\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
\n'}],latestNews:[{slug:"intechopen-signs-new-contract-with-cepiec-china-for-distribution-of-open-access-books-20210319",title:"IntechOpen Signs New Contract with CEPIEC, China for Distribution of Open Access Books"},{slug:"150-million-downloads-and-counting-20210316",title:"150 Million Downloads and Counting"},{slug:"intechopen-secures-indefinite-content-preservation-with-clockss-20210309",title:"IntechOpen Secures Indefinite Content Preservation with CLOCKSS"},{slug:"intechopen-expands-to-all-global-amazon-channels-with-full-catalog-of-books-20210308",title:"IntechOpen Expands to All Global Amazon Channels with Full Catalog of Books"},{slug:"stanford-university-identifies-top-2-scientists-over-1-000-are-intechopen-authors-and-editors-20210122",title:"Stanford University Identifies Top 2% Scientists, Over 1,000 are IntechOpen Authors and Editors"},{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"}]},book:{item:{type:"book",id:"5513",leadTitle:null,fullTitle:"Dynamical Systems - Analytical and Computational Techniques",title:"Dynamical Systems",subtitle:"Analytical and Computational Techniques",reviewType:"peer-reviewed",abstract:"There has been a considerable progress made during the recent past on mathematical techniques for studying dynamical systems that arise in science and engineering. 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Parker",authors:[{id:"67415",title:"Prof.",name:"Tetsuji",middleName:null,surname:"Muto",fullName:"Tetsuji Muto",slug:"tetsuji-muto"}]},{id:"27597",title:"Numerical Geodynamic Modeling of Continental Convergent Margins",slug:"numerical-geodynamic-modeling-of-continental-convergent-margins",signatures:"Zhonghai Li, Zhiqin Xu and Taras Gerya",authors:[{id:"66906",title:"Dr.",name:"Zhong-Hai",middleName:null,surname:"Li",fullName:"Zhong-Hai Li",slug:"zhong-hai-li"},{id:"116531",title:"Prof.",name:"Zhiqin",middleName:null,surname:"Xu",fullName:"Zhiqin Xu",slug:"zhiqin-xu"},{id:"116533",title:"Prof.",name:"Taras",middleName:null,surname:"Gerya",fullName:"Taras Gerya",slug:"taras-gerya"}]},{id:"27598",title:"The Thermogeographic Model in Paleogeography: Application of an Abiotic Model to a Plate Tectonic World",slug:"the-thermogeographic-model-in-paleogeography-application-of-an-abiotic-model-to-a-plate-tectonic-wor",signatures:"Lee-Ann C. Hayek and Walter H. Adey",authors:[{id:"65332",title:"Dr.",name:"Walter",middleName:null,surname:"Adey",fullName:"Walter Adey",slug:"walter-adey"},{id:"117553",title:"Dr.",name:"Lee-Ann C.",middleName:null,surname:"Hayek",fullName:"Lee-Ann C. Hayek",slug:"lee-ann-c.-hayek"}]},{id:"27599",title:"Mesothermal Lode Gold Deposit Central Belt Peninsular Malaysia",slug:"mesothermal-lode-gold-deposit-central-belt-peninsular-malaysia",signatures:"Kamar Shah Ariffin",authors:[{id:"65772",title:"Prof.",name:"Kamar Shah",middleName:null,surname:"Ariffin",fullName:"Kamar Shah Ariffin",slug:"kamar-shah-ariffin"}]},{id:"27600",title:"Computer Aided Ore Body Modelling and Mine Valuation",slug:"computer-aided-ore-body-modelling-and-mine-valuation",signatures:"Kaan Erarslan",authors:[{id:"65290",title:"Prof.",name:"Kaan",middleName:null,surname:"Erarslan",fullName:"Kaan Erarslan",slug:"kaan-erarslan"}]},{id:"27601",title:"Mud Volcano and Its Evolution",slug:"mud-volcano-and-its-evolution",signatures:"Bambang P. Istadi, Handoko T. Wibowo, Edy Sunardi, Soffian Hadi and Nurrochmat Sawolo",authors:[{id:"60519",title:"Mr",name:"Bambang",middleName:null,surname:"Istadi",fullName:"Bambang Istadi",slug:"bambang-istadi"},{id:"60529",title:"Mr.",name:"Nurrochmat",middleName:null,surname:"Sawolo",fullName:"Nurrochmat Sawolo",slug:"nurrochmat-sawolo"},{id:"127917",title:"MSc.",name:"Handoko",middleName:"Teguh",surname:"Wibowo",fullName:"Handoko Wibowo",slug:"handoko-wibowo"},{id:"127918",title:"Dr.",name:"Edy",middleName:null,surname:"Sunardi",fullName:"Edy Sunardi",slug:"edy-sunardi"},{id:"127919",title:"Mr.",name:"Soffian",middleName:null,surname:"Hadi",fullName:"Soffian Hadi",slug:"soffian-hadi"}]},{id:"27602",title:"Xujiaweizi Rift Lower Cretaceous Yingcheng Group Volcanic Sequence Stratigraphic Features",slug:"xujiaweizi-rift-lower-cretaceous-yingcheng-group-volcanic-sequence-stratigraphic-features",signatures:"Zhang Yuangao, Chen Shumin, Feng Zhiqiang, Jiang Chuanjin Zhang Erhua, Xin