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Carbonic Anhydrases and Carbon Metabolism in Plants
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Carbonic Anhydrases and Carbon Metabolism in Plants

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 17201

Special Issue Editors

Dr. Natalia N. Rudenko

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Guest Editor
Institute of Basic Biological Problems, Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, Pushchino 142290, Russia
Interests: photosynthesis; thylakoids; photosystem II; photosystem I; carbonic anhydrase; carbon metabolism; photosynthetic electron transport chain; PCR; gene expression
Special Issues, Collections and Topics in MDPI journals
Dr. Vasily V. Terentyev

E-Mail Website
Guest Editor
Institute of Basic Biological Problems of the Russian Academy of Sciences, Pushchino, Moscow region, Russia
Interests: Green Algae Photosynthesis; Photosystem II and Water-Oxidizing Complex; Thylakoid membrane and Intrathylakoid Lumen; Carbonic Anhydrases; Carbon Concentrating Mechanism; Reaction Centers of Anoxygenic Bacteria; Origin and Evolution of Oxygenic Photosynthesis

Special Issue Information

Dear Colleagues,

Plants is publishing a Special Issue on Carbonic Anhydrases and Carbon Metabolism in Plants. Carbon is the main element of most biomolecules, and its circulation in biochemical reactions in organisms is a necessary condition for life. Along with the transformation of organic molecules, in cells of animals and plants there is a constant interconversion of inorganic carbon forms, carbon dioxide and bicarbonate. In animal cells and heterotrophic bacteria, a large amount of carbon dioxide is constantly produced in processes primarily associated with respiration, but also in a number of other processes. In contrast, in the photosynthetic cells of plants and autotrophic bacteria, carbon dioxide is involved in the processes associated with photosynthesis. Thus, inorganic carbon flows are substantial at both cell and whole-organism levels. A delay in the interconversion of carbon dioxide into bicarbonate and vice versa can not only slow the processes of respiration and photosynthesis, but can also change cell homeostasis and even cause cell death.

Therefore, during evolution carbonic anhydrase (CA) enzymes appeared, which catalyze the reversible hydration of carbon dioxide. These enzymes are found in the cells of all living organisms. CAs often function in connection with transmembrane bicarbonate transporters, making it possible to control the metabolic pathways of inorganic carbon in cells, including a significant increase in its content in certain compartments.

This Special Issue is devoted to the latest research on all aspects of carbon metabolism, transport into plants cells and organoids, the physiological sensing of carbon dioxide and bicarbonate, as well as the participation of CAs in these processes. We also welcome papers concerning the locations, functions, participation in metabolic processes, isolation, structure, interactions with inhibitors of CAs and bicarbonate transporters from algae and higher plants with C3 and C4 types of CO2 fixation, as well as the expression of CAs and bicarbonate-transporter-encoding genes, and the practical use of plant CAs (i.e., their medical relevance, gene manipulation for developing improved agricultural crops, and their application for reducing atmospheric carbon dioxide levels).

Dr. Natalia N. Rudenko
Dr. Vasily V. Terentyev
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Plants is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • algae
  • bicarbonate
  • carbon fixation
  • carbonic anhydrase
  • chloroplasts
  • CO2 concentrating mechanism
  • higher plants
  • photosynthesis

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Published Papers (6 papers)

