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Review

Hydrogen Peroxide Signaling in the Maintenance of Plant Root Apical Meristem Activity

by
Hui Liu
,
Yangwei Mu
,
Yuxin Xuan
,
Xiaolin Wu
,
Wei Wang
* and
Hui Zhang
*
National Key Laboratory of Wheat and Maize Crop Science, College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China
*
Authors to whom correspondence should be addressed.
Antioxidants 2024, 13(5), 554; https://doi.org/10.3390/antiox13050554
Submission received: 28 March 2024 / Revised: 23 April 2024 / Accepted: 29 April 2024 / Published: 30 April 2024
(This article belongs to the Special Issue Reactive Oxygen and Nitrogen Species in Plants―2nd Edition)
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Abstract

:
Hydrogen peroxide (H2O2) is a prevalent reactive oxygen species (ROS) found in cells and takes a central role in plant development and stress adaptation. The root apical meristem (RAM) has evolved strong plasticity to adapt to complex and changing environmental conditions. Recent advances have made great progress in explaining the mechanism of key factors, such as auxin, WUSCHEL-RELATED HOMEOBOX 5 (WOX5), PLETHORA (PLT), SHORTROOT (SHR), and SCARECROW (SCR), in the regulation of RAM activity maintenance. H2O2 functions as an emerging signaling molecule to control the quiescent center (QC) specification and stem cell niche (SCN) activity. Auxin is a key signal for the regulation of RAM maintenance, which largely depends on the formation of auxin regional gradients. H2O2 regulates the auxin gradients by the modulation of intercellular transport. H2O2 also modulates the expression of WOX5, PLTs, SHR, and SCR to maintain RAM activity. The present review is dedicated to summarizing the key factors in the regulation of RAM activity and discussing the signaling transduction of H2O2 in the maintenance of RAM activity. H2O2 is a significant signal for plant development and environmental adaptation.

1. Introduction

Roots are important structures for plant growth, development, and environmental adaptation. It is well known that roots have many functions, such as the uptake and transport of water and nutrients, synthesis and secretion of compounds, storage of substances, and anchorage of the plant. These functions help plants to better adapt to the environment. The external morphology of the root tip of Arabidopsis reveals the presence of three distinct zones, namely the meristematic zone, elongation zone, and differentiation zone. There is a transition zone between the meristematic zone and the elongation zone, where cells leave the meristem and enter the elongation zone. The region where the cortical cells begin to expand is the transition zone. The transition zone is a key point in the study of cell division and cell differentiation [1]. In the differentiation zone, elongated cells differentiate to maturity.
The root apical meristem (RAM), situated within the meristematic zone, plays a crucial role in controlling root growth and development. The quiescent center (QC) and its surrounding stem cells together form a stem cell niche (SCN), providing continuous cell sources for root growth and development. Different stem cells (also called initials), including pericycle/vascular initials, cortex/endodermal initials, epidermis/lateral root cap initials, and columella initials (also called columella stem cells, or CSCs), produce a variety of cell types in roots (Figure 1A) [1]. These distinct stem cell populations are responsible for generating various cell types through processes of division and differentiation. Specifically, pericycle/vascular initials contribute to the formation of stele cells and pericycle cells, cortex/endodermal initials give rise to the endodermis and cortex, epidermis/lateral root cap initials are responsible for the development of the epidermis and lateral root cap, and columella initials contribute to the formation of columella cells.
The phytohormone auxin has been shown to be a central player in multiple biological processes, such as root development, embryo development, and leaf development [2,3,4,5]. During root development, auxin plays an essential role in controlling the organization and function of RAM [4,6]. WUSCHEL-RELATED HOMEOBOX 5 (WOX5) is a HOMEOBOX family gene that is specifically expressed in the QC and plays a crucial role in determining the fate of stem cells. It is generally believed that the establishment and maintenance of the SCN microenvironment are strictly controlled by two core transcription factor pathways: the longitudinal PLETHORA (PLT) pathway and the radial SHORTROOT (SHR)/SCARECROW (SCR) pathway [7].
Higher plants continuously adjust their developmental processes to adapt to complex and changing environmental conditions. The evolution of roots allows vascular plants to adapt to land environments, and some common molecular modules in RAM are employed during root origins in lycophytes and euphyllophytes [8]. Compared to animals, plant roots exhibit strong adaptation in the processes of growth and development, which mainly depend on the activity of SCN in the RAM. RAM organization has evolved to become highly plastic and dynamic in response to environmental triggers, such as water and nutrient availability [9,10]. Under stress conditions, the RAM is rapidly reorganized, and the root growth is enhanced, thus providing effective strategies to cope with the stresses [9,10,11]. This environment-responsive developmental plasticity is linked to reactive oxygen species (ROS) and nitric oxide (NO), which act as signals specifically to regulate RAM function, connecting with hormones [10,12,13]. ROS and NO are considered key players in RAM maintenance and environmental stress responses [14,15,16,17].
ROS, including hydrogen peroxide (H2O2), superoxide (O2•−), singlet oxygen (1O2), and hydroxyl radical (·OH), are considered to be toxic byproducts of metabolism that could harm cells [18]. A high level of ROS results in serious damage to cell structures and cell death. However, many studies have demonstrated that ROS play a significant role in various biological processes when at appropriate concentrations [19]. Among these ROS, H2O2 takes a central role in plant development and stress response [20]. H2O2 serves as a membrane-permeable and diffusible molecule that is less reactive and has a longer lifespan compared to the highly reactive ·OH. This characteristic makes H2O2 well-suited for functioning as a signaling molecule [20]. The production of H2O2 can occur through intracellular and extracellular pathways. Plant cells employ an antioxidant system to regulate H2O2 levels, thereby ensuring the maintenance of a suitable redox environment conducive to cellular growth [21].
ROS are key signals in the regulation of elongation and differentiation in plant roots. Studies on Arabidopsis have shown that O2•− is mainly distributed in the extracellular vesicles of the elongation zone, while H2O2 accumulates in the cell walls of differentiated tissues and root hairs. The decrease in O2•− concentration can reduce root elongation and root hair formation, but removing H2O2 can promote root elongation. The balance between O2•− and H2O2 regulates the transition of root systems between proliferation and differentiation [22]. Recent advances indicate that H2O2 functions as a signaling molecule to control RAM size and SCN maintenance by regulating the factors of auxin, PLTs, SCR, and SHR [11,23,24,25]. In this review, we focus on summarizing the key factors in the regulation of RAM activity and discuss the signaling transduction of H2O2 in the maintenance of RAM activity.

