Environmental constraints and oxidative stress in plants

Plants cannot move and are therefore particularly exposed to environmental fluctuations and external attacks. Environmental conditions are very rarely optimal, leading to the concept of stress, which impacts plant growth and development. Environmental stresses include biotic stresses, caused by a living organism, and abiotic stresses, caused by environmental factors. Recent data in cell and molecular biology show that a number of stress response mechanisms are shared by plants and animals, with the cell being the common point, and even the common target, of all these living beings. In particular, toxic oxidative molecules, present during abiotic stresses, play similar roles in animal and plant cells. This article focuses on the abiotic stresses suffered by plants, which have been led to develop a particularly complex response system in order to adapt and survive.

1. Abiotic stresses

The word stress designates the aggression that a living organism undergoes and its reaction to the resulting state of disturbance. Etymologically, the word “stress” is borrowed from the same English word, but it originally comes from the Old French “déstresse”, which corresponds to distress.

Abiotic stresses [1] caused by a wide variety of environmental factors independent of living beings include the following (Figure 1):

• Temperature:
  – Periods of frost (especially late frost)
  – Too high temperatures (especially over long periods, which is happening more and more often, in connection with climate change); (See Effects of temperature on photosynthesis)
• Water:
  – Excess of water (flooding leading to root asphyxia)
  – Lack of water causing droughts (See Water needs of plants : how to satisfy them ?)
• Solar radiation: excess of light, UV (See Cellular impact of solar UV rays)
• Nutrient deficiencies: mineral elements (especially magnesium), nitrogen
• Soil salinity: excess of sodium and chlorine ions (See focus on Land salinization)
• Soil pollution: heavy metals (cadmium, lead, mercury, copper, aluminum, …)
• Atmospheric pollution: (See What is the impact of air pollutants on vegetation?)
  – Primary pollutants: sulfur dioxide (SO₂), nitrogen oxides (NO_x), ammonia (NH₃), volatile organic compounds (VOC)
  – Secondary pollutant: ozone (O₃). This gaseous compound is a photochemical pollutant. It results from interactions, in the presence of UV, between oxygen O₂, nitrogen oxides (NO and NO₂) and volatile organic compounds (VOC). The concentration of this highly phytotoxic compound has increased considerably in the troposphere between the 19th century and the 2000s. Currently, its annual average concentration is leveling off in the USA and Europe but continues to increase in Asia. However, acute concentration peaks occur over short periods of time and can cause plant damage [2].
  – Carbon dioxide (CO₂): This compound occupies a special place and its presence in the list of air pollutants may be surprising. Indeed, CO₂ is the essential carbon source for plant growth (photosynthesis). However, the considerable increase in its content in the air since the end of the 19th century (its concentration has risen from 290 ppm at the beginning of the Industrial Revolution to nearly 420 ppm today), raises questions about the ability of plants to regulate this increased carbon input. It seems that the increase in CO₂ results in a growth of the leaf surface allowing a proportional increase in photosynthesis [3]. However, at the scale of terrestrial vegetation growth, other constraints, such as drought, temperature increase and/or disruption of the carbon/nitrogen balance, could interfere with this relationship [4].

The adverse effect of abiotic stresses on crop yields has been known for almost half a century. The most incriminated abiotic stress is drought [5], although decreases in productivity have also been attributed to the presence of air pollutants [6].

Very often, plants are subjected to simultaneous stresses. Two cases are interesting in this context:

1. The interaction between the increase of CO₂, which is a priori beneficial, and that of ozone, whose toxicity is obvious [7].
2. Drought combined with the presence of ozone, both of which can be detrimental to plant development [8].

In the latter case, the way in which the two stresses occur over time can change their interaction from synergistic (coordinated action) to antagonistic (opposite effect). For example, the risk of plant damage is greater when ozone pollution occurs in the spring before the drought begins, compared to an early or simultaneous drought with ozone pollution, which would close the stomata and reduce the penetration of the pollutant.

Plants are able to develop mechanisms of perception and response to environmental stresses, allowing them to defend themselves by showing a certain adaptation. However, if the stress intensifies and exceeds the plant’s defensive capacities, the plant may die.

