Antioxidant Responses and Redox Regulation Within Plant-Beneficial Microbe Interaction

Citation: González, M.-C.; Roitsch, T.; Pandey, C. Antioxidant Responses and Redox Regulation Within Plant-Beneficial Microbe Interaction. Antioxidants 2024,13, 1553. https://doi.org/10.3390/ antiox13121553 Academic Editor: Elena Forte Received: 31 October 2024 Revised: 13 December 2024 Accepted: 15 December 2024 Published: 18 December 2024 Copyright: © 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Review Antioxidant Responses and Redox Regulation Within Plant-Beneficial Microbe Interaction María-Cruz González 1,2,* , Thomas Roitsch 3,4 and Chandana Pandey 3,* 1Instituto de Bioquímica Vegetal y Fotosíntesis, Universidad de Sevilla and Consejo Superior de Investigaciones Científicas, 41092 Sevilla, Spain 2Departamento de Bioquímica Vegetal y Biología Molecular, Facultad de Biología, Universidad de Sevilla, 41012 Sevilla, Spain 3Copenhagen Plant Science Centre, Faculty of Science, University of Copenhagen, 1870 Frederiksberg, Denmark; r[email protected] 4CzechGlobe—Global Change Research Institute CAS, 603 00 Brno, Czech Republic *Correspondence: [email protected] (M.-C.G.); [email protected] (C.P.) Abstract: The increase in extreme climate events associated with global warming is a great menace to crop productivity nowadays. In addition to abiotic stresses, warmer conditions favor the spread of infectious diseases affecting plant performance. Within this context, beneficial microbes constitute a sustainable alternative for the mitigation of the effects of climate change on plant growth and productivity. Used as biostimulants to improve plant growth, they also increase plant resistance to abiotic and biotic stresses through the generation of a primed status in the plant, leading to a better and faster response to stress. In this review, we have focused on the importance of a balanced redox status for the adequate performance of the plant and revisited the different antioxidant mechanisms supporting the biocontrol effect of beneficial microbes through the adjustment of the levels of reactive oxygen species (ROS). In addition, the different tools for the analysis of antioxidant responses and redox regulation have been evaluated. The importance of redox regulation in the activation of the immune responses through different mechanisms, such as transcriptional regulation, retrograde signaling, and post-translational modification of proteins, emerges as an important research goal for understanding the biocontrol activity of the beneficial microbes. Keywords: biopriming; biocontrol; redox regulation; antioxidant responses; biotic stress; disease defense; beneficial microbe; symbiosis; sustainable agriculture 1. Introduction Human activity, and specifically the resulting increase in CO 2 concentration in the atmosphere, has led to an increase in global temperature, known as global warming. This in turn is responsible for climate change, including waves of high temperatures, drought, soil salinity, flooding, and chilling. All these conditions impose stress on plant growth that results in a decrease of crop yield, threatening the nourishment of an ever-increasing population. As a consequence, the decrease in the number of undernourished people observed from the 1990s on, due to UN policies [ 1 ], was slowed down from 2007 due, among other factors, to the impact of climate change on agriculture. Moreover, from 2014–2018 the number stopped decreasing [ 2 ], this being attributed to the higher tendency of extreme climate events. Plants possess different mechanisms to cope with stress situations [ 3 ]. Drought and high temperature affect membrane and protein stability and generate an increase in the production of reactive oxygen species (ROS), ultimately leading to an unbalanced metabolism and reduced photosynthetic activity [ 4 ]. To ensure survival under drought and heat stress, plants increase the synthesis of compatible solutes, that prevent the loss of water and play Antioxidants 2024,13, 1553. https://doi.org/10.3390/antiox13121553 https://www.mdpi.com/journal/antioxidants Antioxidants 2024,13, 1553 2 of 20 osmoprotective roles, maintaining membrane integrity and protecting proteins from denaturation. In addition, heat stress tolerance is dependent on the production of an increased amount of heat shock proteins (HSPs), that maintain protein homeostasis. In both cases, an adjustment of ROS levels is required to avoid damage to proteins, lipids, nucleic acids, and chlorophyll. Biotic stress associated with infection by pathogens, addressed in depth in this manuscript, is also associated with an increase in the production of ROS, a key event for the activation of plant immune responses. Moreover, ROS could alter the activity of redox-regulated enzymes. Therefore, an increase in the different antioxidant systems of the plant, reducing ROS levels, is key for plant survival under adverse conditions [5]. Different simulation models suggest that in the coming years productivity of the main crops (wheat, rice, maize, and soybean) will be decreased, due to an increasing degree of climate change [ 1 , 6 – 8 ]. In addition, the chemical composition of the harvested products could be altered, leading to a decrease in nutritional quality [ 9 ]. Therefore, efforts must be undertaken to generate crops that can better resist the actual adverse conditions. With this goal, traditional breeding and different genetic