2. Key Factors in the Maintenance of RAM Activity

The homeodomain transcription factor gene WOX5 is specially expressed in the QC to control the CSC identity (Table 1). Loss of function of WOX5 causes differentiation in CSCs, while increased WOX5 expression inhibits the differentiation of CSCs and causes CSC over-proliferation [26]. WOX5 inhibits QC division by repressing the expression of the D-type cyclin genes CYCD3;3 and CYCD1;1. In particular, the WOX5 protein can directly interact with the promoter of CYCD3;3 [27]. It is necessary that WOX5 suppresses CSC differentiation and maintains CSC identity. Another study indicated that the WOX5 protein moves from the QC into CSCs, where it directly represses the transcription factor gene CYCLING DOF FACTOR 4 (CDF4). WOX5 recruits TPL/TPR co-repressors and the histone deacetylase HDA19 to the CDF4 gene promoter and regulates CDF4 expression. CDF4 antagonizes WOX5 activity and promotes columella cell differentiation. WOX5 functions as a mobile signal from the QC to the CSC to maintain CSC identity by the modulation of CDF4 (Figure 1B and Figure 2) [28]. Differentiated columella cells and CSCs provide the secretion peptide CLAVATA3/ESR-RELATED40 (CLE40) as a feedback signal to control WOX5 expression by the receptor kinases ARABIDOPSIS CRINKLY4 (ACR4) and CLAVATA1 (CLV1) [29,30]. CLV1 can sense the signal of CLE40 by forming dimers or tetramers with ACR4 and negatively regulate the expression of WOX5 to maintain the activity of CSCs (Figure 1B and Table 1) [30,31]. The PHD domain-containing protein REPRESSOR OF WUSCHEL1 (ROW1) directly represses WOX5 expression by histone modification [32]. These findings indicate that multiple players are involved in the regulation of the core factor WOX5 to maintain RAM activity (Figure 1B and Figure 2).
Auxin, along with many other hormones, is a key signal in the regulation of RAM activity [4]. The function of auxin depends on its biosynthesis, transport, and signaling transduction [33]. Auxin levels are critical for the maintenance of QC and SCN activities and RAM size. The auxin maximum is located in the SCN region, which is determined by the auxin-responsive reporters [34,35]. The formation of auxin regional gradients depends on the local biosynthesis at the root tips and intercellular transport [4,36,37]. The PIN proteins are responsible for the polar transport of auxin toward the SCN [4,38]. Auxin gradients play a central role in the regulation of SCN identity. WOX5 is repressed by auxin response factors ARF10 and ARF16 [39]. The QC-localized auxin maximum requires an auxin response repressor indole-3-acetic acid 17 (IAA17), which is responsible for restricting the expression of WOX5 to maintain root stem cell identity (Figure 1B) [40].
Table 1. Expression patterns of the genes involved in RAM maintenance.
Table 1. Expression patterns of the genes involved in RAM maintenance.
GeneExpression PatternsReferences
WOX5WOX5 is expressed in the quiescent center (QC). WOX5 protein can move into the columella stem cells to repress CDF4 expression.[28,39]
CDF4CDF4 is expressed in the upper differentiated columella cells and the columella stem cells.[28]
CLE40CLE40 is expressed in the stele and the differentiated columella cells.[30]
ACR4ACR4 is expressed mainly in the three cell layers (D1, D2, and D3) below the quiescent center, adjacent lateral root cap, and epidermis initial, but only occasionally and at a low level in the quiescent center.[30]
CLV1CLV1 is expressed in the two cell layers (D1 and D2) immediately distal to the QC, the epidermis/lateral root cap initials, and the lateral root cap.[31]
PLT1PLT1 is expressed in the QC, surrounding stem cells, and uppermost layer of differentiated columella cells.[41]
PLT2PLT2 displays the same expression pattern as PLT1.[41]
PLT3PLT3 is expressed in the QC and vascular initial cells.[42,43]
SCRSCR is primarily synthesized in the endodermis, QC, and cortex endodermal initials.[44]
SHRSHR is expressed in the stele cells internal to the endodermis and cortex. The SHR protein can move from the stele to a single layer of adjacent cells.[45]
CYCD3;3CYCD3;3 is expressed in the columella layers, the lateral root cap, the epidermal stem cells, and the stele.[27]
The AP2-domain transcription factors PLTs are key factors that control RAM maintenance. Four PLTs, namely, PLT1, PLT2, PLT3, and PLT4 (also known as BBM), are essential for QC specification and stem cell activity as the multiple plt mutants cannot form RAM [41,42,46]. High levels of PLT activity promote stem cell identity and maintenance, while low levels of PLT activity promote mitotic activity in stem cell daughters [42]. The PLT proteins form a graded distribution with a maximum near the root tip, which is critical for QC specification and SCN identity (Table 1) [46]. Many factors have been identified to control the expression of PLTs in the root meristem [47,48]. The transcriptional coactivator GRF-INTERACTING FACTOR1 (GIF1), also known as ANGUSTIFOLIA3 (AN3), negatively regulates the expression of PLT1 by directly binding to the promoter of PLT1 [48]. JANUS, interacting with PLT1, positively regulates PLT1 expression in the root meristem by recruiting RNA polymerase II (Pol II) on PLT1. JANUS-dependent recruitment of Pol II is inhibited through competitive binding of JANUS by GIF1. GIF1 and JANUS, the antagonistic regulators of PLT1, both depend on IMPORTIN β4 (IMB4) for their nuclear accumulation. The strong signals of GFP-GIF1 and JANUSg-GFP have been detected in the nuclei of wild type but not in the imb4-1 mutant. IMB4 directly interacts with GIF1 and regulates the nucleocytoplasmic transport of GIF1, possibly by an unknown protein modification [49]. IMB4 positively regulates the nuclear accumulation of JANUS by preventing 26S proteasome-mediated degradation (Figure 1B and Figure 2) [47]. The salt overly sensitive (SOS) pathway component SOS2 interacts and phosphorylates PLT1 and PLT2 through their conserved C-terminal motifs to stabilize PLT1 and PLT2 to regulate root apical meristem maintenance for adaptation to salt stress [50]. Pre-mRNA (messenger RNA) splicing participates in the regulation of RAM activity. RDM16 encodes Prp3, a component of U4/U6 snRNP involved in pre-mRNA splicing in Arabidopsis. The mutation of RDM16 results in the abnormal pre-mRNA splicing of PLT1 and PLT2, leading to the disordering of the root stem cell niche and a short-root phenotype [51]. WOX5 and PLT proteins overlap in the SCN, and PLT1, PLT2, PLT3, and PLT4 contain PrD domains. Using fluorescence lifetime imaging microscopy (FLIM), the researchers confirmed that WOX5 interacts with PLTs, including PLT1, PLT2, PLT3, and PLT4. Another study indicated that PrD domains of PLT3 are required for the interaction of WOX5 and are necessary for the maintenance of the SCN. WOX5 forms a complex with PLTs to control stem cell identity [52].
Precise control of cell division is essential for root development. The transcription factors SHR and SCR are required for the formative division in the RAM of Arabidopsis roots. Both SHR and SCR belong to the GRAS family of transcription factors. SHR is expressed in the stele, while SCR is primarily synthesized in the endodermis, QC, and cortex endodermal initials. The movement of the SHR protein to the single layer of adjacent cells regulates the specification of endodermal cell identity and enhances SCR expression [44,45,53]. SCR expression in QC is crucial for the maintenance of the root SCN. The SCR protein directly interacts with the SHR protein, confining SHR to the nucleus (Table 1) [44,53]. Recently, a cell-resolution map of the maize root was generated, revealing an alternative configuration of the tissue formative SHR adjacent to an expanded cortex. The maize SHR protein is hypermobile, moving at least eight cell layers into the cortex [54]. These findings suggest that the movement of SHR proteins exhibits diversity when performing functions. The SHR–SCR complex promotes the expression of WOX5, which plays a pivotal role in maintaining QC identity and preventing the differentiation of surrounding stem cells [26]. The levels of SHR and SCR early in the cell cycle determine the orientation of the division plane, resulting in either formative or proliferative cell division [55].
SEUSS (SEU) proteins, homologous to the animal LIM-domain binding (LDB) proteins, regulate WOX5 expression and QC specification. SEU binds to the WOX5 promoter depending on the transcription factor SCR, and then, SEU physically recruits the SET domain methyltransferase SDG4 to the WOX5 promoter, thus promoting WOX5 expression (Figure 1B and Figure 2) [56]. PLT and SCR genetically and physically interact with the plant-specific teosinte-branched cycloidea PCNA (TCP) transcription factors to specify the SCN identity by the modulation of WOX5 expression (Figure 1B and Figure 2) [43]. The transcription factor NAC1 has been identified as a critical regulator in the asymmetric cell division in root development. Loss of function of NAC1 results in increased periclinal cell division in the root endodermis. The cell cycle regulator CYCLIND6;1 (CYCD6;1) is a positive regulator in periclinal cell division. NAC1 directly represses the expression of CYCD6;1 by recruiting the corepressor TOPLESS (TPL) to maintain proper periclinal cell division. NAC1 physically interacts with SCR to restrict excessive periclinal cell divisions in the endodermis during root middle cortex formation. SHR is able to activate CYCD6;1 expression in the nac1 mutant. NAC1 and SHR antagonize each other to regulate the expression of CYCD6;1 [57].