What is remarkable is that each of the various environmental constraints that plants must face results in the same type of stress: oxidative stress, expressed at the cellular level. Oxidative stress results from an imbalance between the production, or rather the overproduction, of reactive oxygen species (ROS) and cellular antioxidant capacities [9] (Figure 1).

2. Reactive oxygen species (ROS)

2.1. Chemical nature and mechanisms of ROS production

ROS are central to oxygen metabolism and the appearance of aerobic living organisms. Oxygen appears progressively in the Earth’s atmosphere about 3 billion years ago and then increases strongly around 2.3 billion years ago thanks to the multiplication of photosynthetic organisms. In its most stable state, oxygen exists in the form of oxygen, O₂. Aerobic living organisms had to adapt to the presence of oxygen, by consuming it. Oxygen is essential to the respiration of these organ

isms, which delivers reducing power and energy. During normal respiratory metabolism, the reduction of oxygen to water takes place in several steps, providing reduced intermediates called ROS. ROS are radical [i] and molecular entities that are much more reactive than the oxygen that gave them birth and much more dangerous because they will react with biological molecules, requiring their controlled degradation (See The dangerous links between oxygen and life). Among the ROS of a radical nature are (Figure 2):

• O₂^-, superoxide ion;
• HO, hydroxyl radical;
• HO₂, perhydroxyl radical.

There is also ¹O₂, singlet oxygen [ii] and a very important non-radical form, hydrogen peroxide H₂O₂ [10] (Figure 2).

Finally, RO₂^–, peroxyl radical [iii] and RO^–_, alkoxyl radical [iv] are secondary radicals involving organic compounds R oxidized by ¹O₂ or HO^–.

These various molecules are formed within the cell from oxygen (Figure 3):

1. Oxygen, produced by photosynthesis, receives energy from light-excited chlorophyll (triplet [iii] ³Chl^*state), and gives rise to singlet oxygen ¹O₂ (Figure 3).
2. Electrons available from intracellular biochemical reactions can react with oxygen to form superoxide ions [v], O₂ ^–..
3. The superoxide ion is relatively easily converted to hydroperoxide H₂O₂ by the action of the enzyme superoxide dismutase (SOD).
4. The hydroperoxide is then transformed :
   1. In the presence of ferrous ions, it gives the hydroxyl radical HO• during the Fenton reaction [vi];
   2. It can also be broken down by catalases (CAT), enzymes that protect the cell from the oxidizing and harmful action of hydroperoxide (see 2.4).
5. In turn, the superoxide ion can produce the perhydroxyl radical HO_2. by protonation.

2.2. Sites of production of reactive oxygen species

ROS are normally produced in all cellular compartments, plastids (chloroplasts in aerial parts), mitochondria, peroxisomes/glyoxysomes, cytosol, plasma membrane, apoplast (cell wall) (Figure 4). Chloroplasts are the main source of ROS in photosynthetic tissues. Mitochondria are important ROS producers especially in non-photosynthetic tissues.

• Chloroplasts

During the photochemical processes of photosynthesis (see Light on Photosynthesis & The Carbon Pathway in Photosynthesis) energy and electron leakage occurs quite naturally:

– Singlet oxygen ¹O₂ is produced from oxygen delivered during photochemical reactions and which captures energy from excited ³Chl^* at photosystem II.
– The formation of ¹O₂ is favored by a limitation of CO₂ entry following the closure of the stomata, often observed during stress. The decrease of CO₂ causes a slowing down of biochemical reactions resulting in a lower demand of photochemical reaction products and a concomitant electronic bottleneck (over-reduction).
– At the level of photosystem I, oxygen captures electrons to give the superoxide ion O₂^–. It can be further transformed into another ROS, the hydroperoxide H₂O₂ with the help of enzymes, the superoxide dismutases (SOD) (see paragraph 2.4).

• Mitochondria

In mitochondria, during respiration, electron leakage occurs naturally in the respiratory complexes, leading to the production of superoxide ions O₂^–. They  can be converted by a SOD into H₂O₂.

• Peroxisomes

In peroxisomes [vii] the main source of ROS is the reduction of glycolate [viii] to glyoxylate by glycolate oxidase which uses O₂ to give H₂O₂. O₂^– ions can also be produced during the operation of the enzyme xanthine oxidase and transformed into H₂O₂ by a peroxisomal SOD.

