Skultéty L et al (2019) Natural ecotype of Arabidopsis thaliana (L.) Heynh (Chernobyl-07) respond to cadmium stress more intensively than the sensitive ecotypes Oasis and Columbia. Ecotoxicol Environ Saf 173:86–95

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Satone H, Tan E, Kurokochi H et al (2015) Transcriptional responses of a bicarbonate-tolerant monocot, Puccinellia tenuiflora, and a related bicarbonate-sensitive species, Poa annua, to NaHCO3 Stress. Int J Mol Sci 16(1):496–509

    Article  Google Scholar 

  • Kolbe AR, Brutnell TP, Cousins AB, Studer AJ (2018) Carbonic anhydrase mutants in Zea mays have altered stomatal responses to environmental signals. Plant Physiol 177(3):980–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krupa Z (1999) Cadmium against higher plant photosynthesis – a variety of effects and where do they possibly come from? Zeitschrift Für Naturforschung C 54(9–10):723–729

    Article  CAS  Google Scholar 

  • Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L et al (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153(4):1149–1156

    Article  CAS  PubMed  Google Scholar 

  • Kupriyanova EV, Sinetova MA, Markelova AG, Allakhverdiev SI et al (2011) Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes. J Photochem Photobiol B Biol 103(1):78–86

    Article  CAS  Google Scholar 

  • Kupriyanova EV, Sinetova MA, Mironov KS, Novikova GV et al (2019) Highly active extracellular α-class carbonic anhydrase of Cyanothece sp. ATCC 51142. Biochimie 160:200–209

    Article  CAS  PubMed  Google Scholar 

  • Lane TW, Morel FMM (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol 123(1):345–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazova GN, Kicheva MI, Popova LP (1999) The effect of abscisic acid and methyl jasmonate on carbonic anhydrase activity in pea. Photosynthetica 36(4):631–634

    Article  CAS  Google Scholar 

  • Li P, Liu H, Yang H, Pu X et al (2020) Translocation of drought-responsive proteins from the chloroplasts. Cells 9(1):259

    Article  CAS  PubMed Central  Google Scholar 

  • Li T, Sharp CE, Ataeian M, Strous M et al (2018) Role of extracellular carbonic anhydrase in dissolved inorganic carbon uptake in alkaliphilic phototrophic biofilm. Frontiers in Microbiology 9:2490

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin M, Oliver DJ (2008) The role of acetyl-coenzyme A synthetase in Arabidopsis. Plant Physiol 147(4):1822–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lionetto M, Caricato R, Giordano M, Erroi E et al (2012) Carbonic anhydrase as pollution biomarker: An ancient enzyme with a new use. International Journal of Environmental Research and Public Health 9(11):3965–3977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lionetto M, Caricato R, Giordano M, Schettino T (2016) The complex relationship between metals and carbonic anhydrase: New insights and perspectives. Int J Mol Sci 17(1):127

    Article  PubMed Central  Google Scholar 

  • Liska AJ, Shevchenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136(1):2806–2817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Chen K, Zhao X, Wang X et al (2019) Identification of genes for salt tolerance and yield-related traits in rice plants grown hydroponically and under saline field conditions by genome-wide association study. Rice 12(1):88

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Tang Y, Qiu R, Ying R et al (2016) Responses of carbonic anhydrase to cadmium in the zinc/cadmium hyperaccumulator Picris divaricata vant. Pedosphere 26(5):709–716

    Article  CAS  Google Scholar 

  • Liu W, Ming Y, Li P, Huang Z (2012) Inhibitory effects of hypo-osmotic stress on extracellular carbonic anhydrase and photosynthetic efficiency of green alga Dunaliella salina possibly through reactive oxygen species formation. Plant Physiol Biochem 54:43–48

    Article  CAS  PubMed  Google Scholar 

  • Mackinder LCM (2018) The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytol 217(1):54–61