3. H2O2 Homeostasis in RAM Activity Maintenance

The production of H2O2 depends on superoxide dismutases, plasma membrane NADPH oxidases, peroxisomal oxidases, and apoplastic oxidases, whereas the scavenging of H2O2 relies on catalase, peroxiredoxin, glutathione peroxidase-like enzymes, and ascorbate peroxidase [21]. Among the factors that regulate H2O2 homeostasis, NADPH oxidases, known as respiratory burst oxidase homologs (RBOHs), play a major role in H2O2 production in plants. RBOHs are enzymes located in the plasma membrane, utilizing electrons from cytosolic NADPH to reduce oxygen to O2•− in the apoplast. Subsequently, O2•− is either spontaneously or enzymatically converted into H2O2. In Arabidopsis, there are ten RBOHs, each contributing to a diverse array of physiological processes [58]. Increasing salicylic acid (SA) promotes H2O2 production by enhancing the transcript levels of RBOHD and RBOHF and affecting QC division in the RAM [24]. Another study also found that SA promotes H2O2 generation by repressing CAT2 and CAT3 expression [59]. Brassinosteroid (BR)-activated transcription factors BRASSINAZOLE RESISTANT1 (BZR1) elevates H2O2 levels by directly binding to the promoters of RBOHD and RBOHF [60]. Abscisic acid (ABA) promotes H2O2 production by the modulation of mitochondria [61,62]. Auxin can induce H2O2 generation to inhibit root growth and promote lateral root formation [63,64]. Glucose induces H2O2 accumulation to regulate RAM activity by the modulation of autophagy [65]. Some stresses, such as potassium deprivation and salt stress, can also cause H2O2 generation in roots [66,67,68]. H2O2 homeostasis in the RAM is affected by phytohormones and various environmental stresses.
The mutation of AtRBOHC, also known as root hair defective 2 (rhd2), results in lower levels of H2O2 in roots. The primary roots of the rhd2 mutants become shorter and thinner than those of the wild type [23]. Treatment with diphenylene iodonium (DPI), a specific inhibitor of NADPH oxidase that are used to repress H2O2 production, can also cause shorter roots [23]. The plastid-localized glutathione reductase2 (GR2) can catalyze the reduction of glutathione disulfide (GSSG) into reduced glutathione (GSH). Loss of function of GR2 disrupts the redox status of roots, resulting in the strong inhibition of root growth and severe defects in the RAM [69]. Treatment with the reductive reagent GSH or the oxidative reagent H2O2 has been shown to repress CSC differentiation, suggesting that both highly reductive and oxidative environments inhibit CSC identity [70]. The results suggest that the regulation of H2O2 homeostasis to maintain appropriate redox status in root tips is critical for RAM activity maintenance.
WOX5 is a key player in the determination of QC specification and CSC identity [26]. The receptor-like kinases ACR4/CLV1 negatively regulate CSC identity by repressing WOX5 expression [30,31]. The mutation of ACR4 increases the CSC layers, suggesting that ACR4 promotes CSC differentiation [70]. Altering the redox status of RAM using H2O2 or GSH causes CSC differentiation. The stability of ACR4 is regulated by endocytosis. The tumor necrosis factor receptor (TNFR) is the extracellular domain of ACR4, contributing to the maintenance of the stability of ACR4. ACR4 without the TNFR domain is directly localized to endosomes for degradation, implying that the TNFR domain represses the endocytosis of ACR4. The cysteine residues in the TNFR domain are major determinants of the endocytic degradation of ACR4. The redox status of cysteine in the TNFR domain affects the localization and function of ACR4. The cysteine residues in the TNFR domain play a positive role in ACR4 endocytosis. When treated with GSH or H2O2, ACR4 endocytosis is detected in the distal stem cell (DSC) of ProACR4:ACR4-GFP but not in those of ProACR4:ACR4 (harboring TNFR12C-A mutations, i.e., all 12 cysteine residues were mutated to Ala)-GFP. The multiple cysteine residue mutations in the TNFR of ACR4 block endocytosis. The findings indicate that the cysteine residues in the TNFR domain play a positive role in the redox-mediated internalization and turnover of membrane-localized ACR4. The redox status of the TNFR domain is critical for the localization and function of ACR4. GSH or H2O2 represses ACR4 function by affecting ACR4 endocytosis via the modulation of the redox status of cysteine in the TNFR domain [70]. CLE40 is the ligand of the ACR4–CLV1 complex and functions as a negative signal to regulate CSC differentiation [30,31]. Altering the redox status using H2O2 or GSH, the CSC cell layer does not change in the cle40 mutant. Moreover, the CSC cell layers in the cle40acr4 double mutant do not change in response to treatment with H2O2 or GSH, suggesting that both CLE40 and ACR4 participate in the redox regulation of CSC differentiation (Figure 3) [30].

4. H2O2 Signaling in Auxin-Mediated RAM Activity Maintenance

There is a close connection between H2O2 and auxin in the regulation of root development, including primary root growth, root hair growth, and lateral root formation [23,71,72]. During RAM development, auxin distribution is altered by H2O2 [23,72]. Auxin gradients in the RAM play a central role in determining QC specification and stem cell identity [37]. The auxin transporters, i.e., PINs contribute to the formation of auxin gradients and auxin maximum in the root tips [37,38]. In the root stele, the transporters, including PIN1, PIN3, PIN4, and PIN7, are responsible for the flux of auxin to the SCN region. PIN1 plays the main role in auxin distribution. In the columella cells, PIN3, PIN4, and PIN7 transport the auxin toward the lateral root cap [4,38]. After treatment with H2O2, the transcript levels of the auxin transport genes, including PIN1, PIN2, PIN7, and AUX1, are repressed [72].
In chloroplasts, superoxide (O2•−) is predominantly generated through photosystems I and II (PS I and PS II). Meanwhile, in the mitochondria, O2•− primarily originates from the respiratory complexes I, II, and III of the electron transport chain (ETC). The O2•− produced in both chloroplasts and mitochondria can undergo dismutation, leading to the conversion of O2•− to H2O2. Superoxide dismutase (SOD) plays a crucial role in facilitating this conversion, catalyzing the dismutation of O2•− into H2O2 and O2 [49,73,74]. SOD is a kind of metalloenzyme, which can be divided into four types: CuSOD, ZnSOD, FeSOD, and MnSOD. CuSOD, ZnSOD, and FeSOD exist in chloroplasts, and MnSOD is distributed in the mitochondria [21]. Chloroplastic, thylakoid-attached Cu/ZnSOD (chl-Cu/ZnSOD) is encoded by a single gene in Arabidopsis (At2g28190). A knock-down mutant of the At2g28190 gene (KD-SOD) contains higher levels of H2O2 and shows shorter roots with more lateral roots than the wild type [23,75]. Because there are no chloroplasts in roots, it is speculated that the Cu/ZnSOD function may be present in the root plastids. The levels of PIN1, PIN2, and PIN4 proteins are reduced in the KD-SOD seedlings. The polarity of PIN1 is impaired by H2O2 in the division zone of the RAM [23]. These findings suggest that H2O2 regulates the establishment of the auxin gradient in the RAM by the modulation of PIN protein polarity and abundance (Figure 3) [23].
Phosphoethanolamine N-methyltransferase 1 (PEAMT1) catalyzes phosphocholine biosynthesis in Arabidopsis. The mutation of PEAMT1 results in the accumulation of H2O2, leading to RAM consumption and impaired activity of the SCN. The abundance of the auxin transporters, i.e., PIN proteins, including PIN1, PIN2, PIN3, and PIN7, are reduced in the peamt1 mutant. Moreover, the loss of function of PEAMT1 impairs PIN2 polar distribution in the root tip. The suppression of ROS over-accumulation partially prevents RAM differentiation in the peamt1 mutant. PEAMT1 regulates RAM activity by H2O2-mediated auxin distribution via the modulation of PIN proteins (Figure 3) [76]. The Arabidopsis mitochondrial-localized heat shock protein 70-1 (HSC70-1) regulates polar auxin transport by the modulation of ROS homeostasis in roots. The HSC70-1 knockout causes severe growth inhibition and an increase in mitochondrial ROS levels [77]. The mutation of HSC70-1 impairs auxin response and decreases the size and activity of the RAM. The abundance of the auxin transporter carriers, including PIN1, PIN2, PIN3, and PIN7, is reduced in the hsc70-1 mutant. Treatment with H2O2 in the wild type has been shown to decrease the transcript levels of the PINs, while treatment with GSH in the hsp70-1 mutant increases the expression levels of the PINs (Figure 3). These results suggest that HSC70-1-mediated ROS homeostasis regulates auxin distribution by affecting the expression of PINs [78].
Root survival under flooding-induced hypoxic stress depends on the maintenance of QC activity within the RAM, which is controlled by an auxin maximum. Hypoxic stress causes the disruption of auxin transport and auxin maximum formation and shifts the redox state of the QC towards a more reduced environment, leading to the activation of QC, degradation of the meristem, and root abortion. The maize phytoglobin gene ZmPgb1.1 minimizes the damaging effects under hypoxic stress. ZmPgb1.1 contributes to sustaining the PIN-mediated auxin maximum and an oxidized environment in the QC. The findings suggest that maintaining the redox state of QC is critical for root development under stresses [79].