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Research

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17 pages, 5049 KiB  
Article
Features of Photosynthesis in Arabidopsis thaliana Plants with Knocked Out Gene of Alpha Carbonic Anhydrase 2
by Elena M. Nadeeva, Lyudmila K. Ignatova, Natalia N. Rudenko, Daria V. Vetoshkina, Ilya A. Naydov, Marina A. Kozuleva and Boris N. Ivanov
Plants 2023, 12(9), 1763; https://doi.org/10.3390/plants12091763 - 25 Apr 2023
Cited by 1 | Viewed by 1558
Abstract
The knockout of the At2g28210 gene encoding α-carbonic anhydrase 2 (α-CA2) in Arabidopsis thaliana (Columbia) led to alterations in photosynthetic processes. The effective quantum yields of both photosystem II (PSII) and photosystem I (PSI) were higher in α-carbonic anhydrase 2 knockout plants (α-CA2-KO), [...] Read more.
The knockout of the At2g28210 gene encoding α-carbonic anhydrase 2 (α-CA2) in Arabidopsis thaliana (Columbia) led to alterations in photosynthetic processes. The effective quantum yields of both photosystem II (PSII) and photosystem I (PSI) were higher in α-carbonic anhydrase 2 knockout plants (α-CA2-KO), and the reduction state of plastoquinone pool was lower than in wild type (WT). The electron transport rate in the isolated thylakoids measured with methyl viologen was higher in α-CA2-KO plants. The amounts of reaction centers of PSII and PSI were similar in WT and α-CA2-KO plants. The non-photochemical quenching of chlorophyll a fluorescence in α-CA2-KO leaves was lower at the beginning of illumination, but became slightly higher than in WT leaves when the steady state was achieved. The degree of state transitions in the leaves was lower in α-CA2-KO than in WT plants. Measurements of the electrochromic carotenoid absorbance shift (ECS) revealed that the light-dependent pH gradient (ΔpH) across the thylakoid membrane was lower in the leaves of α-CA2-KO plants than in WT plants. The starch content in α-CA2-KO leaves was lower than in WT plants. The expression levels of the genes encoding chloroplast CAs in α-CA2-KO changed noticeably, whereas the expression levels of genes of cytoplasmic CAs remained almost the same. It is proposed that α-CA2 may be situated in the chloroplasts. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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15 pages, 2974 KiB  
Article
CO2 Levels Modulate Carbon Utilization, Energy Levels and Inositol Polyphosphate Profile in Chlorella
by María Morales-Pineda, Maria Elena García-Gómez, Rodrigo Bedera-García, Mercedes García-González and Inmaculada Couso
Plants 2023, 12(1), 129; https://doi.org/10.3390/plants12010129 - 27 Dec 2022
Cited by 3 | Viewed by 2998
Abstract
Microalgae have a growing recognition of generating biomass and capturing carbon in the form of CO2. The genus Chlorella has especially attracted scientists’ attention due to its versatility in algal mass cultivation systems and its potential in mitigating CO2. [...] Read more.
Microalgae have a growing recognition of generating biomass and capturing carbon in the form of CO2. The genus Chlorella has especially attracted scientists’ attention due to its versatility in algal mass cultivation systems and its potential in mitigating CO2. However, some aspects of how these green microorganisms respond to increasing concentrations of CO2 remain unclear. In this work, we analyzed Chlorella sorokiniana and Chlorella vulgaris cells under low and high CO2 levels. We monitored different processes related to carbon flux from photosynthetic capacity to carbon sinks. Our data indicate that high concentration of CO2 favors growth and photosynthetic capacity of the two Chlorella strains. Different metabolites related to the tricarboxylic acid cycle and ATP levels also increased under high CO2 concentrations in Chlorella sorokiniana, reaching up to two-fold compared to low CO2 conditions. The signaling molecules, inositol polyphosphates, that regulate photosynthetic capacity in green microalgae were also affected by the CO2 levels, showing a deep profile modification of the inositol polyphosphates that over-accumulated by up to 50% in high CO2 versus low CO2 conditions. InsP4 and InsP6 increased 3- and 0.8-fold, respectively, in Chlorella sorokiniana after being subjected to 5% CO2 condition. These data indicate that the availability of CO2 could control carbon flux from photosynthesis to carbon storage and impact cell signaling integration and energy levels in these green cells. The presented results support the importance of further investigating the connections between carbon assimilation and cell signaling by polyphosphate inositols in microalgae to optimize their biotechnological applications. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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17 pages, 3118 KiB  
Article
The Role of Carbonic Anhydrase αCA4 in Photosynthetic Reactions in Arabidopsis thaliana Studied, Using the Cas9 and T-DNA Induced Mutations in Its Gene
by Natalia N. Rudenko, Natalya V. Permyakova, Lyudmila K. Ignatova, Elena M. Nadeeva, Alla A. Zagorskaya, Elena V. Deineko and Boris N. Ivanov
Plants 2022, 11(23), 3303; https://doi.org/10.3390/plants11233303 - 29 Nov 2022
Cited by 2 | Viewed by 1594
Abstract
An homozygous mutant line of Arabidopsis thaliana with a knocked out At4g20990 gene encoding thylakoid carbonic anhydrase αCA4 was created using a CRISPR/Cas9 genome editing system. The effects of the mutation were compared with those in two mutant lines obtained by the T-DNA [...] Read more.
