From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation?

Wurlitzer, Wesley Borges; Labudda, Mateusz; Silveira, Joaquim Albenisio G.; Matthes, Ronice Drebel; Schneider, Julia Renata; Ferla, Noeli Juarez

doi:10.3390/ijpb15030043

Open AccessReview

From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation?

by

Wesley Borges Wurlitzer

^1,2,*

,

Mateusz Labudda

³

,

Joaquim Albenisio G. Silveira

⁴

,

Ronice Drebel Matthes

¹,

Julia Renata Schneider

^1,2

and

Noeli Juarez Ferla

^1,2

¹

Laboratory of Acarology, Tecnovates, University of Vale do Taquari—UNIVATES, Av. Avelino Talini, 171, Lajeado 95914-014, RS, Brazil

²

Postgraduate Program in Biotechnology, University of Vale do Taquari—UNIVATES, Av. Avelino Talini, 171, Lajeado 95914-014, RS, Brazil

³

Department of Biochemistry and Microbiology, Institute of Biology, Warsaw University of Life Sciences-SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland

⁴

Plant Metabolism Laboratory (LabPlant), Department of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza 60451-970, CE, Brazil

^*

Author to whom correspondence should be addressed.

Int. J. Plant Biol. 2024, 15(3), 561-585; https://doi.org/10.3390/ijpb15030043

Submission received: 13 June 2024 / Revised: 20 June 2024 / Accepted: 24 June 2024 / Published: 27 June 2024

(This article belongs to the Section Plant Communication)

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Abstract

:

Plants are directly exposed to several biotic factors. Among these, mite species belonging to the superfamilies Eriophyoidea and Tetranychoidea stand out due to their ability to injure or even transmit viruses to their host plants. In response to infestations by these organisms, reactive oxygen species (ROS), regulated by enzymatic and non-enzymatic antioxidants (homeostasis), can act as signaling molecules to induce defenses or even acclimatization in attacked plants. However, depending on the severity of the stress, there can be an imbalance between ROS and antioxidants that can result in oxidative stress, leading to membrane damage by lipid peroxidation, organelle inactivation, and even cell death. In this review, we outline for the first time the current state of understanding regarding the role of cellular processes in ROS metabolism, such as signaling, the potential damage induced by ROS, and the defense role of enzymatic antioxidant systems involved in the plant–mite relationship. Furthermore, we identify several gaps between redox metabolism and plant defense against phytophagous mites.

Keywords:

antioxidants; oxidative stress; biotic factors; redox metabolism; ROS signaling

1. Introduction

Plants are essential for maintaining ecosystems in different environments. In urban areas, they are efficient organisms that contribute to a reduction in high temperatures, improve air quality, and enhance water drainage. In agricultural ecosystems, the intercropping of different plant species promotes diverse agroecosystems that benefit nutrient cycling and soil fertility, facilitating the development of robust and sustainable crops [1,2]. There is also no doubt about the importance of plants as a source of sustenance for both humans and animals. Expectations for the global population exceed nine billion people by 2050, confirming the high demand for global food production [3]. In this scenario, the use of plants in the production of medicines or even in bioregulators is also predicted since they are often rich in phytochemicals beneficial to health [4].

Plants are sessile multi-module organisms that have an evolved, refined, and sophisticated sensorial system capable of rapidly triggering signaling defense mechanisms to perceive, memorize, and constantly learn from a spatiotemporal perspective [5,6]. Plants are constantly exposed to various adverse factors, whether biotic or abiotic [7], with biotic factors alone causing losses on the order of 20–40% [8,9,10]. They are characterized by the attack of pathogens, insects, and other arthropods, such as phytophagous mites [11,12]. Among phytophagous mites, Eriophyidae, Tenuipalpidae, and Tetranychidae are considered the main families with economic importance, as a significant portion of them are associated with damage to the leaves, stems, buds, and fruits of cultivated plants [13,14].

To defend themselves against herbivory, plants trigger various genetic and hormonal mechanisms, including constitutive defenses that are present in their metabolism or are induced when they synthesize compounds at the site and time of damage occurrence [11,15,16,17,18]. Such mechanisms can induce reactive oxygen species (ROS) production, which can be a signal leading to various defense responses [19]. ROS can be beneficial as they can play roles in cell proliferation, metabolic regulation, and stress acclimation [19,20]. However, when the redox metabolism suffers from homeostatic breakdown, the system can generate ROS overaccumulation, which has the strong potential to cause damage via a reduction in chlorophyll concentration and photosynthetic efficiency, an increase in membrane damage, and oxidation of lipids, proteins, and DNA molecules [11,19,20,21].

Studies involving plants and mites are strongly lacking in supplying a robust body of information in the current literature [17]. The signaling redox and defense processes in plants under mite infestations are still obscure, and most studies involving redox homeostasis have focused on unraveling plant responses to Tetranychus urticae Koch (Tetranychidae) infestations. There are other reactive species in plants, such as nitrogen species (RNS), sulfur species (RSS), and carbonyl species (RCS), for which there are still no consolidated studies regarding their responses to phytophagous mite attacks [22]. Thus, to understand and further employ suitable biological tools to control mite infestations in important crops, it is essential to update all available existing knowledge from a critical and physiological perspective.

In this review, we focus on the current understanding of the role of ROS metabolism in cellular processes, the defense role of the enzymatic and non-enzymatic antioxidant systems, the potential damage or protection induced by them, and the involvement of some related transcription factors (TFs) involved in phytophagous mite attacks in plants. In this way, we are providing the current scenario of the scope, outlining the gaps, and suggesting possible existing tools that should still be studied and further employed as defense mechanisms to enhance knowledge and advance the subject. Therefore, we address the following topics: general aspects of the mite–plant relationship; how phytophagous mite infestations can alter plant redox homeostasis; and lipid peroxidation and physiological responses induced by oxidative, transcriptomic, and transcription factor responses engaged in redox state regulation in mite-infested plants.

2. Mite–Plant Relationship: General Aspects

The mites of the Eriophyoidea superfamily are mostly monophagous species [13,23]. They feed on a plant’s cellular contents through a complex of stylets derived from the palps, chelicerae, and lips, which mainly reach the epidermal cells. From there, the cellular contents are sucked, causing weak mechanical damage and chlorotic and necrotic spots resulting from the partial emptying of the cells and/or due to hypersensitivity reactions [13,14,23]. There is no evidence of the action of saliva on the cell cuticle [23]; however, the saliva surely has a lubricating action that allows for the sliding of the stylets among them and their penetration into the cell walls. Mites of this family, in addition to transmitting viruses and toxins, are also capable of causing disorder in plant cells and forming galls or other plant alterations that serve as shelter and a means of feeding [23,24,25].

Mites from the families Tetranychidae and Tenuipalpidae (Tetranychoidea superfamily) are generally polyphagous, feed mainly on mesophyll cells, inject saliva with different properties, and feed through the stylets that are inserted inside the cells, pressed by mobile stylophora [14,26,27]. In addition, the suction process is well known; that is, the palps press the plant tissues while the pharyngeal pump sucks the cellular content [13,14,28]. Tenuipalpidae mites represent important virus vectors [14]. Species of Tetranychidae are considered of economic importance mainly due to their ability to develop resistance to insecticides, severe infestations of different hosts, and fast life cycles [28,29]. They empty and damage photosynthetically active grouped cells in one minute, sucking up fragments of DNA, RNA, proteins, and grana, causing translucent spots occupied by air [13,30].

Infestations by mites belonging to the taxa mentioned above can cause lipid peroxidation, membrane damage, cell death, and reduced photosynthetic activity due to oxidative stresses [26,31,32,33,34]. However, it is exceedingly difficult to differentiate oxidative responses such as signaling-redox metabolism, antioxidant defense, and oxidative damages since redox indicators and diagnosis systems based on threshold levels are lacking to date.

