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Regulation of Central Carbon and Amino Acid Metabolism in Plants

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

Deadline for manuscript submissions: closed (31 January 2020) | Viewed by 56002

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Special Issue Editors

Dr. Stefan Timm

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Guest Editor

Plant Physiology Department, Albert-Einstein-Str.3, 18059 Rostock, Germany
Interests: photorespiration; photosynthesis; Calvin–Benson cycle; metabolic regulation; metabolite signaling; environmental acclimation
Special Issues, Collections and Topics in MDPI journals

Dr. Stéphanie Arrivault

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Guest Editor

Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, D-14476 Potsdam-Golm, Germany
Interests: photosynthesis; Calvin–Benson cycle; primary metabolism; metabolomics

Special Issue Information

Dear Colleagues,

Over the past few decades, considerable effort has been made to understand plant primary metabolism. While the biochemistry and the underlying genetics of central carbon and nitrogen metabolism have been thoroughly studied, there is still a lack of knowledge on how these metabolic branches are regulated and regulate and interact with each other. Improving our current understanding of such regulatory loops is of particular interest given that all oxygenic phototrophs are frequently exposed to environmental changes, including periods of unfavorable conditions that distinctly lower plant growth and yield. To understand how adjustments of metabolism towards a fluctuating environment are achieved on the short- and long-term timescale will also facilitate genetic engineering approaches. One major goal of such attempts is to produce more robust plant varieties that are able to sustain high photosynthetic efficiencies and yields during persistent phases of abiotic stresses.

This Special Issue of Plants aims to highlight the metabolic acclimation and signaling mechanisms of plant central carbon and nitrogen metabolism towards environmental changes, particularly involving alterations in CO₂ and O₂ concentration, light availability and intensity, as well as fluctuations in temperature and water supply during different stages of plant development. Thus, the major focus will be on the acclimation and the regulatory interplay that, among others, involve the operation and interaction of photosynthesis, photorespiration and respiration.

Dr. Stefan Timm
Dr. Stéphanie Arrivault
Guest Editors

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Keywords

photosynthesis
Calvin–Benson cycle
photorespiration
TCA cycle
metabolite signaling/acclimation
redox-regulation
environmental adaptation
photoperiodic changes
CO2/O2 acclimation
temperature stress
water stress

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Published Papers (10 papers)

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Editorial

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4 pages, 219 KiB

Open AccessEditorial

Regulation of Central Carbon and Amino Acid Metabolism in Plants

by Stefan Timm and Stéphanie Arrivault

Plants 2021, 10(3), 430; https://doi.org/10.3390/plants10030430 - 24 Feb 2021

Cited by 4 | Viewed by 2423

Abstract

Fluctuations in the prevailing environmental conditions, including light availability and intensity, CO₂/O₂ ratio, temperature, and nutrient or water supply, require rapid metabolic switches to maintain proper metabolism [...] Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

Research

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22 pages, 8683 KiB

Open AccessArticle

Transcriptional and Biochemical Characterization of Cytosolic Pyruvate Kinases in Arabidopsis thaliana

by Sabine Wulfert, Sören Schilasky and Stephan Krueger

Plants 2020, 9(3), 353; https://doi.org/10.3390/plants9030353 - 11 Mar 2020

Cited by 38 | Viewed by 5217

Abstract

Glycolysis is a central catabolic pathway in every living organism with an essential role in carbohydrate breakdown and ATP synthesis, thereby providing pyruvate to the tricarboxylic acid cycle (TCA cycle). The cytosolic pyruvate kinase (cPK) represents a key glycolytic enzyme by catalyzing phosphate transfer from phosphoenolpyruvate (PEP) to ADP for the synthesis of ATP. Besides its important functions in cellular energy homeostasis, the activity of cytosolic pyruvate kinase underlies tight regulation, for instance by allosteric effectors, that impact stability of its quaternary structure. We determined five cytosol-localized pyruvate kinases, out of the fourteen putative pyruvate kinase genes encoded by the Arabidopsis thaliana genome, by investigation of phylogeny and localization of yellow fluorescent protein (YFP) fusion proteins. Analysis of promoter β-glucuronidase (GUS) reporter lines revealed an isoform-specific expression pattern for the five enzymes, subject to plant tissue and developmental stage. Investigation of the heterologously expressed and purified cytosolic pyruvate kinases revealed that these enzymes are differentially regulated by metabolites, such as citrate, fructose-1,6-bisphosphate (FBP) and ATP. In addition, measured in vitro enzyme activities suggest that pyruvate kinase subunit complexes consisting of cPK2/3 and cPK4/5 isoforms, respectively, bear regulatory properties. In summary, our study indicates that the five identified cytosolic pyruvate kinase isoforms adjust the carbohydrate flux through the glycolytic pathway in Arabidopsis thaliana, by distinct regulatory qualities, such as individual expression pattern as well as dissimilar responsiveness to allosteric effectors and enzyme subgroup association. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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17 pages, 4216 KiB