5. H2O2 Signaling in PLT-Mediated RAM Activity Maintenance

Root meristem growth factors (RGFs), a family of functionally redundant homologous peptide hormones, have been documented as crucial regulators of RAM development. RGF1 is a peptide that regulates RAM size, and treatment with RGF1 in the Arabidopsis roots can increase RAM size, while the rgf1/2/3 triple mutant has a smaller RAM size [80]. Using genetic approaches, the researchers identified a clade of leucine-rich repeat receptor-like kinases, designated as RGF1 INSENSITIVE 1 (RGI1) to RGI5, also named RGF1 RECEPTORS (RGFRs), acting as the receptors of RGF1. The rgi1rgi2rgi3rgi4rgi5 quintuple mutant displays a small RAM and is completely insensitive to RGF1. The expression of PLT1 and PLT2 is almost undetectable in the quintuple mutant. RGF1 and its receptors RGIs regulate RAM activity by modulating the expression of PLT1 and PLT2 (Figure 3) [81]. To find the proteins connecting RGF1-RGIs, the mitogen-activated protein (MAP) kinases kinase 4 (MKK4) and kinase 5 (MKK5), along with their downstream targets MPK3 and MPK6, have been identified as the essential RGI-dependent regulators of RAM development. The MKK4/MKK5-MPK3/MPK6 module functions downstream of YDA, a MAPKKK. RGF1-RGI1 regulates the expression of PLT1 and PLT2 via a YDA-MKK4/MKK5-MPK3/MPK6 signaling cascade [82,83]. RGF1 can induce the expression of RGF1 INDUCIBLE TRANSCRIPTION FACTOR1 (RITF1), which is predominantly active in the meristematic zone of the root tip. RITF1 plays a pivotal role in mediating the signaling cascade initiated by RGF1. The overexpression of RITF1 reduces H2O2 levels in roots and increases the O2•− signal of the root meristematic zone, which enhances the stability of the PLT2 protein to increase root meristem size (Figure 3) [84].
SYNTAXIN OF PLANTS81 (AtSYP81) is a syntaxin gene identified in Arabidopsis thaliana. Staining with DAB and NBT indicated a reduction in H2O2 and O2•− levels in the atsyp81 mutants. The application of H2O2 or O2•− suppresses QC cell division and prevents the differentiation of CSCs in the primary root SCN of atsyp81-1 seedlings. An analysis of RNA-Seq data and qRT-PCR revealed that a subset of genes encoding class III peroxidases (Prxs) are upregulated in atsyp81-1 seedlings. Subsequent investigations elucidated PLT1/PLT2 as downstream elements involved in the regulation of ROS homeostasis and the activity of the RAM mediated by AtSYP81 [25]. This comprehensive analysis provides valuable insights into the intricate molecular mechanisms governed by AtSYP81 in plant growth and development (Figure 3). Prohibitins (PHBs) are recognized as having a potential tumor suppressor role with anti-proliferative activity. It has been shown that the phb3 mutant displays a short-root phenotype [85]. Loss of function of PHB3 results in enhanced root DSC differentiation and increased mitotic activity in QC. PHB overexpression lines display additional cell layers in the DSC. The mutation of PHB3 causes an accumulation of ROS, including H2O2 and O2•−. Three ROS-responsive ethylene response factor (ERF) genes, namely, ERF109, ERF114, and ERF115, are upregulated in the phb3 mutant. The mutation of PHB3 also represses the transcription of PLT1 and PLT2 by increasing ROS levels. Both ERF genes and PLT genes are key ROS-responsive factors in the mediation of RAM activity (Figure 3) [86].
SA and ABA play a critical role in QC maintenance. The SA overaccumulation mutant constitutively activated cell death 1 (cad1) exhibits increased cell division in QC. The application of exogenous SA also promotes QC cell division. SA promotes H2O2 and O2•− production, which is important for QC cell division. SA regulates QC maintenance largely by the ROS-mediated repression of the expression of WOX5, PLT1, and PLT2 (Figure 3) [24]. An ABA overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in the mitochondrial complex I, accumulates more ROS in root tips. The mutation of ABO8 reduces RAM activity, which can be recovered by the reducing agent GSH. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. ABO8 regulates RAM activity by the modulation of PLT expression via ROS homeostasis (Figure 3) [61].

6. H2O2 Signaling in SHR–SCR Module-Mediated RAM Activity Maintenance

The Arabidopsis thaliana P-loop NTPase APP1 exerts regulatory control over RAM identity via the ROS-mediated SHR–SCR pathway. The app1 mutant exhibits aberrant cell divisions in the QC and impairs DSC identity. The mutation of APP1 results in reduced levels of H2O2 and O2•− in the root tip, suppressing the expressions of SCR and SHR and consequently increasing the rate of QC cell division and root DSC differentiation. Conversely, elevated ROS levels in the APP1-overexpression line promote QC cell division and root DSC differentiation. The expression of PLT1 and PLT2 is downregulated in the presence of heightened ROS levels, suggesting that altered ROS levels may modulate RAM activity through distinct pathways (Figure 3) [87].
SHR and SCR are important for the maintenance of a healthy redox status in roots. The mutation of SHR or SCR results in ROS accumulation, probably due to decreased expression of peroxidase gene 3 (PER3) [88]. SHR is capable of establishing an optimal microenvironment for periclinal division in cortex endodermal initial cells by maintaining ROS homeostasis in Arabidopsis roots. SHR achieves this by significantly increasing ROS levels, primarily through the promotion of RESPIRATORY BURST OXIDASE HOMOLOG (RBOH) expression. Scavenging H2O2 has been demonstrated to markedly impair SHR’s ability to induce periclinal division. Interestingly, H2O2, rather than O2•−, plays a crucial role in SHR-mediated periclinal division [59]. Recent investigations have revealed an interaction between SHR and BRASSINAZOLE RESISTANT1 (BZR1), a crucial transcription factor in the BR signaling pathway. Both BZR1 and SHR directly bind to the promoters of RBOHD and RBOHF, thereby promoting their expression and subsequently increasing H2O2 accumulation. This elevated H2O2 level, in conjunction with the presence of BZR1, has the capacity to induce periclinal division. These findings suggest a high level of coordination between BR and H2O2 signals in finely regulating the periclinal division of cortex endodermal initials through the BZR1–SHR module [60].

7. Conclusions

H2O2 homeostasis is critical for the maintenance of RAM activity, and increased or decreased levels of H2O2 have important effects on auxin biosynthesis, transport, and signaling. However, the direct regulation of H2O2 on auxin signaling is not well understood. H2O2 can directly regulate the function of its target proteins by oxidative post-translational modifications. H2O2 reacts with the sulfur atoms of systeine and methionine residues to form S-sulfenylated, S-nitrosated, or persulfidated residues [89]. The identification of new direct targets of H2O2 needs to be investigated further. Additionally, single-cell RNA sequencing has been used to study root development in Arabidopsis, maize, and rice [54,90,91,92,93]. The advancement of new technologies provides new insights into understanding the function of H2O2 in the maintenance of the RAM.
RAM maintenance is very important for root development and stress adaptation. H2O2 acts as a critical signal to help RAM maintenance. The homeostasis and signaling of H2O2 are crucial for stem cell specification and formative cell division. Many key players, such as PLTs, SCR, SHR, and PINs, are regulated by H2O2 in RAM development; however, the fine-tuned regulatory mechanisms of H2O2 controlling the core factors need to be studied in the future. It will be interesting to elucidate the redox regulation of proteins in H2O2-mediated RAM development.