approaches have been used to analyze the effect of particular abiotic stresses on plant growth and productivity. However, the effect of the combination of stresses on plant responses has been overlooked for a long time [ 6 ]. In fact, climate change conditions subject plants to simultaneous abiotic stresses, provoking increased damage to the plants. In addition, warmer climates are responsible for the spread of emerging infectious diseases, related to the appearance of new pathogenic strains [ 6 , 10 ]. Since plants are subjected to multiple simultaneous stresses, understanding and improving plant tolerance to stress combinations is a must nowadays. Plants are associated with a variable number and diversity of microbes. They are referred to as microbiota and collectively encode the microbiome of a plant. The microbes can live in a neutral, beneficial, or pathogenic interaction [ 11 , 12 ]. The beneficial effects of the microbiota can be divided into two functions [ 12 ]: (1) Improvement of environmental adaptability, ecological plasticity, and fitness and (2) support of plant and root growth, development, and architecture. These functions are notably relevant for adaptation within climate change scenarios and also for sustainable and environmentally friendly agricultural production by their application as biostimulants to sustainably improve stress resilience and secure yield and yield stability [ 13 ]. Beneficial microorganisms not only upregulate plant growth under control conditions but also improve plant stress tolerance [ 14 ], inducing a primed state in the plant that results in a quicker and more efficient response to the stress conditions [ 15 ], including the rapid activation of non-enzymatic and enzymatic ROS detoxification mechanisms. In this manuscript, we will review the current knowledge on antioxidant responses elicited by plant-beneficial microbe interaction and discuss the effect on redox regulation, key for the activity of many photosynthetic enzymes and transcription factors. The knowledge on the effect of microbes on plant resistance towards biotic stress will also be revised. 2. Antioxidant Responses and Redox Regulation Increased ROS production is a common element in plant response to abiotic and biotic stresses. These molecules (e.g., H 2 O 2 , 1 O 2 , and O 2− ), with a higher reactivity than O 2 , are by-products of aerobic metabolism that play a key role as signaling molecules in plant responses to adverse conditions. In addition, ROS are also involved in the regulation of multiple processes of plant development [ 16 ]. However, since high ROS levels may damage the cell, inhibit plant growth, and eventually result in cell death, ROS levels must be finely tuned through a balance between production and scavenging mechanisms [ 16 , 17 ]. Stress conditions can alter this balance and plants with a higher tolerance to abiotic and biotic stresses due to priming with beneficial microorganisms show an increase in ROS detoxification mechanisms to prevent the effects of ROS accumulation. As an example, an oxidative burst is characteristic of plant defense against pathogens, due to the activity of plasma membrane NADPH oxidases, which generate O 2− . In addition, apoplastic peroxidases contribute to H 2 O 2 release, which is responsible for the activation of plant Antioxidants 2024,13, 1553 3 of 20 defense responses [ 18 ]. Hypersensitive response, preventing the spread of biotrophic pathogens in the plant, is also associated with an oxidative burst at the site of infection. Under abiotic stress, ROS production can be due an altered metabolism (metabolic ROS) but also a result of stress perception and activation of plasma membrane NADPH oxidases (signaling ROS), generating a ROS signature characteristic of each cell [ 19 ]. Metabolic ROS are associated with the generation of oxygen in the photosynthetic electron transport chain and its consumption by the photosystems within the chloroplasts, the main contributors to ROS production. Since ROS are generated in different cell compartments, different mechanisms operate in each of them to prevent their accumulation [ 16 ]. In the chloroplast, non-enzymatic antioxidants, such as carotenoids, tocopherols, and membrane lipids are involved in the detoxification of singlet oxygen ( 1 O 2 ), produced by energy transference of PSII to O 2 . On the other hand, superoxide anion (O 2− ), generated by the transference of one electron to molecular oxygen at PSI, is dismutated into hydrogen peroxide (H 2 O 2 ) by superoxide dismutases (SODs) (Figure 1). H 2 O 2 is also produced in the peroxisome due to the oxidation of 2-phosphoglycolate, generated by the higher oxygenase activity of Rubisco due to the increase in temperature. In the mitochondria, superoxide anion in the matrix, associated with the electron transport chain, is dismutated by SODs. H 2 O 2 is detoxified by ascorbate (ASC) and ascorbate peroxidases (APXs), glutathione (GSH) and glutathione peroxidases (GPXs), and peroxiredoxins (PRXs) in the stroma (Figure 1), by catalases (CATs) and APXs in the peroxisome, and by APXs, PRXs, and GPXs in the mitochondrial matrix. Antioxidants 2024, 13, x FOR PEER REVIEW 3 of 20 in the plant, is also associated with an oxidative burst at the site of infection. Under abiotic stress, ROS production can be due an altered metabolism (metabolic ROS) but also a result of stress perception and activation of plasma membrane NADPH oxidases (signaling ROS), generating a ROS signature characteristic of each cell [19]. Metabolic ROS are associated with the generation of oxygen in the photosynthetic electron transport chain and its consumption by the photosystems within the chloroplasts, the main contributors to ROS production. Since ROS are generated in different cell compartments, different mechanisms operate in each of them to prevent their accumulation [16]. In the chloroplast, non-enzymatic antioxidants, such as carotenoids, tocopherols, and membrane lipids are involved in the detoxification of singlet oxygen (1O2), produced by energy transference of PSII to O2. On the other hand, superoxide anion (O2.