Next Article in Journal
Sex as a Determinant of Age-Related Changes in the Brain
Next Article in Special Issue
Species of the Sections Hedysarum and Multicaulia of the Genus Hedysarum (Fabaceae): Taxonomy, Distribution, Chromosomes, Genomes, and Phylogeny
Previous Article in Journal
GBA1-Associated Parkinson’s Disease Is a Distinct Entity
Previous Article in Special Issue
Chloroplast Genomes Evolution and Phylogenetic Relationships of Caragana species
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 25
Issue 13
10.3390/ijms25137120
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Research Progress in the Regulation of the ABA Signaling Pathway by E3 Ubiquitin Ligases in Plants

by
Hongyun Kou
†,
Xiaopei Zhang
†,
Jinghao Jia
,
Ming Xin
,
Jinhui Wang
,
Lili Mao
,
Ahmedov Miraziz Baltaevich
and
Xianliang Song
*
State Key Laboratory of Crop Biology, Agronomy College, Shandong Agricultural University, Tai’an 271018, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2024, 25(13), 7120; https://doi.org/10.3390/ijms25137120
Submission received: 25 May 2024 / Revised: 11 June 2024 / Accepted: 21 June 2024 / Published: 28 June 2024
(This article belongs to the Special Issue Plant Phylogenomics and Genetic Diversity (2nd Edition))
Browse Figures
Versions Notes

Abstract

:
E3 ubiquitin ligases (UBLs), as enzymes capable of specifically recognizing target proteins in the process of protein ubiquitination, play crucial roles in regulating responses to abiotic stresses such as drought, salt, and temperature. Abscisic acid (ABA), a plant endogenous hormone, is essential to regulating plant growth, development, disease resistance, and defense against abiotic stresses, and acts through a complex ABA signaling pathway. Hormone signaling transduction relies on protein regulation, and E3 ubiquitin ligases play important parts in regulating the ABA pathway. Therefore, this paper reviews the ubiquitin–proteasome-mediated protein degradation pathway, ABA-related signaling pathways, and the regulation of ABA-signaling-pathway-related genes by E3 ubiquitin ligases, aiming to provide references for further exploration of the relevant research on how plant E3 ubiquitin ligases regulate the ABA pathway.

1. Introduction

Plants, as sessile organisms, cannot relocate like animals to find suitable habitats. Instead, they have evolved a series of molecular and physiological mechanisms to maximize the reduction of damage caused by both biotic and abiotic stresses [1]. When plants encounter abiotic stresses such as drought, salinity, low temperature, and high temperature, they activate stress-responsive genes to produce various stress proteins to combat the stress. However, the excessive accumulation of abnormal proteins can damage cells, disrupt cellular structures and functions, and affect plant metabolism and growth development. Therefore, a protein degradation system is required to remove abnormal proteins and maintain normal plant growth and development [2].
The ubiquitin/26S proteasome system (UPS) is an important protein degradation pathway in eukaryotic cells involved in finely regulating the growth and development of organisms and their adaptability to the surrounding environment, thereby playing a crucial role in alleviating and reducing damage caused by biotic and abiotic stresses [3]. The UPS comprises several essential components, including ubiquitin molecules (Ub), ubiquitin-activating enzyme E1 (UBA), ubiquitin-conjugating enzyme E2 (UBC), ubiquitin ligase E3 (UBL), and deubiquitinating enzymes (DUBs), as well as proteins involved in substrate recognition and translocation, 26S proteasomes, and ubiquitinated target substrate proteins [4]. Among them, E3 ubiquitin ligases, as key enzymes in the UPS, play a crucial role in recognizing proteins and exert specific recognition during the process of identifying target substrates [5].
Plant responses to external stresses and the maintenance of normal growth development are also regulated by various endogenous hormones. ABA plays an important role in regulating plant growth and development and in defense against biotic and abiotic stresses [6,7]. Since the discovery in 2014 that the ABA receptor PYL8/RCAR3 is regulated by the CUL4-type multi-subunit E3 ligase DET1-, DDB1-ASSOCIATED1 (DDA1), thereby negatively regulating ABA signaling [8], the regulation of the ABA pathway by E3 ubiquitin ligase has gradually become a focus of life science research. Therefore, this paper aims to review the research progress on the regulation of the ABA pathway by E3 ubiquitin ligase in order to provide a reference for subsequent studies.

