Most cited article - PubMed ID 24726298
Ultra-weak photon emission from biological samples: definition, mechanisms, properties, detection and applications
The oxidative damage induced by abiotic stress factors such as salinity, drought, extreme temperatures, heavy metals, pollution, and high irradiance has been studied in Arabidopsis thaliana. Ultra-weak photon emission (UPE) is presented as a signature reflecting the extent of the oxidation process and/or damage. It can be used to predict the physiological state and general health of plants. This study presents an overview of a potential research platform where the technique can be applied. The results presented can aid in providing invaluable information for developing strategies to mitigate abiotic stress in crops by improving plant breeding programs with a focus on enhancing tolerance. This study evaluates the applicability of charged couple device (CCD) imaging in evaluating plant stress and degree of damage and to discuss the advantages and limitations of the claimed non-invasive label-free tool.
- Keywords
- Antioxidants, Reactive oxygen species, Stress imaging, Two-dimensional photon emission imaging, Wounding,
- MeSH
- Arabidopsis * physiology MeSH
- Photons * MeSH
- Stress, Physiological * MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Technologies based on pulsed electric field (PEF) are increasingly pervasive in medical and industrial applications. However, the detailed understanding of how PEF acts on biosamples including proteins at the molecular level is missing. There are indications that PEF might act on biomolecules via electrogenerated reactive oxygen species (ROS). However, it is unclear how this action is modulated by the pro- and antioxidants, which are naturally present components of biosamples. This knowledge gap is often due to insufficient sensitivity of the conventionally utilized detection assays. To overcome this limitation, here we employed an endogenous (bio)chemiluminescence sensing platform, which enables sensitive detection of PEF-generated ROS and oxidative processes in proteins, to inspect effects of pro-and antioxidants. Taking bovine serum albumin (BSA) as a model protein, we found that the chemiluminescence signal arising from its solution is greatly enhanced in the presence of H 2 O 2 as a prooxidant, especially during PEF treatment. In contrast, the chemiluminescence signal decreases in the presence of antioxidant enzymes (catalase, superoxide dismutase), indicating the involvement of both H 2 O 2 and electrogenerated superoxide anion in oxidation-reporting chemiluminescence signal before, during, and after PEF treatment. We also performed additional biochemical and biophysical assays, which confirmed that BSA underwent structural changes after H 2 O 2 treatment, with PEF having only a minor effect. We proposed a scheme describing the reactions leading from interfacial charge transfer at the anode by which ROS are generated to the actual photon emission. Results of our work help to elucidate the mechanisms of action of PEF on proteins via electrogenerated reactive oxygen species and open up new avenues for the application of PEF technology. The developed chemiluminescence technique enables label-free, in-situ and non-destructive sensing of interactions between ROS and proteins. The technique may be applied to study oxidative damage of other classes of biomolecules such as lipids, nucleic acids or carbohydrates.
- MeSH
- Antioxidants * metabolism MeSH
- Electricity MeSH
- Catalase metabolism MeSH
- Luminescence MeSH
- Luminescent Measurements * methods MeSH
- Oxidation-Reduction * MeSH
- Hydrogen Peroxide metabolism MeSH
- Reactive Oxygen Species * metabolism MeSH
- Serum Albumin, Bovine * metabolism MeSH
- Cattle MeSH
- Animals MeSH
- Check Tag
- Cattle MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Antioxidants * MeSH
- Catalase MeSH
- Hydrogen Peroxide MeSH
- Reactive Oxygen Species * MeSH
- Serum Albumin, Bovine * MeSH
Nowadays, modern medicine is looking for new, more gentle, and more efficient diagnostic methods. A pathological state of an organism is often closely connected with increased amount of reactive oxygen species. They can react with biomolecules and subsequent reactions can lead to very low endogenous light emission (biological autoluminescence-BAL). This phenomenon can be potentially used as a non-invasive and low-operational-cost tool for monitoring oxidative stress during diseases. To contribute to the understanding of the parameters affecting BAL, we analyzed the BAL from yeast Saccharomyces cerevisiae as a representative eukaryotic organism. The relationship between the BAL intensity and the amount of reactive oxygen species that originates as a result of the Fenton reaction as well as correlation between spontaneous BAL and selected physical and chemical parameters (pH, oxygen partial pressure, and cell concentration) during cell growth were established. Our results contribute to real-time non-invasive methodologies for monitoring oxidative processes in biomedicine and biotechnology.