Zhaokun and Dai Shili",authors:[{id:"72093",title:"Dr.",name:"Zhang",middleName:null,surname:"Yuangao",fullName:"Zhang Yuangao",slug:"zhang-yuangao"},{id:"119233",title:"Dr.",name:"Chen",middleName:null,surname:"Shumin",fullName:"Chen Shumin",slug:"chen-shumin"},{id:"119245",title:"Dr.",name:"Jiang",middleName:null,surname:"Chuanjin",fullName:"Jiang Chuanjin",slug:"jiang-chuanjin"},{id:"119319",title:"MSc.",name:"Xin",middleName:null,surname:"Zhaokun",fullName:"Xin Zhaokun",slug:"xin-zhaokun"},{id:"119320",title:"Dr.",name:"Feng",middleName:null,surname:"Zhiqiang",fullName:"Feng Zhiqiang",slug:"feng-zhiqiang"},{id:"119321",title:"MSc.",name:"Dai",middleName:null,surname:"Shili",fullName:"Dai Shili",slug:"dai-shili"},{id:"119322",title:"Dr.",name:"Zhang",middleName:null,surname:"Erhua",fullName:"Zhang Erhua",slug:"zhang-erhua"}]},{id:"27603",title:"Laser Altimetry: What Can Be Learned About Geology and Surface Processes from Detailed Topography",slug:"laser-altimetry-what-can-be-learned-about-geology-and-surface-processes-from-detailed-topography",signatures:"Tim Webster",authors:[{id:"71734",title:"Dr.",name:"Tim",middleName:null,surname:"Webster",fullName:"Tim Webster",slug:"tim-webster"}]},{id:"27604",title:"Remote Predictive Mapping: An Approach for the Geological Mapping of Canada’s Arctic",slug:"remote-predictive-mapping-an-approach-for-the-geological-mapping-of-canada-s-arctic",signatures:"J. R. Harris, E. Schetselaar and P. Behnia",authors:[{id:"63447",title:"Dr.",name:"Jeff",middleName:null,surname:"Harris",fullName:"Jeff Harris",slug:"jeff-harris"}]},{id:"27605",title:"Monitoring of Heavy Metal Concentration in Groundwater of Mamundiyar Basin, India",slug:"monitoring-of-heavy-metal-concentration-in-groundwater-of-mamundiyar-basin-india",signatures:"Imran Ahmad Dar, K. Sankar, Dimitris Alexakis and Mithas Ahmad Dar",authors:[{id:"64247",title:"Dr.",name:"Imran Ahmad",middleName:null,surname:"Dar",fullName:"Imran Ahmad Dar",slug:"imran-ahmad-dar"}]},{id:"27606",title:"Age Dating of Middle-Distillate Fuels Released to the Subsurface Environment",slug:"age-dating-of-middle-distillate-fuels-released-to-the-subsurface-environment",signatures:"Gil Oudijk",authors:[{id:"73697",title:"Mr.",name:"Gil",middleName:null,surname:"Oudijk",fullName:"Gil Oudijk",slug:"gil-oudijk"}]},{id:"27607",title:"Geology and Geomorphology in Landscape Ecological Analysis for Forest Conservation and Hazard and Risk Assessment, Illustrated with Mexican Case Histories",slug:"geology-and-geomorphology-in-landscape-ecological-analysis-for-forest-conservation-and-hazard-and-ri",signatures:"María Concepción García-Aguirre, Román Álvarez and Fernando Aceves",authors:[{id:"71409",title:"Dr",name:null,middleName:null,surname:"GarcĂa-Aguirre",fullName:"GarcĂa-Aguirre",slug:"garcaa-aguirre"}]},{id:"27608",title:"Radiolarian Age Constraints of Mid-Cretaceous Black Shales in Northern Tunisia",slug:"radiolarian-age-constraints-of-mid-cretaceous-black-shales-in-northern-tunisia",signatures:"Ben Fadhel Moez, Soua Mohamed, Zouaghi Taher, Layeb, Mohsen, Amri Ahlem and Ben Youssef Mohamed",authors:[{id:"39860",title:"Dr.",name:"Taher",middleName:null,surname:"Zouaghi",fullName:"Taher Zouaghi",slug:"taher-zouaghi"},{id:"101309",title:"Dr.",name:"Moez",middleName:null,surname:"Ben Fadhel",fullName:"Moez Ben Fadhel",slug:"moez-ben-fadhel"}]},{id:"27609",title:"Miogypsinid Foraminiferal Biostratigraphy from the Oligocene to Miocene Sedimentary Rocks in the Tethys Region",slug:"miogypsinid-foraminiferal-biostratigraphy-from-the-oligocene-to-miocene-sedimentary-rocks-in-the-tet",signatures:"Kuniteru Matsumaru",authors:[{id:"101793",title:"Prof.",name:"Kuniteru",middleName:null,surname:"Matsumaru",fullName:"Kuniteru Matsumaru",slug:"kuniteru-matsumaru"}]}]}]},onlineFirst:{chapter:{type:"chapter",id:"71704",title:"Role of Plant Carbonic Anhydrases under Stress Conditions",doi:"10.5772/intechopen.91971",slug:"role-of-plant-carbonic-anhydrases-under-stress-conditions",body:'Carbonic anhydrases (CAs) are the group of Zn-containing enzymes that are the biological catalysts accelerating both the carbon dioxide hydration reaction and the bicarbonate dehydration reaction:
In the absence of CA, these reactions proceed relatively slowly to ensure the physiological needs of the cell. The CAs were found in cells of all living organisms: prokaryotes, fungi, plants, and animals. Notably, both binding and release of protons in this reaction are important for many biochemical processes in cellular metabolism. All metabolic processes in higher plants and algae, including the electrolyte balance and pH, gluconeogenesis, lipogenesis, ethylene synthesis, and others depend on/require the components of this reaction. In this review, we focus on the functioning of plant CAs, including algae and angiosperms with different types of CO2 fixation: on C3 and C4 organic matter as well as under normal and stress conditions respectively.
CO2 is the main source of carbon in higher plants and algae cells. The compounds with a common name “inorganic carbon” (Ci) were found in nature both in the form of an unhydrated or hydrated carbon dioxide molecule and in the form of a bicarbonate or carbonate ion. The content of various forms of Ci in solution is pH-dependent. CO2 prevails at pH value lower than 6.4, HCO3− at pH between 6.4 and 10.3, and CO32− at a pH of 10.3 and higher [1]. The substrate for the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), which carries out the first Ci fixation reaction in the Benson-Calvin cycle, is the CO2 molecule. This poses difficulties for aquatic photosynthetic organisms, since at pH of 8.0–8.3 in seawater about 95% of Ci is in the form of НСО3−, whereas the dissolved CO2 represents only a small part of Ci. Thus, the main stress that the aquatic photosynthesizers, namely cyanobacteria and algae, especially in the habitats with alkaline water in seas and oceans, have to face is a low CO2 content in their environment. Therefore, these organisms have evolved the mechanisms of Ci concentrating to increase CO2 content near Rubisco. The main role in supplying Ci and converting it from HCO3− to CO2 is played by CAs located in various cellular compartments of cells in aqueous photosynthesizers [2].
The terrestrial higher plants have adapted to survival under constant stress conditions, such as high temperature, high illumination, and low soil moisture, leading to the closure of stomata. They do not suffer from CO2 deficiency since another type of Ci concentrating mechanism, C4 type of photosynthesis, has evolved. The first reaction that ensures the concentrating of Ci in plants of C4 species is converting CO2 to bicarbonate, which is used by phosphoenolpyruvate carboxylase in forming a four-carbon product. It has been established that the CA, which is mainly located in cytoplasm in C4 plants, plays a key role in this transformation. In C4 species, the suppression of the synthesis of these CAs leads to dramatic effects in these plants [3, 4].
In C3 plant leaves, the existence of a Ci-concentrating mechanism has not been stated. At the same time, the story is much more complicated since C3 plants have a large number of genes encoding CAs, the physiological role of which has not been established yet. It is still not entirely clear whether all these genes are expressed, since the expression of a number of CA genes is induced under certain conditions, such as low CO2 [5] and high illumination [6] and osmotic stress [7].
In chloroplasts, performing C3 photosynthesis, at least six CAs have been discovered to date, both soluble and membrane-bound [8], and belonging to different CA families. In the review, we discuss the possible role of two soluble CAs in photosynthesis, one of them was known for a long time [9] and another one discovered rather recently [10]. Both of them are situated in the chloroplast stroma, where carbohydrates from Ci are formed. Thus, here we discuss the functional relationship of these CAs with Rubisco and their response to stress factors. Recent studies show that the CAs are important not only for photosynthesis and for a number of metabolic pathways, including the interconversion of Ci forms, but also they are necessary under certain stress conditions. In this case, changes (fluctuations) in the CA activity can orchestrate the intensity of certain metabolic processes including the rate of photosynthesis [11, 12, 13].
Recently, a functional relationship between cytoplasmic and chloroplast CAs and aquaporins has been found [14, 15, 16]. The last ones are the protein channels that facilitate the transport not only of water, but also of CO2, and even of H2O2 [16], known as a signal molecule in retrograde signaling.