3. Phytophagous Mite Infestation Alters Plant Redox Homeostasis

3.1. Production of Reactive Oxygen Species in Infested Plants

The ROS, produced by different organelles (Figure 1B), are mainly singlet oxygen (¹O₂), superoxide anion (O₂^•−), hydrogen peroxide (H₂O₂), and hydroxyl radical (OH^•). Among them, O₂^•− and H₂O₂ are well known but little studied in plants under mite infestations (Table 1). Each ROS has specific chemical characteristics and half-life time (Figure 2). The signaling triggering these oxidative species in plants is capable of alerting cells to threats caused by phytophagous mites (Figure 3). These signaling mechanisms can involve other physiological plant processes such as senescence, memory, and others [6,35,36,37].

Figure 1. Simplified representation of the organelles involved in the production of O₂^•− and H₂O₂ in plants under phytophagous mite infestation. The generation of ROS in plants is closely linked to central physiological processes of energy generation and consumption, such as photosynthesis. The level of ROS depends on a delicate balance between production (oxidative activity) and removal (antioxidative activity), resulting in a redox balance (redox homeostasis). Plants under infestation by phytophagous mites produce ROS such as H₂O₂ and O₂^•− for defense signaling. These ROS are mainly produced by apoplast, mitochondria, vacuoles, chloroplasts, endoplasmic reticulum, and cytoplasm. In this process, when mite infestation becomes stressful for plants, ROS lose redox homeostasis with the antioxidant defense system, leading to oxidative stress, lipid peroxidation, membrane damage, DNA and RNA damage, cellular death, and stomatal closure. (A) Biological agroecosystem with wheat (a), corn (b), soybean (c), and grapevine (d) plants under the infestation of phytophagous mites. (B) Organelles of the plants involved in the production of O₂^•− and H₂O₂. (C) Oxidative stress, including lipid peroxidation (enhanced level of malondialdehyde (MDA)) as a response to redox imbalance between O₂^•− and H₂O₂, and enzymatic antioxidants, represented by the structure of chloroplastic Fe superoxide dismutase (Fe-SOD). Created in Biorender.com [38].

Figure 2. Formation of reactive oxygen species (ROS), their respective t_½ half-life times, and general characteristics. ROS are characterized as being derived from oxygen, formed from an atom or molecule that loses or gains an electron, with unique and specific definitions. In the process of formation, oxygen (O₂) undergoes a change in its reactive state, forming singlet oxygen (¹O₂) or undergoing a reduction with the gain of e-, forming the superoxide anion (O₂^•−). Oxygen can also undergo a second reduction and form the peroxide ion, to which two hydrogens are bonded, forming hydrogen peroxide (H₂O₂), which can interact with Fe²⁺ to form the hydroxyl radical (OH^•) through the Fenton reaction. Most of the time, the O₂^•− is the first radical to be produced; it has low mobility because it does not cross membranes, and it can be considered an initiator of reaction cascades that generate other ROS. Hydrogen peroxide is a considerably stable ROS. It is characterized by its strong signaling potential and the ability to cross membranes through aquaporins. Created in Biorender.com [38], adapted from Mittler [19].

Table 1. Levels of reactive oxygen species (ROS) in plants under infestation with different species of phytophagous mites, time of infestation, and cultivars.

Mite Family	Species	Plant	Cultivar	Time of Infestation	Levels of ROS (%)	References
Eriophyidae	Aceria tosichella	Hordeum vulgare	Airway	18 *	↑680 H₂O₂ ↓25 O₂^•−	[34]
	Eriophyes tiliae	Tilia platyphyllos	−	−	in situ H₂O₂	[25]
	Colomerus vitis	Vitis vinifera	Ghalati (Su)	7 *	↑3 H₂O₂	[32]
				14 *	↑20 H₂O₂
				28 *	↑32 H₂O₂
			Rishbaba (Su)	7 *	↑9 H₂O₂
				14 *	↑24 H₂O₂
				28 *	↑56 H₂O₂
			Neyshaboori (Su)	7 *	↑7 H₂O₂
				14 *	↑15 H₂O₂
				28 *	↑46 H₂O₂
			Muscat (Su)	7 *	↑7 H₂O₂
				14 *	↑48 H₂O₂
				28 *	↑84 H₂O₂
			White Thompson (Re)	7 *	↑25 H₂O₂
				14 *	↑50 H₂O₂
				28 *	↑104 H₂O₂
			Sahebi (Re)	7 *	↑23 H₂O₂
				14 *	↑53 H₂O₂
				28 *	↑78 H₂O₂
			Koladari (Re)	7 *	↑28 H₂O₂
				14 *	↑62 H₂O₂
				28 *	↑101 H₂O₂
			Atabaki (Re)	7 *	↑9 H₂O₂
				14 *	↑24 H₂O₂
				28 *	↑105 H₂O₂
Tenuipalpidae	Brevipalpus yothersi	Arabidopsis thaliana	genotypes +	6 **	in situ H₂O₂	[26]
				12 **	in situ H₂O₂
				24 **	in situ H₂O₂
				8 *	in situ H₂O₂
Tetranychidae	Schizotetranychus oryzae	Oryza sativa	IRGA 424	60 *	in situ H₂O₂ and O₂^•−	[21]
Tetranychidae	Tetranychus macfarlanei	Plumbago zeylanica	−	0 *	↑2 H₂O₂	[39]
				15 *	↑19 H₂O₂
				30 *	↑60 H₂O₂
				60 *	↑92 H₂O₂
				90 *	↑134 H₂O₂
				120 *	↑92 H₂O₂
	Tetranychus urticae	Phaseolus vulgaris	Bronco	55 *	↑110 H₂O₂	[31]
		Arabidopsis thaliana	genotypes +	24 **	↑119 H₂O₂	[40]
		Medicago truncatula	ecotype +	1 *	↑100 H₂O₂	[41]
		Ocimum basilicum	−	1 *	↑300 H₂O₂	[42]
				7 *	↑444 H₂O₂
				14 *	↑233 H₂O₂
		Melissa officinalis	−	1 *	↑32 H₂O₂
				7 *	↑8 H₂O₂
				14 *	↑12 H₂O₂
		Salvia officinalis	−	1 *	↑82 H₂O₂
				7 *	↑12 H₂O₂
				14 *	↑106 H₂O₂
		Ocimum basilicum	Sweet basil (Su)	1 *	↑280 H₂O₂	[33]
				7 *	↑390 H₂O₂
				14 *	↑190 H₂O₂
			Purpurascens (Su)	1 *	↑200 H₂O₂
				7 *	↑210 H₂O₂
				14 *	↑180 H₂O₂
			Fino Verde (Su)	1 *	↑25 H₂O₂
				7 *	↓10 H₂O₂
				14 *	↓5 H₂O₂

* days; ** hours; − no information. Su: susceptible; Re: resistant. + For work carried out with different genotypes or ecotypes, the values were averaged. Hydrogen peroxide (H₂O₂) and superoxide (O₂^•−). % Levels of increase (↑) and decrease (↓) of treatment in relation to the control.

Figure 3. Hypothetical systemic diagram of the redox state and H₂O₂ levels in plant communication when under infestation by phytophagous mites. At the moment of infestation, mites can secrete specific proteins produced by glands that lead to physical and chemical modifications in the host plant. The initiation of defenses occurs when pattern recognition receptors (PRRs) detect the presence of herbivore-associated molecular patterns (HAMPs), microbe-associated molecular patterns (MAMPs), or damage-associated molecular patterns (DAMPs) on the leaf epidermis (I). The plant exhibits a local response that spreads systemically to neighboring, unaffected cells. In this process, the production of ROS such as H₂O₂ can occur, and it can be considered an active process called the ‘ROS/H₂O₂ wave’ that determines the propagation of H₂O₂ levels and the redox state from cell to cell. Specifically, the redox state can be propagated through plasmodesmata pores and/or through the membranes they traverse, while H₂O₂ can be propagated between cells through the apoplast and/or plasmodesmata (II). Therefore, cell-to-cell signaling in sheath cells, xylem, phloem, and throughout the plant must also occur (III and IV). In this process, specific proteins participate in the plant defense transduction pathway against mites, and genes like MATI, in addition to acting in this control, also lead hormonal crosstalk in the jasmonic acid (JA)/salicylic acid (SA) balance and reduce levels of H₂O₂ in cells (II). Studies with other species of mites need to be carried out. This information is based on reports from trials conducted with T. urticae. Signaling in the cells of the sheath, xylem, and phloem and in different regions of the plant is hypothetical. Therefore, new studies based on these considerations are also strongly suggested. A, plasmodesmata; B, apoplast; C, nuclei; D, metabolism redox; E, receptor H₂O₂-induced Ca²⁺ increases 1 (HPCA1); F, NADPH oxidases; G, cell wall; H, O₂^•−; I, peroxiporin; J, H₂O₂; K, chloroplast; L, mitochondria; M, peroxisomes; N, endoplasmic reticulum; O, phytophagous mite infestation; P, xylem; Q, phloem; R, redox state propagating process; S, H₂O₂ propagating process; T, a hypothetical propagation/signaling in plants under phytophagous mite infestation; U, bundle sheath cells. Created in Biorender.com [38], adapted from Santamaria et al. [11] and Mittler and Jones [43].