- MeSH
- Hydrogen-Ion Concentration MeSH
- Luminescent Measurements MeSH
- Oxidation-Reduction MeSH
- Reactive Oxygen Species metabolism MeSH
- Saccharomyces cerevisiae growth & development metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Reactive Oxygen Species MeSH
Normal or excessive oxidative metabolism in organisms is essential in physiological and pathophysiological processes, respectively. Therefore, monitoring of biological oxidative processes induced by the chemical or physical stimuli is nowadays of extreme importance due to the environment overloaded with various physicochemical factors. Current techniques typically require the addition of chemical labels or light illumination, which perturb the samples to be analyzed. Moreover, the current techniques are very demanding in terms of sample preparation and equipment. To alleviate these limitations, we propose a label-free monitoring tool of oxidation based on biological autoluminescence (BAL). We demonstrate this tool on Saccharomyces cerevisiae cell culture. We showed that BAL can be used to monitor chemical perturbation of yeast due to Fenton reagents initiated oxidation-the BAL intensity changes with hydrogen peroxide concentration in a dose-dependent manner. Furthermore, we also showed that BAL reflects the effects of low-frequency magnetic field on the yeast cell culture, where we observed a disturbance of the BAL kinetics in the exposed vs. control case. Our results contribute to the development of novel techniques for label-free, real-time, noninvasive monitoring of oxidative processes and approaches for their modulation.
- MeSH
- Cellulose analogs & derivatives pharmacology MeSH
- Drug Combinations MeSH
- Culture Techniques MeSH
- Luminescence * MeSH
- Oxidation-Reduction drug effects MeSH
- Povidone pharmacology MeSH
- Saccharomyces cerevisiae cytology drug effects metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cellulose MeSH
- Drug Combinations MeSH
- hyetellose, povidone drug combination MeSH Browser
- Povidone MeSH
It is well established that every living organism spontaneously emits photons referred to as ultra-weak photon emission (synonym biophotons or low-level chemiluminescence) which inherently embodies information about the wellbeing of the source. In recent years, efforts have been made to use this feature as a non-invasive diagnostic tool related to the detection of food quality, agriculture and biomedicine. The current study deals with stress resulting from wounding (mechanical injury) on Arabidopsis thaliana and how it modifies the spontaneous ultra-weak photon emission. The ultra-weak photon emission from control (non-wounded) and stressed (wounded) plants was monitored using different modes of ultra-weak photon emission measurement sensors like charge-coupled device (CCD) cameras and photomultiplier tubes (PMT) and the collected data were analyzed to determine the level of stress generated, photon emission patterns, and underlying biochemical process. It is generally considered that electronically excited species formed during the oxidative metabolic processes are responsible for the ultra-weak photon emission. In the current study, a high-performance cryogenic full-frame CCD camera was employed for two-dimensional in-vivo imaging of ultra-weak photon emission (up to several counts/s) and the spectral analysis was done by using spectral system connected to a PMT. The results show that Arabidopsis subjected to mechanical injury enhances the photon emission and also leads to changes in the spectral pattern of ultra-weak photon emission. Thus, ultra-weak photon emission can be used as a tool for oxidative stress imaging and can pave its way into numerous plant application research.
- Keywords
- Arabidopsis, mechanical injury, oxidative radical reaction, reactive oxygen species, spectral properties, ultra-weak photon emission, wounding,
- Publication type
- Journal Article MeSH
Biological systems manifest continuous weak autoluminescence, which is present even in the absence of external stimuli. Since this autoluminescence arises from internal metabolic and physiological processes, several works suggested that it could carry information in the time series of the detected photon counts. However, there is little experimental work which would show any difference of this signal from random Poisson noise and some works were prone to artifacts due to lacking or improper reference signals. Here we apply rigorous statistical methods and advanced reference signals to test the hypothesis whether time series of autoluminescence from germinating mung beans display any intrinsic correlations. Utilizing the fractional Brownian bridge that employs short samples of time series in the method kernel, we suggest that the detected autoluminescence signal from mung beans is not totally random, but it seems to involve a process with a negative memory. Our results contribute to the development of the rigorous methodology of signal analysis of photonic biosignals.
- MeSH
- Germination physiology MeSH
- Luminescence * MeSH
- Vigna growth & development MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
It is well known that biological systems, such as microorganisms, plants, and animals, including human beings, form spontaneous electronically excited species through oxidative metabolic processes. Though the mechanism responsible for the formation of electronically excited species is still not clearly understood, several lines of evidence suggest that reactive oxygen species (ROS) are involved in the formation of electronically excited species. This review attempts to describe the role of ROS in the formation of electronically excited species during oxidative metabolic processes. Briefly, the oxidation of biomolecules, such as lipids, proteins, and nucleic acids by ROS initiates a cascade of reactions that leads to the formation of triplet excited carbonyls formed by the decomposition of cyclic (1,2-dioxetane) and linear (tetroxide) high-energy intermediates. When chromophores are in proximity to triplet excited carbonyls, the triplet-singlet and triplet-triplet energy transfers from triplet excited carbonyls to chromophores result in the formation of singlet and triplet excited chromophores, respectively. Alternatively, when molecular oxygen is present, the triplet-singlet energy transfer from triplet excited carbonyls to molecular oxygen initiates the formation of singlet oxygen. Understanding the mechanism of the formation of electronically excited species allows us to use electronically excited species as a marker for oxidative metabolic processes in cells.