−), generated by the transference of one electron to molecular oxygen at PSI, is dismutated into hydrogen peroxide (H2O2) by superoxide dismutases (SODs) (Figure 1). H2O2 is also produced in the peroxisome due to the oxidation of 2-phosphoglycolate, generated by the higher oxygenase activity of Rubisco due to the increase in temperature. In the mitochondria, superoxide anion in the matrix, associated with the electron transport chain, is dismutated by SODs. H2O2 is detoxified by ascorbate (ASC) and ascorbate peroxidases (APXs), glutathione (GSH) and glutathione peroxidases (GPXs), and peroxiredoxins (PRXs) in the stroma (Figure 1), by catalases (CATs) and APXs in the peroxisome, and by APXs, PRXs, and GPXs in the mitochondrial matrix. Figure 1. Reactive oxygen species (ROS) production, ROS enzymatic detoxification, and redox regulation within the chloroplast. In the chloroplast, ROS are produced due to energy transference at PSII (singlet oxygen, 1O2) and electron transference to oxygen in PSI (superoxide anion, O2−). Superoxide anion is dismutated to hydrogen peroxide, which is in turn reduced by APX and ASC/GSH, through the ASC-GSH cycle. APX uses ascorbate to reduce hydrogen peroxide, generating monodehydroascorbate (MDA), which can be in turn reduced by monodehydroascorbate reductase (MDAR) using reducing equivalents. Spontaneous dismutation of MDA generates dehydroascorbate (DHA). Regeneration of ASC is catalyzed by dehydroascorbate reductase (DHAR) using GSH as source of reducing equivalents. GSH reduction is driven by glutathione reductase (GR). Redox regulation (represented by green arrows) in the chloroplast is dependent on disulfide–dithiol exchange of target proteins by Trxs, which are in turn reduced by FTR using Fd as source of reducing power. NTRC uses NADPH generated by FNR for the reduction of 2-Cys PRX, leading to hydrogen peroxide reduction. Whereas Trxs can also reduce 2-Cys-PRX, although less efficiently than NTRC, direct involvement of NTRC on protein reduction remains to be determined. Dashed lines indicate Figure 1. Reactive oxygen species (ROS) production, ROS enzymatic detoxification, and redox regulation within the chloroplast. In the chloroplast, ROS are produced due to energy transference at PSII (singlet oxygen, 1 O 2 ) and electron transference to oxygen in PSI (superoxide anion, O 2− ). Superoxide anion is dismutated to hydrogen peroxide, which is in turn reduced by APX and ASC/GSH, through the ASC-GSH cycle. APX uses ascorbate to reduce hydrogen peroxide, generating monodehydroascorbate (MDA), which can be in turn reduced by monodehydroascorbate reductase (MDAR) using reducing equivalents. Spontaneous dismutation of MDA generates dehydroascorbate (DHA). Regeneration of ASC is catalyzed by dehydroascorbate reductase (DHAR) using GSH as source of reducing equivalents. GSH reduction is driven by glutathione reductase (GR). Redox regulation (represented by green arrows) in the chloroplast is dependent on disulfide–dithiol exchange of target proteins by Trxs, which are in turn reduced by FTR using Fd as source of reducing power. NTRC uses NADPH generated by FNR for the reduction of 2-Cys PRX, leading to hydrogen peroxide reduction. Antioxidants 2024,13, 1553 4 of 20 Whereas Trxs can also reduce 2-Cys-PRX, although less efficiently than NTRC, direct involvement of NTRC on protein reduction remains to be determined. Dashed lines indicate not yet established direct interaction. Protein complexes were schematized for a better understanding. Leaves image: https://www.flaticon.com/free-icon/leaves_1635265?term=leaves&page=1&position=4& origin=search&related_id=1635265 (accessed on 16 September 2024). The production and detoxification of H 2 O 2 in the chloroplasts (Figure 1) through 2-Cys PRXs, which are reduced using reduced ferredoxin (Fd red ) produced by the photosynthetic electron transport chain, through the activity of Fd-tiorredoxin-reductase (FTR) and thioredoxins (Trxs), the so-called Fd/FTR/Trx system, are closely linked to redox regulation of protein activity through dithiol–disulfide exchange. However, although plastidial Trxs can reduce 2-Cys PRXs with different efficiencies, the main reductant in vivo is NTRC, a bimodal enzyme with NADPH-thioredoxin reductase (NTR) and Trx domains in one polypeptide, which can use NADPH as source of reducing power [ 20 ]. Since NTRC and Trxs are responsible for the reductive activation of plastidial enzymes, through dithiol–disulfide exchange, the drainage of electrons from Trxs to 2-Cys PRXs in an ntrc mutant affects the activation of Calvin–Benson cycle (CBC) enzymes, ATP, and chlorophyll biosynthesis, between other processes, resulting in a decrease in plant growth [ 21 ]. In addition, Cys residues are sensitive to oxidation by H 2 O 2 , leading to the