Quick Facts of Textual Content:
1. What is ROS
The oxygen-rich atmosphere on Earth determines the evolution of multicellular life forms, and many organisms depend on oxygen to survive, and physiological processes related to oxygen molecules (O2) occur in cells all the time, and O2 inevitably produces reactive oxygen species (ROS) with changes in electrons and energy (Raymond and Segrè, 2006; waszczak et al., 2018)。ROS is a family of molecules derived from O2 that are chemically more reactive than O2 (Waszczak et al.)., 2018)。The main forms of ROS in cells include hydrogen peroxide (H2O2), superoxide radicals (O2).), singlet oxygen (1O2), hydroxyl radical (Hoand various forms of organic and inorganic peroxides (Mittler et al.).Anderson et al., 2022) (Figure 1). Since ROS is unstable and extremely reactive, which allows it to destroy various molecules and structures of cells, ROS was considered a toxic by-product of aerobic metabolism in the past. With the continuous development of research, ROS has been found to play an active role in many physiological processes in plants, and abnormal high levels of ROS within cells can be toxic to plant cells (Foyer and Noctor, 2005; mittler, 2017)。
Figure 1 Generation and chemical structure of ROS (Waszczak et al.)., 2018)。The dots represent electrons, and 3p680 is the triplet state of the main electron donor of photosystem II.
2. The role of ROS in plants.
Now that we understand what ROS is, let's take a look at what ROS does. Overall, ROS acts as a key signaling molecule that allows cells to respond quickly to different stimuli. In plants, ROS plays a crucial role in abiotic and biotic stresses, as well as signaling (Mittler et al.)., 2022)。It is important to note that ROS does not only play a role in the response of plants to external stimuli, but also plays an important role in the normal growth and development of plants. In addition, under abnormal circumstances, low or high levels of ROS can also cause damage to the plant itself, but this will not be discussed in depth in this article. Next, we will focus on the positive effects of ROS on plants (Mhamdi and Van Breusegem, 2018;). mittler, 2017)。
ROS in biological stress
When talking about the response of plants to biological stress, we have to mention the concepts of PTI (pattern-triggered immunity) and ETI (effector-triggered immunity) in plant innate immunity. In the process of confrontation between plants and pathogens, plants have established two "lines of defense" in order to resist the infection of pathogens. The first line of defense is PTI excited by pathogen-associated molecular patterns (PAMP), and the second line of defense is ETI excited by effector. While PTI and ETI were previously seen as separate mechanisms, they have now been found to complement each other and work together to help plants defend against pathogens (Yuan et al.).Anderson et al., 2021) (Fig. 2). An important aspect of the downstream immune response shared by both is the outbreak of ROS. ROS can not only directly cause damage to pathogens, induce programmed death of plant cells and thus limit pathogens, but can also act as signaling molecules to transmit signals and synergize with other defense substances (Kim et al.)., 2022; van breusegem and dat, 2006)。
Fig.2 Plant PTI and ETI induced outbreak of ROS (Yuan et al.)., 2021)。
ROS in plant PTI reactions is mainly produced by the activation of membrane-bound Nadph oxidase RBOHs, which catalyze the formation of O2 from O2and subsequently converted to H2O2 by peroxidase (Wang et al.)., 2020)。Nadph has been studied as a raw material for the production of H2O2. In May 2022, Yan Liang's group at Zhejiang University published a study titled "The receptor-like cytosolic kinase ripk activates nadp-malic enzyme 2 to generate nadph for fueling the ros production" in Molecular Plant**. In this study, the authors identified an enzyme in Arabidopsis thaliana that catalyzes the production of NADPH, nadp-me2, and found that the deletion of this enzyme leads to a decrease in its activity, which in turn leads to a decrease in NADPH content (Fig. 3a, b). In addition, the Arabidopsis ROS outbreak was significantly attenuated after the PTI response of the NADP-ME2 mutant (Figure 3C).
