•Reactive oxygen species (ROS) are produced in abundance by photosynthesis.•ROS and antioxidants function in redox signal transduction that is important in chloroplast to nucleus communication.•Some ...chloroplasts have specialized signaling functions that regulate epigenetic as well as genetic programming.•Photoinhibition and slowly reversible decreases in photosynthetic capacity are not necessarily the result of light-induced damage to PSII reaction centers.
Reduction-oxidation (redox) reactions, in which electrons move from a donor to an acceptor, are the functional heart of photosynthesis. It is not surprising therefore that reactive oxygen species (ROS) are generated in abundance by photosynthesis, providing a plethora of redox signals as well as functioning as essential regulators of energy and metabolic fluxes. Chloroplasts are equipped with an elaborate and multifaceted protective network that allows photosynthesis to function with high productivity even in resource-limited natural environments. This includes numerous antioxidants with overlapping functions that provide enormous flexibility in redox control. ROS are an integral part of the repertoire of chloroplast signals that are transferred to the nucleus to convey essential information concerning redox pressure within the electron transport chain. Current evidence suggests that there is specificity in the gene-expression profiles triggered by the different ROS signals, so that singlet oxygen triggers programs related to over excitation of photosystem (PS) II while superoxide and hydrogen peroxide promote the expression of other suites of genes that may serve to alleviate electron pressure on the reducing side of PSI. Not all chloroplasts are equal in their signaling functions, with some sub-populations appearing to have better contacts/access to the nucleus than others to promote genetic and epigenetic responses. While the concept that light-induced increases in ROS result in damage to PSII and photoinhibition is embedded in the photosynthesis literature, there is little consensus concerning the extent to which such oxidative damage happens in nature. Slowly reversible decreases in photosynthetic capacity are not necessarily the result of light-induced damage to PSII reaction centers.
Food security and the protection of the environment are urgent issues for global society, particularly with the uncertainties of climate change. Changing climate is predicted to have a wide range of ...negative impacts on plant physiology metabolism, soil fertility and carbon sequestration, microbial activity and diversity that will limit plant growth and productivity, and ultimately food production. Ensuring global food security and food safety will require an intensive research effort across the food chain, starting with crop production and the nutritional quality of the food products. Much uncertainty remains concerning the resilience of plants, soils, and associated microbes to climate change. Intensive efforts are currently underway to improve crop yields with lower input requirements and enhance the sustainability of yield through improved biotic and abiotic stress tolerance traits. In addition, significant efforts are focused on gaining a better understanding of the root/soil interface and associated microbiomes, as well as enhancing soil properties.
Recent years have witnessed enormous progress in understanding redox signaling related to reactive oxygen species (ROS) in plants. The consensus view is that such signaling is intrinsic to many ...developmental processes and responses to the environment. ROS-related redox signaling is tightly wedded to compartmentation. Because membranes function as barriers, highly redox-active powerhouses such as chloroplasts, peroxisomes, and mitochondria may elicit specific signaling responses. However, transporter functions allow membranes also to act as bridges between compartments, and so regulated capacity to transmit redox changes across membranes influences the outcome of triggers produced at different locations. As well as ROS and other oxidizing species, antioxidants are key players that determine the extent of ROS accumulation at different sites and that may themselves act as signal transmitters. Like ROS, antioxidants can be transported across membranes. In addition, the intracellular distribution of antioxidative enzymes may be modulated to regulate or facilitate redox signaling appropriate to the conditions. Finally, there is substantial plasticity in organellar shape, with extensions such as stromules, peroxules, and matrixules playing potentially crucial roles in organelle-organelle communication. We provide an overview of the advances in subcellular compartmentation, identifying the gaps in our knowledge and discussing future developments in the area.
ROS-related redox regulation and signaling in plants Noctor, Graham; Reichheld, Jean-Philippe; Foyer, Christine H.