• Glyoxysomes

In glyoxysomes [ix] the β-oxidation [11] of fatty acids produces hydroperoxide H₂O₂.

• Plasma membrane & apoplast

The plasma membrane contains an NADPH oxidase [12] that delivers into the apoplast [x] O₂^.- superoxide ions formed from oxygen. In the apoplast, hydroperoxide is found which comes either from (i) the transformation of superoxide ions by a SOD, (ii) the action of peroxidases (POX), and (iii) directly from the transformation of ozone O₃. Finally, HO- radicals originate from H₂O₂ in this rather acidic medium (pH around 5). [13]

2.3 ROS toxicity

• Singlet oxygen ¹O₂

It has a rather short life span, of the order of 3 to 4 microseconds (µs), and moves little outside its place of production, essentially chloroplastic. It is, however, highly reactive and attacks photosystem pigments, photosystem II protein D1, DNA nucleosides and membrane lipids (Figure 5). Singlet oxygen reacts with the double bonds of polyunsaturated fatty acids to form lipid hydroperoxides ROOH.

• Hydroxyl radicals HO

Despite a very short lifetime, in the order of microseconds (µs), hydroxyl radicals HO• possess the highest reactivity of ROS. They therefore diffuse very little and act on their place of production:

– They attack the double bonds of the nucleic bases of DNA, which can lead to the cutting of the DNA strands.
– Amino acids of proteins are targets of HO•, which can cause the inactivation of the active site of enzymatic proteins.
– The hydroxyl radical can also attack, by lipid peroxidation, the double bonds of polyunsaturated fatty acids of membrane phospholipids and lipoproteins (Figure 6).

Besides lipid peroxyl radicals RO₂– , alkoxyl radicals RO- can be produced, in the presence of Fe²⁺, from lipid hydroperoxides. These highly oxidizing radicals participate in the propagation of lipid peroxidation chain reactions, leading to a decrease in membrane fluidity.

The ultimate outcome of the degradation process leads to the formation of aldehydes [xi] in particular malonic dialdehyde (MDA). The latter is often considered as a marker of severe oxidative stress. RO₂^– (peroxyl) and RO^– (alkoxyl) radicals are also formed during oxidation reactions of the polypeptide chains that make up proteins.

• The superoxide ion O₂^.–

It has a longer lifetime than the HO• radical, around one millisecond (ms), which allows it to diffuse into the cells. Its direct toxicity is however less than the previous molecular species and it is quite easily transformed into H₂O₂ hydroperoxide.

• The hydroperoxide H₂O₂

It has an even longer lifetime, up to one second, which allows it to circulate in the cell by crossing the different membranes, probably using aquaporins (see Figure 7). It is considered to be not very reactive and has a role as a signal molecule.

However, the latter two ROS are quite capable, if present in high concentrations, of oxidizing lipids and proteins. As we will see later (paragraph 3), cells must achieve a subtle balance between ROS production and destruction in order to survive, otherwise they enter a deleterious spiral leading to programmed cell death (PCD).

2.4. Mechanisms to fight against ROS

ROS detoxification mechanisms involve both non-enzymatic and enzymatic antioxidant systems, which are expressed in different cellular compartments (Figure 7).

• Flavonoids and phenolic compounds are mostly represented in the vacuole.
• Β-carotene and α-tocopherol are present in the chloroplast where they mainly neutralize the singlet oxygen ¹O₂ but also the HO• radical.
• The two most represented antioxidant molecules are ascorbate, synthesized in the mitochondria, and glutathione, which is synthesized in the chloroplasts and cytosol. Ascorbate concentrations are globally 10 to 20 times higher than those of glutathione.
  • Ascorbate is predominantly represented in the peroxisomes and cytosol, but chloroplasts and mitochondria also contain high concentrations. The apoplast contains little ascorbate, although it constitutes a first barrier to oxidative attacks.
  • Glutathione is mainly present in the mitochondria but is almost absent from the apoplast.
  • Ascorbate and glutathione can individually participate in ROS detoxification operations, but their essential role results from their association in the context of the ascorbate-glutathione cycle (AGC), also called the Halliwell-Asada-Foyer cycle, after the scientists who identified it (see Focus on Hydroperoxide detoxification). This mechanism, is present in chloroplasts, cytosol and mitochondria (Figure 7). This cycle detoxifies the hydroperoxide H₂O₂ (Figure 7).
• Catalases (CATs), especially in peroxisomes and glyoxysomes, can also dismantle H₂O₂ into H₂O₂ and O₂ (Figures 4 & 7).
• Another group of enzymes plays an essential, even preliminary role, since its role is the transformation of the superoxide anion O₂– into hydroperoxide H₂O₂. These are the superoxide dismutases (SOD), characterized by the metal present in their active site: Copper, Zinc, Iron or Manganese. They have been identified in chloroplasts (CuZn-SOD thylakoidal, Fe-SOD stromatic), in mitochondria (Mn-SOD), in peroxisomes (CuZn-SOD) and in the cytosol (CuZn-SOD) (Figure 7).