formation of sulfenic acid, which can react with glutathione or other thiol groups, in a process reversed by glutarredoxins (Grxs) and Trxs. Otherwise, they can be further oxidized to sulfinic and, irreversibly, to sulfonic acid, provoking protein damage. The de-protonated form of the Cys residue can also react with reactive nitrogen species (RNS), leading to the formation of nitrosothiols, through S-nitrosylation. Some of these post-translational modifications associated with retrograde signaling, gene transcription regulation [22], and plant immune responses [23] will be discussed later. Trxs, Trx-like proteins, and Grxs are present in different cell compartments as a multigenic family, allowing the adjustment of plant physiology to the environmental conditions, through reduction and oxidation of proteins [ 24 , 25 ]. In the chloroplast, f1-2 and m1-4 Trxs are involved in redox regulation of carbon fixation and reducing power exchange with the cytosol [ 26 , 27 ] whereas xand y1-2 Trxs function mainly as antioxidants [ 28 , 29 ], due to their ability to reduce 2-Cys PRXs and PRX-Q, respectively. This is also the case of NTRC, the most efficient reductant of 2-Cys PRXs. Though several interactors of NTRC have been identified, the participation of NTRC in direct redox regulation of protein targets is under discussion (Figure 1) [ 20 , 30 ]. Finally, Trx zis a component of plastid-encoded RNA polymerase, essential for chloroplast biogenesis. The mitochondria possess two otype Trxs, with Trx o1 regulating the Krebs cycle, and a Trx h2 able to regulate alternative oxidase (AOX). Finally, hTrxs, modulating the response to biotic and abiotic stresses, are widely distributed in the cytosol, nucleus, apoplast, and endoplasmic reticulum. Grxs, using GSH as electron donor, are in turn present in cytosol, plastid, nucleus, and mitochondria. In addition to regulating protein activity, Trxs participate in the regulation of signaling pathways and as chaperones. Furthermore, recent studies have revealed a key role of some Trx-like proteins, such as TrxL2 and ACHT, and even a typical Trx, Trx f1, in the oxidation and inactivation of proteins through the transference of electrons to 2-Cys PRX [31]. The study of ROS in plant responses to abiotic and biotic stresses requires the use of various advanced techniques and platforms. These methods enable the precise detection, quantification, and understanding of ROS dynamics, contributing to the validation and extension of existing research. Biochemical assays, especially enzyme activity assays, are pivotal in providing direct insights into the physiological status of plants by measuring the catalytic activities of enzymes involved in ROS detoxification [ 32 – 35 ]. The traditional assays involve preparing protein extracts from plant materials and subjecting them to spectrophotometric measurements to determine enzyme activities, offering robust and reliable data critical for understanding cell physiological processes [ 34 , 35 ]. Despite being labor-intensive, recent technological advancements have significantly enhanced the throughput of these Antioxidants 2024,13, 1553 5 of 20 assays. Robot-based platforms now automate enzyme activity measurements, utilizing a microtiter plate format for end-point determinations and product detection through cycling reactions, increasing throughput by up to 100-fold. Cost-efficient alternatives have also been developed, using a 96-well microtiter plate format and microplate spectrophotometers for real-time monitoring of reaction linearity through kinetic assays [ 34 , 35 ]. These setups enable semi-high-throughput enzyme activity analysis, making the technique accessible to a broader range of researchers, allowing a more complete picture on how abiotic or biotic stresses are affecting enzymatic antioxidant activity. Notably, an analytical platform has been established to assess the activity signature of nine antioxidant enzymes [ 35 ]. However, in some cases, a more detailed analysis of the levels and activity of ROS non-enzymatic and enzymatic detoxification methods in the different cell compartments would be required. Complementing enzyme activity assays, metabolic flux analysis, histochemical activity staining, and redox status monitoring techniques provide a holistic view of metabolic capacities and regulatory mechanisms. Metabolic flux analysis links enzyme activity profiles with flux distributions in metabolic networks, employing isotope-based methods and mathematical models to predict metabolic responses to genetic and environmental changes [ 36 – 38 ]. Different methods allowing monitoring the cellular redox status in planta have been recently developed based on redox-sensitive fluorescent proteins, such as roGFP or rxYFP, for the analysis of H 2 O 2 , NAD(P)H, and glutathione redox status in different cell compartments [ 39 ]. In addition, a 2-Cys PRX biosensor allows the determination of its oxidation levels in the chloroplast, associated with photosynthesis performance [ 40 ]. However, although there has been substantial improvement in understanding how primed plants maintain redox homeostasis, so far only a few reports deal with the changes in redox regulation associated with plant-beneficial microbe interaction. For this, in addition to biochemical assays, genetic and molecular biology techniques, such as mutant analysis, gene expression analysis, and protein interaction studies, are essential. Mutant