As a first warning process, in addition to the important signaling resulting from ROS (redox metabolism) (Figure 3), depolarization in membrane potential (V_m), electrical signals, together with cytosolic Ca²⁺ influxes, ion channel activities, and an increase in RNS, can be triggered in plants under infestation by phytophagous mites [11,44]. One of the few studies in the literature involving T. urticae demonstrated changes in ROS levels, cytosolic Ca²⁺ influxes, and V_m in the cells of its host plant [45]. In this way, it is obvious that an infestation of phytophagous mites goes far beyond causing just injuries; that is, a cascade of signals in their host plants is activated, and they are able to integrate local responses at a systemic, non-local level [46]. It is also evident that PRRs recognize the phytophagy signals of T. urticae; however, more studies need to be carried out to understand whether this fact is repeated among other plant–mite species. Furthermore, the RNS response in plants infested by phytophagous mites is not yet known for certain, and so far, information is scarce.

Redox metabolism signaling processes also participate in the senescence processes of plant leaves, together with phytohormones, transcription factors, and other diverse genetic and molecular mechanisms [47]. In fact, ROS have been considered one of the main signs of senescence in plants infested by phytophagous mites (Figure 3). Blasi et al. [21] concluded that H₂O₂ and O₂^•− in situ, along with senescence gene expression OsSGR, were marked for rice plants infested by Schizotetranychus oryzae Rossi de Simons (Tetranychidae), suggesting a relationship (ROS/senescence). Similarly, it was also observed that the infestation of Tetranychus macfarlenei Baker & Pritchard (Tetranyhichidae) caused a reduction in photosynthetic pigments, contrary to the increased levels of H₂O₂ in Plumbago zeylanica L. (Plumbaginaceae) [39]. Therefore, infestations of phytophagous mites obviously caused this process in the leaves of their host plants; however, systemic studies, taking into account the different types of leaves and the region of the plant that will be evaluated, are essential for an accurate diagnosis. To date, there are no published studies that prove this response in the plant–mite relationship. However, the preliminary results of our research revealed that soybean plants infested by Tetranychus sp. accelerated the breakdown of redox homeostasis in old leaves, associated with strong signs of senescence, unlike mature leaves, which maintained homeostasis and stability (unpublished data).

In most of the studies, we found that infested plants showed oscillations in redox metabolism (Table 1 and Table 2). This is a good indicator of the state of stress, which briefly begins with the alarm state (transient stage), followed by moderate stress (when it does not significantly affect the plant’s essential functions), severe or chronic stress (affects the plant’s vital functions leading to death), or a non-stressful phase (with mild stress), which activates different epigenetic mechanisms guaranteeing memory and resistance [48]. Thus, the senescence processes mentioned above can be classified (depending on the intensity) as moderate to severe stress. Taking into account the memory and acclimatization processes of plants, in general the most important mechanism in the process is signaling by H₂O₂, which can react directly with sulfhydryl groups (SH) of proteins and transcription factors. This mechanism changes their redox states, triggers a signaling cascade into the nucleus, and induces changes in gene expression through transcription factors [44]. In this way, a memory process could occur in the cultivar “Ghalati” of Vitis vinifera L. (Vitaceae) under the infestation of Colomerus vitis (Pagenstecher) (Eriophyidae) and their erinea, which presented relatively low levels of H₂O₂ and lipid peroxidation and a slight increase in the activity levels of antioxidant enzymes, revealing a low oscillation in redox metabolism (a mild stress) [32].

Interestingly, in addition to the damage, the anomalies induced by mite infestations, such as galls and erineas, also result in a redox metabolism signaling process. It is possible that redox homeostasis may also be imbalanced in the apoplast and symplast of plant tissues, where mites such as Eriophyes tiliae (Pagenstecher) (Eriophyidae) induce gall formation [49] on Tilia platyphyllos Scop. Hydrogen peroxide was detected in the gall tissue induced by mites on this plant. A large number of chloroplasts and mitochondria can also be found in these structures, which can also contribute to the imbalance due to the high rate of ROS production in these organelles [50]. Infestations of C. vitis induce the formation of erinea on grapevines [51,52]. It is very likely that the same metabolic process known for galls is found in erinea; however, to date, there is no concrete information about which genetic and biochemical phenomena occur.

3.2. Action of Antioxidant Enzymes as a Defense Mechanism on Infested Plants

To maintain the important homeostasis of redox metabolism, plants display complex genetic, metabolic, and physiological responses to maintain their redox homeostasis, essentially controlling their ROS accumulation through the antioxidant systems (Table 2). A common response is an increase in the activity of antioxidant enzymes or the accumulation of reduced and total antioxidant compounds [19,43]. Antioxidant enzymes work by directly eliminating ROS or converting them into other ROS and further into non-harmful molecules, such as H₂O [19]. Enzymes act as biological catalysts; that is, they reduce the free energy of activation of a reaction, increasing the rates of biochemical reactions and making them fast and possible [53]. The main antioxidant enzymes are SODs (EC 1.15.1.1), catalases (CATs) (EC 1.11.1.6), ascorbate peroxidases (APXs) (EC 1.11.1.11), glutathione-S-transferases (GST) (EC 2.5.1.18), glutathione reductases (GR) (EC 1.6.4.2), guaiacol peroxidases (GPOX) (EC 1.11.1.7), and glutathione peroxidases (GPX) (EC 1.11.1.9), among several others [19,54]. In addition to enzymes, plants have some important non-enzymatic compounds that are essential as reducing and enzymatic cofactors. The most important are ascorbate, glutathione, and single phenols, which can be found in their reduced and oxidized forms in plant cells.

It is in this context that some studies have focused. For example, T. urticae showed better performance in Arabidopsis thaliana plants that had the silencing of the genes that encode oxidative enzymes, GPX7, GSTU4, and ascorbate, which are involved in the degradation of H₂O₂ [40]. Silencing of nitrosoglutathione reductase (GSNOR) in Nicotiana attenuata Torr. ex S. (Solanaceae) under the herbivory of Manduca sexta (L.) (Sphingidae) decreased the accumulation of jasmonic acid (JA) and ethylene (ET) [55]. Thus, although GSNOR does not act directly on H₂O₂, it is an important enzyme that regulates hormonal defense levels. The only study involving the GSNOR enzyme evaluated Hordeum vulgare plants under Aceria tosichella infestation, and in these plants the activity was increased [34]. Thus, it is strongly suggested that JA and ET are accumulated in plants infested by mites as well; however, studies involving enzymatic and hormonal metabolism are extremely necessary to understand the plant–mite defense relationship.

Plants can also express several SOD isoforms widely distributed in several cellular compartments, such as the apoplast, cytosol, mitochondria, chloroplasts, and peroxisomes [19]. For Shi et al. [56], SOD activity appeared to be dependent on C. vitis density, with an increase to a certain level followed by a decrease with high density. However, SOD activity can largely vary depending on the time at which the plant is evaluated [54,57], since it is a metallic enzyme that acts on the front line as the first to be activated in plants in response to some stressful factors [58,59]. Additionally, it converts O₂^•− into H₂O₂ [60], thus revealing that SOD activity is not dependent on infestation intensity. Furthermore, it must be taken into account that the plant–mite relationship is very complex, as the distribution of mites on plants is not homogeneous and also depends on other factors, such as the behavior of each species of mite. Recent results indicate that the age of the leaves defines the distribution of mites on their host plants, with a greater preference for young leaves [61]. In this way, more refined and systemic studies are highly encouraged, from a plant/redox metabolism perspective (modular host) versus species/phytophagous mite (behavior).

