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Dual Nature of Reactive Oxygen Species; An Ally or Adversary
for Plant
By: 1P. Tripathi*, 2S. Dwivedi*,
3D. Ckakraborty*, 4P.K. Trivedi*,
5R.D.Tripathi*
What are Reactive oxygen species (ROS)?
Palaeo-climatically, the introduction of molecular oxygen (O2) into our
atmosphere by O2-evolving photosynthetic organisms 2.7 billion years ago,
reactive oxygen species (ROS) have been the undesirable companion of aerobic
life. Accordingly, the evolution of all aerobic organisms has been dependent on
the development of efficient ROS-scavenging mechanisms. ROS are free radicals
produced as by-products of oxidation–reduction (REDOX) reactions. ROS are
produced as a consequence of electron transport processes in photosynthesis and
aerobic respiration. The total reduction of oxygen produces water, however
partial reduction produces ROS including superoxide anion (·-), hydrogen
peroxide (H2O2) and the hydroxyl radical (OH·). ROS
are generated at very high rates in plants. They are produced by organelles with
a high oxidising metabolic activity or intense rate of electron flow, e.g.
chloroplasts, mitochondria and microbodies, or by the oxidases, a large class of
enzymes. Examples of ROS-producing oxidases include the plasma membrane NADPH
oxidases, peroxidases, oxalate oxidases and amine oxidases. The mechanism of
activation is by the stepwise monovalent reduction of oxygen to form superoxide
(O2·-), hydrogen peroxide (H2O2), hydroxyl radical (OH·) and finally water
according to the scheme. The first step in the reduction of oxygen forming
superoxide is endothermic but subsequent reductions are exothermic. Superoxide
can act as either an oxidant or a reductant; it can oxidise sulphur, ascorbic
acid or NADPH; it can reduce cytochrome C and metal ions. A dismutation reaction
leading to the formation of hydrogen peroxide and oxygen can occur spontaneously
or is catalysed by the enzyme superoxide dismutase. In its protonated form (pKa
= 4.8) superoxide forms the perhydroxyl radical (·OOH) which is a powerful
oxidant (Gebicki and Bielski, 1981), but its biological relevance is probably
minor because of its low concentration at physiological pH.
Reactive oxygen species as an Ally
According to the most of recent studies, a new task for ROS has been
recognized in plants: the control and regulation of a group of essential
biological processes, such as, hormone signaling, immune defense, growth and
development, seed germination and the alleviation of seed dormancy, programmed
cell death; and stress acclimation. At low levels, they are beneficial for plant
and act as signaling molecules during local and systemic acquired resistance. In
addition to sensing the environment and abiotic stresses, ROS also play an
important role in plant defense responses to pathogens. They are involved in the
hypersensitive response typical of plant-pathogen incompatible interactions. The
hypersensitive response (HR), is an example of programmed cell death (PCD)
characterized by cell death at the site of infection. One of the earliest events
in HR is the rapid accumulation of ROS, which can be directly toxic to the
pathogen, but recent evidence suggests that the ROS, in particular H2O2, are the
signal molecules that trigger HR and other defense mechanisms such as systemic
acquired resistance (SAR) and activation of defense genes. The production of ROS
occurs in two distinct phases: an initial, non-specific phase probably
originates from an NADPH-dependent oxidase follows within minutes of pathogen
addition, and a secondary phase, dependent on recognition of incompatible
pathogens by the host begins 1–3 h after the initial burst. The produced O2.- is dismutated by SOD to H2O2 and will activate benzoic acid 2-hydroxylase leading
to salicylic acid (SA) accumulation. This rise in SA, in combination with H2O2,
is necessary for inducing defense gene expression. The second, longer-lasting
burst is involved in activating defense responses, even if thought to be NAD(P)H
dependent. H2O2 and O2.- can induce different genes, in combination or
separately, thereby giving more flexibility to the ROS signaling function. ROS
are also produced in response to many hormones such as auxin, abscisic acid and
salicylic acid. It is no surprise therefore that ROS are important not only in
sensing and responding to environmental changes, but also in orchestrating plant
movement (stomatal closure and tropism) responses and in development. Liam Dolan
and his colleagues at John Innes Centre (UK) have demonstrated a role for ROS in
the development of root hairs. The production of the ROS signal for root growth
is highly ordered and tightly coordinated to ensure the production of a single
root hair. Redox signaling events are also involved in plant responses to
temperature stresses. Here the ROS appear to play a more direct role in the
induction of heat shock proteins, but this does not rule out other indirect
mechanisms. It would appear that stress sensors in the photosynthetic and
respiratory electron transport chains activate redox-sensitive transcription
factors that in turn up-regulate the expression of genes that encode HSPs and
related proteins, ROS-scavenging enzymes and factors involved in the
amplification of the ROS signal by activation of NADPH oxidases. According to
beyond depiction it will be able to predict that at minimum concentration ROS
may act as an ally or defender for plant.