analysis elucidates the functional roles of genes involved in ROS metabolism and detoxification pathways, complemented by RNA sequencing (RNA-seq) to measure gene expression under oxidative stress [ 41 , 42 ]. Protein interaction studies, employing co-immunoprecipitation (Co-IP) and yeast two-hybrid (Y2H) assays, elucidate intricate networks of antioxidant enzymes vital for cellular defense mechanisms. Additionally, proteomics techniques, such as mass spectrometry (MS) and redox proteomics, provide comprehensive insights into ROS- responsive proteins, detailing theirdynamics and modifications during stress conditions [ 43 , 44 ]. Advanced imaging methods like confocal microscopy and live-cell imaging play an important role in visualizing ROS production and distribution within plant cells, linking these dynamics to physiological outcomes under oxidative stress. This integrated approach establishes a robust framework for studying ROS and antioxidant responses in plants. It not only ensures precise experimental outcomes but also enhances our understanding of plants’ adaptive strategies against oxidative stress. This contributes significantly to advancements in the knowledge on plant stress physiology and resilience mechanisms. Accordingly, Ameztoy et al. [ 45 ], based on redox proteomics and the analysis of mutants lacking different components of chloroplast redox detoxification, 2-Cys PRX, and redox regulation, NTRC, have identified thiol redox proteome changes affecting photosynthesis as a component of plant responses to fungal volatiles emitted by Alternaria alternata. On one hand, fungal volatile organic compounds (VOCs) failed to increase photosynthetic capacity in ntrc plants. On the other hand, the analysis of the redox proteome showed that whereas VOCs promote the reduction of the thiol redox proteome in wildtype plants, the effect in ntrc plants was the opposite, promoting protein oxidation. This effect was reverted when ntrc plants had reduced levels of 2-Cys PRXs, in the ntrc- ∆ 2cp mutant plants, showing that NTRC-dependent modification of the status of the redox proteome is key for plant responses to VOCs. Furthermore, the analysis of a mutant devoid of one of the plastidial isoforms of fructose-1,6-bisphosphatase, cfbp1, that is subjected to redox regulation, showed that fungal VOCs regulate photosynthetic plant responses through chloroplast-to-nucleus retrograde signaling [ 46 ]. In particular, cfbp1 plants showed downregulation of plastidial Antioxidants 2024,13, 1553 6 of 20 Trxs and enzymes related to the methyl erythritol (MEP) pathway and photosynthesis and failed to show any growth promotion by VOCs. 3. Impact of Plant-Beneficial Microbe Interaction on Biological Processes Involving ROS and Redox Regulation 3.1. Growth and Development Under Normal and Abiotic Stress Conditions ROS play a crucial dual role in plant growth and development. On one hand, ROS function as essential signaling molecules regulating key biological processes; on the other hand, as mentioned before, their overaccumulation can cause oxidative stress and cellular damage. Therefore, maintaining a delicate balance between ROS production and scavenging is fundamental for normal plant development. During plant growth, ROS are involved in multiple developmental stages, including seed germination, root elongation, shoot growth, and the differentiation of various tissues. For instance, H 2 O 2 , one of the primary forms of ROS, is known to participate in cell wall loosening during root hair formation and in the promotion of cell expansion. Furthermore, O 2− is crucial for controlling the rate of cell division in meristematic tissues. These ROS-mediated processes ensure proper organogenesis and are tightly regulated by both ROS-producing enzymes, such as NADPH oxidases, and antioxidant systems, such as SOD, CAT, and peroxidases (POX). The inoculation of plants with plant-beneficial microbes typically results in an impact on the antioxidant machinery of plants. Through these interactions, beneficial microbes are expected to help plants manage oxidative stress and promote healthy development and contribute to coping with stress and support growth and development (Figure 2). This correlation was shown by activity profiling of antioxidant enzymes (POX, APX, CAT, SOD, GR, DHAR, and MDAR) [ 35 ] for the stimulation of growth of tomato by different Pseudomonas strains [ 42 , 47 ]. The effect of beneficial microbes on plant resistance to abiotic stress has been reviewed in several recent reports, with a special focus on the alleviation of salinity stress through the activation of antioxidant systems [ 48 – 51 ] and, therefore, will not be addressed in depth in this review. As an example, improvement of water use efficiency by Bacillus licheniformis FMCH001 [ 52 ] in maize, salt tolerance in quinoa by Burkholderia phytofirmans PsJN [ 53 ], and drought responses in tomato by Pseudomonas fluorescens G20- 18 [ 42 ] correlated with specific antioxidant enzyme activity fingerprints compared to the corresponding mock controls. Also, at a whole microbiome level such correlations are evident. A correlation between the distinct difference in the activity profile of specific antioxidant enzymes of Abies plants of the same age but with different growth patterns and the relative abundances of specific taxa of the microbiome could be established [54]. In addition to the direct role of ROS in regulating plant development, ROS