    Article  CAS  PubMed  Google Scholar 

  • Mackinder LCM, Chen C, Leib RD, Patena W et al (2017) A spatial interactome reveals the protein organization of the algal CO2 concentrating mechanism. Cell 171(1):133-147.e14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda S, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942: Mechanism of CO2 uptake in cyanobacteria. Molecular Microbiology 43(2):425–435

  • Mager S, Schönberger B, Ludewig U (2018) The transcriptome of zinc deficient maize roots and its relationship to DNA methylation loss. BMC Plant Biol 18(1):372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Majeau N, Arnoldo M, Coleman JR (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol Biol 25(3):377–385

    Article  CAS  PubMed  Google Scholar 

  • Majeau N, Coleman JR (1996) Effect of CO2 concentration on carbonic anhydrase and ribulose-1,5 -bisphosphate carboxylase/oxygenase expression in pea. Plant Physiol 112:569–574

  • Malasarn D, Kropat J, Hsieh SI, Finazzi G et al (2013) Zinc deficiency impacts CO2 assimilation and disrupts copper homeostasis in Chlamydomonas reinhardtii. J Biol Chem 288(15):10672–10683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin CL, Tortell PD (2008) Bicarbonate transport and extracellular carbonic anhydrase in marine diatoms. Physiol Plant 133(1):106–116

    Article  CAS  PubMed  Google Scholar 

  • Medina-Puche L, Castelló MJ, Canet JV, Lamilla J et al (2017) β-carbonic anhydrases play a role in salicylic acid perception in Arabidopsis. PLoS ONE 12(7):e0181820

    Article  PubMed  PubMed Central  Google Scholar 

  • Mizokami Y, Noguchi K, Kojima M, Sakakibara H et al (2015) Mesophyll conductance decreases in the wild type but not in an ABA-deficient mutant (aba1) of Nicotiana plumbaginifolia under drought conditions: Stomatal and mesophyll CO2 conductances under drought conditions. Plant, Cell Environ 38(3):388–398

    Article  CAS  Google Scholar 

  • Momayyezi M, Guy RD (2017) Substantial role for carbonic anhydrase in latitudinal variation in mesophyll conductance of Populus trichocarpa Torr. & Gray. Plant Cell Enviro 40(1):138–149

  • Momayyezi M, McKown AD, Bell SCS, Guy RD (2020) Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis. Plant J 101(4):831–844

    Article  CAS  PubMed  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79(1):177–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6(8):1251–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller WEG, Qiang L, Schröder HC, Hönig N et al (2014) Carbonic anhydrase: A key regulatory and detoxifying enzyme for Karst plants. Planta 239(1):213–229

    Article  PubMed  Google Scholar 

  • Nettles WL, Song H, Farquhar ER, Fitzkee NC et al (2015) Characterization of the copper(II) binding sites in human carbonic anhydrase II. Inorg Chem 54(12):5671–5680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osborn HL, Alonso-Cantabrana H, Sharwood RE, Covshoff S et al (2017) Effects of reduced carbonic anhydrase activity on CO2 assimilation rates in Setaria viridis: A transgenic analysis. J Exp Bot 68(2):299–310

    Article  CAS  PubMed  Google Scholar 

  • Pal A, Borthakur D (2014) Tissue-specific differential expression of two β-carbonic anhydrases in Leucaena leucocephala under abiotic stress conditions. Journal of Applied Biotechnology 2(2):43–64

    Article  Google Scholar 

  • Pannetier F, Ohanessian G, Frison G (2011) Comparison between α- and β-carbonic anhydrases: Can Zn(His)3(H2O) and Zn(His)(Cys)2(H2O) sites lead to equivalent enzymes? Dalton Trans 40(12):2696–2698

    Article  CAS  PubMed  Google Scholar 

  • Perales M, Eubel H, Heinemeyer J, Colaneri A et al (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I+III2 levels and alters mitochondrial physiology in Arabidopsis. J Mol Biol 350(2):263–277