Reactive oxygen species as an Adversary
Nevertheless, the effects of ROS are dose dependent and high levels of ROS
production lead to a process that is often referred to as 'oxidative stress' on
the cell, and call up reflective changes in gene expression. The adverse effects
of ROS have been coupled with aging, carcinogenesis and atherosclerosis in
humans. These oxygen radicals are highly reactive, forming hydroperoxides with
enes and dienes. Furthermore, specific amino acids, such as histidine,
methionine, and tryptophan can be oxidized by O2.-. In the cellular
environment, O2.- will also cause lipid peroxidation, thereby weakening cell membranes. The
following O2 reduction produces hydrogen peroxide (H2O2), a quite long-lasting
molecule (1 µs) that can diffuse some distance from its site of production. The
biological toxicity of H2O2 through oxidation of SH groups has long been
recognized and it can be enhanced in the presence of metal catalysts through
Haber-Weiss or Fenton-type reactions. Likewise, O2.- may react with other
molecules such as lipid peroxides. It can also react with nitric oxide, leading
to the formation of peroxynitrite, a species considered less reactive than
peroxides. These reactions depend on concentration and on the preferential
scavenging capacity of the cell. The plant may favor formation of one or the
other species by preferentially scavenging H2O2 with antioxidants or, in
contrast, accumulate H2O2 by activating superoxide dismutase (SOD). In addition,
H2O2 accumulation may itself lead to higher ROS production. The H2O2 disruption
of photosynthesis, as well as the probable direct role of H2O2 in the activation
of an NAD(P)H-dependent oxidase , suggests that H2O2 itself can stimulate ROS
accumulation. The various sites of oxygen activation in the plant cell are
highly controlled and firmly coupled to avoid release of intermediate products.
Under stress situations, it is probable that this control or coupling breaks
down and the process "dysfunctions" leaking activated oxygen. This is probably a
common occurrence in plants especially when we consider that a plant has minimal
mobility and control of its environment. These uncoupling events are not
unfavorable that they are short in duration and that the oxygen scavenging
systems are able to detoxify the various forms of activated oxygen. If the
production of activated oxygen exceeds the plant's capacity to detoxify it,
deleterious degenerative reactions occur, the typical symptoms being loss of
osmotic responsiveness, wilting, and necrosis. At the sub cellular level,
disintegration of membranes and aggregation of proteins are typical symptoms.
Under abiotic stress, such as heavy metal stress condition, a large quantity of
ROS generates in the cell and degrades chlorophyll, protein, nucleic acid
molecules and causes lipid peroxidation. The degree of lipid peroxidation is
measured by MDA( manoldialdehyde), the end product of the reaction. Therefore
the undesirable product of ROS action in the cell under abiotic stress
illustrates the adverse nature of reactive oxygen species.