Open AccessArticle

Growth under Fluctuating Light Reveals Large Trait Variation in a Panel of Arabidopsis Accessions

by Elias Kaiser, Dirk Walther and Ute Armbruster

Plants 2020, 9(3), 316; https://doi.org/10.3390/plants9030316 - 3 Mar 2020

Cited by 16 | Viewed by 3890

Abstract

The capacity of photoautotrophs to fix carbon depends on the efficiency of the conversion of light energy into chemical potential by photosynthesis. In nature, light input into photosynthesis can change very rapidly and dramatically. To analyze how genetic variation in Arabidopsis thaliana affects photosynthesis and growth under dynamic light conditions, 36 randomly chosen natural accessions were grown under uniform and fluctuating light intensities. After 14 days of growth under uniform or fluctuating light regimes, maximum photosystem II quantum efficiency (F_v/F_m) was determined, photosystem II operating efficiency (Φ_PSII) and non-photochemical quenching (NPQ) were measured in low light, and projected leaf area (PLA) as well as the number of visible leaves were estimated. Our data show that Φ_PSII and PLA were decreased and NPQ was increased, while F_v/F_m and number of visible leaves were unaffected, in most accessions grown under fluctuating compared to uniform light. There were large changes between accessions for most of these parameters, which, however, were not correlated with genomic variation. Fast growing accessions under uniform light showed the largest growth reductions under fluctuating light, which correlated strongly with a reduction in Φ_PSII, suggesting that, under fluctuating light, photosynthesis controls growth and not vice versa. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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19 pages, 1714 KiB

Open AccessFeature PaperArticle

Evolution of Photorespiratory Glycolate Oxidase among Archaeplastida

by Ramona Kern, Fabio Facchinelli, Charles Delwiche, Andreas P. M. Weber, Hermann Bauwe and Martin Hagemann

Plants 2020, 9(1), 106; https://doi.org/10.3390/plants9010106 - 15 Jan 2020

Cited by 12 | Viewed by 6498

Abstract

Photorespiration has been shown to be essential for all oxygenic phototrophs in the present-day oxygen-containing atmosphere. The strong similarity of the photorespiratory cycle in cyanobacteria and plants led to the hypothesis that oxygenic photosynthesis and photorespiration co-evolved in cyanobacteria, and then entered the eukaryotic algal lineages up to land plants via endosymbiosis. However, the evolutionary origin of the photorespiratory enzyme glycolate oxidase (GOX) is controversial, which challenges the common origin hypothesis. Here, we tested this hypothesis using phylogenetic and biochemical approaches with broad taxon sampling. Phylogenetic analysis supported the view that a cyanobacterial GOX-like protein of the 2-hydroxy-acid oxidase family most likely served as an ancestor for GOX in all eukaryotes. Furthermore, our results strongly indicate that GOX was recruited to the photorespiratory metabolism at the origin of Archaeplastida, because we verified that Glaucophyta, Rhodophyta, and Streptophyta all express GOX enzymes with preference for the substrate glycolate. Moreover, an “ancestral” protein synthetically derived from the node separating all prokaryotic from eukaryotic GOX-like proteins also preferred glycolate over l-lactate. These results support the notion that a cyanobacterial ancestral protein laid the foundation for the evolution of photorespiratory GOX enzymes in modern eukaryotic phototrophs. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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14 pages, 5780 KiB

Open AccessArticle

The Development of Crassulacean Acid Metabolism (CAM) Photosynthesis in Cotyledons of the C₄ Species, Portulaca grandiflora (Portulacaceae)