The enzymatic activity and the content of thylakoid CAs also change under stress conditions. CA activity in thylakoids of higher plants was detected in granal thylakoid membranes, enriched with PSII, as well as in lamellar membranes, enriched with PSI and ATPase in thylakoid lumen [17, 18, 19, 20]. Incorporation of these CAs in plant defense systems of higher plants under changing environmental conditions is reviewed.
Based on the conservative nucleotide sequences in the genes encoding CAs, they could be classified into nine evolutionarily independent families (α, β, γ, δ, ζ, ε, η, θ and the recently discovered ι-CAs) [21, 22, 23, 24]. Some researchers do not ascribe ε-CAs to a separate family, since these CAs are highly modified β-CAs [25]. Although these enzymes have completely different primary, tertiary, and quaternary structures and differ in the organization of the active center, they all are called CAs because they catalyze the same reaction using similar catalysis mechanisms.
Representatives of rare and small δ-, ζ-, θ-, and ι-CA families in eukaryotes were found in diatoms and some other unicellular microalgae, whereas α-, β-, and γ-CAs were discovered in most algae species and in all higher plants, including mosses and Lycopodium.
Since all CAs in human cells belong to the α-CA family, this family is the most studied and widespread. Representatives of this family were found in eubacteria [26, 27], ascomycetes [28], algae [29, 30], higher plants [5, 31], and animals [32]. In green algae
All functionally active α-CAs contain three residues of histidine, which are conservative in all active α-CAs. These histidines are the ligands of Zn atom [40, 41] located at the bottom of the conical cavity of the active center. Histidines in α-CAs’ structure enhance the net positive charge of the metal ion, which is essential to achieve effective catalysis [42]. Most α-CAs are the monomers with molecular mass of about 30 kDa, although the periplasmic CA in
The representatives of β-CAs were found in archaebacteria [44], cyanobacteria [45], eubacteria [46], chemoautotrophic bacteria [47], fungi [48], algae [49], higher plants with C3- and C4-type photosynthesis, dicotyledons and monocotyledons [50, 51]. In
The enzymes of this family are as effective in catalysis as α-CAs are. One histidine and two cysteine residues are zinc ligands in the active center of β-CAs [52, 53]. The active site in β-CAs’ structure is a tight pocket and the only access to it from the bulk solvent is via a bottleneck between Gln, Gly, Asp, and Tyr residues. This bottleneck is too narrow for anything larger than a water molecule, meaning that to implement the catalytic cycle some rearrangement should take place [54]. The study of the structure of β-CAs revealed the presence of the so-called non-catalytic bicarbonate binding site [55], which represents a “pocket” located 8 Å from the active center zinc. A network of at least seven molecules linked together by hydrogen bonds is capable of holding a bicarbonate molecule. Studies have shown that this is not just an anion-binding site, the addition of bicarbonate leads to the reorganization in the protein molecule and in the active center optimizing its functioning [56]. The hydrogen bonds of the Trp, Arg, and Tyr residues in this site are well organized to recognize the bicarbonate ion such anions as acetate or nitrate are not able to carry out all the necessary interactions with the hydrogen bonds of these amino acid residues. Tyr residues in the active site and bicarbonate binding site structures were recently found to be the key amino acids for the reversible modification by phosphorylation and nitration in response to abiotic and biotic stresses [11, 12]. Such modifications allow for blocking the passage of substrate and inhibiting the activity of β-CAs under stress conditions.
γ-CAs are present in cells of bacteria, green algae, diatoms [2], and higher plants [57]. In
γ-CAs function as trimers consisting of identical subunits [61], which contain one zinc atom per subunit; however, unlike α and β-CAs, the active center is located between the subunits. In the active center of γ-CAs, there are three histidine and one H2O residues coordinating Zn atom, like in α-CAs, but these are histidines of two opposite subunits. The mechanism of catalysis is similar to that of α-CAs [62].
To increase the CO2 content near Rubisco during the evolutionary adaptation to growth conditions, some groups of plants, that is, aquatic photosynthesizers, developed CO2 concentrating mechanisms (CCMs) in their cells. All currently known CCM pathways require at least one or, more often, several CAs.
In cyanobacteria, negatively charged HCO3− penetrates the cells through specialized transporters on the plasma membrane, utilizing the energy of ATP and NADPH [63]. The dissolved Сi is captured with the help of extracellular CA, supplying НСО3− to bicarbonate transporters and preventing leakage of Сi from the cell [45]. The other CAs situated in cyanobacterial carboxysomes accelerate the formation of CO2 for Rubisco. The last one is also placed in carboxysomes, which serve as a barrier to CO2 leakage.
