scholarly journals Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Glen Wheeler ◽  
Takahiro Ishikawa ◽  
Varissa Pornsaksit ◽  
Nicholas Smirnoff

Ascorbic acid (vitamin C) is an enzyme co-factor in eukaryotes that also plays a critical role in protecting photosynthetic eukaryotes against damaging reactive oxygen species derived from the chloroplast. Many animal lineages, including primates, have become ascorbate auxotrophs due to the loss of the terminal enzyme in their biosynthetic pathway, l-gulonolactone oxidase (GULO). The alternative pathways found in land plants and Euglena use a different terminal enzyme, l-galactonolactone dehydrogenase (GLDH). The evolutionary processes leading to these differing pathways and their contribution to the cellular roles of ascorbate remain unclear. Here we present molecular and biochemical evidence demonstrating that GULO was functionally replaced with GLDH in photosynthetic eukaryote lineages following plastid acquisition. GULO has therefore been lost repeatedly throughout eukaryote evolution. The formation of the alternative biosynthetic pathways in photosynthetic eukaryotes uncoupled ascorbate synthesis from hydrogen peroxide production and likely contributed to the rise of ascorbate as a major photoprotective antioxidant.

2007 ◽  
Vol 407 (3) ◽  
pp. 419-426 ◽  
Author(s):  
Flora J. Logan ◽  
Martin C. Taylor ◽  
Shane R. Wilkinson ◽  
Harparkash Kaur ◽  
John M. Kelly

Humans lack the ability to synthesize vitamin C (ascorbate) due to the absence of gulonolactone oxidase, the last enzyme in the biosynthetic pathway in most other mammals. The corresponding oxidoreductase in trypanosomes therefore represents a target that may be therapeutically exploitable. This is reinforced by our observation that Trypanosoma cruzi, the causative agent of Chagas' disease, lacks the capacity to scavenge ascorbate from its environment and is therefore dependent on biosynthesis to maintain intracellular levels of this vitamin. Here, we show that T. cruzi galactonolactone oxidase (TcGAL) can utilize both L-galactono-γ-lactone and D-arabinono-γ-lactone as substrates for synthesis of vitamin C, in reactions that obey Michaelis–Menten kinetics. It is >20-fold more active than the analogous enzyme from the African trypanosome Trypanosoma brucei. FMN is an essential cofactor for enzyme activity and binds to TcGAL non-covalently. In other flavoproteins, a histidine residue located within the N-terminal flavin-binding motif has been shown to be crucial for cofactor binding. Using site-directed mutagenesis, we show that the corresponding residue in TcGAL (Lys-55) is not essential for this interaction. In contrast, we find that histidine and tryptophan residues (His-447 and Trp-448), localized within a C-terminal motif (HWXK) that is a feature of ascorbate-synthesizing enzymes, are necessary for the FMN association. The conserved lysine residue within this motif (Lys-450) is not required for cofactor binding, but its replacement by glycine renders the protein completely inactive.


2011 ◽  
Vol 440 (3) ◽  
pp. 375-385 ◽  
Author(s):  
Harriet T. Parsons ◽  
Tayyaba Yasmin ◽  
Stephen C. Fry

L-Ascorbate catabolism involves reversible oxidation to DHA (dehydroascorbic acid), then irreversible oxidation or hydrolysis. The precursor–product relationships and the identity of several major DHA breakdown products remained unclear. In the presence of added H2O2, DHA underwent little hydrolysis to DKG (2,3-dioxo-L-gulonate). Instead, it yielded OxT (oxalyl L-threonate), cOxT (cyclic oxalyl L-threonate) and free oxalate (~6:1:1), essentially simultaneously, suggesting that all three product classes independently arose from one reactive intermediate, proposed to be cyclic-2,3-O-oxalyl-L-threonolactone. Only with plant apoplastic esterases present were the esters significant precursors of free oxalate. Without added H2O2, DHA was slowly hydrolysed to DKG. Downstream of DKG was a singly ionized dicarboxy compound (suggested to be 2-carboxy-L-xylonolactone plus 2-carboxy-L-lyxonolactone), which reversibly de-lactonized to a dianionic carboxypentonate. Formation of these lactones and acid was minimized by the presence of residual unreacted ascorbate. In vivo, the putative 2-carboxy-L-pentonolactones were relatively stable. We propose that DHA is a branch-point in ascorbate catabolism, being either oxidized to oxalate and its esters or hydrolysed to DKG and downstream carboxypentonates. The oxidation/hydrolysis ratio is governed by reactive oxygen species status. In vivo, oxalyl esters are enzymatically hydrolysed, but the carboxypentonates are stable. The biological roles of these ascorbate metabolites invite future exploration.