Finally, redoxins, thioredoxins (TRX), glutaredoxins (GRX) and peroxyredoxins (PRX), found in chloroplasts, mitochondria and cytosol, play an important role in detoxification processes (see Focus on hydroperoxide detoxification).

3. ROS roles in the response to abiotic stress

3.1 General diagram of ROS function

3.1.1 Impact of oxidative stress

ROS have long been considered only as toxic by-products of naturally occurring biochemical reactions of cellular metabolism, and their significant increase during abiotic stresses causes oxidative stress that can lead to disruption of homeostasis and cell death. Cell damage includes (Figure 8):

• Membrane destructuring;
• Loss of electrolytes;
• Imbalances in carbon metabolism including reduced photosynthesis and increased respiration;
• Programmed cell death as the final step.

To counteract this scenario, plant cells are equipped, as described in the previous paragraph, with a whole arsenal of antioxidant systems, which allow the destruction of ROS in order to maintain a balance conducive to ensure cell survival.

3.1.2. Double function of ROS

However, fairly recent studies have shown that the balance between ROS production and detoxification also appears to be an essential mechanism of cell signaling which participates in the maintenance of cell homeostasis [14]. ROS would thus have a double function, as actors of a deleterious oxidative stress, but also as signal molecules activating gene transduction and activation processes, regulating the normal processes of growth and development, but also presumed to participate in cellular defense (Figure 9). These considerations have led to the proposal of the term “ROS processing systems”, which would be more precise than the term “antioxidative systems”, to describe the cellular components that interact with ROS [15].

3.2 Example of a response to oxidative stress: the ozone response of leaf cells

When faced with ozone exposure, leaf cells respond in two phases (Figure 10) [2].

1. The first response to aggression is avoidance, with the stomata tending to close. This response is observed during many abiotic stresses even if it seems natural in the case of drought (to avoid losing water) or ozone (to prevent the penetration of the oxidizing species ozone). This closure has negative consequences on the entry of CO₂, but limits the internal production of ROS.
2. Then, ROS present in the intercellular spaces attack the stomatal cells and penetrate into the apoplasm of the mesophyll cells. ROS are detoxified by the antioxidants present, mainly ascorbate.

However, these constitutive defenses are relatively weak and ROS can attack intracellular targets, such as the chloroplast carbon-fixing enzyme Rubisco.

A concomitant increase in carbon-degrading enzyme systems is often observed, with a concomitant increase in reducing power to enable the operation of ascorbate-regenerating antioxidant systems. This defense system, based on the present metabolic equipment, cannot be maintained if the ROS content increases:

1. When ROS levels are still moderate, they act in parallel as signals and, through changes in gene expression, allow a reorientation of metabolism by promoting the synthesis of antioxidants and enzymatic proteins involved in the production of reducing power. ROS are also involved in the synthesis of phytohormones that act positively or negatively on cellular homeostasis and interact with each other.
2. When ROS levels exceed the capacity of cells to deploy their adaptive arsenal, cellular structures are dismantled and cellular organelles lose their function, in a process of programmed cell death or apoptosis.

3.3. Perception of stress and cell signaling

3.3.1. General mode of operation

The stress response consists of several steps:

• Perception of stress,
• Involvement of membrane receptors,
• Mobilization of intracellular signals/messengers,
• Transduction/transmission of signals to transcription factors
• Changes in gene expression [16].