Efficient management of steady state level of ROS
According to dual nature of ROS, it acts as both a defender and as a
destroyer to plant. How this dual role is controlled in plants is a little bit
mysterious. Although there has been rapid progress in recent years, there are
still many uncertainties and gaps in our understanding of how ROS affect the
stress response of plants. Nonetheless, it is obvious that the steady-state
level of ROS in cells needs to be strongly regulated. Thus, the plant's dilemma
is not how to eliminate the activation of oxygen, but how to control and manage
the potential reactions of activated oxygen. Complex systems of scavenging
activated oxygen therefore exist in plant cells with complimentary and
interdependent strategies. Some components such as the carotenoids prevent the
formation of activated oxygen by competing for the energy leaked from the
photosystems. Other components are lipid soluble and reside in the membrane
bilayer to terminate the lipid peroxidation chain reactions. Still others,
ascorbate and glutathione, are aqueous scavenger that detoxify activated oxygen
directly or serve to recycle other protective components back to their reduced
state. The enzymes that catalyse the synthesis, degradation and recycling of
these antioxidants are essential to viability. Consequently they are highly
conserved among plants, and exist in multiple forms in different subcellular
compartments and different tissues to allow precise regulation. For ROS to be
effective in these roles Graham Noctor of the University of Paris, notes that
“the production and concentration of ROS requires effective regulation by a
powerful antioxidant system”. The plant antioxidative system is continuously
processing ROS, by acting as electron donors the antioxidants are themselves
oxidised in the process of neutralizing the ROS. The omnipresence of
O2 in the environment and the various cellular locations where ROS
are produced render oxidant scavengers necessary for plant growth and survival.
The capacity for ROS to serve as signals adds to the importance of antioxidants
to specifically regulate different ROS in various cellular locations. Plants
have several antioxidant enzymes and metabolites located in different plant cell
compartments, the main ones being SODs, a family of metalloenzymes catalyzing
the dismutation of O2.- to H2O2, catalases (CATs), which are heme proteins that
catalyze the removal of H2O2, and the enzymes and metabolites of the ascorbate-glutathione
cycle that are involved in the removal of H2O2.The majority of enzymes of the
ascorbate-glutathione cycle [ascorbate peroxidase (APX), glutathione reductase (GR),
and dehydroascorbate reductase (DHAR)] have been found in chloroplasts, cytosol,
mitochondria, and peroxisomes. Catalase and the ascorbate-glutathione cycle are
important in H2O2 scavenging. Although their properties and requirements are
different, they function effectively in parallel. Catalase does not require
reducing power and has a high reaction rate but a low affinity for H2O2, thereby
only removing the bulk of H2O2. In contrast, APX requires a reductant (ascorbate)
and has a higher affinity for H2O2, allowing for the scavenging of small amounts
of H2O2 in more specific locations. Non-enzymatic antioxidant include redox
buffers such as glutathione, ascorbate, tocopherol, flavonoids, carotenoids and
alkaloids vis-ŕ-vis ROS detoxification. Antioxidant capacity is very much
dependent on the severity of the stress as well as the species and its
developmental stage (Apel & Hirt, 2004).
A highly dynamic and redundant network of more than 150 genes is implicated in
Arabidopsis(a model plant for genomics, proteomics and stress related
physiology) for managing the concentration of ROS and also encodes ROS-scavenging
and ROS-producing proteins. Recent studies have unraveled some of the key
players in the network, but many questions related to its mode of regulation,
its protective roles and its modulation of signaling networks that control
growth, development and stress response remain unanswered. The hunt for ROS
receptors in plants is still open. It has been proposed that plant cells sense
ROS by at least three different mechanisms: (i) unidentified receptor proteins;
(ii) redox-sensitive transcription factors, such as NPR1 or Heat Shock Factors;
and (iii) direct inhibition of phosphatases by ROS. Multiple efforts involving
genomics, proteomics and metabolomics and other coming up technologies are
likely to provide a better picture of the networks involved in different ROS-related
plant processes (http://www.scitopics.com/Reactive_Oxygen_Species_in_Plants.html).
Since active oxygen species contribute a regulatory function in plants response
and adaptation to both biotic and abiotic stress conditions, new insights into
the ROS gene network might also allow the identification of genes that can
eventually be exploited to modulate ROS-related plant processes that direct the
development of better performing yield plants through detoxification of excess
ROS at subcellular level. Therefore it is essential to sustain the balance
between the production and the scavenging of activated oxygen that is critical
to the maintenance of active growth and metabolism of the plant and overall
environmental stress tolerance.
*National Botanical Research Institute(CSIR), Lucknow-226001
E-mail: 1[email protected],
2[email protected], 3[email protected],
4[email protected], 5[email protected] |