In algae cells, Ci should cross the cell wall, plasma membrane, and chloroplast membrane to reach the place of CO2 fixation. Like in cyanobacteria, CAs in algae cells play a crucial role in CCM, which is important under conditions of low CO2 in water. Periplasmic CA in
The plants constantly growing under stress conditions, such as drought, salinity, or high temperature, have to keep stomata closed most of the day to reduce water loss as a result of transpiration. At the same time, to avoid starvation in the absence of CO2 in leaves, a C4 type of photosynthesis has evolved. It includes an additional carbon conversion cycle, called the Hatch-Slack cycle. CCM exists in the form of the so-called four-carbon (C4) photosynthesis with the spatial separation of the primary carboxylation reactions and the Calvin cycle. The Hatch-Slack cycle allows Ci to be concentrated in leaf tissues, carrying out the primary fixation of carbon dioxide through the carboxylation of phosphoenolpyruvate using the enzyme phosphoenolpyruvate carboxylase (PEPC). In the cytosol of the mesophyll cells of C4 plants, there is a high amount of CA [68]. This enzyme plays a decisive role in C4 photosynthesis. CA catalyzes the first reaction of C4 pathway, increasing its rate by 104 times, due to providing bicarbonate to PEPC [3]. After that, four-carbon acids produced as a result of PEPC activity are decarboxylated in bundle-sheath cells. This leads to an increase in carbon dioxide concentration around Rubisco, which is located in the chloroplasts of the bundle-sheath cells in C4 plants [69]. Interestingly, the Genomic Southern analysis by Tetu et al. in 2007 [70] revealed the presence of two forms of CA from the β-family in the cytoplasm in the cells of
The mechanisms of CO2 penetration inside leaf cells have been studied for decades. Chemically, CO2 is a lipophilic compound and it should easily diffuse through membranes [73, 74]. However, biological membranes appear to have a low CO2 permeability [75] due to a high level of protein and sterol content [74, 76]. Recently, using plasma membrane vesicles of pea leaves it has been demonstrated that plasma membrane aquaporins could facilitate CO2 transport [77]. The same data were earlier presented for tobacco, Arabidopsis, fava bean, and others [78, 79, 80]. The plant aquaporins are the plasma membrane intrinsic proteins (PIPs). They are mainly represented by two groups: PIP1 and PIP2, which possess some structural differences in the N and C terminal end and are subdivided into several subgroups [81, 82]. Each aquaporin has different transport properties for H2O, CO2, and solutes; however, the functional interaction between PIP1 and PIP2 was proposed to occur with the emphasis on their coupling under stress conditions [82]. Using the inhibitor analysis, the presence of CA located in the plasma membrane of photosynthetic pea leaf cells was proved [83] and the importance of the CA functioning in the plasma membrane for Ci transport into higher plant leaves was confirmed [84]. Later, the presence of β-CA4 in the plasma membrane was shown [5].
Wang et al. in 2016 [14] identified β-CA4 as an interactor with aquaporin PIP2;1 in Arabidopsis. This connection allows CO2 permeability across the plasma membrane to be facilitated. Further, the decrease in the CA concentration was shown to lead to a lower CO2 permeability in plasma membrane vesicles [77]. Therefore, it can be proposed that the functioning of plasma membrane aquaporins depends on the CA activity under both normal and stress conditions. The roles of aquaporins and CA in plant defense responses against biotic and abiotic stress factors are broadly discussed [85]. Aquaporins should interact with CAs at the membrane-liquid phase interfaces, and a term that describes their combined functioning as “cooporin” was proposed [86]. The extent of water and CO2 permeability via aquaporins of the plasma membrane is consistent with the expression levels of both PIPs and CA when exposed to environmental challenges. Experimental evidence suggests that aquaporins and CA are mutually involved in the regulation of CO2 in stomatal and mesophyll conductance in leaves of higher plants [15] that is crucial for both processes: acclimation to stress and recovery after stress. A number of studies conducted using genetic transformation methods showed that changes in the content of aquaporins per unit area of leaves lead to the corresponding changes in mesophyll conductance [87, 88, 89].