The diagram in Figure 11 reflects, in a rather simplified way, the general state of knowledge on the systems of reception and transmission of signals (see The fixed life of plants and its constraints). The ROS are clearly essential players, the hydroperoxide H₂O₂ being the emblematic representative because of its intracellular mobility:

1. H₂O₂ can enter the cytosol through dedicated aquaporins [xii] called peroxyporins.
2. In the cytosol, H₂O₂ initiates a cascade of kinases [xiii], the MAP kinases [17].
3. H₂O₂ also acts on plasmalemma channels allowing calcium entry (3a) and on receptors embedded in the plasma membrane (3b, RLK from the English Receptor-Like Kinase).
4. However, the perception of the stress signal can directly mobilize an RLK that could perceive changes in membrane fluidity caused, for example, by temperature stress (excessive cold or heat).
5. Calcium and calcium-dependent kinases (CDPKs, 5a) activate an NADPH oxidase-like enzyme, RBOH (Respiratory Burst Oxidase Homolog, 5b), which produces superoxide ion in the apoplast, which is immediately converted into H₂O₂.
6. The loop system linking H₂O₂, the Ca²⁺ channel and RBOH functions as a synergistic positive feedback mechanism.

Abscisic acid [xiv] (ABA), which belongs to the group of plant hormones, is often involved in the perception of stress and, although there are ABA-independent pathways, is very often associated with H₂O₂ [18].

• ABA can be derived from conjugated forms or have its synthesis stimulated by H₂O₂. ABA is recognized by a specific receptor in the plasma membrane and is at the origin of a mechanism linking it to the production of other phytohormones,ethylene [xv] (ET), salicylic acid [xvi] (SA) and jasmonate [xvii] (JA).
• Jasmonate can be derived from oxylipins, oxidative breakdown products of polyunsaturated fatty acids. It is rather considered as protective.
• Ethylene, is a phytohormone linked to tissue and organ senescence and cellular aging mechanisms while salicylic acid is generally associated with positive effects at low concentrations but toxic at higher concentrations.

These three phytohormones are constantly interacting and will maintain a cross-talk that will affect stress responses. If we consider ABA, its role will be decisive in the closure of stomata, which is conditioned by an outflow of anions and K+ ions causing a change in osmotic potential. But the role of ABA is also important in the cells of the chlorophyll mesophyll.

The set of protein kinase cascades will activate transcription factors [xviii] necessary for the regulation of gene expression. Gene expression will be modified (stimulation and/or repression of protein synthesis) depending on the participants of these cascades which are dependent on the intensity of the stress.

The signaling chains may show partial specificities depending on the type of abiotic stress, in particular drought, cold and salinity [19], heavy metals [20], high temperature [21] and ozone [22].

3.3.2. Adjustment of function according to stress intensity

The cellular mechanisms of stress response are very complex and the adjustments are subtle. The system must react according to the balance of power between a tolerable presence of ROS, allowing an adapted regulation with the help of signaling leading to homeostatic equilibrium mechanisms, and an excessive production of ROS overcoming the defences, disorganizing the regulation and provoking the setting up of cellular destruction mechanisms leading to apoptosis.

When the stress is of low intensity:

• ROS content is maintained at a reasonable level, due to the action of enzymatic and non-enzymatic antioxidant systems already present in the cells and their accelerated synthesis related to the role of these ROS in defense-adapted signaling.
• The privileged targets of photosynthetic organs are chloroplasts and the RubisCO is often affected by ROS, very early, even before photosystems. The synthesis of the subunits of the enzymatic protein is also repressed.
• Conversely, an increase in the degradation systems of carbohydrate compounds is often observed (respiratory metabolism), either by increasing enzymatic performance or by synthesis of key enzymes.
• The imbalance of the cellular redox state is then avoided by the increased production of reducing power, associated with all this degradative metabolism. The reducing power will also be used in antioxidant reactions with an increase in the synthesis of the associated enzymatic arsenal.
• The primary metabolism of carbon compounds production is in any case modified with less carbon assimilated and more carbon lost by respiration, which leads to a rarefaction of the total quantity of available compounds.
• In addition, to combat stress, a detour of biosynthetic pathways to secondary metabolism is also observed, leading to the production of flavonoid and phenolic compounds. These changes in carbon distribution can have a long-term negative effect on plant growth.