Author Contributions

H.Z., W.W. and H.L. designed and wrote the manuscript. Y.M., Y.X. and X.W. prepared the figures, collected the literature, and reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The work was supported by the National Natural Science Foundation of China (32000147, 31800165), the Key Project, Special Foundation of Research, Development and Promotion in Henan Province, China (222102110070), and the Program for Innovative Research Team (in Science and Technology) at the University of Henan Province (221RTSTHN0230).

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Ou, Y.; Kui, H.; Li, J. Receptor-like kinases in root development: Current progress and future directions. Mol. Plant 2021, 14, 166–185. [Google Scholar] [CrossRef] [PubMed]
  2. Cohen, J.D.; Strader, L.C. An auxin research odyssey: 1989–2023. Plant Cell 2024, koae054. [Google Scholar] [CrossRef] [PubMed]
  3. Wang, Q.; Marconi, M.; Guan, C.; Wabnik, K.; Jiao, Y. Polar auxin transport modulates early leaf flattening. Proc. Natl. Acad. Sci. USA 2022, 119, e2215569119. [Google Scholar] [CrossRef] [PubMed]
  4. Roychoudhry, S.; Kepinski, S. Auxin in root development. Cold Spring Harb. Perspect. Biol. 2022, 14, a039933. [Google Scholar] [CrossRef] [PubMed]
  5. Verma, S.; Attuluri, V.P.S.; Robert, H.S. An essential function for auxin in embryo development. Cold Spring Harb. Perspect. Biol. 2021, 13, a039966. [Google Scholar] [CrossRef] [PubMed]
  6. Yamoune, A.; Cuyacot, A.R.; Zdarska, M.; Hejatko, J. Hormonal orchestration of root apical meristem formation and maintenance in Arabidopsis. J. Exp. Bot. 2021, 72, 6768–6788. [Google Scholar] [CrossRef] [PubMed]
  7. Dubrovsky, J.G.; Vissenberg, K. The quiescent centre and root apical meristem: Organization and function. J. Exp. Bot. 2021, 72, 6673–6678. [Google Scholar] [CrossRef] [PubMed]
  8. Liu, W.; Cai, G.; Zhai, N.; Wang, H.; Tang, T.; Zhang, Y.; Zhang, Z.; Sun, L.; Zhang, Y.; Beeckman, T.; et al. Genome and transcriptome of Selaginella kraussiana reveal evolution of root apical meristems in vascular plants. Curr. Biol. 2023, 33, 4085–4097.e4085. [Google Scholar] [CrossRef] [PubMed]
  9. Zeng, J.; Geng, X.; Zhao, Z.; Zhou, W. Tipping the balance: The dynamics of stem cell maintenance and stress responses in plant meristems. Curr. Opin. Plant Biol. 2024, 78, 102510. [Google Scholar] [CrossRef]
  10. De Tullio, M.C.; Jiang, K.; Feldman, L.J. Redox regulation of root apical meristem organization: Connecting root development to its environment. Plant Physiol. Biochem. 2010, 48, 328–336. [Google Scholar] [CrossRef]
  11. Zhang, H.; Mu, Y.; Zhang, H.; Yu, C. Maintenance of stem cell activity in plant development and stress responses. Front. Plant Sci. 2023, 14, 1302046. [Google Scholar] [CrossRef]
  12. Fernández-Marcos, M.; Sanz, L.; Lewis, D.R.; Muday, G.K.; Lorenzo, O. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. USA 2011, 108, 18506–18511. [Google Scholar] [CrossRef]
  13. Sanchez-Corrionero, A.; Sánchez-Vicente, I.; Arteaga, N.; Manrique-Gil, I.; Gómez-Jiménez, S.; Torres-Quezada, I.; Albertos, P.; Lorenzo, O. Fine-tuned nitric oxide and hormone interface in plant root development and regeneration. J. Exp. Bot. 2023, 74, 6104–6118. [Google Scholar] [CrossRef]
  14. Mira, M.M.; Ibrahim, S.; So, K.; Kowatsch, R.; Duncan, R.W.; Hill, R.D.; Stasolla, C. Specificity in root domain accumulation of Phytoglobin1 and nitric oxide (NO) determines meristematic viability in water-stressed Brassica napus roots. Ann. Bot. 2023, 131, 475–490. [Google Scholar] [CrossRef] [PubMed]
  15. Mukherjee, S.; Corpas, F.J. H2O2, NO, and H2S networks during root development and signalling under physiological and challenging environments: Beneficial or toxic? Plant Cell Environ. 2023, 46, 688–717. [Google Scholar] [CrossRef] [PubMed]
  16. Mira, M.M.; El-Khateeb, E.A.; Youssef, M.S.; Ciacka, K.; So, K.; Duncan, R.W.; Hill, R.D.; Stasolla, C. Arabidopsis root apical meristem survival during waterlogging is determined by phytoglobin through nitric oxide and auxin. Planta 2023, 258, 86. [Google Scholar] [CrossRef]
  17. Singh, T.; Bisht, N.; Ansari, M.M.; Chauhan, P.S. The hidden harmony: Exploring ROS-phytohormone nexus for shaping plant root architecture in response to environmental cues. Plant Physiol. Biochem. 2024, 206, 108273. [Google Scholar] [CrossRef]
  18. Hasanuzzaman, M.; Raihan, M.R.H.; Masud, A.A.C.; Rahman, K.; Nowroz, F.; Rahman, M.; Nahar, K.; Fujita, M. Regulation of reactive oxygen species and antioxidant defense in plants under salinity. Int. J. Mol. Sci. 2021, 22, 9326. [Google Scholar] [CrossRef]
  19. Waszczak, C.; Carmody, M.; Kangasjärvi, J. Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 2018, 69, 209–236. [Google Scholar] [CrossRef]
  20. Mittler, R.; Zandalinas, S.I.; Fichman, Y.; Van Breusegem, F. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 2022, 23, 663–679. [Google Scholar] [CrossRef]
  21. Smirnoff, N.; Arnaud, D. Hydrogen peroxide metabolism and functions in plants. New Phytol. 2019, 221, 1197–1214. [Google Scholar] [CrossRef] [PubMed]
  22. Dunand, C.; Crèvecoeur, M.; Penel, C. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: Possible interaction with peroxidases. New Phytol. 2007, 174, 332–341. [Google Scholar] [CrossRef] [PubMed]
  23. Pasternak, T.; Palme, K.; Pérez-Pérez, J.M. Role of reactive oxygen species in the modulation of auxin flux and root development in Arabidopsis thaliana. Plant J. 2023, 114, 83–95. [Google Scholar] [CrossRef] [PubMed]
  24. Wang, Z.; Rong, D.; Chen, D.; Xiao, Y.; Liu, R.; Wu, S.; Yamamuro, C. Salicylic acid promotes quiescent center cell division through ROS accumulation and down-regulation of PLT1, PLT2, and WOX5. J. Integr. Plant Biol. 2021, 63, 583–596. [Google Scholar] [CrossRef] [PubMed]
  25. Wang, M.; Zhang, H.; Zhao, X.; Zhou, J.; Qin, G.; Liu, Y.; Kou, X.; Zhao, Z.; Wu, T.; Zhu, J.K.; et al. SYNTAXIN OF PLANTS81 regulates root meristem activity and stem cell niche maintenance via ROS signaling. Plant Physiol. 2023, 191, 1365–1382. [Google Scholar] [CrossRef] [PubMed]
  26. Sarkar, A.K.; Luijten, M.; Miyashima, S.; Lenhard, M.; Hashimoto, T.; Nakajima, K.; Scheres, B.; Heidstra, R.; Laux, T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 2007, 446, 811–814. [Google Scholar] [CrossRef]
  27. Forzani, C.; Aichinger, E.; Sornay, E.; Willemsen, V.; Laux, T.; Dewitte, W.; Murray, J.A. WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr. Biol. 2014, 24, 1939–1944. [Google Scholar] [CrossRef]