also interact with other signaling pathways that influence plant growth [ 55 – 57 ]. One such pathway is target of rapamycin (TOR) signaling, a central regulator of nutrient-dependent growth in plants. TOR signaling integrates sugar and light signals to drive plant growth, but its activity must be tightly controlled to prevent excessive growth at the cost of stress tolerance. Under nutrient-rich conditions, TOR promotes growth by stimulating anabolic processes, while during stress, TOR activity is inhibited, allowing the plant to allocate resources to survival mechanisms. The negative feedback loop involving the plant-specific protein FLZ8 is critical in moderating TOR activity [ 58 ]. FLZ8 reduces TOR signaling under unfavorable growth conditions, allowing for enhanced SnRK1 signaling, which is essential for stress responses. This regulatory balance ensures that plants can grow when resources are available but remain ready to activate stress responses during environmental challenges [ 59 ]. FLZ8 stabilizes SnRK1 signaling by promoting the interaction between SnRK1a1 and RAPTOR1B, a key component of TOR, thereby ensuring that TOR activity is kept in check during nutrient sufficiency [ 60 ]. This fine-tuned regulation prevents TOR hyperactivation and contributes to the plant’s ability to respond to stress. The dynamic balance between TOR and SnRK1, modulated by ROS and other signaling molecules, allows plants to prioritize growth or stress responses depending on environmental conditions. Recent studies have demonstrated that plant growth under stressful conditions, such as drought, Antioxidants 2024,13, 1553 7 of 20 salinity, or nutrient deficiency, is often accompanied by increased ROS generation [ 42 , 61 , 62 ]. However, plants primed with beneficial microbes exhibit enhanced stress tolerance due to their ability to quickly detoxify ROS [ 42 , 63 ]. This microbial modulation of ROS not only promotes plant growth under optimal conditions but also enhances growth resilience under environmental stresses. In addition to enzymatic antioxidant responses, beneficial microbes may induce the accumulation of non-enzymatic antioxidants such as ascorbate and glutathione, further contributing to the maintenance of redox homeostasis during plant development. The fungus Acremonium alternatum enhances salt stress tolerance by regulating host redox homeostasis in combination with phytohormone signaling [64]. Antioxidants 2024, 13, x FOR PEER REVIEW 7 of 20 Figure 2. Effect of Plant-Growth-Promoting Rhizobacteria (PGPRs), Nitrogen-fixing bacteria, and Mychorriza on plant growth and resistance to abiotic and biotic stresses. The inoculation of the plant with microbes, which can be attracted by root exudates, alters nutrient availability, thus promoting plant growth and development. In addition, the microbes generate a primed state in the plants leading to enhanced resistance towards biotic and abiotic stresses. This effect is dependent on the control of ROS levels, through activation of enzymatic and non-enzymatic antioxidant mechanisms, and also on redox regulation mediated by Trxs, NTRC, and 2-Cys PRX. At the genome level, post-tran- scriptional modification of Cys alters subcellular localization of some TFs and results in the regulation of gene expression. PTMs of Cys residues, mediated directly or indirectly by ROS, also underlie operational retrograde signaling, allowing the adjustment of protein levels. Epigenetic modifications, such as DNA methylation, are emerging as key components in plant response to biotic stress and transgenerational priming, underlying the biocontrol activity of some microbes. At the proteome level, regulation of protein structure and/or activity through PTMs constitutes an additional layer of regulation. Dithiol–disulfide exchange of Cys residues results in the activation of key enzymes in photosynthesis. Some other PTMs, such as S-nitrosylation and glutathionylation, have been associated with gene transcription regulation and plant immunity. Figure was created in Bio- Render (https://BioRender.com/z93q802, accessed on 16 September 2024). In addition to the direct role of ROS in regulating plant development, ROS also interact with other signaling pathways that influence plant growth [55–57]. One such pathway is target of rapamycin (TOR) signaling, a central regulator of nutrient-dependent growth in plants. TOR signaling integrates sugar and light signals to drive plant growth, but its activity must be tightly controlled to prevent excessive growth at the cost of stress tolerance. Under nutrient-rich conditions, TOR promotes growth by stimulating anabolic processes, while during stress, TOR activity is inhibited, allowing the plant to allocate resources to survival mechanisms. The negative feedback loop involving the plant-specific protein FLZ8 is critical in moderating TOR activity [58]. FLZ8 reduces TOR signaling under unfavorable growth conditions, allowing for enhanced SnRK1 signaling, which is essential for stress responses. This regulatory balance ensures that plants can grow when resources are available but remain ready to activate stress responses during environmental challenges [59]. FLZ8 stabilizes SnRK1 signaling by promoting the interaction between SnRK1a1 and RAPTOR1B, a key component of TOR, thereby ensuring that TOR activity is Figure 2. Effect of Plant-Growth-Promoting Rhizobacteria (PGPRs), Nitrogen-fixing bacteria, and Mychorriza on plant growth