In addition to these responses, which are mostly common to all types of abiotic stress, some proteins are synthesized specifically according to the nature of the stress:

• Osmoprotectants such as proline and glycinebetaine [xix] (osmotic stress, including water stress),
• HSP (Heat Shock Proteins, during high temperature stress),
• Proteins against aggregation/inactivation such as LEA (Late Embryogenesis Abundant Protein) during drought or cold stress, etc….

When the stress intensifies, by increasing its mode of action (increase in temperature, ozone concentration, salt content; etc…) or when it lasts very -too- long, the balance that allows a fair balance between production and destruction of ROS is broken. The signaling is disrupted and ROS play their full toxic role by destroying the membranes, allowing the synthesis of protein-destroying enzymes, leading to cellular disorganization and organ death.

4. ROS and the signaling relationships between cellular organelles and the nucleus

4.1. Redox balance and cellular compartmentalization

The redox balance within cells is ensured by the collaboration between the cytosol and the cellular organelles, mainly chloroplasts and mitochondria. During abiotic stresses, the usual production of ROS increases and tends to cause damage to organelles. Signaling systems, commonly called retrograde signals, allow chloroplasts and mitochondria to alert the nucleus, prompting it to synthesize repair compounds or antioxidant enzymes.

• In the case of chloroplasts, the singlet oxygen ¹O₂ causes the oxidation of carotenoids. The product of this oxidation acts as a stress signal [23]. The outcome of this retrograde signaling from the chloroplast to the nucleus is a change in gene expression in favor of photoacclimation.
• In the case of mitochondria, abiotic stresses lead to an increase in internal ROS production at respiratory chain complexes (see Figure 4). The influx of electrons to the different elements of the respiratory chain causes an increase in the transport of electrons, which becomes difficult to channel towards the final transformation of oxygen into water and causes a bottleneck favorable to the production of superoxide ions O₂–^.. A backup system, consisting of a particular oxidase, AOX (alternative oxidase, see Figure 4), allows direct capture of electrons and reduction of oxygen to water without participating in the establishment of the protomotive force necessary for the production of ATP. This valve minimizes the formation of superoxide ions [24]. There is, also in this case, a retrograde signaling, from the mitochondria to the nucleus, which pushes the latter to trigger the synthesis of AOX (Figure 12).

Communication between cellular organelles, chloroplasts and mitochondria, with the nucleus, through retrograde signaling, is therefore essential to maintain intracellular energy homeostasis at least during low and medium amplitude stress (Figure 12).[25]

4.2 Memory effect and epigenetics

A memory effect allows plants to trigger more adaptive responses when stresses recur (Figure 13) [26]. This memory effect is linked to epigenetic mechanisms that allow the genome to regulate its function while retaining genetic information. The importance of epigenetic regulations in the memory process has been highlighted [27] through the involvement of small regulatory RNAs, DNA methylation and histone modifications (proteins structuring DNA within chromatin). The modifications could be inherited and transmitted to the next generation (see Epigenetics: the genome and its environment).

4.3. Systemic response

Finally, it is important to understand the means by which the abiotic stress signal perceived by one part of a plant (leaf, root) spreads throughout the plant. The transmission of the stress signal from one leaf to its neighbors addresses the need for coordination of the response of all organs of a plant to that stress (systemic response). This coordination could be achieved by a self-propagating wave of ROS production, initiated at the level of a group of leaf cells and then spreading to the rest of the plant [28].

5. Prospects for the use of knowledge on signaling networks

The question arises as to the possible use of the findings on signaling networks and, in particular, on the multitude of transcription factors that are involved. Conventional methods of breeding stress-tolerant plant varieties, although useful, are proving to have their limitations. Attempts to improve stress resistance have therefore consisted in overexpressing certain types of enzymes, for example those involved in the synthesis of osmoprotectors [xx]. But the modification of a single enzyme is not sufficient because of the multiplicity of metabolic responses to stress.

Instead, genetic engineering using regulatory proteins, such as transcription factors, could be a more attractive approach to facilitate plant tolerance to stress [29]. Indeed, a single transcription factor is capable of controlling the expression of a large number of genes and current knowledge allows linking the role of several of these transcription factors to the response of plants to abiotic stresses.