  28. Pi, L.; Aichinger, E.; van der Graaff, E.; Llavata-Peris, C.I.; Weijers, D.; Hennig, L.; Groot, E.; Laux, T. Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev. Cell 2015, 33, 576–588. [Google Scholar] [CrossRef]
  29. Berckmans, B.; Kirschner, G.; Gerlitz, N.; Stadler, R.; Simon, R. CLE40 signaling regulates root stem cell fate. Plant Physiol. 2020, 182, 1776–1792. [Google Scholar] [CrossRef]
  30. Stahl, Y.; Wink, R.H.; Ingram, G.C.; Simon, R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 2009, 19, 909–914. [Google Scholar] [CrossRef]
  31. Stahl, Y.; Grabowski, S.; Bleckmann, A.; Kühnemuth, R.; Weidtkamp-Peters, S.; Pinto, K.G.; Kirschner, G.K.; Schmid, J.B.; Wink, R.H.; Hülsewede, A.; et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 2013, 23, 362–371. [Google Scholar] [CrossRef] [PubMed]
  32. Zhang, Y.; Jiao, Y.; Liu, Z.; Zhu, Y.X. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nat. Commun. 2015, 6, 6003. [Google Scholar] [CrossRef] [PubMed]
  33. Fukui, K.; Hayashi, K.I. Manipulation and sensing of auxin metabolism, transport and signaling. Plant Cell Physiol. 2018, 59, 1500–1510. [Google Scholar] [CrossRef] [PubMed]
  34. Brunoud, G.; Wells, D.M.; Oliva, M.; Larrieu, A.; Mirabet, V.; Burrow, A.H.; Beeckman, T.; Kepinski, S.; Traas, J.; Bennett, M.J.; et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 2012, 482, 103–106. [Google Scholar] [CrossRef] [PubMed]
  35. Liao, C.Y.; Smet, W.; Brunoud, G.; Yoshida, S.; Vernoux, T.; Weijers, D. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods 2015, 12, 207–210. [Google Scholar] [CrossRef] [PubMed]
  36. Liu, Y.; Xu, M.; Liang, N.; Zheng, Y.; Yu, Q.; Wu, S. Symplastic communication spatially directs local auxin biosynthesis to maintain root stem cell niche in Arabidopsis. Proc. Natl. Acad. Sci. USA 2017, 114, 4005–4010. [Google Scholar] [CrossRef] [PubMed]
  37. Grieneisen, V.A.; Xu, J.; Marée, A.F.; Hogeweg, P.; Scheres, B.J.N. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 2007, 449, 1008–1013. [Google Scholar] [CrossRef] [PubMed]
  38. Blilou, I.; Xu, J.; Wildwater, M.; Willemsen, V.; Paponov, I.; Friml, J.; Heidstra, R.; Aida, M.; Palme, K.; Scheres, B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 2005, 433, 39–44. [Google Scholar] [CrossRef]
  39. Ding, Z.; Friml, J. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 2010, 107, 12046–12051. [Google Scholar] [CrossRef]
  40. Tian, H.; Wabnik, K.; Niu, T.; Li, H.; Yu, Q.; Pollmann, S.; Vanneste, S.; Govaerts, W.; Rolcík, J.; Geisler, M.; et al. WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol. Plant 2014, 7, 277–289. [Google Scholar] [CrossRef]
  41. Aida, M.; Beis, D.; Heidstra, R.; Willemsen, V.; Blilou, I.; Galinha, C.; Nussaume, L.; Noh, Y.S.; Amasino, R.; Scheres, B. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 2004, 119, 109–120. [Google Scholar] [CrossRef]
  42. Galinha, C.; Hofhuis, H.; Luijten, M.; Willemsen, V.; Blilou, I.; Heidstra, R.; Scheres, B. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 2007, 449, 1053–1057. [Google Scholar] [CrossRef]
  43. Shimotohno, A.; Heidstra, R.; Blilou, I.; Scheres, B. Root stem cell niche organizer specification by molecular convergence of PLETHORA and SCARECROW transcription factor modules. Genes Dev. 2018, 32, 1085–1100. [Google Scholar] [CrossRef]
  44. Sabatini, S.; Heidstra, R.; Wildwater, M.; Scheres, B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 2003, 17, 354–358. [Google Scholar] [CrossRef]
  45. Nakajima, K.; Sena, G.; Nawy, T.; Benfey, P.N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 2001, 413, 307–311. [Google Scholar] [CrossRef]
  46. Mähönen, A.P.; Ten Tusscher, K.; Siligato, R.; Smetana, O.; Díaz-Triviño, S.; Salojärvi, J.; Wachsman, G.; Prasad, K.; Heidstra, R.; Scheres, B. PLETHORA gradient formation mechanism separates auxin responses. Nature 2014, 515, 125–129. [Google Scholar] [CrossRef]
  47. Xiong, F.; Zhang, B.K.; Liu, H.H.; Wei, G.; Wu, J.H.; Wu, Y.N.; Zhang, Y.; Li, S. Transcriptional regulation of PLETHORA1 in the root meristem through an importin and its two antagonistic cargos. Plant Cell 2020, 32, 3812–3824. [Google Scholar] [CrossRef]
  48. Ercoli, M.F.; Ferela, A.; Debernardi, J.M.; Perrone, A.P.; Rodriguez, R.E.; Palatnik, J.F. GIF transcriptional coregulators control root meristem homeostasis. Plant Cell 2018, 30, 347–359. [Google Scholar] [CrossRef]
  49. Liu, H.H.; Xiong, F.; Duan, C.Y.; Wu, Y.N.; Zhang, Y.; Li, S. Importin β4 Mediates Nuclear Import of GRF-Interacting Factors to Control Ovule Development in Arabidopsis. Plant Physiol. 2019, 179, 1080–1092. [Google Scholar] [CrossRef]
  50. Hao, R.; Zhou, W.; Li, J.; Luo, M.; Scheres, B.; Guo, Y. On salt stress, PLETHORA signaling maintains root meristems. Dev. Cell 2023, 58, 1657–1669.e1655. [Google Scholar] [CrossRef]
  51. Lv, B.; Hu, K.; Tian, T.; Wei, K.; Zhang, F.; Jia, Y.; Tian, H.; Ding, Z. The pre-mRNA splicing factor RDM16 regulates root stem cell maintenance in Arabidopsis. J. Integr. Plant Biol. 2021, 63, 662–678. [Google Scholar] [CrossRef] [PubMed]
  52. Burkart, R.C.; Strotmann, V.I.; Kirschner, G.K.; Akinci, A.; Czempik, L.; Dolata, A.; Maizel, A.; Weidtkamp-Peters, S.; Stahl, Y. PLETHORA-WOX5 interaction and subnuclear localization control Arabidopsis root stem cell maintenance. EMBO Rep. 2022, 23, e54105. [Google Scholar] [CrossRef]
  53. Cui, H.; Levesque, M.P.; Vernoux, T.; Jung, J.W.; Paquette, A.J.; Gallagher, K.L.; Wang, J.Y.; Blilou, I.; Scheres, B.; Benfey, P.N. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 2007, 316, 421–425. [Google Scholar] [CrossRef]
  54. Ortiz-Ramírez, C.; Guillotin, B.; Xu, X.; Rahni, R.; Zhang, S.; Yan, Z.; Coqueiro Dias Araujo, P.; Demesa-Arevalo, E.; Lee, L.; Van Eck, J.; et al. Ground tissue circuitry regulates organ complexity in maize and Setaria. Science 2021, 374, 1247–1252. [Google Scholar] [CrossRef] [PubMed]
  55. Winter, C.M.; Szekely, P.; Popov, V.; Belcher, H.; Carter, R.; Jones, M.; Fraser, S.E.; Truong, T.V.; Benfey, P.N. SHR and SCR coordinate root patterning and growth early in the cell cycle. Nature 2024, 626, 611–616. [Google Scholar] [CrossRef] [PubMed]
  56. Zhai, H.; Zhang, X.; You, Y.; Lin, L.; Zhou, W.; Li, C. SEUSS integrates transcriptional and epigenetic control of root stem cell organizer specification. EMBO J. 2020, 39, e105047. [Google Scholar] [CrossRef] [PubMed]