An homozygous mutant line of Arabidopsis thaliana with a knocked out At4g20990 gene encoding thylakoid carbonic anhydrase αCA4 was created using a CRISPR/Cas9 genome editing system. The effects of the mutation were compared with those in two mutant lines obtained by the T-DNA insertion method. In αCA4 knockouts of all three lines, non-photochemical quenching of chlorophyll a fluorescence was lower than in the wild type (WT) plants due to a decrease in its energy-dependent component. The αCA4 knockout also affected the level of expression of the genes encoding all proteins of the PSII light harvesting antennae, the genes encoding cytoplasmic and thylakoid CAs and the genes induced by plant immune signals. The production level of starch synthesis during the light period, as well as the level of its utilization during the darkness, were significantly higher in these mutants than in WT plants. These data confirm that the previously observed differences between insertional mutants and WT plants were not the result of the negative effects of T-DNA insertion transgenesis but the results of αCA4 gene knockout. Overall, the data indicate the involvement of αCA4 in the photosynthetic reactions in the thylakoid membrane, in particular in processes associated with the protection of higher plants’ photosynthetic apparatus from photoinhibition. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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23 pages, 4226 KiB  
Article
Effect of CO2 Content in Air on the Activity of Carbonic Anhydrases in Cytoplasm, Chloroplasts, and Mitochondria and the Expression Level of Carbonic Anhydrase Genes of the α- and β-Families in Arabidopsis thaliana Leaves
by Natalia N. Rudenko, Lyudmila K. Ignatova, Ilya A. Naydov, Natalia S. Novichkova and Boris N. Ivanov
Plants 2022, 11(16), 2113; https://doi.org/10.3390/plants11162113 - 14 Aug 2022
Cited by 2 | Viewed by 2295
Abstract
The carbonic anhydrase (CA) activities of the preparations of cytoplasm, mitochondria, chloroplast stroma, and chloroplast thylakoids, as well as the expression levels of genes encoding αCA1, αCA2, αCA4, βCA1, βCA2, βCA3, βCA4, βCA5, and βCA6, were measured in the leaves of Arabidopsis thaliana [...] Read more.
The carbonic anhydrase (CA) activities of the preparations of cytoplasm, mitochondria, chloroplast stroma, and chloroplast thylakoids, as well as the expression levels of genes encoding αCA1, αCA2, αCA4, βCA1, βCA2, βCA3, βCA4, βCA5, and βCA6, were measured in the leaves of Arabidopsis thaliana plants, acclimated to different CO2 content in the air: low (150 ppm, lCO2), normal (450 ppm, nCO2), and high (1200 ppm, hCO2). To evaluate the photosynthetic apparatus operation, the carbon assimilation and chlorophyll a fluorescence were measured under the same conditions. It was found that the CA activities of the preparations of cytoplasm, chloroplast stroma, and chloroplast thylakoids measured after two weeks of acclimation were higher, the lower CO2 concentration in the air. That was preceded by an increase in the expression levels of genes encoding the cytoplasmic form of βCA1, and other cytoplasmic CAs, βCA2, βCA3, and βCA4, as well as of the chloroplast CAs, βCA5, and the stromal forms of βCA1 in a short-term range 1–2 days after the beginning of the acclimation. The dependence on the CO2 content in the air was most noticeable for the CA activity of the preparations of the stroma; it was two orders higher in lCO2 plants than in hCO2 plants. The CA activity of thylakoid membranes from lCO2 plants was higher than that in nCO2 and hCO2 plants; however, in these plants, a significant increase in the expression levels of the genes encoding αCA2 and αCA4 located in thylakoid membranes was not observed. The CA activity of mitochondria and the expression level of the mitochondrial βCA6 gene did not depend on the content of carbon dioxide. Taken together, the data implied that in the higher plants, the supply of inorganic carbon to carboxylation sites is carried out with the cooperative functioning of CAs located in the cytoplasm and CAs located in the chloroplasts. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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19 pages, 5732 KiB  
Article
A Rapid Method for Detecting Normal or Modified Plant and Algal Carbonic Anhydrase Activity Using Saccharomyces cerevisiae
by Ashwani K. Rai, Robert J. DiMario, Remmy W. Kasili, Michael Groszmann, Asaph B. Cousins, David Donze and James V. Moroney
Plants 2022, 11(14), 1882; https://doi.org/10.3390/plants11141882 - 20 Jul 2022
Cited by 1 | Viewed by 3069
Abstract
In recent years, researchers have attempted to improve photosynthesis by introducing components from cyanobacterial and algal CO2-concentrating mechanisms (CCMs) into terrestrial C3 plants. For these attempts to succeed, we need to understand the CCM components in more detail, especially carbonic [...] Read more.
In recent years, researchers have attempted to improve photosynthesis by introducing components from cyanobacterial and algal CO2-concentrating mechanisms (CCMs) into terrestrial C3 plants. For these attempts to succeed, we need to understand the CCM components in more detail, especially carbonic anhydrase (CA) and bicarbonate (HCO3−) transporters. Heterologous complementation systems capable of detecting carbonic anhydrase activity (i.e., catalysis of the pH-dependent interconversion between CO2 and HCO3−) or active HCO3− transport can be of great value in the process of introducing CCM components into terrestrial C3 plants. In this study, we generated a Saccharomyces cerevisiae CA knock-out (ΔNCE103 or ΔCA) that has a high-CO2-dependent phenotype (5% (v/v) CO2 in air). CAs produce HCO3− for anaplerotic pathways in S. cerevisiae; therefore, the unavailability of HCO3− for neutral lipid biosynthesis is a limitation for the growth of ΔCA in ambient levels of CO2 (0.04% (v/v) CO2 in air).  ΔCA can be complemented for growth at ambient levels of CO2 by expressing a CA from human red blood cells. ΔCA was also successfully complemented for growth at ambient levels of CO2 through the expression of CAs from Chlamydomonas reinhardtii and Arabidopsis thaliana. The ΔCA strain is also useful for investigating the activity of modified CAs, allowing for quick screening of modified CAs before putting them into the plants. CA activity in the complemented ΔCA strains can be probed using the Wilbur–Anderson assay and by isotope exchange membrane-inlet mass spectrometry (MIMS). Other potential uses for this new ΔCA-based screening system are also discussed. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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Review