Seminars in cell & developmental biology,
August 2018, 2018-08-00, 20180801, 2018-08, Letnik:
80
Journal Article
Recenzirano
Odprti dostop
As sessile oxygenic organisms with a plastic developmental programme, plants are uniquely positioned to exploit reactive oxygen species (ROS) as powerful signals. Plants harbor numerous ...ROS-generating pathways, and these oxidants and related redox-active compounds have become tightly embedded into plant function and development during the course of evolution. One dominant view of ROS-removing systems sees them as beneficial antioxidants battling to keep damaging ROS below dangerous levels. However, it is now established that ROS are a necessary part of subcellular and intercellular communication in plants and that some of their signaling functions require ROS-metabolizing systems. For these reasons, it is suggested that “ROS processing systems” would be a more accurate term than “antioxidative systems” to describe cellular components that are most likely to interact with ROS and, in doing so, transmit oxidative signals. Within this framework, our update provides an overview of the complexity and compartmentation of ROS production and removal. We place particular emphasis on the importance of ROS-interacting systems such as the complex cellular thiol network in the redox regulation of phytohormone signaling pathways that are crucial for plant development and defense against external threats.
SUMMARY
Reactive oxygen species (ROS) such as singlet oxygen, superoxide (O2●−) and hydrogen peroxide (H2O2) are the markers of living cells. Oxygenic photosynthesis produces ROS in abundance, which ...act as a readout of a functional electron transport system and metabolism. The concept that photosynthetic ROS production is a major driving force in chloroplast to nucleus retrograde signalling is embedded in the literature, as is the role of chloroplasts as environmental sensors. The different complexes and components of the photosynthetic electron transport chain (PETC) regulate O2●− production in relation to light energy availability and the redox state of the stromal Cys‐based redox systems. All of the ROS generated in chloroplasts have the potential to act as signals and there are many sulphhydryl‐containing proteins and peptides in chloroplasts that have the potential to act as H2O2 sensors and function in signal transduction. While ROS may directly move out of the chloroplasts to other cellular compartments, ROS signalling pathways can only be triggered if appropriate ROS‐sensing proteins are present at or near the site of ROS production. Chloroplast antioxidant systems serve either to propagate these signals or to remove excess ROS that cannot effectively be harnessed in signalling. The key challenge is to understand how regulated ROS delivery from the PETC to the Cys‐based redox machinery is organised to transmit redox signals from the environment to the nucleus. Redox changes associated with stromal carbohydrate metabolism also play a key role in chloroplast signalling pathways.
Significance Statement
Chloroplasts are major producers of reactive oxygen species (ROS) that are important signals in the communication between the chloroplasts and the nucleus. The photosynthetic electron transport chain (PETC) has evolved to control ROs production and thus limit collateral damage while facilitating essential signalling functions. We consider current concepts of ROS production and processing in chloroplasts, highlighting new directions and gaps in our current knowledge.
Drought is considered to cause oxidative stress, but the roles of oxidant-induced modifications in plant responses to water deficit remain obscure. Key unknowns are the roles of reactive oxygen ...species (ROS) produced at specific intracellular or apoplastic sites and the interactions between the complex, networking antioxidative systems in restricting ROS accumulation or in redox signal transmission. This Update discusses the physiological aspects of ROS production during drought, and analyzes the relationship between oxidative stress and drought from different but complementary perspectives. We ask to what extent redox changes are involved in plant drought responses and discuss the roles that different ROS-generating processes may play. Our discussion emphasizes the complexity and the specificity of antioxidant systems, and the likely importance of thiol systems in drought-induced redox signaling. We identify candidate drought-responsive redox-associated genes and analyze the potential importance of different metabolic pathways in drought-associated oxidative stress signaling.