2. The Ubiquitin–Proteasome-Mediated Protein Degradation Pathway

When plants are subjected to biotic and abiotic stressors, proteins within plant cells undergo abnormal expression, leading to impaired cellular function, senescence, and even cell death, which forms an important pathological basis for the occurrence of various diseases [9]. The main protein degradation pathways in eukaryotic cells include the autophagy–lysosome pathway, the mitochondrial calpain pathway, and the ubiquitin–proteasome pathway (UPP). Among these, the UPP is the predominant protein degradation pathway in eukaryotic cells and is responsible for the degradation of 80% of normal or aberrant proteins within cells, serving as a key regulatory factor for cellular homeostasis [10]. Ubiquitin (Ub) is a small molecule widely present in eukaryotic cells, consisting of 76 amino acids with a molecular weight of approximately 8.5 kDa. It is highly conserved in evolution. The full-length ubiquitin molecule contains seven lysine (Lys) residues (K6, K11, K27, K33, K48, and K63), a methionine (Met) residue at the N-terminus (M1), and a glycine (Gly) residue at the C-terminus (G76). Plant ubiquitin differs from animal and yeast ubiquitin by only two and three amino acids, respectively [11].
Protein ubiquitination refers to the process of ubiquitin covalently attached to the target protein under the catalysis of a series of enzymes. The “series of enzymes” here refers to three enzymes that synergically participate in the ubiquitination cascade reaction: E1 (ubiquitin-activating enzymes), E2 (ubiquitin-conjugating enzymes), and E3 (ubiquitin ligases) [12]. The transfer of ubiquitin molecules requires the joint participation of E1, E2, and E3 (Figure 1): E1 utilizes the energy provided by ATP to activate ubiquitin molecules to form Ub-E1 complex, which then transfers ubiquitin to E2 through transesterification to form Ub-E2 complex [4]. Ub-E2 complex transfers ubiquitin to target proteins through two pathways. The first pathway involves the direct attachment of the C-terminus of ubiquitin to the Lys residue ε-amino group on the target protein after specific recognition by E3. The second pathway involves transferring ubiquitin to E3 through transesterification, followed by the specific recognition of the target protein by E3, and then attaching the C-terminus of ubiquitin to the Lys residue ε-amino group on the target protein. Finally, most of the ubiquitinated target proteins are degraded by the 26S proteasome, releasing ubiquitin for reuse [13,14]; additionally, some ubiquitinated target proteins are degraded via the autophagy pathway [15]. In summary, under the successive catalysis of E1, E2, and E3 enzymes, ubiquitin is specifically linked to target proteins or to ubiquitin chains already attached to target proteins. Among them, E3 ubiquitin ligase determines the specific recognition of target proteins [16].
The specificity of substrate ubiquitination is primarily determined by the numerous E3 ubiquitin ligases. As enzymes responsible for specifically recognizing target proteins, E3 ligases play a crucial role in protein ubiquitination, making the genes encoding E3 ligases the most abundant among the three enzymes involved in the ubiquitination cascade within the same plant genome. For example, in the genome of Arabidopsis thaliana, approximately 1600 genes, accounting for 6% of the total genome, are associated with the UPS pathway. Among them, the genes encoding E1 are the least with only two, while there are at least 37 genes encoding E2 and E2-like enzymes, and over 1500 genes encoding E3 ligases [14,17]. Based on the structure of E3 ubiquitin ligases, they can be divided into two classes: single-subunit and multi-subunit. Single-subunit E3 ligases include the RING (really interesting new gene), U-box (a modified RING motif without the full complement of Zn2+-binding ligands) domain, HECT (homologous to E6-associated protein C-terminus), and RBR (ring between ring) types. Multi-subunit E3 ligases mainly include the CRLs family (cullin-RING ligases family) and APC/C type (anaphase-promoting complex/cyclosome) [18,19].
The ubiquitin–proteasome pathway is one of the most important pathways for regulating protein abundance within cells, and E3 ubiquitin ligases, as one of the key components of the UPS, have been demonstrated to take crucial regulatory roles in plant responses to abiotic stress. Plant E3 ubiquitin ligases are involved in various abiotic stress responses, primarily including the regulation of plant immune responses [20,21], the promotion of pollen development [22,23], the enhancement of drought tolerance [24,25,26,27], the improvement of salt tolerance [28,29], the enhancement of cold tolerance [30,31], and the enhancement of heat tolerance [32,33].