Promising trials have already taken place with the creation of transgenic plants using transcription factors, notably to improve tolerance to drought, cold and salinity. However, for this technique to be beneficial in obtaining stable and productive transgenic plants, research is still needed, particularly on the dialogue between the different components of the signaling system and on the regulation of the behavior of these transgenic plants under favorable environmental conditions.

6. Messages to remember

• Under favorable environmental conditions, plants usually produce ROS, oxidative compounds that are known to be toxic to plant cells.
• The balance between ROS production and destruction is finely regulated, using the constitutively present antioxidant system. Cellular homeostasis is ensured and, at the same time, ROS play a major role, in association with phytohormones, in the cell signaling that ensures growth and development.
• When environmental stresses occur, the production of ROS is increased causing changes in membrane status and ionic balance.
• Signaling processes, combining ROS and hormones, will have to ensure the renewal of non-enzymatic and enzymatic antioxidant systems. A reorganization of the metabolism then follows from a modification of the expression of the genes, controlled by the signals coming from the cytosolic transmission cascades (messengers, kinases, transcription factors), but also carried by the organelles supplying energy, chloroplasts and mitochondria.
• The ROS-dependent stress signal is transmitted from cell to cell and then, in a systemic way, to the whole plant, so that an adapted response is proposed.
• The adjustments resulting from this intracellular mobilization may not be sufficient during more intense or prolonged stresses and the backup mechanisms may be overwhelmed. Membrane disorganization due to uncontrolled ROS attack is accompanied by disruptions in ionic balance and energy homeostasis, leading to a deleterious spiral leading to programmed cell death.
• A memory effect seems to be a decisive advantage allowing a plant having undergone a stress to respond with more efficiency to the reiteration of this stress.
• Genetic engineering could allow the construction of transgenic plants overexpressing transcription factors involved in the signaling and expression of adaptation genes, thus improving stress tolerance. In the current context of increasing adverse environmental conditions on plants, these techniques would be likely to maintain their productivity at an acceptable level.

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Notes and captions

Cover image. This plant, Welwitschia mirabilis, grows in Namibia in a hot, dry environment. Photo P. Dizengremel

[1] As opposed to biotic stresses resulting from the deleterious action of a living organism on another living organism such as an attack by a pathogen (bacteria, fungi, insects, etc.)

[2] Dizengremel P (2021) Ozone and plants, the history of a toxic relationship. The Conversation, May 2, 2021.

[3] Cernusak LA, Haverd V, Brendel O, Le Thiec D, Guehl JM & Cuntz M (2019) Robust response of terrestrial plants to rising CO₂. Trends in Plant Science, 24, 578-586.

[4] Boretti A & Florentine S . (2019) Atmospheric CO₂ concentration and other limiting factors in the growth of C3 and C4 plants. Plants, 8, 92 DOI:10.3390/plants8040092

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[8] Matyssek R, Le Thiec D, Löw M, Dizengremel P, Nunn AJ & Häberle KH (2006). Interactions between drought and O3 stress in forest trees. Plant Biology, 8, 11-17. DOI 10.1055/s-2005-873025.

[9] Das K & Roychoudhury A (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science, 2, 53. doi: 10.3389/fenvs.2014.00053.

[10] Hydrogen peroxide is best known by its aqueous formulation: hydrogen peroxide.

[11] https://fr.wikipedia.org/wiki/B%C3%AAta-oxydation

[12] Often called Rboh, for respiratory burst oxidase homolog

[13] Note that HO- production is also possible in the chloroplast lumen and in the mitochondrial intermembrane space.

[14] Waszczak C, Carmody M & Kangasjärvi J (2018). ReactivOxygen Species in Plant Signaling. Ann. Rev. Plant Biol., 69, 209-236.

[15] Noctor G, Reichheld JP & Foyer C (2018). ROS-related redox regulation and signaling in plants. Semin. Cell Dev. Biol. 80, 3-12. doi: 10.1016/j.semcdb.2017.07.013.

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[17] MAP Kinases or Mitogen-Activated Protein Kinases.

[18] Kumar M, Kesawat MS, Ali A, Lee SC, Gill SS & Kim HU (2019). Integration of abscisic acid signaling with other signaling pathways in plant stress responses and development. Plants, 8, 592. doi:10.3390/plants8120592.

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[21] Mansour A (2008). Heat schock activation of phospholipase C signaling pathway in tobacco cells. Plant Stress, 2, 131-137.

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