Oxidative stress and reactive oxygen species (ROS) are common to many fundamental responses of plants. Enormous and ever‐growing interest has focused on this research area, leading to an extensive ...literature that documents the tremendous progress made in recent years. As in other areas of plant biology, advances have been greatly facilitated by developments in genomics‐dependent technologies and the application of interdisciplinary techniques that generate information at multiple levels. At the same time, advances in understanding ROS are fundamentally reliant on the use of biochemical and cell biology techniques that are specific to the study of oxidative stress. It is therefore timely to revisit these approaches with the aim of providing a guide to convenient methods and assisting interested researchers in avoiding potential pitfalls. Our critical overview of currently popular methodologies includes a detailed discussion of approaches used to generate oxidative stress, measurements of ROS themselves, determination of major antioxidant metabolites, assays of antioxidative enzymes and marker transcripts for oxidative stress. We consider the applicability of metabolomics, proteomics and transcriptomics approaches and discuss markers such as damage to DNA and RNA. Our discussion of current methodologies is firmly anchored to future technological developments within this popular research field.
Summary Statement
Oxidative stress and related redox processes have become integrated into many parts of plant biology research. Here, we provide a critical methodological evaluation of some of the approaches that are used to monitor, gauge and dissect oxidative stress and related redox signalling in plants. Our Forward Look review discusses current obstacles to progress and foreseeable technological developments that are likely to promote ever faster advances within this intensely studied area.
Reactive oxygen species (ROS) have a profound influence on almost every aspect of plant biology. Here, we emphasize the fundamental, intimate relationships between light‐driven reductant formation, ...ROS, and oxidative stress, together with compartment‐specific differences in redox buffering and the perspectives for their analysis. Calculations of approximate H2O2 concentrations in the peroxisomes are provided, and based on the likely values in other locations such as chloroplasts, we conclude that much of the H2O2 detected in conventional in vitro assays is likely to be extracellular. Within the context of scant information on ROS perception mechanisms, we consider current knowledge, including possible parallels with emerging information on oxygen sensing. Although ROS can sometimes be signals for cell death, we consider that an equally important role is to transmit information from metabolism to allow appropriate cellular responses to developmental and environmental changes. Our discussion speculates on novel sensing mechanisms by which this could happen and how ROS could be counted by the cell, possibly as a means of monitoring metabolic flux. Throughout, we place emphasis on the positive effects of ROS, predicting that in the coming decades they will increasingly be defined as hallmarks of viability within a changing and challenging environment.
The multifaceted roles of reactive oxygen species (ROS) in plants and animals continue to fascinate biologists, not least because of the dynamic relationships between reduction/oxidation (redox) signalling leading to growth and defence responses and oxidative stress leading to cell suicide programmes. We propose that ROS production is a hallmark of viable cells within a changing and challenging environment. We discuss compartment‐specific differences in redox buffering capacity, the transition from hypoxia to oxidative metabolism and ROS sensing and signalling mechanisms as central future research directions.
Reactive oxygen species (ROS) have multifaceted roles in the orchestration of plant gene expression and gene-product regulation. Cellular redox homeostasis is considered to be an "integrator" of ...information from metabolism and the environment controlling plant growth and acclimation responses, as well as cell suicide events. The different ROS forms influence gene expression in specific and sometimes antagonistic ways. Low molecular antioxidants (e.g., ascorbate, glutathione) serve not only to limit the lifetime of the ROS signals but also to participate in an extensive range of other redox signaling and regulatory functions. In contrast to the low molecular weight antioxidants, the "redox" states of components involved in photosynthesis such as plastoquinone show rapid and often transient shifts in response to changes in light and other environmental signals. Whereas both types of "redox regulation" are intimately linked through the thioredoxin, peroxiredoxin, and pyridine nucleotide pools, they also act independently of each other to achieve overall energy balance between energy-producing and energy-utilizing pathways. This review focuses on current knowledge of the pathways of redox regulation, with discussion of the somewhat juxtaposed hypotheses of "oxidative damage" versus "oxidative signaling," within the wider context of physiological function, from plant cell biology to potential applications.
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