by Lonnie J. Guralnick, Kate E. Gilbert, Diana Denio and Nicholas Antico

Plants 2020, 9(1), 55; https://doi.org/10.3390/plants9010055 - 2 Jan 2020

Cited by 6 | Viewed by 7662

Abstract

Portulaca grandiflora simultaneously utilizes both the C₄ and Crassulacean acid metabolism (CAM) photosynthetic pathways. Our goal was to determine whether CAM developed and was functional simultaneously with the C₄ pathway in cotyledons of P. grandiflora. We studied during development whether CAM would be induced with water stress by monitoring the enzyme activity, leaf structure, JO₂ (rate of O₂ evolution calculated by fluorescence analysis), and the changes in titratable acidity of 10 and 25 days old cotyledons. In the 10 days old cotyledons, C₄ and CAM anatomy were evident within the leaf tissue. The cotyledons showed high titratable acid levels but a small CAM induction. In the 25 days old cotyledons, there was a significant acid fluctuation under 7 days of water stress. The overall enzyme activity was reduced in the 10 days old plants, while in the 25 days old plants CAM activity increased under water-stressed conditions. In addition to CAM, the research showed the presence of glycine decarboxylase in the CAM tissue. Thus, it appears both pathways develop simultaneously in the cotyledons but the CAM pathway, due to anatomical constraints, may be slower to develop than the C₄ pathway. Cotyledons showed the ancestral Atriplicoid leaf anatomy, which leads to the question: Could a CAM cell be the precursor to the C₄ pathway? Further study of this may lead to understanding into the evolution of C₄ photosynthesis in the Portulaca. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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14 pages, 1024 KiB

Open AccessArticle

Enzymatic Properties of Recombinant Phospho-Mimetic Photorespiratory Glycolate Oxidases from Arabidopsis thaliana and Zea mays

by Mathieu Jossier, Yanpei Liu, Sophie Massot and Michael Hodges

Plants 2020, 9(1), 27; https://doi.org/10.3390/plants9010027 - 24 Dec 2019

Cited by 9 | Viewed by 3542

Abstract

In photosynthetic organisms, the photorespiratory cycle is an essential pathway leading to the recycling of 2-phosphoglycolate, produced by the oxygenase activity of ribulose-1,5-bisphosphate carboxylase/oxygenase, to 3-phosphoglycerate. Although photorespiration is a widely studied process, its regulation remains poorly understood. In this context, phosphoproteomics studies have detected six phosphorylation sites associated with photorespiratory glycolate oxidases from Arabidopsis thaliana (AtGOX1 and AtGOX2). Phosphorylation sites at T4, T158, S212 and T265 were selected and studied using Arabidopsis and maize recombinant glycolate oxidase (GOX) proteins mutated to produce either phospho-dead or phospho-mimetic enzymes in order to compare their kinetic parameters. Phospho-mimetic mutations (T4D, T158D and T265D) led to a severe inhibition of GOX activity without altering the K_M glycolate. In two cases (T4D and T158D), this was associated with the loss of the cofactor, flavin mononucleotide. Phospho-dead versions exhibited different modifications according to the phospho-site and/or the GOX mutated. Indeed, all T4V and T265A enzymes had kinetic parameters similar to wild-type GOX and all T158V proteins showed low activities while S212A and S212D mutations had no effect on AtGOX1 activity and AtGOX2/ZmGO1 activities were 50% reduced. Taken together, our results suggest that GOX phosphorylation has the potential to modulate GOX activity. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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15 pages, 3599 KiB

Open AccessFeature PaperArticle

Faster Removal of 2-Phosphoglycolate through Photorespiration Improves Abiotic Stress Tolerance of Arabidopsis

by Stefan Timm, Franziska Woitschach, Carolin Heise, Martin Hagemann and Hermann Bauwe

Plants 2019, 8(12), 563; https://doi.org/10.3390/plants8120563 - 2 Dec 2019

Cited by 45 | Viewed by 5173

Abstract

Photorespiration metabolizes 2-phosphoglyolate (2-PG) to avoid inhibition of carbon assimilation and allocation. In addition to 2-PG removal, photorespiration has been shown to play a role in stress protection. Here, we studied the impact of faster 2-PG degradation through overexpression of 2-PG phosphatase (PGLP) on the abiotic stress-response of Arabidopsis thaliana (Arabidopsis). Two transgenic lines and the wild type were subjected to short-time high light and elevated temperature stress during gas exchange measurements. Furthermore, the same lines were exposed to long-term water shortage and elevated temperature stresses. Faster 2-PG degradation allowed maintenance of photosynthesis at combined light and temperatures stress and under water-limiting conditions. The PGLP-overexpressing lines also showed higher photosynthesis compared to the wild type if grown in high temperatures, which also led to increased starch accumulation and shifts in soluble sugar contents. However, only minor effects were detected on amino and organic acid levels. The wild type responded to elevated temperatures with elevated mRNA and protein levels of photorespiratory enzymes, while the transgenic lines displayed only minor changes. Collectively, these results strengthen our previous hypothesis that a faster photorespiratory metabolism improves tolerance against unfavorable environmental conditions, such as high light intensity and temperature as well as drought. In case of PGLP, the likely mechanism is alleviation of inhibitory feedback of 2-PG onto the Calvin–Benson cycle, facilitating carbon assimilation and accumulation of transitory starch. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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Review