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39 pages, 4587 KiB  
Review
Adapting from Low to High: An Update to CO2-Concentrating Mechanisms of Cyanobacteria and Microalgae
by Elena V. Kupriyanova, Natalia A. Pronina and Dmitry A. Los
Plants 2023, 12(7), 1569; https://doi.org/10.3390/plants12071569 - 6 Apr 2023
Cited by 18 | Viewed by 4460
Abstract
The intracellular accumulation of inorganic carbon (Ci) by microalgae and cyanobacteria under ambient atmospheric CO2 levels was first documented in the 80s of the 20th Century. Hence, a third variety of the CO2-concentrating mechanism (CCM), acting in aquatic [...] Read more.
The intracellular accumulation of inorganic carbon (Ci) by microalgae and cyanobacteria under ambient atmospheric CO2 levels was first documented in the 80s of the 20th Century. Hence, a third variety of the CO2-concentrating mechanism (CCM), acting in aquatic photoautotrophs with the C3 photosynthetic pathway, was revealed in addition to the then-known schemes of CCM, functioning in CAM and C4 higher plants. Despite the low affinity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) of microalgae and cyanobacteria for the CO2 substrate and low CO2/O2 specificity, CCM allows them to perform efficient CO2 fixation in the reductive pentose phosphate (RPP) cycle. CCM is based on the coordinated operation of strategically located carbonic anhydrases and CO2/HCO3− uptake systems. This cooperation enables the intracellular accumulation of HCO3−, which is then employed to generate a high concentration of CO2 molecules in the vicinity of Rubisco’s active centers compensating up for the shortcomings of enzyme features. CCM functions as an add-on to the RPP cycle while also acting as an important regulatory link in the interaction of dark and light reactions of photosynthesis. This review summarizes recent advances in the study of CCM molecular and cellular organization in microalgae and cyanobacteria, as well as the fundamental principles of its functioning and regulation. Full article
(This article belongs to the Special Issue Carbonic Anhydrases and Carbon Metabolism in Plants)
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