    Article  CAS  PubMed  Google Scholar 

  • Perez-Martin A, Michelazzo C, Torres-Ruiz JM, Flexas J et al (2014) Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: Correlation with gene expression of carbonic anhydrase and aquaporins. J Exp Bot 65(12):3143–3156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poincelot RP (1972) Intracellular distribution of carbonic anhydrase in spinach leaves. Biochimica et Biophysica Acta (BBA) - Enzymology 258(2):637–642

  • Polesani M, Desario F, Ferrarini A, Zamboni A et al (2008) cDNA-AFLP analysis of plant and pathogen genes expressed in grapevine infected with Plasmopara viticola. BMC Genomics 9(1):142

    Article  PubMed  PubMed Central  Google Scholar 

  • Polishchuk AV, Semenikhin AV, Topchyi NM, Zolotareva EK (2018) Inhibition of multiple forms of carbonic anhydrases of spinach chloroplasts by Cu ions. Rep Nat Acad Sci Ukraine 4:94–101

  • Popova PL, Stoinova ZC (2000) Photosynthetic characteristics in drought-stressed wheat (Triticum aestivum L.) plants. Comptes Rendus de l'Academie Bulgare des Sciencesi 53(9):77–80

  • Popova LP, Tsonev TD, Lazova GN, Stoinova ZG (1996) Drought- and ABA-induced changes in photosynthesis of barley plants. Physiol Plant 96(4):623–629

    Article  CAS  Google Scholar 

  • Poschenrieder C, Fernández J, Rubio L, Pérez L et al (2018) Transport and use of bicarbonate in plants: Current knowledge and challenges ahead. Int J Mol Sci 19(5):1352

    Article  PubMed Central  Google Scholar 

  • Price GD, 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 

  • Proietti S, Bertini L, Timperio AM, Zolla L et al (2013) Crosstalk between salicylic acid and jasmonate in Arabidopsis investigated by an integrated proteomic and transcriptomic approach. Mol BioSyst 9(6):1169

    Article  CAS  PubMed  Google Scholar 

  • Qu C, He Y, Zheng Z, An M et al (2017) Cloning, expression analysis and enzyme activity assays of the α-carbonic anhydrase gene from Chlamydomonas sp. ICE-L. Molecular Biotechnology 60(1):21–30

    Article  Google Scholar 

  • Randall PJ, Bouma D (1973) Zinc deficiency, carbonic anhydrase, and photosynthesis in leaves of spinach. Plant Physiol 52(3):229–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao S, Wu Y (2017) Root-derived bicarbonate assimilation in response to variable water deficit in Camptotheca acuminate seedlings. Photosynth Res 134(1):59–70

    Article  CAS  PubMed  Google Scholar 

  • Rawat M, Moroney JV (1995) The regulation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiol 109:937–944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Restrepo S, Myers KL, del Pozo O, Martin GB et al (2005) Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol Plant Microbe Interact 18(9):913–922

    Article  CAS  PubMed  Google Scholar 

  • Riazunnisa K, Padmavathi L, Bauwe H, Raghavendra AS (2006) Markedly low requirement of added CO2 for photosynthesis by mesophyll protoplasts of pea (Pisum sativum): Possible roles of photorespiratory CO2 and carbonic anhydrase. Physiol Plant 128(4):763–772

    Article  CAS  Google Scholar 

  • Rowlett RS (2010) Structure and catalytic mechanism of the β-carbonic anhydrases. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 1804(2):362–373

  • Rudenko NN, Borisova-Mubarakshina MM, Ignatova LK, Fedorchuk TP et al (2020) Role of plant carbonic anhydrases under stress conditions [Online First], IntechOpen, https://doi.org/10.5772/intechopen.91971

  • Rudenko NN, Vetoshkina DV, Fedorchuk TP, Ivanov BN (2017) Effect of light intensity under different photoperiods on expression level of carbonic anhydrase genes of the α- and β-families in Arabidopsis thaliana leaves. Biochemistry (Moscow) 82(9):1025–1035