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18 pages, 1379 KiB

Open AccessEditor’s ChoiceReview

Plant Mitochondrial Carriers: Molecular Gatekeepers That Help to Regulate Plant Central Carbon Metabolism

by M. Rey Toleco, Thomas Naake, Youjun Zhang, Joshua L. Heazlewood and Alisdair R. Fernie

Plants 2020, 9(1), 117; https://doi.org/10.3390/plants9010117 - 17 Jan 2020

Cited by 29 | Viewed by 6632

Abstract

The evolution of membrane-bound organelles among eukaryotes led to a highly compartmentalized metabolism. As a compartment of the central carbon metabolism, mitochondria must be connected to the cytosol by molecular gates that facilitate a myriad of cellular processes. Members of the mitochondrial carrier family function to mediate the transport of metabolites across the impermeable inner mitochondrial membrane and, thus, are potentially crucial for metabolic control and regulation. Here, we focus on members of this family that might impact intracellular central plant carbon metabolism. We summarize and review what is currently known about these transporters from in vitro transport assays and in planta physiological functions, whenever available. From the biochemical and molecular data, we hypothesize how these relevant transporters might play a role in the shuttling of organic acids in the various flux modes of the TCA cycle. Furthermore, we also review relevant mitochondrial carriers that may be vital in mitochondrial oxidative phosphorylation. Lastly, we survey novel experimental approaches that could possibly extend and/or complement the widely accepted proteoliposome reconstitution approach. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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23 pages, 3753 KiB

Open AccessReview

Ascorbate and Thiamin: Metabolic Modulators in Plant Acclimation Responses

by Laise Rosado-Souza, Alisdair R. Fernie and Fayezeh Aarabi

Plants 2020, 9(1), 101; https://doi.org/10.3390/plants9010101 - 13 Jan 2020

Cited by 31 | Viewed by 6157

Abstract

Cell compartmentalization allows incompatible chemical reactions and localised responses to occur simultaneously, however, it also requires a complex system of communication between compartments in order to maintain the functionality of vital processes. It is clear that multiple such signals must exist, yet little is known about the identity of the key players orchestrating these interactions or about the role in the coordination of other processes. Mitochondria and chloroplasts have a considerable number of metabolites in common and are interdependent at multiple levels. Therefore, metabolites represent strong candidates as communicators between these organelles. In this context, vitamins and similar small molecules emerge as possible linkers to mediate metabolic crosstalk between compartments. This review focuses on two vitamins as potential metabolic signals within the plant cell, vitamin C (L-ascorbate) and vitamin B₁ (thiamin). These two vitamins demonstrate the importance of metabolites in shaping cellular processes working as metabolic signals during acclimation processes. Inferences based on the combined studies of environment, genotype, and metabolite, in order to unravel signaling functions, are also highlighted. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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Other

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22 pages, 1255 KiB

Open AccessEditor’s ChoicePerspective

Flexibility in the Energy Balancing Network of Photosynthesis Enables Safe Operation under Changing Environmental Conditions

by Berkley J. Walker, David M. Kramer, Nicholas Fisher and Xinyu Fu

Plants 2020, 9(3), 301; https://doi.org/10.3390/plants9030301 - 1 Mar 2020

Cited by 71 | Viewed by 7659

Abstract

Given their ability to harness chemical energy from the sun and generate the organic compounds necessary for life, photosynthetic organisms have the unique capacity to act simultaneously as their own power and manufacturing plant. This dual capacity presents many unique challenges, chiefly that energy supply must be perfectly balanced with energy demand to prevent photodamage and allow for optimal growth. From this perspective, we discuss the energy balancing network using recent studies and a quantitative framework for calculating metabolic ATP and NAD(P)H demand using measured leaf gas exchange and assumptions of metabolic demand. We focus on exploring how the energy balancing network itself is structured to allow safe and flexible energy supply. We discuss when the energy balancing network appears to operate optimally and when it favors high capacity instead. We also present the hypothesis that the energy balancing network itself can adapt over longer time scales to a given metabolic demand and how metabolism itself may participate in this energy balancing. Full article

(This article belongs to the Special Issue Regulation of Central Carbon and Amino Acid Metabolism in Plants)

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