Fig.3 Determination of Nadp-Me2 enzyme activity, NaDPH content and ROS outbreak (Wu et al.)., 2022)。
ROS in abiotic stress
When plants live in a complex environment, in addition to various biotic stresses, they also need to deal with various abiotic stresses, such as drought, high temperature, high salinity, and bright light. There are two main types of ROS in abiotic stress, including metabolic ROS due to disruption of metabolic activity and signaling ROS as part of a signaling network in response to abiotic stress (Choudhury et al.)., 2017)。Unlike biotic stress, ROS cannot directly deal with the adverse effects of various abiotic stresses, so ROS can only "save the country" and help plants cope with abiotic stresses through other indirect means. Metabolic ROS can directly alter the redox state of rate-limiting enzymes and control intracellular metabolic fluxes, thereby altering different metabolic responses to counteract the effects of abiotic stresses (Miller et al.)., 2010)。In addition, ROS can also modulate key regulatory proteins through oxidative modification (OXIPTMS) to improve plant adaptation to abiotic stresses by signaling (Noctor and Foyer, 2016) (Fig. 4). More about Oxiptms will be introduced to you in the following content!
Fig.4 ROS (Choudhury et al.) in abiotic stress, 2017)。
In September 2023, Fengning Xiang's group at Shandong University published a study titled "H2O2-dependent oxidation of the transcription factor GMNTL1 promotes salt tolerance in soy bean" in The Plant Cell. In this study, the authors identified a membrane-bound transcription factor GMNTL1 in soybean that may be involved in salt stress. Under the induction of salt and H2O2, the localization of GMNTL1 shifted from the endoplasmic reticulum to the nucleus, and further studies found that GMNTL1-mediated salt tolerance was H2O2-dependent. In order to deepen the intrinsic relationship between **H2O2 and GMNTL1 in the process of salt tolerance, the authors first speculated whether H2O2 directly oxidized GMNTL1, and found that the 247th cys of GMNTL1 was oxidized by H2O2 by verifying the possible oxidation modification site of GMNTL1, and this site was crucial for the nucleation of GMNTL1. After elucidating the upstream pathway of GMNTL1, the authors finally identified the key targets of GMNTL1 downstream to regulate salt tolerance, GMNHX1 and GMCHX1. In summary, salt-induced H2O2 mediates the post-translational modification and migration of GMNTL1 cysteine, enhancing its ability to transcriptionally activate downstream target genes, thereby improving salt tolerance in soybean (Fig. 5).
Fig. 5 Patterns of H2O2-mediated GMNTL1 oxidation and improvement of salt tolerance in soybean (Zhang et al.)., 2023)。
ROS in Signaling
In the first two sections, Xiaoyuan and everyone ** the role of ROS in plants in response to stress. Attentive friends can find that in addition to using itself to deal with various coercions, ROS often transmits signals as a signaling molecule. ROS signaling can be divided into intracellular signaling and intercellular signaling, and Xiaoyuan will introduce these two aspects next.
1 Intracellular ROS signaling.
In the complex subcellular environment of plants, ROS perception and activation of different signaling pathways can occur in different regions. Overall, ROS signaling can be divided into exogenous (apoplast and cell wall), endogenous (cytoplasm and nucleus), and organelles (chloroplasts, mitochondria, peroxisomes, and other organelles). Under stress conditions, the ROS signals in these different regions remain interactive or independent of each other (Mittler et al.)., 2022)。
RBOHS, AQPS (aquaporins) and cell wall-bound peroxidases (Maurel et al.) play a major role in exogenous ROS signaling, 2015; mittler et al., 2022; wang et al., 2020)。In addition, Ca2+ channels on the cell membrane, as well as various membrane receptors, also play an important role in the downward transmission of signals (Castro et al.)., 2021; r**i et al., 2023)。RBOHS is known as the "engine of ROS signaling", and its cytosolic amino or carboxyl terminus can be regulated by processes such as phosphorylation and dephosphorylation, thereby regulating ROS production (Kimura et al.)., 2020)。In order to transmit signals down the cell, ROS must enter the cell, usually through AQPS, but also by endocytosis (Golani et al.).Anderson et al., 2013) (Fig. 6).
During endogenous ROS signaling, the cytoplasmic matrix receives ROS from exogenous and organelles. The cytoplasmic matrix contains a number of enzymes that regulate ROS production and clearance (Mittler et al.).Anderson et al., 2022), these enzymes can regulate the amount of ROS in the cytoplasmic matrix, thereby regulating the signaling centers downstream of ROS in the cytoplasmic matrix. In addition to the cytoplasmic matrix, the nucleus also receives ROS signals and regulates the expression of different genes. In addition, redox regulatory proteins are also present in the nucleus, which can regulate ROS signaling in the nucleus, and thus also participate in the regulation of downstream genes (Gutsche and Zachgo, 2016; murmu et al.Anderson et al., 2010) (Fig. 6).