3. ABA-Related Signaling Pathways

ABA, as one of the nine endogenous hormones in plants, is a plant hormone with a sesquiterpene structure [34]. Natural ABA exists as enantiomers, with the biologically active form being the S-enantiomer (S-ABA) [35,36]. Since its successful discovery by Ohkuma in 1963, the chemical structure, synthesis, and metabolism pathways, as well as the biological functions of ABA, have been reported successively. ABA plays a crucial role in regulating plant growth and development processes [37], such as seed and seedling development, seed dormancy [38], response to pathogens [39], drought [40], high salt, low temperature, and various biotic and abiotic stresses [41].
In 2009, the isolation and functional identification of PYR/PYLs/RCARs-type ABA receptors provided a deeper understanding of the ABA signaling pathway [7,42]. The PYR/PYLs/RCARs family comprises 14 members (PYR1/PYL1-13 or RCAR1-14). It is now widely recognized that PYR/PYLs/RCARs-type receptors play a significant part in the ABA signal transduction pathway [43]. Through the elucidation of protein structures and various biochemical and genetic analyses, it has been revealed that the signaling pathway initiated by PYR/PYLs/RCARs-type receptors involves ABA promoting the inhibition of protein phosphatases PP2Cs (type 2C protein phosphatases) by PYR/PYLs/RCARs, thereby releasing the inhibition of PP2Cs on protein kinase SnRK2s (sucrose non-fermenting 1 (SNF1)-related protein kinase 2s), promoting the phosphorylation modification of SnRK2s substrates, and regulating the expression of ABA-responsive genes [44,45,46]. Various biochemical and omics experiments have identified SnRK2s phosphorylation substrates, including transcription factors located in the nucleus and ion channel proteins on the cell membrane, some of which functionally depend on endocytosis and protein transport processes involving the intracellular membrane system [40,47].
Previous studies using systems biology and other methods have found that ABA signaling networks contain hundreds of interactions between more than 100 proteins, greatly expanding the original ABA signaling pathway. The ABA pathway in plants has now evolved from a simple linear signal to a complex signaling network [48,49]. Among them, the ABA signaling regulatory network (TRAIN) not only includes the traditional PYR/PYL/RCARs→PP2Cs→SnRKs→ABIs/ABFs→target gene signaling pathway, but also direct interactions between PP2Cs and ABIs/ABFs, such as the interaction between PYL8 and the transcription factor MYB49, forming a specific helix–loop–helix structure [48].

4. E3 Ubiquitin Ligases Regulate the ABA Signaling Pathway

E3 ubiquitin ligases, as important enzymes in the ubiquitin–proteasome system, participate in various processes of ABA synthesis, signal reception, signal transduction, and downstream factor response in the ABA pathway [50,51,52]. Different E3 ubiquitin ligases finely regulate the ABA signaling pathway by affecting the stability or activity of various ABA-related factors in different subcellular structures. Furthermore, E3 ubiquitin ligases can also influence the ABA pathway by regulating other phytohormones [53].