    Article  CAS  Google Scholar 

  • Rudenko NN, Fedorchuk TP, Terentyev VV, Dymova OV et al (2019) The role of carbonic anhydrase α-CA4 in the adaptive reactions of photosynthetic apparatus: The study with α-CA4 knockout plants. Protoplasma 257(2):489–499

    Article  PubMed  Google Scholar 

  • Rudenko NN, Ignatova LK, Zhurikova EM, Novichkova NS et al (2018) Plant carbonic anhydrases, their role in stress defense and possible practical use. J Stress Physiol Biochem 14(1):27–38

    Google Scholar 

  • Rumeau D, Cuiné S, Fina L, Gault N et al (1996) Subcellular distribution of carbonic anhydrase in Solanum tuberosum L. leaves: Characterization of two compartment-specific isoforms. Planta 199(1):79–88

  • Salama ZA, El-Fouly MM, Lazova G, Popova LP (2006) Carboxylating enzymes and carbonic anhydrase functions were suppressed by zinc deficiency in maize and chickpea plants. Acta Physiol Plant 28(5):445–451

    Article  CAS  Google Scholar 

  • Samukawa M, Shen C, Hopkinson BM, Matsuda Y (2014) Localization of putative carbonic anhydrases in the marine diatom. Thalassiosira pseudonana Photosynthesis Research 121(2–3):235–249

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP et al (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci 97(21):11655–11660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuller JM, Saura P, Thiemann J, Schuller SK et al (2020) Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nature Communications 11(1):494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semenikhin AV, Vodka MV, Polishchuk OV (2016) Cofactor and structural role of CO2 in chloroplasts. Ukrainian Botanical Journal 73(3):290–297

    Article  Google Scholar 

  • Shiraiwa Y, Miyachi S (1983) Factors controlling induction of carbonic anhydrase and efficiency of photosynthesis in Chlorella vulgaris 11h cells. Plant Cell Physiol 24(5):919–923

    Article  CAS  Google Scholar 

  • Shitov AV, Terentyev VV, Zharmukhamedov SK, Rodionova MV et al (2018) Is carbonic anhydrase activity of photosystem II required for its maximum electron transport rate? Biochimica et Biophysica Acta (BBA) - Bioenergetics 1859(4):292–299

  • Siedlecka A, Gardeström P, Samuelsson G, Kleczkowski LA et al (1999) A relationship between carbonic anhydrase and Rubisco in response to moderate cadmium stress during light activation of photosynthesis. Zeitschrift Für Naturforschung C 54(9–10):759–763

    Article  CAS  Google Scholar 

  • Slaymaker DH, Navarre DA, Clark D, del Pozo O et al (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci 99(18):11640–11645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorrentino G, Haworth M, Wahbi S, Mahmood T et al (2016) Abscisic acid induces rapid reductions in mesophyll conductance to carbon dioxide. PLoS ONE 11(2):e0148554

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto D, Córdoba JP, Villarreal F, Bartoli C et al (2015) Functional characterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I in Arabidopsis thaliana. Plant J 83(5):831–844

    Article  CAS  PubMed  Google Scholar 

  • Studer AJ, Gandin A, Kolbe AR, Wang L et al (2014) A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant Physiol 165(2):608–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun N, Han X, Xu M, Kaplan A et al (2019) A thylakoid‐located carbonic anhydrase regulates CO2 uptake in the cyanobacterium Synechocystis sp. PCC 6803. New Phytologist 222(1):206–217

  • Sun Q, Zybailov B, Majeran W, Friso G et al (2009) PPDB, the plant proteomics database at cornell. Nucleic Acids Research 37(suppl_1):D969–D974

  • Sun WH, Wu QX, Wen XY, He HG et al (2015) Changes of carbonic anhydrase activities in tomato leaves under drought stress. Zhiwu Shengli Xuebao/Plant Physiology Journal 51(4):424–428