2012 ◽  
Vol 367 (1588) ◽  
pp. 477-482 ◽  
Author(s):  
David J. Beerling

Exciting evidence from diverse fields, including physiology, evolutionary biology, palaeontology, geosciences and molecular genetics, is providing an increasingly secure basis for robustly formulating and evaluating hypotheses concerning the role of atmospheric carbon dioxide (CO 2 ) in the evolution of photosynthetic eukaryotes. Such studies span over a billion years of evolutionary change, from the origins of eukaryotic algae through to the evolution of our present-day terrestrial floras, and have relevance for plant and ecosystem responses to future global CO 2 increases. The papers in this issue reflect the breadth and depth of approaches being adopted to address this issue. They reveal new discoveries pointing to deep evidence for the role of CO 2 in shaping evolutionary changes in plants and ecosystems, and establish an exciting cross-disciplinary research agenda for uncovering new insights into feedbacks between biology and the Earth system.


Plants ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 1250
Author(s):  
Shun Tamaki ◽  
Keiichi Mochida ◽  
Kengo Suzuki

Eukaryotic microalgae have been classified into several biological divisions and have evolutionarily acquired diverse morphologies, metabolisms, and life cycles. They are naturally exposed to environmental stresses that cause oxidative damage due to reactive oxygen species accumulation. To cope with environmental stresses, microalgae contain various antioxidants, including carotenoids, ascorbate (AsA), and glutathione (GSH). Carotenoids are hydrophobic pigments required for light harvesting, photoprotection, and phototaxis. AsA constitutes the AsA-GSH cycle together with GSH and is responsible for photooxidative stress defense. GSH contributes not only to ROS scavenging, but also to heavy metal detoxification and thiol-based redox regulation. The evolutionary diversity of microalgae influences the composition and biosynthetic pathways of these antioxidants. For example, α-carotene and its derivatives are specific to Chlorophyta, whereas diadinoxanthin and fucoxanthin are found in Heterokontophyta, Haptophyta, and Dinophyta. It has been suggested that AsA is biosynthesized via the plant pathway in Chlorophyta and Rhodophyta and via the Euglena pathway in Euglenophyta, Heterokontophyta, and Haptophyta. The GSH biosynthetic pathway is conserved in all biological kingdoms; however, Euglenophyta are able to synthesize an additional thiol antioxidant, trypanothione, using GSH as the substrate. In the present study, we reviewed and discussed the diversity of microalgal antioxidants, including recent findings.


2014 ◽  
Vol 4 (1) ◽  
pp. 1 ◽  
Author(s):  
Takeshi Nagai ◽  
Misuzu Tamai ◽  
Masato Sato ◽  
Yasuhiro Tanoue ◽  
Norihisa Kai ◽  
...  