4.1. E3 Ubiquitin Ligases Regulate the ABA Biosynthesis and Degradation Metabolism

ABA is a sesquiterpene compound containing 15 carbon atoms, and plants synthesize ABA via the carotenoid pathway [54,55]. Zeaxanthin epoxidase (ZEP), 9-cis-epoxycarotenoid dioxygenase (NCED), and abscisic-aldehyde oxidase (AAO3) are key enzymes in plants responsible for ABA biosynthesis [56].
The generation of ABA signals is crucial for ABA signal transduction, and E3 ubiquitin ligases can regulate the expression of ABA-synthesis-related genes, thereby modulating ABA levels. The overexpression of OsRHP1 (encoding a novel RING-H2 finger protein) in rice increases the expression of key enzymes involved in ABA biosynthesis, such as OsZEP, OsNCED, and OsAAO, significantly enhancing rice drought and salt tolerance [57] (Table 1). XERICO in Arabidopsis encodes a small protein (162 amino acids) with a C-terminal RING-H2 zinc finger domain and induces the upregulation of the ABA biosynthesis gene AtNCED3 under drought conditions, thereby increasing ABA levels in cells [58]. The U-box type E3 ubiquitin ligase SAUL1/AtPUB44 can interact with ABA aldehyde oxidase AAO3, mediating its ubiquitination via the UPP, leading to a reduction in ABA levels [59].
The dynamic balance of ABA synthesis and degradation metabolism in plants collectively regulates endogenous ABA levels. The ABA 8′-hydroxylation pathway is the main route for endogenous ABA metabolism in higher plants. E3 ubiquitin ligases can regulate the stability of ABA-metabolism-related proteins to modulate ABA levels. In maize, the RING-H2-type E3 ubiquitin ligase ZmXerico1 interacts with ZmABA8ox1a and ZmABA8ox3a and destabilizes them, thereby reducing ABA degradation and enhancing maize drought tolerance [60].

4.2. E3 Ubiquitin Ligases Regulate PYR/PYLs/RCARs Receptor Protein Stability

The reception of the ABA signal is crucial for the transduction of the ABA signaling pathway, with E3 ubiquitin ligases playing a significant role in regulating the reception of the ABA signal.
In Arabidopsis, the monomeric RING-type E3 ubiquitin ligase RSL1 (ring finger of seed longevity 1) negatively regulates ABA signaling by promoting the degradation of PYR/PYLs/RCARs-like ABA receptor proteins [61] (Table 2). Conversely, XBAT35 degrades the inner membrane sorting complex component VPS23A, releasing VPS23A’s inhibitory effect on the PYL4 protein, thereby aiding in the activation of the ABA signaling pathway to cope with environmental stresses [52]. U-box type ubiquitin ligases PUB22 and PUB23 interact with the ABA receptor PYL9, leading to the degradation of RCAR1, negatively regulating plant drought tolerance [24]. PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7 [62]. RBR-type E3 ligases RFA1 and RFA4, after interaction with the E2 conjugating enzyme UBC26, bind to ABA receptors such as PYR1 (RCAR11), PYL4 (RCAR10), PYL5 (RCAR8), and PYL8 (RCAR3), thereby negatively regulating ABA signaling by controlling ABA receptor stability [63]. The multi-subunit CULLIN-RING-type E3 ubiquitin ligase substrate receptor protein DDA1 mediates the ubiquitination of PYL8/RCAR3 receptors, negatively regulating ABA signaling [8]. RIFP1 is a subunit of the SCF (SKP1/Cullin/F-box) complex E3 ligase, which ubiquitinates RCAR3, thus regulating RCAR3 levels after drought stress [64]. The CUL4-DDB1-DWD-type E3 ubiquitin ligase AtRAE1 similarly ubiquitinates RCAR1 and negatively regulates the ABA signaling pathway [65].