Catalases are another important family of plant peroxidases that stand out for maintaining redox homeostasis, catalyzing the decomposition of H₂O₂ into H₂O [60,62], and oxidizing hydrogen donors such as phenols [63]. In the literature, most works have supported a significant decrease in CAT activity in plants infested with mites (Table 2). As CATs have a very high Michaelis–Menten constant (K_m) for H₂O₂, these peroxidases should be mostly important in circumstances of high H₂O₂ accumulation inside peroxisomes during high photorespiration rates or immediately after an oxidative burst [64]. Thus, an induced decrease in CAT activity could indicate several scenarios, especially spatiotemporal changes after infestations [65]. Unfortunately, to understand the physiological roles of CATs and other antioxidant enzymes in response to mite infestation, several study types are lacking, especially from a spatiotemporal perspective.

Table 2. Levels of antioxidant enzymes in plants under infestation with different species of phytophagous mites, times of infestation, and cultivars.

Mite Family	Species	Plant	Cultivar	Time of Infestation	Antioxidant Enzyme Levels (%)	References
Eriophyidae	Aceria cladophthirus	Solanum dulcamara	−	3 *	↑850 POD	[66]
	Aculops lycopersici	Lycopersicon esculentum	Castlemart	4 *	↑239 POD, ↑100 LOX, ↑57 PPO	[67]
	Colomerus vitis	Vitis vinifera	Ghalati (Su)	7 *	↑24 SOD, ↑5 CAT, 0 POD, ↓2 PAL, ↑8 PPO	[32]
				14 *	↓15 SOD, ↓6 CAT, ↑16 POD, ↓0 PAL, ↑2 PPO
				28 *	↑36 SOD, ↓9 CAT, ↑25 POD, ↑13 PAL, ↑36 PPO
			Rishbaba (Su)	7 *	0 SOD, ↑4 CAT, ↑1 POD, ↑2 PAL, ↓3 PPO
				14 *	↑66 SOD, ↑8 CAT, ↑27 POD, ↑3 PAL, ↑31 PPO
				28 *	↑61 SOD, ↑7 CAT, ↑80 POD, ↑3 PAL, ↑50 PPO
			Neyshaboori (Su)	7 *	↓2 SOD, ↑6 CAT, ↓16 POD, ↑6 PAL, ↓5 PPO
				14 *	↑4 SOD, ↓5 CAT, ↑13 POD, ↑28 PAL, ↑8 PPO
				28 *	↑1 SOD, ↓10 CAT, ↑41 POD, ↑23 PAL, ↑25 PPO
			Muscat (Su)	7 *	↑24 SOD, ↑7 CAT, 0 POD, ↑12 PAL, ↑5 PPO
				14 *	↑68 SOD, ↑2 CAT, ↓2 POD, ↑8 PAL, ↑10 PPO
				28 *	↑56 SOD, ↑15 CAT, ↑81 POD, 0 PAL, ↑54 PPO
Eriophyidae	Colomerus vitis	Vitis vinifera	White Thompson (Re)	7 *	↑27 SOD, ↑9 CAT, ↑37 POD, ↑3 PAL, ↑24 PPO	[32]
				14 *	↑152 SOD, ↑17 CAT, ↑74 POD, ↑3 PAL, ↑58 PPO
				28 *	↑61 SOD, ↑23 CAT, ↑71 POD, ↑13 PAL, ↑80 PPO
			Sahebi (Re)	7 *	↑46 SOD, ↑68 CAT, ↑33 POD, ↑12 PAL, ↑43 PPO
				14 *	↑20 SOD, ↑80 CAT, ↑1 POD, ↑4 PAL, ↑167 PPO
				28 *	↑53 SOD, ↑75 CAT, ↑19 POD, ↑25 PAL, ↑178 PPO
			Koladari (Re)	7 *	↑69 SOD, ↑13 CAT, ↑63 POD, ↑14 PAL, ↑31 PPO
				14 *	↑61 SOD, ↑19 CAT, ↑73 POD, ↑12 PAL, ↑42 PPO
				28 *	↑126 SOD, ↑14 CAT, ↑101 POD, ↑18 PAL, ↑78 PPO
			Atabaki (Re)	7 *	↑84 SOD, ↑8 CAT, ↑41 POD, ↑12 PAL, ↑32 PPO
				14 *	↑162 SOD, ↑14 CAT, ↑66 POD, ↑7 PAL, ↑49 PPO
				28 *	↑131 SOD, ↑21 CAT, ↑81 POD, ↑10 PAL, ↑74 PPO
			Cabernet Sauvignon	15 *	↑168 SOD, ↑2167 CAT, ↓27 POD, ↑82 PPO	[56]
	Aceria tristriata	Juglans regia	Chandler	15 *	↑113 POD, ↑66 PPO	[68]
			Hartly	15 *	↑4 POD, ↑32 PPO
			Pedro	15 *	↑81 POD, ↑57 PPO
			Jamal	15 *	↑38 POD, ↑76 PPO
			Franquette	15 *	↑33 POD, ↑24 PPO
			Lara	15 *	↑8 POD, ↑15 PPO
			genotypes +	15 *	↑45 POD, ↑53 PPO
Eriophyidae	Aceria tosichella	Hordeum vulgare	Airway	18*	↓30 SOD, ↓39 CAT, ↓21 POD, ↓36 APX, ↓22 DHAR, ↓29 GR, ↑27 GSNOR, ↑20 ARG	[34]
Tetranychidae	Schizotetranychus oryzae	Oryza sativa	IRGA 424	60*	↑57 POD, ↑18 GST	[21]
	Schizotetranychus oryzae	Oryza sativa	IRGA 424	−	↑100 GST	[69]
	Tetranychus macfarlanei	Plumbago zeylanica	−	0 *	0 SOD, ↑5 CAT	[39]
				15 *	↓11 SOD, ↓17 CAT
				30 *	↓38 SOD, ↓32 CAT
				60 *	↓47 SOD, ↓42 CAT
				90 *	↓54 SOD, ↓46 CAT
				120 *	↓64 SOD, ↓53 CAT
	Tetranychus evansi	Solanum lycopersicum	Moneymaker	4 *	↑152 POD, ↑127 PPO	[70]
	Tetranychus evansi	Solanum lycopersicum	Moneymaker	10 *	↑88 POD, ↑58 PPO	[70]
	Tetranychus urticae	Phaseolus vulgaris	Bronco	55 *	↓37 CAT, ↑43 POD	[31]
		Cucumis melo	genotypes +	2 *	↑50 POD, 0 PPO	[71]
				4 *	↑50 POD, 0 PPO
				6 *	0 POD, ↑33 PPO
				8 *	0 POD, ↑33 PPO
		Arabidopsis thaliana	genotypes +	24 **	↓5 CAT, ↑24 APX, ↑14 DHAR, ↓17 GR	[40]
		Ocimum basilicum	−	1 *	↓40 CAT, ↑131 GPOX	[42]
				7 *	↓20 CAT, ↑275 GPOX
				14 *	↓60 CAT, ↑525 GPOX
		Melissa officinalis	−	1 *	↑8 CAT, ↑1900 GPOX
				7 *	↑8 CAT, ↑3400 GPOX
				14 *	↑31 CAT, ↑1400 GPOX
Tetranychidae	Tetranychus urticae	Salvia officinalis	−	1 *	↑6 CAT, ↑1346 GPOX	[42]
				7 *	↓67 CAT, ↑1247 GPOX
				14 *	↓72 CAT, ↑573 GPOX
		Humulus lupulus	Hallertauer Mittelfruh	10*	↑100 POD	[72]
		Glycine max	Williams (Re)	20 *	↑96 SOD, ↓25 CAT, ↑13 POD, ↑920 LOX	[73]
			Williams (Re)	34 *	↑17 SOD, ↑14 CAT, ↑31 POD, ↑270 LOX
			Bonus (Su)	20 *	↓30 SOD, ↑17 CAT, ↑36 POD, ↑73 LOX
			Bonus (Su)	34 *	↓44 SOD, ↑107 CAT, ↑72 POD
		Ocimum basilicum	Sweet basil (Su)	1 *	↓67 CAT, ↑250 GPOX	[33]
				7 *	↓17 CAT, ↑120 GPOX
				14 *	↓67 CAT, ↑900 GPOX
			Purpurascens (Su)	1 *	↑76 CAT, ↑100 GPOX
				7 *	↓60 CAT, ↑120 GPOX
				14 *	↓16 CAT, ↑380 GPOX
			Fino Verde (Su)	1 *	↓50 CAT, ↑1081 GPOX
				7 *	↓100 CAT, ↑1869 GPOX
				14 *	0 CAT, ↑1869 GPOX
		Zea mays	Bosman	6 *	↑4 SOD, ↓67 CAT, ↓6 APX, ↑67 GR, ↑7 POD, ↓8 PPO	[74]