In tobacco plants, aquaporin NtAQP1 has been identified as a membrane CO2 pore not only in the plasma membrane but also in the inner chloroplast envelope membranes [79]. Therefore, it was proposed that aquaporins may be involved in CO2 transfer in both the plasma membrane and in the chloroplast envelope [75]. Along with PIP, various forms of tonoplast intrinsic proteins (TIPs) and other intrinsic proteins were described in the Arabidopsis envelope fraction [90]. We have previously provided data showing the presence of the CA activity, associated with the isolated chloroplast envelope [16]. CA activity was also detected in chloroplast envelope membranes of
CA protects the cells from H2O2-induced apoptosis [92]. It is known that among various chloroplast signals H2O2 plays a major role in various signaling pathways under stress conditions [93, 94]. An essential factor to implement the retrograde signal (the signal from the organelle to the nucleus) is the ability of H2O2 to diffuse over long distances from the place of formation to the place of signaling. Earlier, we demonstrated that H2O2 that was produced inside chloroplasts diffused from a chloroplast to cytoplasm through chloroplast envelope membranes and the amount of H2O2 outside the chloroplasts increased under the conditions of ascorbate peroxidase inhibition [95]. Using acetazolamide (AZA), which is known as CA inhibitor, as a non-specific aquaporin inhibitor, we have shown that aquaporins facilitate the diffusion of H2O2 molecules through the chloroplast membrane [16]. AZA was established to be an efficient inhibitor of aquaporins through interacting with the guanidyl group of Arg, backbone carbonyl of Gly, carboxyl of Asp, Ser, His, Ile and Asn of aquaporins [96, 97, 98]. Taking into consideration that AZA also inhibits the activity of CA, we cannot exclude that inhibition of H2O2 diffusion through the envelope membrane in the presence of AZA was the only result of blocking of the aquaporins. This inhibition could also result from inhibiting the envelope CA, especially if this CA is attached to aquaporins in the envelope. If this is the case, the inhibitory effect of AZA on the H2O2 diffusion could be a consequence of AZA binding to envelope CA, leading to the conformational changes of CA with subsequent conformational changes of aquaporin proteins and therefore blocking the envelope aquaporins. Thus, the data in [16] can represent the evidence of the joint functioning of the envelope CA with aquaporins in diffusing hydrogen peroxide through the chloroplast envelope. Considering the presence of CA of β-family in the chloroplast envelope (see above) and the facilitation of not only CO2, but also H2O2 diffusion through the envelope by the functioning of envelope aquaporins, several propositions on the mechanisms of the CA incorporation in signaling under stress conditions can be made. One of them is that CA is involved in the cascades of mitogen-activated protein kinases (MAPKs), which are serine-threonine kinases mediating intracellular signaling through changes in the redox state of their cysteine residues. Since cysteine residues are the main target of hydrogen peroxide in MAPK cascades [99], and two cysteine residues are located in the β-CAs active center, we can assume that H2O2 changes the redox status of cysteine residues of β-CAs, resulting in incorporation of CA in the global MAPK signaling network in plant cells.
It was quantified that the amount of water in chloroplast stroma and thylakoid lumen was much lower than it is enough to perform photosynthetic water oxidation per day. Therefore, the existence of aquaporins in the thylakoid membrane was also suggested [100]. This question is still under debate, some researches have detected some forms of TIPs in the thylakoid membranes of
C3 higher plants are believed to lack any mechanisms of CO2 concentrating. The carbon dioxide content in a liquid phase in leaves is not very high, about 11 μM at the current concentration of CO2 in the atmosphere. Under the illumination pH value of the chloroplast stroma, where Rubisco is located in higher plant cells, increases up to 7.7. The bicarbonate content there reaches 230 μM at 25°C. This effect can be considered as inorganic carbon concentrating.
For higher plants, especially when they grow under stress conditions, such as high light or high temperature, Zabaleta et al. [103] supposed the existence of CMM as in plants in such conditions stomata are closed leading to the decrease of Ci content in chloroplasts. At the same time, a large amount of CO2 is released in mitochondria due to the reactions of both the tricarboxylic acid cycle and photorespiration. The authors supposed that CO2 from mitochondria can be used by chloroplasts in the Calvin cycle. Possibly, CO2 may transfer into chloroplast by diffusion, harnessing some mechanisms of an active HCO3− transport would be more efficient. In the genome of
Interestingly, in double mutants without γ-CA4 and γ-CA5, light-dependent activation of the key enzyme for the synthesis of anthocyanins, chalcone synthase, was observed [105]. The authors suggested that both these CAs play an important role in the growth and development of
The most known and the most studied CA in chloroplasts of C3 higher plants is the stromal CA, which belongs to β-family. This CA was named β-CA1 by Fabre et al. in 2007 [5] in the study of CAs of β-family in Arabidopsis leaves. Later, this name started to be used to designate the corresponding stromal CAs in leaves of other plants [12, 15]. This enzyme is the second after Rubisco in terms of the amount of protein in the cell (0.5–2% of the total) [106]. The rate of the spontaneous interconversion of Ci forms is low, which implies the role of CA in accelerating the supply of CO2 to carboxylation centers; however, direct data on the role of the enzyme in this process are lacking.