and resistance to abiotic and biotic stresses. The inoculation of the plant with microbes, which can be attracted by root exudates, alters nutrient availability, thus promoting plant growth and development. In addition, the microbes generate a primed state in the plants leading to enhanced resistance towards biotic and abiotic stresses. This effect is dependent on the control of ROS levels, through activation of enzymatic and non-enzymatic antioxidant mechanisms, and also on redox regulation mediated by Trxs, NTRC, and 2-Cys PRX. At the genome level, posttranscriptional modification of Cys alters subcellular localization of some TFs and results in the regulation of gene expression. PTMs of Cys residues, mediated directly or indirectly by ROS, also underlie operational retrograde signaling, allowing the adjustment of protein levels. Epigenetic modifications, such as DNA methylation, are emerging as key components in plant response to biotic stress and transgenerational priming, underlying the biocontrol activity of some microbes. At the proteome level, regulation of protein structure and/or activity through PTMs constitutes an additional layer of regulation. Dithiol–disulfide exchange of Cys residues results in the activation of key enzymes in photosynthesis. Some other PTMs, such as S-nitrosylation and glutathionylation, have been associated with gene transcription regulation and plant immunity. Figure was created in BioRender (https://BioRender.com/z93q802, accessed on 16 September 2024). In conclusion, the interaction between plants and beneficial microbes can improve plant growth and development by regulating ROS production and enhancing antioxidant responses. This symbiotic relationship provides an efficient system for plants to cope with oxidative stress, ensuring sustained growth under both normal and adverse environmental conditions. As a result, the incorporation of plant-beneficial microbes into agricultural practices presents a promising strategy for enhancing crop yield and resilience in the face of growing environmental challenges. Antioxidants 2024,13, 1553 8 of 20 3.2. Disease Defense, Biocontrol, and Biopriming Disease generated by different plant pathogens, such as bacteria, fungi, oomycetes, viruses, and herbivores, is one of the main causes of crop losses worldwide. Crop yield losses due to pathogens are estimated at USD 220 billion, a value further increased by the post-harvest losses caused by some pathogens [ 10 ], especially fungi, which affect all stages of crop production, accounting for 20–25% of total post-harvest losses [ 65 ]. Viruses and fungi are the main pathogens responsible for plant diseases, followed by pathogenic bacteria. The development of a disease depends on the detection methods present in the plant that give rise to the different protection mechanisms but also on the evasion of detection by the pathogens that suppresses the plant defense response. In brief, recognition of the pathogens takes place primarily at the plasma membrane, where pathogen recognition receptors (PRRs) are able to detect some common pathogenic elements collectively named as pathogen-, microbe-, or herbivore-associated molecular patterns (PAMPs/MAMPs/HAMPs), such as bacterial flagellin or elongation factor Tu (EF-Tu) and fungal chitin, among others. In addition, in cell wall damage, producing glycans or an increase in the extracellular levels of ATP, so-called damage-associated molecular patterns (DAMPs) can be detected by PRRs, triggering a defense response. This response, known as PRR-mediated immunity (PMI), extracellular triggered immunity (ExTI), or surface-receptor-mediated immunity (SRMI), is characterized by a signaling cascade involving the activation of protein kinases. Evolution of pathogens allows the suppression of PMI by the production of effector molecules, leading to effector-triggered susceptibility (ETS). Plants in turn have evolved resistance genes coding for intracellular nucleotide-binding leucine-rich repeat receptors (NLRs), which can recognize effectors and promote a defense response denoted as NLR-mediated immunity (NMI), intracellular triggered immunity (InTI), or intracellular-receptor-mediated immunity (IRMI). This response requires in some cases the assistance of helper NLRs which activate immune responses by formation of calcium channels and activation of transcription factors. Although specific signaling components participate in PRR- and NLR-mediated immunity, recent studies suggest that there is an interdependency between them [ 66 ]. In any case, the plant–pathogen interaction determining susceptibility to or resistance against a particular pathogen of a crop is under constant co-evolution, with the development of new recognition receptors or resistance genes by the plants and new effectors that challenge plant immune systems by the pathogen. However, the development of a disease depends not only on the plant and the pathogen itself but also on the environmental and culture conditions, with high-density crops facilitating the spread of pathogens. The environmental conditions affect plant– pathogen interaction in multiple ways. First, by altering pathogen dynamics, favoring its survival and replication and leading to the appearance of new more aggressive strains due to the increases in temperature associated with global warming. Second, by altering plant physiology and biochemistry, leading to enhanced susceptibility due to the suppression