- Keywords
- chromophores, electronically excited species, hydrogen peroxide, hydroxyl radical, oxidative radical reactions, reactive oxygen species, singlet oxygen, superoxide anion radical,
- MeSH
- Oxygen metabolism MeSH
- Humans MeSH
- Oxidation-Reduction MeSH
- Energy Transfer MeSH
- Reactive Oxygen Species metabolism MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Oxygen MeSH
- Reactive Oxygen Species MeSH
Mechanical injury or wounding in plants can be attributed to abiotic or/and biotic causes. Subsequent defense responses are either local, i.e. within or in the close vicinity of affected tissue, or systemic, i.e. at distant plant organs. Stress stimuli activate a plethora of early and late reactions, from electric signals induced within seconds upon injury, oxidative burst within minutes, and slightly slower changes in hormone levels or expression of defense-related genes, to later cell wall reinforcement by polysaccharides deposition, or accumulation of proteinase inhibitors and hydrolytic enzymes. In the current study, we focused on the production of reactive oxygen species (ROS) in wounded Arabidopsis leaves. Based on fluorescence imaging, we provide experimental evidence that ROS [superoxide anion radical (O2 •-) and singlet oxygen (1O2)] are produced following wounding. As a consequence, oxidation of biomolecules is induced, predominantly of polyunsaturated fatty acid, which leads to the formation of reactive intermediate products and electronically excited species.
- Keywords
- Arabidopsis, confocal microscopy, fluorescent probes, mechanical injury, wounding,
- Publication type
- Journal Article MeSH
BACKGROUND: A brief review is given of Peter W. Barlows' contributions to research on gravity tide-related phenomena in plant biology, or 'selenonastic' effects as he called them, including his early research on root growth. Also, new results are presented here from long-term recordings of spontaneous ultra-weak light emission during germination, reinforcing the relationship between local lunisolar tidal acceleration and seedling growth. SCOPE: The main ideas and broad relevance of the work by Barlow and his collaborators about the effects of gravity on plants are reviewed, highlighting the necessity of new models to explain the apparent synchronism between root growth and microscale gravity changes 107 times lower than that exerted by the Earth's gravity. The new results, showing for the first time the germination of coffee beans in sequential tests over 2 months, confirm the co-variation between the patterns in ultra-weak light emission and the lunisolar tidal gravity curves for the initial growth phase. For young sprouts (<1 month old), the rhythm of growth as well as variation in light emission exhibit the once a day and twice a day periodic variations, frequency components that are the hallmark of local lunisolar gravimetric tides. Although present, this pattern is less pronounced in coffee beans older than 1 month. CONCLUSIONS: The apparent co-variation between ultra-weak light emission and growth pattern in coffee seedlings and the lunisolar gravity cycles corroborate those previously found in seedlings from other species. It is proposed here that such patterns may attenuate with time for older sprouts with slow development. These data suggest that new models considering both intra- and intercellular interactions are needed to explain the putative sensing and reaction of seedlings to the variations in the gravimetric tide. Here, a possible model is presented based on supracellular matrix interconnections.
- MeSH
- Coffea physiology MeSH
- History, 20th Century MeSH
- History, 21st Century MeSH
- Plant Physiological Phenomena * MeSH
- Gravitation * MeSH
- Germination physiology MeSH
- Light * MeSH
- Check Tag
- History, 20th Century MeSH
- History, 21st Century MeSH
- Publication type
- Biography MeSH
- Journal Article MeSH
- Historical Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- About
- Barlow, Peter
It is well known that all biological systems which undergo oxidative metabolism or oxidative stress generate a small amount of light. Since the origin of excited states producing this light is generally accepted to come from chemical reactions, the term endogenous biological chemiluminescence is appropriate. Apart from biomedicine, this phenomenon has potential applications also in plant biology and agriculture like monitoring the germination rate of seeds. While chemiluminescence capability to monitor germination has been measured on multiple agriculturally relevant plants, the standard model plant Arabidopsis thaliana has not been analyzed for this process so far. To fill in this gap, we demonstrate here on A. thaliana that the intensity of endogenous chemiluminescence increases during the germination stage. We showed that the chemiluminescence intensity increases since the second day of germination, but reaches a plateau on the third day, in contrast to other plants germinating from larger seeds studied so far. We also showed that intensity increases after topical application of hydrogen peroxide in a dose-dependent manner. Further, we demonstrated that the entropy of the chemiluminescence time series is similar to random Poisson signals. Our results support a notion that metabolism and oxidative reactions are underlying processes which generate endogenous biological chemiluminescence. Our findings contribute to novel methods for non-invasive and label-free sensing of oxidative processes in plant biology and agriculture.
- MeSH
- Arabidopsis genetics growth & development metabolism MeSH
- Biomarkers MeSH
- Germination * genetics MeSH
- Luminescence * MeSH
- Oxidation-Reduction drug effects MeSH
- Oxidative Stress MeSH
- Hydrogen Peroxide metabolism pharmacology MeSH
- Seeds genetics growth & development metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Biomarkers MeSH
- Hydrogen Peroxide MeSH