  57. Xie, C.; Li, C.; Wang, F.; Zhang, F.; Liu, J.; Wang, J.; Zhang, X.; Kong, X.; Ding, Z. NAC1 regulates root ground tissue maturation by coordinating with the SCR/SHR-CYCD6;1 module in Arabidopsis. Mol. Plant 2023, 16, 709–725. [Google Scholar] [CrossRef]
  58. Foreman, J.; Demidchik, V.; Bothwell, J.H.; Mylona, P.; Miedema, H.; Torres, M.A.; Linstead, P.; Costa, S.; Brownlee, C.; Jones, J.D.; et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003, 422, 442–446. [Google Scholar] [CrossRef] [PubMed]
  59. Li, P.; Cai, Q.; Wang, H.; Li, S.; Cheng, J.; Li, H.; Yu, Q.; Wu, S. Hydrogen peroxide homeostasis provides beneficial micro-environment for SHR-mediated periclinal division in Arabidopsis root. New Phytol. 2020, 228, 1926–1938. [Google Scholar] [CrossRef]
  60. Tian, Y.; Zhao, N.; Wang, M.; Zhou, W.; Guo, J.; Han, C.; Zhou, C.; Wang, W.; Wu, S.; Tang, W.; et al. Integrated regulation of periclinal cell division by transcriptional module of BZR1-SHR in Arabidopsis roots. New Phytol. 2022, 233, 795–808. [Google Scholar] [CrossRef]
  61. Yang, L.; Zhang, J.; He, J.; Qin, Y.; Hua, D.; Duan, Y.; Chen, Z.; Gong, Z. ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet. 2014, 10, e1004791. [Google Scholar] [CrossRef] [PubMed]
  62. He, J.; Duan, Y.; Hua, D.; Fan, G.; Wang, L.; Liu, Y.; Chen, Z.; Han, L.; Qu, L.J.; Gong, Z. DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 2012, 24, 1815–1833. [Google Scholar] [CrossRef]
  63. Ma, F.; Wang, L.; Li, J.; Samma, M.K.; Xie, Y.; Wang, R.; Wang, J.; Zhang, J.; Shen, W. Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol. Biol. 2014, 85, 49–61. [Google Scholar] [CrossRef] [PubMed]
  64. Ivanchenko, M.G.; den Os, D.; Monshausen, G.B.; Dubrovsky, J.G.; Bednárová, A.; Krishnan, N. Auxin increases the hydrogen peroxide (H2O2) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth. Ann. Bot. 2013, 112, 1107–1116. [Google Scholar] [CrossRef]
  65. Huang, L.; Yu, L.J.; Zhang, X.; Fan, B.; Wang, F.Z.; Dai, Y.S.; Qi, H.; Zhou, Y.; Xie, L.J.; Xiao, S. Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis. Autophagy 2019, 15, 407–422. [Google Scholar] [CrossRef]
  66. Fu, Y.; Yang, Y.; Chen, S.; Ning, N.; Hu, H. Arabidopsis IAR4 modulates primary root growth under salt stress through ROS-mediated modulation of auxin distribution. Front. Plant Sci. 2019, 10, 522. [Google Scholar] [CrossRef]
  67. Kim, M.J.; Ciani, S.; Schachtman, D.P. A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol. Plant 2010, 3, 420–427. [Google Scholar] [CrossRef]
  68. Shin, R.; Schachtman, D.P. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl. Acad. Sci. USA 2004, 101, 8827–8832. [Google Scholar] [CrossRef] [PubMed]
  69. Yu, X.; Pasternak, T.; Eiblmeier, M.; Ditengou, F.; Kochersperger, P.; Sun, J.; Wang, H.; Rennenberg, H.; Teale, W.; Paponov, I.; et al. Plastid-localized glutathione reductase2-regulated glutathione redox status is essential for Arabidopsis root apical meristem maintenance. Plant Cell 2013, 25, 4451–4468. [Google Scholar] [CrossRef]
  70. Qin, Y.; Yang, L.; Sun, Z.; Wang, X.; Wang, Y.; Zhang, J.; Rehman, A.U.; Chen, Z.; Qi, J.; Wang, B.; et al. Redox-mediated endocytosis of a receptor-like kinase during distal stem cell differentiation depends on its tumor necrosis factor receptor domain. Plant Physiol. 2019, 181, 1075–1095. [Google Scholar] [CrossRef]
  71. Mangano, S.; Denita-Juarez, S.P.; Choi, H.-S.; Marzol, E.; Hwang, Y.; Ranocha, P.; Velasquez, S.M.; Borassi, C.; Barberini, M.L.; Aptekmann, A.A.; et al. Molecular link between auxin and ROS-mediated polar growth. Proc. Natl. Acad. Sci. USA 2017, 114, 5289–5294. [Google Scholar] [CrossRef] [PubMed]
  72. Su, C.; Liu, L.; Liu, H.; Ferguson, B.J.; Zou, Y.; Zhao, Y.; Wang, T.; Wang, Y.; Li, X.J.J.o.P.B. H2O2 regulates root system architecture by modulating the polar transport and redistribution of auxin. J. Plant Biol. 2016, 59, 260–270. [Google Scholar] [CrossRef]
  73. Huang, S.; Van Aken, O.; Schwarzländer, M.; Belt, K.; Millar, A.H. The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol. 2016, 171, 1551–1559. [Google Scholar] [CrossRef] [PubMed]
  74. Murphy, M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417, 1–13. [Google Scholar] [CrossRef]
  75. Rizhsky, L.; Liang, H.; Mittler, R. The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 2003, 278, 38921–38925. [Google Scholar] [CrossRef] [PubMed]
  76. Zou, Y.; Zhang, X.; Tan, Y.; Huang, J.B.; Zheng, Z.; Tao, L.Z. Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis. New Phytol. 2019, 224, 258–273. [Google Scholar] [CrossRef]
  77. Wei, S.S.; Niu, W.T.; Zhai, X.T.; Liang, W.Q.; Xu, M.; Fan, X.; Lv, T.T.; Xu, W.Y.; Bai, J.T.; Jia, N.; et al. Arabidopsis mtHSC70-1 plays important roles in the establishment of COX-dependent respiration and redox homeostasis. J. Exp. Bot. 2019, 70, 5575–5590. [Google Scholar] [CrossRef]
  78. Shen, T.; Jia, N.; Wei, S.; Xu, W.; Lv, T.; Bai, J.; Li, B. Mitochondrial HSC70-1 regulates polar auxin transport through ROS homeostasis in Arabidopsis roots. Antioxidants 2022, 11, 2035. [Google Scholar] [CrossRef]
  79. Mira, M.M.; El-Khateeb, E.A.; Gaafar, R.M.; Igamberdiev, A.U.; Hill, R.D.; Stasolla, C. Stem cell fate in hypoxic root apical meristems is influenced by phytoglobin expression. J. Exp. Bot. 2020, 71, 1350–1362. [Google Scholar] [CrossRef]
  80. Matsuzaki, Y.; Ogawa-Ohnishi, M.; Mori, A.; Matsubayashi, Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 2010, 329, 1065–1067. [Google Scholar] [CrossRef]
  81. Ou, Y.; Lu, X.; Zi, Q.; Xun, Q.; Zhang, J.; Wu, Y.; Shi, H.; Wei, Z.; Zhao, B.; Zhang, X.; et al. RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res. 2016, 26, 686–698. [Google Scholar] [CrossRef] [PubMed]
  82. Lu, X.; Shi, H.; Ou, Y.; Cui, Y.; Chang, J.; Peng, L.; Gou, X.; He, K.; Li, J. RGF1-RGI1, a peptide-receptor complex, regulates Arabidopsis root meristem development via a MAPK signaling cascade. Mol. Plant 2020, 13, 1594–1607. [Google Scholar] [CrossRef] [PubMed]
  83. Shao, Y.; Yu, X.; Xu, X.; Li, Y.; Yuan, W.; Xu, Y.; Mao, C.; Zhang, S.; Xu, J. The YDA-MKK4/MKK5-MPK3/MPK6 cascade functions downstream of the RGF1-RGI ligand-receptor pair in regulating mitotic activity in root apical meristem. Mol. Plant 2020, 13, 1608–1623. [Google Scholar] [CrossRef] [PubMed]
  84. Yamada, M.; Han, X.; Benfey, P.N. RGF1 controls root meristem size through ROS signalling. Nature 2020, 577, 85–88. [Google Scholar] [CrossRef] [PubMed]