* days; ** hours; − no information. Su: susceptible; Re: resistant. + For work carried out with different genotypes or ecotypes, the average of the values was calculated. Dehydroascorbate reductase (DHAR); catalase (CAT); phenylalanine ammonia-lyase (PAL); peroxidase (POD); guaiacol peroxidase (GPOX); glutathione S-transferase (GST); ascorbate peroxidase (APX); glutathione reductase (GR); superoxide dismutase (SOD); nitrosoglutathione reductase (GSNOR); arginase (ARG); lipoxygenase (LOX). % Levels of increase (↑) and decrease (↓) of treatment in relation to the control.

It has been proposed that APX acts in the fine regulation of low H₂O₂ levels involved in retrograde signaling due to the very low K_m of this enzyme for H₂O₂ [75]. Some authors have considered the role of APX activity to be essential to eliminating ROS and protecting plant cells [65], but few studies have evaluated its activity in plants under mite infestation. In a study with Eriophid, APX had its activity reduced after infestation, and in another study with Tetranychid, its activity was increased (Table 2). Eriophyid mites cause mild mechanical damage with still-unknown mechanisms, while Tetranychid mites cause complex and well-known mechanical damage. Thus, it is very possible that there is a relationship between the redox metabolism state of the host plant (especially the relationship of APX with H₂O₂) and the intensity of stress caused by different groups of mites.

Glutathione reductases are another important family of peroxidases involved in oxidative protection. These enzymes play an important role in the functioning of the ascorbate–glutathione cycle, a defense mechanism against oxidative stress, and in maintaining suitable glutathione levels in cells [65,76]. These enzymes had their activity reduced in infested plants in some of the studies reported in Table 2. In turn, type III peroxidases, or guaiacol peroxidases (GPOX), represent an immense family of peroxidases localized especially in the cell wall, apoplast, and vacuoles of plants.

Guaiacol peroxidases are considered key antioxidant enzymes, playing a crucial role in H₂O₂ detoxification and the redox regulation of plant growth [77]. This class of enzymes is multifunctional, capable of decomposing indoleacetic acid, and plays a role in the defense against biotic stresses [65,76]. These functions include the biosynthesis of lignin and ET, cell wall expansion, and oxidative defense against H₂O₂, especially after pathogen attack, herbivory, and oxidative burst [60,72,76,78,79]. GPOX is one of the peroxidases that has been frequently studied, is strongly related to plant resistance to pathogens and parasites [67], and displays an immediate reaction against insect damage [80,81]. It acts by catalyzing the reduction in H₂O₂ by removing electrons from donors (phenolic compounds, secondary metabolites) [68] or by oxidizing phenols, thus producing phenolics, tissue lignification, and hypersensitivity reactions [82]. This thickens the wall and leaves the structure stronger [83], making it more difficult for mites to infest [56], as demonstrated in studies with medicinal plants infested with T. urticae [33,42]. These studies revealed a considerable increase in GPOX enzyme activity in response to infestation.

Another important enzyme that is widely studied is polyphenol oxidase (PPO) (EC 1.10.3.1), which has a direct effect on the nutritional properties of plants and a toxic and anti-feeding effect on mites [68]. Polyphenol oxidase is involved in the induction of signaling pathways and the oxidation of polyphenols to quinones. The phenolic compounds themselves decrease the palatability of the plant tissues, preventing consumption by mites, and their oxidation into quinones decreases the nutritional properties, also interfering with the digestion of proteins by arthropods [68,79]. In a study that aimed to evaluate C. vitis infestation in grapevines, PPO activity increased shortly after infestation [56].

Phenylalanine ammonia-lyase (PAL) (EC 4.3.1.24) is an enzyme from a metabolic pathway named the phenylpropanoid pathway. This enzyme acts as a source of lignin, phytoalexins, and phenolic compounds. What is important in the context of our considerations is that PAL initiates phenylpropanoid metabolism, which then synthesizes anthocyanins. Products synthesized by PAL as phenolic compounds, more specifically flavonoids, may have antimicrobial and insect deterrent activity [84,85,86]. The PAL responses in plants infested by phytophagous mites are still unclear, although a study has carried out the evaluation of this enzyme in different cultivars of V. vinifera under the infestation of C. vitis (Table 2). Advanced studies using molecular tools need to be conducted to truly understand whether the defense effect against microorganisms and insects also influences phytophagous mites.

Lipoxygenases (LOX) (EC 1.13.11.12) are another important isoenzyme that produces hydroperoxides by catalyzing the oxidation of fatty acids [73,87]. Substances such as JA and aldehydes can be formed through hydroperoxides [88,89,90], and these are involved in the plant’s response to pests and injuries, including signaling and induction of gene expression. Different genes can be expressed in response to different stresses [91], such as induction of the expression of defense genes, and two lipoxygenase isoenzymes (LOX1 and LOX2) were identified in cucumber plants infested with Polyphagotarsonemus latus Banks (Tarsonemidae) [92]. Mechanical damage to soybean leaves, on the other hand, induced the expression of the LOX7 and LOX8 genes [93]. LOX activity also increased in soybean plants under other biotic stresses, such as caterpillar attacks [90]. In general, isoenzymes are encoded by different genes and are characterized by their similar catalytic functions [53].

Dehydroascorbate reductases (DHAR) (EC 1.8.5.1) are other enzymes important to the functioning of the ascorbate–glutathione cycle, playing a role in maintaining cellular redox balance via control of the redox state of ascorbate and glutathione [19]. These enzymes are strongly involved in tolerance to oxidative stress, mainly those generated by abiotic factors [65,76].

In addition to GSTs acting in redox metabolism, they are also known to have other important functions [94]. In plants, GSTs are also well known for catalyzing numerous reactions to remove xenobiotics (chemical substances foreign to the organism). It is worth highlighting that GSTs act together with reduced glutathione (GSH); that is, they “facilitate” the binding of GSH with xenobiotic compounds, forming a new compound that is less toxic than the original compound [94]. Two studies involving rice plants under S. oryzae infestation showed high levels of GST activity in the infested plants (Table 2). It is known that some mites, such as T. urticae, have genes related to the transport of xenobiotics [11]. The authors suggest the presence of xenobiotic compounds for S. oryzae as well [21,69]; however, there is no concrete evidence and more studies need to be carried out. Furthermore, it is well known that some species, such as Tetranychus evansi Baker et Pritchard (Tetranychidae) and Tetranychus ludeni Zacher (Tetranychidae), have the characteristic of suppressing the defenses of their host plants [16]. Therefore, studies involving these species and the GST response are encouraged, as nothing prohibits the suppression of this important enzyme from occurring.

The variability in antioxidant enzymatic activity is apparent across various studies, and the causes for this diversity are multifaceted (Table 2). Some enzymes exhibit a decrease in activity, while others may be favored, depending on the specific ROS (Table 1). Additionally, factors such as the plant’s developmental stage, whether the stress is isolated or combined with other stressors, whether it represents the initial stress event, the duration of the infestation, and the particular species of mite attacking all contribute to this variability.