In some studies, no association of CA activity with photosynthesis was found. Growing plants under conditions of zinc deficiency showed that the rate of photosynthesis in these plants remained almost unchanged with a sharp decrease in CA activity [107]. In transgenic plants of
Another group of researchers has found that plants compensated for a decrease in CA activity by increasing the permeability of stomata, which, however, has led to a higher rate of water loss [109]. Plant growth under conditions of nitrogen deficiency in the soil led to a significant decrease in the activity of soluble CA in leaves of sugar beet plants, and upon restoration of nitrogen nutrition, a gradual reverse increase in CA activity by 80% of the initial values has been observed (Novichkova, personal comunication). Importantly, many researchers have discovered the convincing evidence of the functional relationship of Rubisco and stromal β-CA. In
In the study of the drought tolerance mechanisms in
Nevertheless, the activity of CA in leaves of plants exposed to water deficit was lower than in the control plants grown under normal conditions [12] due to the phosphorylation of several amino acid residues in the active site and substrate-binding site of β-CA1. The same mechanism of inhibition of CA activity was observed by studying the action of high-temperature stress in the leaves of
It is not entirely clear why the content of CA protein increases with the simultaneous suppression of CA activity. It can be assumed that plants apply this mechanism to prepare for normal moisture conditions. The answer to this question is very important to determine the physiological role of β-CA1 stroma in higher plant metabolism. Although the participation of β-CA1 in photosynthesis is not considered to be proved, the described facts support this suggestion. The fact that it turned out to be one of the main differentially abundant proteins in response to drought testifies to the assumption that β-CA1 supplies CO2 for Rubisco activity by catalyzing the reversible reaction of bicarbonate to carbon dioxide and thus regulating the rate of photosynthesis under stress condition. Water deficit is known to cause stomatal closure with a reduction in plant photosynthetic efficiency and inhibition of Rubisco activity [114]. These responses often result in a change in photosynthetic and energy metabolism-associated protein accumulation. The inhibition of the activity of β-CA1 under stress by phosphorylation and nitration [11, 12] may play an important role in regulating the photosynthetic process in response to stress.
Herewith Yu et al. [7] showed that in rice seedlings the expression of the gene encoding CA of β-family (OsCA1) as well as the total CA activity were upregulated by osmotic stress, in particular, by salt stress. Moreover, the same group showed that
The experimental data presented, however, show that the role of β-CA1 in photosynthesis, as well as the participation of this enzyme in regulating the rate of photosynthetic processes under stress conditions, is still controversial. This contradiction can be explained by the suggestion that two stromal CAs, β-CA1 and α-CA1, participate in CO2 supply to Rubisco. The latter was detected in the chloroplast stroma in the study of the pathway of newly synthesized proteins into the chloroplast through the endo-membrane system of the Golgi apparatus [10]. The data on the decrease in photosynthetic activity, as well as the ability to accumulate starch in plants with a knockout of the gene encoding α-CA1 [116], may indicate the role of α-CA1 in photosynthesis and the possibility that this CA is involved in CO2 supply to Rubisco. Using primers designed for possible alternative splicing of the template RNA of the
Studies using double mutants showed that the reduced synthesis of several CAs had an effect on photosynthesis. Plants with knocked-out genes encoding β-CA1 and β-CA4, which are located in the stroma and plasma membrane, respectively, showed a higher stomata conductivity compared to WT plants [117]. Plants are known to activate anion channels in response to environmental signals such as drought, high levels of carbon dioxide, and bacterial invasion. Recently, two new gene families encoding major groups of anion channels have been identified. SLAC/SLAH channels are the representatives of this group characterized by slow voltage-dependent activation (S-type) [118]. Xue et al. in 2011 [119] and Tian et al. in 2015 [120] showed that β-CA4 and β-CA1 take part in the regulation of gas exchange between the atmosphere and leaves by opening/closing the stomatal aperture. Intracellular bicarbonate generated by β-CA4 and β-CA1 acts as a second messenger and activates S-type anion channels in guard cells.
Evidence suggests that β-CA1 may be important not only for photosynthetic processes but, for example, for the synthesis of ethylene during plant germination, a process that is also dependent on CO2. The seeds of the
To understand the role of β-CA1 in plants, we should take into account that this CA located in the stroma of the chloroplast not only exhibits CA activity but can also bind salicylic acid (SA) [123]. As it is known, SA plays a role in signaling cascades that activate the synthesis of the proteins involved in protecting plants from oxidative stress at both the transcription and translation levels. The intensity of stromal CAs’ gene expression was shown to respond to signals associated with activation of biotic stress protection systems: infection with the late blight of potato plants [124], treatment of tomatoes with mycotoxin fusicoccin [125] and treatment of Arabidopsis plants with methyl jasmonates [126].
There is also a hypothesis that the stromal β-CA can ensure protection against the stress through the biosynthesis of fatty acids. The lower content of stromal β-CA was shown [128] to suppress the fatty acid synthesis leading to a lower expression of genes regulated by jasmonic acid, another signaling molecule that triggers an alternative gene cascade of a protective response. Omega-6 fatty acids are the intermediate compounds of biosynthesis of fatty acids that are synthesized in the stroma of chloroplasts.