  85. Van Aken, O.; Pecenková, T.; van de Cotte, B.; De Rycke, R.; Eeckhout, D.; Fromm, H.; De Jaeger, G.; Witters, E.; Beemster, G.T.; Inzé, D.; et al. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development. Plant J. 2007, 52, 850–864. [Google Scholar] [CrossRef] [PubMed]
  86. Kong, X.; Tian, H.; Yu, Q.; Zhang, F.; Wang, R.; Gao, S.; Xu, W.; Liu, J.; Shani, E.; Fu, C.; et al. PHB3 maintains root stem cell niche identity through ROS-Responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep. 2018, 22, 1350–1363. [Google Scholar] [CrossRef] [PubMed]
  87. Yu, Q.; Tian, H.; Yue, K.; Liu, J.; Zhang, B.; Li, X.; Ding, Z. A P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet. 2016, 12, e1006175. [Google Scholar] [CrossRef]
  88. Fu, J.; Zhang, X.; Liu, J.; Gao, X.; Bai, J.; Hao, Y.; Cui, H. A mechanism coordinating root elongation, endodermal differentiation, redox homeostasis and stress response. Plant J. 2021, 107, 1029–1039. [Google Scholar] [CrossRef]
  89. Zhou, H.; Huang, J.; Willems, P.; Van Breusegem, F.; Xie, Y. Cysteine thiol-based post-translational modification: What do we know about transcription factors? Trends Plant Sci. 2023, 28, 415–428. [Google Scholar] [CrossRef]
  90. Cao, Y.; Ma, J.; Han, S.; Hou, M.; Wei, X.; Zhang, X.; Zhang, Z.J.; Sun, S.; Ku, L.; Tang, J.; et al. Single-cell RNA sequencing profiles reveal cell type-specific transcriptional regulation networks conditioning fungal invasion in maize roots. Plant Biotechnol. J. 2023, 21, 1839–1859. [Google Scholar] [CrossRef]
  91. Zhang, T.Q.; Xu, Z.G.; Shang, G.D.; Wang, J.W. A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol. Plant 2019, 12, 648–660. [Google Scholar] [CrossRef] [PubMed]
  92. Farmer, A.; Thibivilliers, S.; Ryu, K.H.; Schiefelbein, J.; Libault, M. Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level. Mol. Plant 2021, 14, 372–383. [Google Scholar] [CrossRef] [PubMed]
  93. Zhang, T.Q.; Chen, Y.; Liu, Y.; Lin, W.H.; Wang, J.W. Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root. Nat. Commun. 2021, 12, 2053. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Key signaling in the regulation of the root apical meristem. (A). The structure of the root apical meristem (RAM). The quiescent center (QC) and its surrounding stem cells together form a stem cell niche (SCN). Different stem cells (also called initials) produce a variety of cell types in roots. (B). The key signals for controlling SCN maintenance. WOX5 is a critical factor for the regulation of SCN maintenance. Auxin represses WOX5 expression by ARF10, ARF16, and IAA17. ROW1 and the module CLE40/ACR4/CLV1 can also inhibit WOX5 expression. The modules SHR/SCR, PLT/TCP/SCR, and SEU/SDG4/SCR promote WOX5 expression. In addition, WOX5 promotes PLT1 expression to control SCN activity. GIF1 and JANUS are antagonistic to regulate PLT1 expression (B).
Figure 1. Key signaling in the regulation of the root apical meristem. (A). The structure of the root apical meristem (RAM). The quiescent center (QC) and its surrounding stem cells together form a stem cell niche (SCN). Different stem cells (also called initials) produce a variety of cell types in roots. (B). The key signals for controlling SCN maintenance. WOX5 is a critical factor for the regulation of SCN maintenance. Auxin represses WOX5 expression by ARF10, ARF16, and IAA17. ROW1 and the module CLE40/ACR4/CLV1 can also inhibit WOX5 expression. The modules SHR/SCR, PLT/TCP/SCR, and SEU/SDG4/SCR promote WOX5 expression. In addition, WOX5 promotes PLT1 expression to control SCN activity. GIF1 and JANUS are antagonistic to regulate PLT1 expression (B).
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Figure 2. Direct regulation of the key genes involved in root apical meristem. The modules SEU/SCR/SDG4 and PLT3/SCR/TCP20 directly bind to the promoter of WOX5 to activate its expression. ROW1 directly represses WOX5 expression. WOX5 can inhibit CDF4 and CYCD3;3 expression by binding to their promoters. The module PLT1/JANUS/POLII directly promotes PLT1 expression. GIF1 functions to repress the expression of PLT1.
Figure 2. Direct regulation of the key genes involved in root apical meristem. The modules SEU/SCR/SDG4 and PLT3/SCR/TCP20 directly bind to the promoter of WOX5 to activate its expression. ROW1 directly represses WOX5 expression. WOX5 can inhibit CDF4 and CYCD3;3 expression by binding to their promoters. The module PLT1/JANUS/POLII directly promotes PLT1 expression. GIF1 functions to repress the expression of PLT1.
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Figure 3. H2O2 signaling in the regulation of root apical meristem activity. Hydrogen peroxide (H2O2) plays a crucial role in the regulation of root apical meristem (RAM) activity. Many factors are involved in the regulation of H2O2 homeostasis. PEAMT1, ABO8, PHB3, CAD1, RITF1, and HSC70-1 contribute to the repression of H2O2 production, whereas APP1 and SYB81 promote H2O2 accumulation in the RAM. The factors that induce the alteration of H2O2 levels regulate RAM activity maintenance via the modulation of PINs, PLTs, SHR, SCR, CLE40, ACR4, and ERFs. H2O2 homeostasis is important for RAM activity maintenance.
Figure 3. H2O2 signaling in the regulation of root apical meristem activity. Hydrogen peroxide (H2O2) plays a crucial role in the regulation of root apical meristem (RAM) activity. Many factors are involved in the regulation of H2O2 homeostasis. PEAMT1, ABO8, PHB3, CAD1, RITF1, and HSC70-1 contribute to the repression of H2O2 production, whereas APP1 and SYB81 promote H2O2 accumulation in the RAM. The factors that induce the alteration of H2O2 levels regulate RAM activity maintenance via the modulation of PINs, PLTs, SHR, SCR, CLE40, ACR4, and ERFs. H2O2 homeostasis is important for RAM activity maintenance.
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Liu, H.; Mu, Y.; Xuan, Y.; Wu, X.; Wang, W.; Zhang, H. Hydrogen Peroxide Signaling in the Maintenance of Plant Root Apical Meristem Activity. Antioxidants 2024, 13, 554. https://doi.org/10.3390/antiox13050554

AMA Style

Liu H, Mu Y, Xuan Y, Wu X, Wang W, Zhang H. Hydrogen Peroxide Signaling in the Maintenance of Plant Root Apical Meristem Activity. Antioxidants. 2024; 13(5):554. https://doi.org/10.3390/antiox13050554

Chicago/Turabian Style

Liu, Hui, Yangwei Mu, Yuxin Xuan, Xiaolin Wu, Wei Wang, and Hui Zhang. 2024. "Hydrogen Peroxide Signaling in the Maintenance of Plant Root Apical Meristem Activity" Antioxidants 13, no. 5: 554. https://doi.org/10.3390/antiox13050554

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