4. Lipid Peroxidation and Physiological Responses

4.1. Infested Plants and Oxidative Stress

The occurrence of lipid peroxidation is known in three different phases [76,95,96,97,98]. In the first phase, OH^• or O₂^•− capture a hydrogen atom from the methylene group (polyunsaturated fatty acids—PUFAs), producing the lipid alkyl radical [76,96]. In the second phase, the alkyl lipid is established by a double bond rearrangement, forming the conjugated diene, which reacts with oxygen molecules. This results in the production of another radical, known as lipid peroxyl, which can propagate throughout the lipid chain, leading to the removal of hydrogen atoms from adjacent PUFA side chains. Finally, the third phase comprises the elimination of the radicals produced, with the subsequent generation of more stable molecules, such as malondialdehyde (MDA), resulting from the conversion of multiple side chains of fatty acids into lipid hydroperoxides due to the lipid peroxyl radical [95,96].

As seen above, Eriophyid and Tetranychid mites cause an increase in antioxidant enzymes, which do not always support fine-tuning oxidation reduction due to the exacerbated increase in ROS, resulting in oxidative stress (Table 1 and Table 2). Such stress results in lipid peroxidation in plant cells and an increase in MDA levels, mainly due to an increase in OH^• or O₂^•− levels (Figure 1A–C) (Table 3) [76,96].

In general, the average results from the compilation of studies we collected show that plants infested with Tetranychid mites showed about 150% enhanced lipid peroxidation compared to plants infested with Eriophyids. This fact may be associated with the different strategies that species belonging to Tetranychidae use to delay the host plant’s defense response and cause serious infestations. Indeed, T. urticae is associated with more than 1000 species of plants and is also well known in its genome for the genes of the families cytochrome P450, carboxyl/cholinesterases (CCEs), GSTs, and ATP-binding cassette transporters (ABC) with detoxification functions, thus revealing the ability of this species to adapt easily to different plant species [11]. Contrary to this, Eriophyid species are strictly specialists on their host plants, and many of the metabolic processes involved during their phytophagy are unclear [23].

In barley plants infested by A. tosichella, in addition to low SOD and O₂^•− concentrations (Table 1 and Table 2), the photosynthetic apparatus in general did not show high changes [34]. It can be suggested that barley plants may have become acclimated to such an infestation, where redox homeostasis may have acted successfully on signaling and the cellular defense mechanism without causing severe damage. Contrary to this, for vines infested by C. vitis, high levels of lipid peroxidation were observed. The radicals OH^• and O₂^•− (ROS not quantified) may have been the inducers of this process. Furthermore, this species, in addition to its damage, presents the formation of erinea, which may have contributed to the high rates of MDA.

In addition to Eriophyidae, it was also observed that T. urticae induced lipid peroxidation in grapevine plants, with different intensities varying according to the characteristics of each cultivar. In addition to the high diversity of host plants that this mite feeds on, another hypothesis that may be involved is related to the ability of T. urticae to feed on the contents of the mesophyll, causing the death of each cell [99], contributing in a certain way to the increase in peroxidation lipid and, consequently, the effect on the photosynthetic apparatus of those plants that they infest.

In addition to the increase in MDA levels, protein carbonylation, oxidative stress, damage, and membrane instability caused by lipid peroxidation, other physiological and consequently morphological changes are observed in plants infested by phytophagous mites [21,34]. It is possible to find changes in stomatal conductance indices, chlorophyll content, CO₂ assimilation, induction of chemical alleles, and changes in agronomic indices such as fruit size, leaf area, and root area [39,73,100,101,102,103].

Tetranychus macfarlanei, when infesting P. zeylanica, in addition to inducing peroxidation levels in plants, varying according to the time of infestation, also drastically reduced the levels of chlorophyll a and b [103]. Tetranychus urticae influenced membrane integrity, relative chlorophyll content, and photosynthetic activity in grapevine plants. The reduction in photosynthetic efficiency demonstrated in these studies is possibly related to lipid peroxidation in the thylakoid membranes present in the chloroplasts of these plants.

To verify these reports, we suggest the following methodologies: In addition to measuring MDA indices, the integrity of the membrane affected by lipid peroxidation can also be assessed by the increase in conductivity induced by ions in cellular extravasation in aqueous media (a simple and quick method) [39,60]. Furthermore, cell death or loss of membrane stability can be identified from histochemical analysis of the Evans Blue reaction [104]. These methods are capable of reporting the damage caused to plants by various stressful factors, including infestation by phytophagous mites (Figure 1C) [21,31,34].

4.2. Mites: Dangerous or Promising?

The leaf photosystem can be considered the vital metabolism of plants because it plays a role in the synthesis of photoassimilates, which are transported via transporter (apoplastic) or plasmodesmata (symplastic), suppressing the demand for sinks such as roots, fruits, and even young leaves [105,106,107]. Based on these concepts, T. macfarlanei was able to progressively reduce the stomatal conductance indexes, CO₂ assimilation, and consequently, the height, stem diameter, number of leaves, and fresh biomass of the area and root of P. zeylanica during 30 to 120 days of infestation [39]. Likewise, T. urticae, in addition to causing apparent damage, also induced dwarfism in cucumber plants (Cucumis sativus) grown in a protected environment and reduced the fruit yield per plant, i.e., it is clear that at the initial stage of the culture, during 10 weeks of infestation, each T. urticae specimen was reduced by 0.112 g of fruit yield per plant [103]. In short, the reduction in cucumber fruit yield (sink) as well as the morphophysiological impacts (sink) found in P. zeylanica may have been a form of response to the damage caused to the photosynthetic apparatus (source), both by the process of phytophagy of mites and the oxidative stress caused by them.

In the same context, when plants are attacked by certain species of phytophagous mites, their fruits are also susceptible to changes in the levels of their biochemical components, such as sugars, ascorbic acid, and flavonoids such as phenolic and non-flavonoid compounds such as resveratrol [101,108,109,110].

Panonychus ulmi (Koch), considered a pest in grapevine cultivation, causes significant damage to the leaves of the plants it infests [111,112]. However, biological control with the release of predatory mites of the species Neoseiulus californicus McGregor (Phytoseiidae) reduces infestations [113], and higher levels of sugar, phenolic compounds, and resveratrol in berries are accumulated [109]. In strawberry cultivation (Fragaria × ananassa), T. urticae also infests the plant leaves and is considered one of the main pests [114]. Biological control is carried out with the release of predatory mites of the species Phytoseiulus macropilis Banks (Phytoseiidae), which are effective [115] and increase the concentration of phenolic compounds and ascorbic acid in fruits, a fact not observed in plant fruits where acaricides were applied to plants without infestation [101]. In the case of these findings, the infestations may have induced the production of ROS in the plants, and the concentrations of non-enzymatic antioxidants may have occurred beyond the leaves, concentrating in the fruits. Furthermore, the xenobiotic effect can be suggested for the non-occurrence of an increase in these elements in plants with the application of acaricides.

In general, in plants, sugars are able to eliminate OH^• during the Fenton reaction, acting mainly on chloroplasts and vacuoles [19,116,117,118]. Therefore, ascorbic acid, in addition to eliminating OH^•, also neutralizes O₂^•− and ¹O₂, and has activity in several compartments, such as the apoplast, cytoplasm, chloroplast, mitochondria, peroxisome, and vacuole [37]. Meanwhile, flavonoids are located in the vacuole, chloroplasts, nucleus, endoplasmic reticulum, and cell wall, acting to eliminate OH^•, ¹O₂, and H₂O₂ [37,65,119]. In addition to the vine, as already mentioned, resveratrol is a phytoalexin already identified in more than 60 plant species [120], among which are the peanut (Arachis hypogaea), the blackberry (Morus rubra), and others [110]. In in vitro evaluations, the antioxidant was able to present reducing power in H₂O₂ and O₂^•− [121]. Based on these findings, it is possible to suggest that biological control, in addition to maintaining phytophagous mite populations at low levels, also provides an increase in the concentrations of enzymatic and non-enzymatic antioxidant compounds. However, to date, few studies have evaluated these conditions.