Background: In recent years, a new everbearing strawberry cultivar, ‘Summertiara’ was cultivated to supply the strawberries in pre-harvest season from July to October in Japan. For highly research and development of processing of this cultivar, ‘Summertiara’ berries, the objective of this study was to characterize these berries, with relation to chemical parameters, total phenols, total flavonoids, total vitamin C, and total anthocyanins, and was to investigate the solubility and the stability of anthocyanins from the berries. Moreover, the functional properties such as antioxidative activity, active oxygen species scavenging activity, and antihypertensive activity were also evaluated.Methods: Chemical analysis, colour measurement, and sensory evaluation of new everbearing strawberry cultivar, ‘Summertiara’ berries were performed. Next, the solubility of anthocyanins from the berries and stability of these against pH, temperature, and an incandescent lighting were investigated. Moreover, functional properties of the extracts prepared from berries were elucidated using 5 different methods.Results: The contents of water, proteins, lipids, carbohydrates, and ash were the same as those of other cultivar berries. The sugar-acid ratio in the berries was low; these were acidulous. By sensory evaluation, the main factors were vivid red colour, aroma, and acidity. The berries were rich in phenols, flavonoids, vitamin C, and anthocyanins. The anthocyanins of the berries became unstable by heat treatment and light exposures such as visible rays. On the other hand, the extracts prepared from the berries showed the functionalities such as antioxidant activity, active oxygen species scavenging activities, and antihypertensive activity.  Conclusions: The strawberry cultivar, ‘Summertiara’ berries were the most suitable for processing ingredient of strawberry-derived products with superior health promoting functionalities.Keywords: Summertiara, everbearing strawberry cultivar, characterization, sensory evaluation, color and storage, functional property


2021 ◽  
Vol 46 (1) ◽  
pp. 77-87
Author(s):  
Arnaud Tauffenberger ◽  
Pierre J. Magistretti

AbstractCellular homeostasis plays a critical role in how an organism will develop and age. Disruption of this fragile equilibrium is often associated with health degradation and ultimately, death. Reactive oxygen species (ROS) have been closely associated with health decline and neurological disorders, such as Alzheimer’s disease or Parkinson’s disease. ROS were first identified as by-products of the cellular activity, mainly mitochondrial respiration, and their high reactivity is linked to a disruption of macromolecules such as proteins, lipids and DNA. More recent research suggests more complex function of ROS, reaching far beyond the cellular dysfunction. ROS are active actors in most of the signaling cascades involved in cell development, proliferation and survival, constituting important second messengers. In the brain, their impact on neurons and astrocytes has been associated with synaptic plasticity and neuron survival. This review provides an overview of ROS function in cell signaling in the context of aging and degeneration in the brain and guarding the fragile balance between health and disease.


2017 ◽  
Vol 121 (suppl_1) ◽  
Author(s):  
Adolfo G Mauro ◽  
Donatas Kraskauskas ◽  
Bassem M Mohammed ◽  
Bernard J Fisher ◽  
Eleonora Mezzaroma ◽  
...  

Introduction: L-gulonolactone oxidase (Gulo) is the rate limiting enzyme for Vitamin C (VitC) biosynthesis. Humans rely on dietary VitC for collagen synthesis, extracellular matrix formation, and tissue regeneration. VitC deficiency is an unrecognized condition and its role in cardiac homeostasis and post-acute myocardial infarction (AMI) remodeling is unknown. Hypothesis: Low levels of VitC impair cardiac function and tissue repair following AMI. Methods: Adult male Gulo -/- knockout mice (C57BL6 background, N=8) and control C57BL (N=8), which are able to synthesize VitC were used. VitC deficiency was maintained supplying low levels of VitC (30mg/l) to Gulo -/- mice in drinking water. Mice underwent M-mode and Doppler echocardiography to measure left ventricular (LV) diameters and wall thicknesses, fractional shortening (FS), E and A waves, E/A ratio, isovolumetric relaxation time (IRT) and myocardial performance index (MPI). Experimental AMI was induced by coronary artery ligation for 7 days. An additional group of Gulo -/- were mice supplemented with physiological levels of VitC (330 mg/l) and underwent AMI. Results: VitC deficient Gulo -/- mice exhibited significantly reduced LV wall thicknesses, reduced FS, and impaired diastolic function, measured as significantly reduced E/A ratio and longer IRT (Panel A, B & C). Following AMI, 100% (8/8) of deficient Gulo -/- mice died within 5 days. Supplementation with physiological levels of VitC significantly improved survival after AMI (Panel D). Conclusion: VitC deficiency impairs systolic and diastolic function. Moreover, VitC is critical for the post-AMI survival.


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