    CAS  Google Scholar 

  • Sun WH, Wu YY, Wen XY, Xiong SJ et al (2016) Different mechanisms of photosynthetic response to drought stress in tomato and violet orychophragmus. Photosynthetica 54(2):226–233

    Article  CAS  Google Scholar 

  • Supuran CT (2016) Structure and function of carbonic anhydrases. Biochemical Journal 473(14):2023–2032

    Article  CAS  Google Scholar 

  • Tachibana M, Allen AE, Kikutani S, Endo Y et al (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth Res 109(1–3):205–221

    Article  CAS  PubMed  Google Scholar 

  • Tavallali V, Rahemi M, Maftoun M, Panahi B et al (2009) Zinc influence and salt stress on photosynthesis, water relations, and carbonic anhydrase activity in pistachio. Sci Hortic 123(2):272–279

    Article  CAS  Google Scholar 

  • Tcherkez G, Bligny R, Gout E, Mahe A et al (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proc Natl Acad Sci 105(2):797–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tcherkez G, Gauthier P, Buckley TN, Busch FA et al (2017) Leaf day respiration: Low CO2 flux but high significance for metabolism and carbon balance. New Phytol 216(4):986–1001

    Article  Google Scholar 

  • Tchernov D, Helman Y, Keren N, Luz B et al (2001) Passive entry of CO2 and its energy-dependent intracellular conversion to HCO3- in cyanobacteria are driven by a photosystem I-generated ΔμH +. J Biol Chem 276(26):23450–23455

    Article  CAS  PubMed  Google Scholar 

  • Terentyev VV, Shukshina AK, Shitov AV (2019) Carbonic anhydrase CAH3 supports the activity of photosystem II under increased pH. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1860(7):582–590

  • Tholen D, Zhu X-G (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol 156(1):90–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Topchiy NM, Polishchuk OV, Zolotareva EK, Sytnyk SK (2019) The influence of Cd2+ ions on the activity of stromal carbonic anhydrases of spinach chloroplasts. Fiziol Rast Genet 51(2):172–182

    Article  Google Scholar 

  • Uehlein N, Sperling H, Heckwolf M, Kaldenhoff R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant, Cell Environ 35(6):1077–1083

    Article  CAS  Google Scholar 

  • Villarejo A, Shutova T, Moskvin O, Klimov VV (2002) A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J 21(8):1930–1938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vodka MV, Polishchuk OV, Bilyavs’ka NO, Zolotareva EK (2013) Effects of heavy metals on photosynthetic apparatus and carbonic anhydrase activity in pea chloroplasts. Newsletter of the Kharkiv National agrarian university 30(3):46–55

    Google Scholar 

  • Von Caemmerer S, Quinn V, Hancock NC, Price GD et al (2004) Carbonic anhydrase and C4 photosynthesis: A transgenic analysis. Plant, Cell Environ 27(6):697–703

    Article  Google Scholar 

  • Wang L, Jin X, Li Q, Wang X et al (2016) Comparative proteomics reveals that phosphorylation of β carbonic anhydrase 1 might be important for adaptation to drought stress in Brassica napus. Scientific Reports 6(1):39024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Yang C, Chen H, Song C et al (2017) Transcriptomic basis for drought-resistance in Brassica napus L. Scientific Reports 7(1):40532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Wu Y, Xing D, Hang H et al (2017) Biomass production of three biofuel energy plants’ use of a new carbon resource by carbonic anhydrase in simulated karst soils: Mechanism and capacity. Energies 10(9):1370

    Article  Google Scholar 

  • Wang Y, Spalding MH (2014) Acclimation to very low CO2: Contribution of limiting CO2 inducible proteins, LCIB and LCIA, to inorganic carbon uptake in Chlamydomonas reinhardtii. Plant Physiol 166(4):2040–2050

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y-Q, Feechan A, Yun B-W, Shafiei R et al (2009) S-Nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284(4):2131–2137