of salicylic acid production or increases in abscisic and jasmonic acid biosynthesis under high temperatures. Third, by altering the expression of hormone-responsive genes within the plant cell [ 10 ]. Besides temperature, two other factors associated with climate change affect pathogen infectivity, atmospheric carbon dioxide levels and water availability. The increase in atmospheric CO2positively affects crop yield but, on the other hand, has been shown to increase wheat susceptibility towards Fusarium graminarearum, powdery mildew severity on cucurbits, and head blight and blotch on wheat. However, in other cases the severity of the disease was reduced in these conditions, so a general assumption on the effect of CO 2 concentration on pathogen spread cannot be drawn. Higher temperatures increase the amount of water vapor in air after rain, promoting the infectivity of pathogens affecting aerial tissues, mainly fungi. On the contrary, the effect of soil moisture levels on diseases provoked by soil-inhabiting pathogens is diverse. In any case, the combined effect of these environmental factors could have altered the plant immunity mechanisms described before [67]. Antioxidants 2024,13, 1553 9 of 20 The generation of ROS associated with the interaction of plants with different types of pathogens, such as bacteria, fungi, and viruses, is essential for triggering signaling cascades that contribute to plant resistance. Already at the plant cell surface ROS are produced by a family of NADPH oxidases, known as respiratory burst oxidase homologs (RBOHs), activated upon pathogen recognition by PRRs, in a process that seems to be pathogen specific. In addition, apoplastic POXs contribute to the generation of ROS. In fact, the production of ROS by POXs seems to be required for the activation of NADPH oxidases and the consequent oxidative burst. Moreover, it has been suggested that H 2 O 2 and superoxide anion produced by POXs and RBOHs, respectively, can specifically activate signaling pathways leading to plant resistance [ 68 – 70 ]. A second-wave production of ROS has been linked to the interaction with avirulent pathogens associated with NLR-mediated immunity, resulting in the hypersensitivity response, crosslinking of the membrane cell wall, deposition of callose, and stomatal closure. However, a reduced accumulation of H 2 O 2 was observed in compatible interactions of wheat with Septori tritici [ 71 ], showing that ROS production is a key element in wheat defense. Although the inhibition of biotrophic pathogens by H 2 O 2 is clear, its effects on necrotrophic pathogens are diverse [ 70 ]. While chloroplasts, mitochondria, and peroxisomes contribute to the generation of ROS, the chloroplast is the main organelle responsible for ROS production. Within the chloroplast, the effect of different bacterial effectors alters electron transport and ROS production resulting in pathogenesis, showing that plastidial production of ROS is essential for plant defense [ 23 ]. Furthermore, plastidial ROS generation alters redox homeostasis in the cytosol and mitochondria [ 72 ]. In addition to oxidative burst and hypersensitive response, apoplastic ROS produced by RBOHs also underlie systemic acquired resistance [73]. Oxidation of Cys residues due to pathogen-induced ROS has been described as related to plant immunity responses (Figure 2). This modification can alter protein structure/function, localization, and stability. As an example, the release of non-expressor of pathogenesis-related genes 1 (NPR1) monomers by reduction mediated by TRX his essential for its translocation to the nucleus and the elicitation of transcriptional regulation [ 74 ], showing that an adequate shaping of the redox proteome is essential to plant immunity. In addition, the formation of NPR1 oligomers is favored by protein nitrosylation promoted by the pathogen. RBOHD activity, and the subsequent ROS production, is impaired by Cys nitrosylation [ 75 ]. ROS-induced oxidation is also necessary to activate MAPK cascades [ 76 ]. Finally, oxidation of HPCA, a receptor kinase involved in stomata closure under stress, is necessary for its activation by autophosphorylation [ 76 , 77 ]. In addition, since Trxs can revert the oxidation of Cys, not only of disulfide but also of sulfenic and nitrosothiols, a key role of these proteins in immune response was suggested, that is supported by experimental evidence [ 23 , 78 ]. Taking into account that the oxidation of proteins is dependent on the ROS levels, the maintenance of the ROS balance is essential for the plant response toward pathogens. Consequently, antioxidant enzymes (CAT, APX, POX, PRX) and non-enzymatic antioxidants (ascorbate and glutathione) are suggested to play a key role in the immune response [ 23 , 79 , 80 ]. Interestingly, some of the antioxidant enzymes, cytosolic APXs and PRXs, have been reported to be regulated by oxidative modification [23]. Priming plants for a quicker and better response to pathogens constitutes a promising and sustainable alternative to the use of pesticides, overcoming, in addition, the development of pathogen resistance. Besides natural active compounds, such as vitamins, hormones, or hormone antagonists, the use of beneficial fungi and bacteria as biostimulants, promoting plant growth, and biocontrol agents, promoting plant resistance, has gained attention in the last decade [ 15 , 81 ]. 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