5. Molecular Responses Produced by Oxidative Stress: Transcriptomic Responses and Transcription Factors Engaged in Redox State Regulation in Mite-Infested Plants

Plants are equipped with an innate immune system capable of identifying evolutionarily preserved herbivore-associated molecular patterns [122]. The presence of intracellular proteins of the nucleotide-binding domain, leucine-rich repeat superfamily, and transmembrane pattern recognition receptors facilitates the reconnaissance of herbivores by plants, which results in the activation of a defense headed by signaling molecules such as salicylic acid (SA), abscisic acid (ABA), JA, ET, ROS, and nitric oxide (NO) [123,124,125]. When it comes to redox homeostasis, it is well known that the infestation by herbivores alters ROS and NO that can be recognized directly by redox-sensitive transcription factors and receptors or integrated into SA, ABA, JA, and ET signaling pathways to control gene expression, protein biosynthesis, and metabolism [126,127,128,129,130].

Pingault et al. [131] investigated T. aestivum transcriptomic responses against A. tosichella infestation. It was revealed that genes from pathways related to the redox state were affected (especially peroxidases and GST) as a result of the A. tosichella infestation. The same pathosystem has been exploited by Kiani et al. [132], and they provided important details to better understand redox regulation at the transcriptional level in A. tosichella-infested wheat. The expression of thirteen genes from the phenylpropanoid pathway was induced in response to A. tosichella in resistant and susceptible wheat varieties. What is important is that significantly more expressed genes involved in this pathway were detected in the resistant wheat plants. Transcripts for PAL, peroxidases, shikimate O-hydroxycinnamoyl transferases, and cinnamoyl-CoA reductase were identified. More precisely, eight PAL transcripts revealed more than a 2-fold enhancement in response to A. tosichella infestation in the resistant wheat varieties. These authors concluded that the induction of expression of the above-mentioned genes indicates that resistant wheat plants can elicit antioxidant responses, which are missing in the A. tosichella-susceptible T. aestivum variety [132].

Significant insight into the involvement of TFs in the plant response to mites was provided by [133]. TFs reported in this research are commonly indicated to be committed in host plant defense, namely, myeloblastosis (MYB)-related TFs, WRKY (pronounced ‘worky’), ethylene responsive factors (ERFs), which are TFs from the APETALA2/ERF family, zinc finger domain proteins, and basic helix-loop-helix (bHLH). It was found that MYB113 had significantly increased gene expression in resistant common bean cultivars infested with T. urticae. TRANSPARENT TESTA4 (TT4) encodes chalcone synthase (CHS), an enzyme from the biosynthesis of flavonoids (non-enzymatic antioxidants) [134]. Interestingly, TT4 together with TRANSPARENT TESTA8 (TT8) (a bHLH DNA-binding superfamily protein) is necessary for the regulation of the expression of dihydroflavonol 4-reductase (DFR), and a putative leucoanthocyanidin reductase (idiosyncratically involved in proanthocyanidin biosynthesis) encoded by the banylus gene [135] was identified to be in the interaction network with MYB113 [133].

To distinguish TFs involved in the response by cucumber plants against T. urticae, Bouwmeester et al. [126] performed transcriptional analysis of the infested plants. These authors identified the 1212 genes with a putative TF function. The level of 119 TF transcripts was differentially altered by the T. urticae attack, of which 60 were enhanced and 59 were decreased. Among them, 119 TF transcripts, the WRKY TFs, constituted 21%, followed by APETALA2/ERF (16%), bHLH (14%), and MYB (10%). The authors concluded that ERFs were upregulated and WRKYs were downregulated in T. urticae-infested C. sativus plants.

Phytohormones play a key role in shaping and managing redox transcriptome defense responses to herbivore feeding. Direct experimental evidence for this can be found in the literature. The cross-talk between JA and anthocyanin production is regulated by MYC2 (MYC proto-oncogene, bHLH transcription factor), and as a result, the activation of a specific WD-repeat/bHLH/MYB complex occurs [136]. The gene expression of TFs like PAP1 (MYB75), bHLH TT8, and GL3 was enhanced upon herbivore infestation. These TF components can induce the expression of enzymes necessary for the synthesis of anthocyanins, such as DFR, the leucoanthocyanidin dioxygenases/anthocyanidin synthases, or the anthocyanin glucosyltransferases [137]. In this context, [138] presented a defense response mediated by JA in A. thaliana infested with T. urticae. This study indicated at the transcriptomic level the participation of flavonols and anthocyanins in the defense of the T. urticae-infested A. thaliana plants, the co-occurrence of a changed metabolism of aromatic amino acids, and the biosynthesis of tocopherols.

Innovative results were provided by Ojeda-Martinez et al. [139] regarding the fact that treatment with T. urticae egg extract can change the A. thaliana defense response to future colonization. From this article, we can learn about some aspects of redox regulation and connections in the transcriptomic response, including TFs depending on phytohormones. These discoveries showed that the earliest plant responses included metabolic processes connected with ROS. Therefore, it is not surprising that among the induced genes were respiratory burst oxidase homolog protein C and respiratory burst oxidase homolog protein D, encoding the plasma membrane nicotinamide adenine dinucleotide phosphate oxidases. These oxidoreductases produce superoxide free radicals, which can affect redox balance and lead to oxidative stress if antioxidative mechanisms are not sufficiently efficient. This study also indicates JA as the central phytohormonal hub of plant defense responses against mites. For example, the induction of MYC2 and its subordinate gene, vegetative storage protein 2 (VSP2), which acts as a marker of herbivore infestation, was noted. In addition, the alteration in expression level of the jasmonate ZIM-domain (JAZ) genes JAZ2, JAZ6, and three transcripts of JAZ9 also indicated the importance of the JA-dependent signaling pathway in these discussed experiments. It should be emphasized here that JAZ genes are negative regulatory elements of JA signaling, being inhibited at the initiation signaling stage and then induced as a negative regulator when the amount of JA is significantly enhanced [139]. They also produce evidence showing that ET signaling (next to the one dependent on JA) is important in T. urticae-infested A. thaliana plants. The activation of the ERFs, ERF056, ERF4, and ERF1A, indicated an involvement of ET signaling. The reliable markers of ET signaling were the induction of expression of plant defensin 1.2 (PDF1.2) and pathogenesis-related 4 (PR4) genes. It is known that PDF1.2 and PR4 are regulated by ERFs, and this is a typical molecular badge of the merging of the JA and ET signaling pathways during biotic stress. JA signaling interfaces with ET signaling using two branches. The first one, which restricts the expression of JAZ genes (keeping the restriction of ET signaling), elicits a defense response by MYC2 and VSP2. The second one, which engages JAZ, can activate ERFs and, in turn, PDF1.2 expression. Data by Ojeda-Martinez et al. [139] showed that, at an earlier response stage, A. thaliana had an increased level of the MYC2 and VSP2 branches and next induced the second branch, namely PDF1.2 and PR4-dependent defense. Moreover, there were noticeable redox alterations in the plants. For instance, the expression of the catalase gene CAT3 was enhanced.

Studies at the transcriptomic level of another pathosystem (A. thaliana-Brevipalpus yothersi) provide us with further insight into the issue of TFs and phytohormones (JA and SA) cross-talk [140]. These authors showed that in the group of upregulated differentially expressed genes (DEGs), 254 (9.2%) TFs from 30 various families were described, and 16 families were overrepresented. The largest and most prominent of these were WRKY (33 genes) and AP2/ERF (40 genes), which are known to act as mediators of SA signaling and the ERF branch of the JA-dependent signal cascade, respectively. From the analysis using the group of downregulated DEGs, 141 (6.3%) TFs from 30 families were noted. A total of 23 of these families were also detected in the group of upregulated DEGs. The TFs were from 18 overrepresented families. The largest and most importantly overrepresented families were the bHLH (22 genes), which include regulators of the MYC-branch of JA signaling, and the Cysteine3Histidine zinc finger gene family (17 genes).

A substantial TF for T. urticae resistance turned out to be the WD-repeat (WD40), whose gene expression was visible only in the resistant common bean cultivar during T. urticae infestation. Many investigations have revealed that a conserved MYB-bHLH-WD40 (MBW) complex is linked with anthocyanin synthesis, which once again indicates the involvement of redox regulation in mite-infested plants through flavonoids and specific TFs [133,141]. Additionally, TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) can be a TF participating in mite resistance, as the gene expression of TCP was enhanced in the resistant P. vulgaris cultivar upon spider mite attack [133]. TCPs are also involved in plant responses to biotic stresses other than mite infection; as it has been observed, these TFs participate in systemic acquired resistance induced by pathogens [142].