    Article  CAS  PubMed  Google Scholar 

  • Wani AS, Ahmad A, Hayat S, Fariduddin Q (2013) Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi Journal of Biological Sciences 20(2):183–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams JR (1996) Photosynthetic gas exchange and discrimination against 13CO2, and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. Plant Physiol 112:319–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193(4):530–535

    Article  CAS  Google Scholar 

  • Wood J, Sibly PM (1952) Carbonic anhydrase activity in plants in relation to zinc content. Aust J Biol Sci 5(2):244–255

    Article  CAS  Google Scholar 

  • Wu Y-Y, Liu C-Q, Li P-P, Wang J-Z et al (2009) Photosynthetic characteristics involved in adaptability to Karst soil and alien invasion of paper mulberry (Broussonetia papyrifera (L.) Vent.) in comparison with mulberry (Morus alba L.). Photosynthetica 47(1):155–160

  • Wu Y, Vreugdenhil D, Liu C, Fu W (2012) Expression of carbonic anhydrase genes under dehydration and osmotic stress in Arabidopsis thaliana leaves. Adv Sci Lett 17(1):261–265

  • Xing DK, Wu YY, Wang R, Fu WG et al (2015) Effects of drought stress on photosynthesis and glucose-6-phosphate dehydrogenase activity of two biomass energy plants (Jatropha curcas L. and Vernicia fordii h.). J. Anim. Plant Sci. 25(3 Suppl. 1):172–179

  • Yang S-Y, Tsuzuki M, Miyachi S (1985) Carbonic anhydrase of Chlamydomonas: Purification and studies on its induction using antiserum against Chlamydomonas carbonic anhydrase. Plant Cell Physiol 26(1):25–34

  • Yamano T, Tsujikawa T, Hatano K, Ozawa S et al (2010) Light and low-CO2-dependent LCIB–LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 51(9):1453–1468

    Article  CAS  PubMed  Google Scholar 

  • Ynalvez RA, Xiao Y, Ward AS, Cunnusamy K et al (2008) Identification and characterization of two closely related β-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol Plant 133(1):15–26

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Chen S, Wang T, Sun G et al (2013) Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress. Int J Mol Sci 14(1):1740–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J-W, Price GD, Song L, Badger MR (1992) Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100(2):794–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu S, Zhang X, Guan Q, Takano T et al (2007) Expression of a carbonic anhydrase gene is induced by environmental stresses in Rice (Oryza sativa L.). Biotechnology Letters 29(1):89–94

  • Zabaleta E, Martin MV, Braun H-P (2012) A basal carbon concentrating mechanism in plants? Plant Sci 187:97–104

    Article  CAS  PubMed  Google Scholar 

  • Zhang C-K, Lang P, Ebel RC, Dane F et al (2005) Down-regulated gene expression of cold acclimated Poncirus trifoliata. Can J Plant Sci 85(2):417–424

    Article  CAS  Google Scholar 

  • Zhou Y, Vroegop-Vos IA, Van Dijken AJH, Van der Does D et al (2020) Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance. Planta 251(4):75

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author is very thankful to prof. Elena Zolotareva, head of Membranology and Phytochemistry Department of M.G. Kholodny Institute of botany of NAS of Ukraine for continuous encouraging support.

Author information

Authors and Affiliations

  1. Membranology and Phytochemistry Department, M.G. Kholodny Institute of Botany of NAS of Ukraine, 2 Tereshchenkivska Str, Kyiv, 01004, Ukraine

    O. V. Polishchuk

Authors
  1. O. V. Polishchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Polishchuk.

Additional information

Communicated by Gerhard Leubner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Polishchuk, O.V. Stress-Related Changes in the Expression and Activity of Plant Carbonic Anhydrases. Planta 253, 58 (2021). https://doi.org/10.1007/s00425-020-03553-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-020-03553-5

Keywords

Search

Navigation