In the process of organelle ROS signaling, organelles, as the main site of ROS production, can produce ROS and can also autonomously clear ROS to regulate their own ROS levels (Waszczak et al.)., 2018)。In addition to autonomously regulating the amount of ROS and thus regulating signaling, ROS signals can also be transmitted between organelles or from organelles to the nucleus, although some ROS signals do not cross the cytoplasm or only cross the cytoplasm at a very short distance (Ding et al.)., 2019)。In addition to this, ROS between different organelles can also be transmitted through the mediation of intermediate signals, resulting in an alteration of ROS content in the delivered organelles (Mittler et al.).Anderson et al., 2022) (Figure 6).
Fig.6 ROS signaling process in cells (Mittler et al.), 2022)。
2 ROS signaling between cells.
In the previous section, Xiao Yuan and everyone learned about intracellular ROS transmission, and I believe that everyone has a certain understanding of the process of intracellular ROS transmission. In fact, when ROS is transmitted in plants, it is impossible to be limited to only one cell, and it is usually necessary to transmit it in a long-distance area, because when a cell senses stress, it needs to transmit signals to other cells and even the whole plant in order to cope with stress. However, as mentioned earlier, ROS generally exists for a very short period of time (Figure 1) and is therefore unlikely to be transported over long distances. Thus, the long-distance transport of ROS between cells is first a change in the ROS content of a single cell, and then it is sensed by neighboring cells, causing its ROS content to also change, and propagating between cells in this way, which is also known as "ROS wave" (Castro et al.).Anderson et al., 2021) (Fig. 7a). The propagation of ROS waves between adjacent cells is via plasmodesmata or apoplast pathways (Fichman et al.)., 2021)。In addition, when talking about the long-distance transmission of ROS signaling, it is easy to think of systemic acquired resistance (SAR) in plant immunity, because SAR is characterized by the stimulation of local defense signals leading to a defense response in the plant distally or even in the whole plant. Unfortunately, current studies do not appear to have a significant relationship between ROS waves, which are induced by substances such as N-hydroxy-pipecolic acid (NHP) and salicylic acid (SA) (Yildiz et al.)., 2021)。Interestingly, ROS waves are a very fast process, while NHP transfer is a relatively lagging process. In addition, in tomato RBOHD and RBOHF mutants, the level of H2O2 decreased along with the content of NHP precursor pipecolic acid (Gilroy et al.)., 2014; wang et al., 2018)。These instructions ROS may serve as an indication of SAR and remind plants to prepare for SAR.
Fig. 7 Intercellular ROS signaling process (Mittler et al.), 2022)。(A) Schematic diagram of intercellular ROS signaling. (b) The process of local extension of ROS to the whole plant after Arabidopsis thaliana stress.
3 Perception of ROS signals.
After the ROS signal is conducted, the cell needs to receive and respond to the signal, which requires the ROS signal to be perceived. However, due to the nature of ROS, it is less likely to be sensed in a "ligand-receptor" manner, but more likely to be sensed through oxidative modification, in which cells respond to ROS signaling by changing the structure, localization, and activity of the modified protein (Castro et al.)., 2021; zhou et al., 2023)。
Oxiptms (oxidative modification) refers to the covalent modification of small molecules with redox activity (such as H2O2, etc.) on the sulfhydryl group of protein cysteine. Common OXIPTMS include sulfonic acid (-SOH), sulfonic acid (-SO2H), and sulfonic acid (-SO3H) (Fig. 8), which can affect plant growth and development and stress response processes (Zhou et al.)., 2023)。Related cases can be found in "22 ROS in Abiotic Stress "Oh!
Fig. 8 Generation and mutual transformation of oxiptms (Zhou et al.)., 2023)。
ROS regulation of plant growth and development.
In the previous sections, Xiao Yuan talked about the role of ROS when plants are under stress and how to signal and be perceived. These descriptions of ROS are mainly for plants that have been subjected to stress, but in fact, in addition to responding to external stresses through ROS, plants themselves also regulate physiological processes such as apical meristem differentiation, cell wall lignification, stomatal and flower development, seed germination, and root development through ROS signaling (Mhamdi and Van Breusegem 2018; wang et al.Et al., 2023) (Figure 9). Due to the transmission of ROS signals as well as perception in 2It has already been introduced in 3, so I won't introduce it too much here. If you want to know the specific cases of ROS regulation of plant growth and development, you can consult the literature by yourself!