In addition, Hoseinzadeh et al. [133] also showed that the gene expression of WRKY50 was significantly stimulated in the resistant P. vulgaris cultivar upon T. urticae infestation. The same authors presented that the gene expression of Cys2/His2 and C2H2-zinc finger proteins was enhanced in resistant and susceptible cultivars, respectively. The involvement of ERFs, which also regulate the biosynthesis of flavonoids, was also demonstrated in the defense response of the resistant P. vulgaris cultivar during spider mite feeding. This is an interesting discovery because it once again demonstrates the contribution of flavonoids in the response to mites, and more generally, this group of TFs is responsible for the integration of ET and JA-dependent signaling. In more detail, it was observed to enhance the expression of ERF1 and ERF9 [133], which are known to mediate responses to environmental stress conditions, including pathogens [143,144].

6. Conclusions and Perspectives

This compilation of results illustrates the oxidation-reduction imbalance caused by phytophagous mites in various plant species (Figure 1A–C). Plant responses are involved in the complex signaling, defense, and suppression mechanisms activated in the arms race between plants and herbivores [17]. In these signal cascades, most of the findings present in this study show an increase in ROS such as O₂^•− and H₂O₂, with variations depending on the species of host plant, cultivar, species of infesting phytophagous mite, injected toxins, and time of infestation. Furthermore, it is possible to observe oxidative stress caused by the imbalance of oxidation-reduction between ROS and antioxidant components, as indicated in those studies with high levels of lipid peroxidation. In the few studies found, there is also evidence of the negative impact on the source and sink relationship of plants due to infestations.

It is worth noting that even with these reports on plants under infestation by phytophagous mites, there is still a significant lack of information. In other words, details about the oxidative response, ROS, antioxidant enzymes, and signaling in various contexts deserve attention. To date, the literature presents scarce and fragmented information, making it difficult to reach other concise and precise conclusions. Given this scenario, the following questions are proposed: To what level are ROS beneficial, acting in signaling? When exactly do they turn into toxic threats to plant cells? How does the transgenerational effect of the memory of previously infested plants occur, based on signals (ROS) and antioxidant compounds (enzymes)? How does the redox metabolism response occur, considering the plant as a systemic/modular organism, when faced with the within-plant distribution of mites [61] of phytophagous mites from older to mature leaves? Studies related to the time course (in short periods) of ROS in infested plants need to be strongly considered, as most of the findings in this study present data resulting from a long period of infestation. Furthermore, for greater detail, techniques such as scanning electron microscopy, transmission electron microscopy, and the combination of omics, quantitative, and qualitative techniques, in addition to molecular markers, are essential. We strongly suggest that a better understanding of these techniques may result in important tools for the rapid and accurate diagnosis of genotypes with enhanced or decreased tolerance to phytophagous mites.

Author Contributions

W.B.W. and J.R.S. conceptualized the study. W.B.W., J.R.S., J.A.G.S., M.L., R.D.M. and N.J.F. structured the study. W.B.W. created the figures and tables. W.B.W., J.R.S., M.L. and N.J.F. wrote and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors are grateful to the Brazilian National Council for Scientific and Technological Development (CNPq) for their financial support and research fellowships (CNPq No. 310146/2023-2); to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES); to the University of Taquari Valley—UNIVATES for research support; and to Luana Fabrina Rodighero for reviewing the English of the manuscript and Anderson de Azevedo Meira for the photo of the mite.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 3. Levels of lipid peroxidation in plants under infestation with different species of phytophagous mites, times of infestation, and cultivars.

Mite Family	Species	Plant	Cultivar	Time of Infestation	MDA (%)	References
Eriophyidae	Aceria tosichella	Hordeum vulgare	Airway	18 *	↑27	[34]
	Colomerus vitis	Vitis vinifera	Ghalati (Su)	7 *	↑1	[32]
				14 *	↑83
				28 *	↑94
			Rishbaba (Su)	7 *	↓2
				14 *	↑119
				28 *	↑191
			Neyshaboori (Su)	7 *	↑19
				14 *	↑130
				28 *	↑191
			Muscat (Su)	7 *	↑17
				14 *	↑203
				28*	↑361
			White Thompson (Re)	7 *	↑24
				14 *	↑135
				28 *	↑360
			Sahebi (Re)	7 *	↑23
				14 *	↑172
				28 *	↑202
			Koladari (Re)	7 *	↑19
				14 *	↑145
				28 *	↑294
			Atabaki (Re)	7 *	↑28
				14 *	↑159
				28 *	↑397
Tetranychidae	Tetranychus macfarlanei	Plumbago zeylanica	−	0 *	↑2	[39]
				15 *	↑83
				30 *	↑100
				60 *	↑190
				90 *	↑225
				120 *	↑109
	Tetranychus urticae	Phaseolus vulgaris	Bronco	55 *	↑75	[31]
		Medicago truncatula	Ecotype +	1 *	↑33	[41]
		Ocimum basilicum	−	1 *	↑267	[42]
				7 *	↑292
				14 *	↑339
		Melissa officinalis	−	1 *	↑16
				7 *	↑23
				14 *	↑78
Tetranychidae	Tetranychus urticae	Salvia officinalis	−	1 *	↑42	[42]
				7 *	↑55
				14 *	↑71
		Glycine max	Williams (Re)	30 *	↑14	[73]
				33 *	↑24
				37 *	↑51
				40 *	↑83
				44 *	↑46
				47 *	↑59
			Bonus (Su)	30 *	↑28
				33 *	↑16
				37 *	↑71
				40 *	↑58
				44 *	↑40
				47 *	↑35
		Ocimum basilicum	Sweet basil (Su)	1 *	↑263	[33]
				7 *	↑300
				14 *	↑250
			Purpurascens (Su)	1 *	↑1400
				7 *	↑2720
				14 *	↑2460
			Fino Verde (Su)	1 *	↑663
				7 *	↑1175
				14 *	↑2000

* days; ** hours; − no information. Su: susceptible; Re: resistant. + For work carried out with different genotypes or ecotypes, the values were averaged. Lipid peroxidation by malondialdehyde (MDA). % Levels of increase (↑) and decrease (↓) of treatment in relation to the control.

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Wurlitzer, W.B.; Labudda, M.; Silveira, J.A.G.; Matthes, R.D.; Schneider, J.R.; Ferla, N.J. From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation? Int. J. Plant Biol. 2024, 15, 561-585. https://doi.org/10.3390/ijpb15030043

AMA Style

Wurlitzer WB, Labudda M, Silveira JAG, Matthes RD, Schneider JR, Ferla NJ. From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation? International Journal of Plant Biology. 2024; 15(3):561-585. https://doi.org/10.3390/ijpb15030043

Chicago/Turabian Style

Wurlitzer, Wesley Borges, Mateusz Labudda, Joaquim Albenisio G. Silveira, Ronice Drebel Matthes, Julia Renata Schneider, and Noeli Juarez Ferla. 2024. "From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation?" International Journal of Plant Biology 15, no. 3: 561-585. https://doi.org/10.3390/ijpb15030043

APA Style

Wurlitzer, W. B., Labudda, M., Silveira, J. A. G., Matthes, R. D., Schneider, J. R., & Ferla, N. J. (2024). From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation? International Journal of Plant Biology, 15(3), 561-585. https://doi.org/10.3390/ijpb15030043

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From Signaling to Stress: How Does Plant Redox Homeostasis Behave under Phytophagous Mite Infestation?

Abstract

1. Introduction

2. Mite–Plant Relationship: General Aspects

3. Phytophagous Mite Infestation Alters Plant Redox Homeostasis

3.1. Production of Reactive Oxygen Species in Infested Plants

3.2. Action of Antioxidant Enzymes as a Defense Mechanism on Infested Plants

4. Lipid Peroxidation and Physiological Responses

4.1. Infested Plants and Oxidative Stress

4.2. Mites: Dangerous or Promising?

5. Molecular Responses Produced by Oxidative Stress: Transcriptomic Responses and Transcription Factors Engaged in Redox State Regulation in Mite-Infested Plants

6. Conclusions and Perspectives

Author Contributions

Funding

Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement

Acknowledgments

Conflicts of Interest

References

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