In the early 2000s, the information on the presence of more than one carrier of CA activity in the thylakoid membranes began to appear [17, 129]. The CA activity was identified in preparations of lamellar thylakoid membranes enriched with PSI and ATP synthase complexes isolated from pea and Arabidopsis plants [18, 20]. The activity of this CA differed in properties from the CA activity of granular thylakoid membranes enriched with PSII complexes. The CAs in lamellar and granal thylakoid membranes were different in their effect on the activity of inhibitors and detergents, their molecular masses were different. The CAs’ activity of lamellar thylakoid membranes was inhibited equally by both ethoxyzolamide, which is able to penetrate into membranes and acetazolamide, poorly penetrating into lipid membranes. These data show that this CA is situated at the stromal surface of the thylakoid membrane, where it is accessible to both inhibitors. Recently [130, 131] the stimulating effect of adding bicarbonate on the rate of phosphorylation in isolated thylakoids that is known since the 60th of the last century was explained by the presence of CAs in lamellar thylakoid membranes. We have shown that mafenide, a water-soluble inhibitor of CAs, suppressed the phosphorylation stimulation by НСО3− without inhibiting the rate of electron transport and had no effect on phosphorylation rate in the absence of bicarbonate [132].
We suggested a hypothesis of the mechanism of this CA’s involvement in the increase of photophosphorylation in thylakoid membranes. In the reaction of bicarbonate dehydration catalyzed by membrane-bound CAs, CO2 molecules are formed near or even in the surface layer of the thylakoid membrane. With an increase in their local concentration, a stream of CO2 in the thylakoid lumen is possible. In the lumen, CO2 is hydrated by the luminal CAs (see below) with proton release. As a result, an increase in proton concentration in lumen may cause an intensification in ATP production, that is, acceleration of photophosphorylation. Since the uncoupling effect of ammonium salts on ATP synthesis in thylakoids resulted mainly from proton bonding in the thylakoid lumen by NH3 molecules penetrating there, the facts that the addition of bicarbonate reduced the uncoupling effect of these salts [132, 133] is in line with the proposed hypothesis.
Thus, CAs located in lamellar thylakoid membranes, that is, directed immediately to the stromal phase, may operate as one of the suppliers of CO2 for Rubisco, and in the case of low effectiveness of CO2 fixation under some stressful conditions can be involved in the extra production of ATP that is especially important under such conditions.
In 2004, α-CA4 was detected among the proteins of thylakoid membranes [35]. We have shown that the fresh weight of the plant leaves with knocked-out
Our research has provided evidence that one more CA, α-CA2, is present in higher plant thylakoids. The knockout of
Since the regulation of the energy-dependent component of NPQ taking place with the participation of α-CA4 and α-CA2 is based on a change in proton concentration in the lumen, these CAs are also able to regulate the redox state of plastoquinone pool by the regulation of plastohydroquinone oxidation rate by cytochrome complex in the photosynthetic electron transport chain. According to a number of studies [137, 138, 139], it regulates the adaptive response of plants to environmental conditions’ changes. In addition, the concentration of protons is important for the functional activity of enzymes such as thioredoxins and kinases, whose activities are dependent on the state of sulfhydryl groups.
The CA activity in thylakoid membranes of higher plants was discovered in the early 1980s. A number of properties distinguish the CA activity of thylakoid membranes from the activity of soluble stromal CA. In particular, the dehydration activity of thylakoid CA depends on pH with a maximum at 6.8–7.0, and the activity of soluble CA does not depend on pH [140]. Antibodies against soluble CA from spinach have also shown a strong cross-reaction with soluble CA from pea chloroplasts, but not with thylakoids exhibiting similar CA activity [141]. In our studies, a soluble CA that belongs to β-family located in the thylakoid lumen has been discovered [19, 142], and it was suggested that this is β-CA5, previously detected in chloroplasts from Arabidopsis [5]. The exact position of β-CA5 in Arabidopsis chloroplasts is unknown, but it cannot be excluded that there are two forms of this enzyme with one located in the chloroplast envelope (see above) and the other situated in the thylakoid lumen.
The expression level of the
The role of CAs in mechanisms of stress tolerance has been studied in plants possessing CCM, that is, in algae and C4 higher plants. The lack of understanding of the functions of individual CAs in higher plants with C3 type of photosynthesis may be explained by an involvement of more than one of CAs in one biochemical pathway. The effect of the absence of CAs in mutants is more obvious under various adverse conditions, which are comfortable for plants. These are the conditions when CO2 supply and fixation are not limited to the general plant metabolism under optimal light intensity, temperature, mineral nutrition, etc. Moreover, the effect of the absence of CAs in mutants is more obvious in various adverse conditions. That means that the functioning of CAs in plants is the most important under stress.
The preparation of the manuscript was supported by the Russian Science Foundation (project no. 17-14-01371) and by the Ministry of Science and Higher Education of the Russian Federation, State Scientific Program, theme no. АААА-А17-117030110135-1.
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