Fig.9 ROS signaling regulates plant growth and development (Wang et al.)., 2023)。
Brief summary.
In the second part, Xiaoyuan introduced the role, transmission and how to perceive ROS signals, and I believe you have a general understanding of how ROS works. ROS, which was originally thought to be a harmful substance, can transmit signals and help plants resist various stresses, and the concept of ROS being considered as a second messenger has gradually become widely recognized due to its key role in the signaling process (Qi et al.)., 2024)。The question of when ROS is toxic to cells and when it plays an important role as a second messenger may depend on the amount of ROS in the cell, with abnormally high levels of ROS likely to have a negative effect and low levels of ROS playing an active role in signaling (Wang et al.)., 2023)。In addition, it is interesting to note that in the previous description, the ROS signals under different stresses appear to be separate from each other, but it has been found that ROS signals can link different stresses (biotic or non-biotic) (Berrios and Rentsch 2022).
3. Maintenance of ROS homeostasis in plant cells.
As mentioned earlier, the role that ROS plays in a cell depends on its content, and the maintenance of ROS homeostasis is essential for its function. Next, Xiaoyuan will talk about the sites where ROS is produced in cells and how to maintain their homeostasis. In plant cells, ROS is produced mainly by apoplast bodies and various organelles such as mitochondria, chloroplasts, and peroxisomes (Castro et al.).Anderson et al., 2021), these sites essentially contain antioxidant systems to buffer the local redox environment. In addition, this regionalization is more helpful in reducing the toxicity of high levels of ROS to cells, and it also helps to form a complex system to cope with different stresses (Castro et al.)., 2021; waszczak et al., 2018)。Next, Xiaoyuan will maintain the homeostasis of the main parts of ROS production.
Fig.10 Sites of ROS production in plant cells (Castro et al.)., 2021)。
ROS in chloroplasts
Chloroplasts are known to be sites of photosynthesis. Under light conditions, the photosystem and ROS are generated, and the main ROS type is O2, H2O2 and 1O2, etc. (Castro et al..), 2021)。For these ROs, chloroplasts have corresponding systems to remove. For the O2 produced by the photosystemand h2o2, o2H2O2 can be disproportionated by superoxide dismutase (SODS) in the matrix of thylakoid membranes or spontaneously formed by superoxide dismutase (SODS) (ASADA 2006). H2O2 is detoxified by ascorbate peroxidase (APXS), glutathione peroxidase (GPXLS), and peroxidase (PRXRS) (ASADA 2006). For 1O2 produced by photosystems, although there is currently no enzyme that directly removes 1O2, it can be eliminated by reacting with other molecules, such as tocopherols and carotenoids (Krieger-Liszkay and Trebst 2006; ramel et al., 2012)。
Fig. 11 ROS in chloroplasts (Waszczak et al..), 2018)。
ROS in mitochondria
Mitochondria are the site of cellular respiration, and their ROS production is closely related to the mitochondrial electron transport chain (METC). Mitochondrial complexes I, II, and III are thought to produce O2All three complexes produce and release O2 into the mitochondrial matrixIn addition, Complex III can also release O2 into the intermembrane space−(huang et al., 2016)。O2 in the mitochondrial matrixIt can be converted to H2O2, which is eventually cleared by a series of oxidases, similar to the removal of H2O2 in chloroplasts. However, H2O2 in the intermembrane space can be cleared by ascorbic acid (ASC) and may be transferred to the cytoplasmic matrix due to the permeability of the outer mitochondrial membrane (Wazczak et al.)., 2018)。
Fig. 12 ROS in mitochondria (Waszczak et al.)., 2018)。
Xiaoyuan chatteredIn this tweet, Xiao Yuan talks to you about the role of ROS in plants in responding to various stresses and signaling, how it is transmitted and perceived within cells, and how to maintain its homeostasis. Although there is a better understanding of ROS, there are still many questions that need to be studied in depth, such as how ROS is transmitted in different locations, how the nucleus distinguishes between different ROS signals, how ROS signals are perceived, and the role of ROS in the complex intracellular signaling network as a whole. ROS, which was originally thought to be harmful to plants, has gradually shown its important role and can now be seen in many important studies, such as ferroptosis. It is believed that with the deepening of research, the "true face" of ROS will gradually be revealed.
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