4.3. E3 Ubiquitin Ligases Regulate PP2Cs Phosphatase Activity

In addition to regulating the reception of ABA signals, E3 ubiquitin ligases also participate in ABA signal transduction. PP2C-type phosphatases serve as co-receptors for ABA signal reception, responding to ABA signals alongside PYR/PYLs/RCARs-type ABA receptors [66]. The PP2C-type phosphatase ABI1 protein can be degraded by the 26S proteasome. Two members of the U-box family, PUB12 and PUB13, participate in the process of 26S proteasome-mediated degradation of the ABI1 protein, with PUB12 and PUB13 only ubiquitinating ABI1 in the presence of both ABA and PYR1 [67] (Table 3).
In Arabidopsis, the RING-type E3 ubiquitin ligase RGLG1 can respond to increased ABA and its target levels, altering its subcellular localization and promoting nuclear interaction with PP2CA, therefore enhancing PP2CA degradation [68]. RGLG5, by mediating the ubiquitination degradation of PP2CA, promotes the activation mechanism of the ABA signaling pathway, enhancing Arabidopsis drought tolerance [69]. PIR1 (PP2CA-interacting RING finger protein 1) and PIR2 positively regulate ABA signal transduction by targeting the degradation of PP2CA [70]. AIRP3 can form an E2–E3 pair with the E2-conjugating enzyme UBC27, and both AIRP3 and UBC27 interact with ABI1, affecting the ubiquitination and degradation of ABI1 [71]. COP1 interacts with ABI/HAB and AHG3, leading to their ubiquitination, and is a key participant in ABA signal transduction, providing a new pathway for regulating stomatal closure in Arabidopsis [72]. In pepper (Capsicum annuum), the E3 ligase CaAIRF1 interacts with CaADIP1 and ubiquitinates it, positively regulating ABA signaling [73]. OsRF1 (RING finger E3 ligase 1) in rice is a novel small RING-H2 type E3 ligase, positively regulating ABA signal transduction by targeting the degradation of OsPP2C09, increasing ABA biosynthesis, and, thus, responding to drought and salt stress [74]. Different E3 ubiquitin ligases affect ABA signaling by influencing PP2Cs activity.

4.4. E3 Ubiquitin Ligases Regulate SnRK2s Kinase Activity

The transition of SnRK2s from an inactive dephosphorylated state to an activated state within plant cells is a crucial step in the response to ABA and environmental stress. The regulation of SnRK2s kinase activity by E3 ubiquitin ligases significantly impacts ABA signal transduction.
In Arabidopsis, AtPP2-B11 is a part of the SCF E3 ubiquitin ligase complex and can specifically promote the degradation of SnRK2.3 to negatively regulate the plant response to ABA [75] (Table 4). HOS15 is a substrate receptor of the CUL4-DDB1-type E3 ubiquitin ligase, which interacts specifically with OST1, SnRK2.3, and ABI1/2. HOS15 negatively regulates ABA signal transduction and drought stress resistance by interfering with the stability of OST1 [76]. In cucumber, a RING-type E3 ligase, CsCHYR1, exhibits auto-ubiquitination activity. CsCHYR1 interacts with CsSnRK2.6 and CsATAF1, forming a regulatory model, CsSnRK2.6-CsCHYR1-CsATAF, which regulates plant response to drought stress through an ABA-dependent pathway [51].

4.5. E3 Ubiquitin Ligases Regulate ABIs/ABFs and Other Downstream Response Transcription Factors

ABA signals are transmitted sequentially and eventually reach the nucleus, activating or inhibiting the activity of various transcription factors to initiate the expression of downstream response genes [77]. Different types of E3 ubiquitin ligases can regulate ABA response gene expression either positively or negatively, thereby influencing ABA pathway transduction.

4.5.1. RING Type

In Arabidopsis, the RING-type E3 ligase AtAIRP3/LOG2 (Lonely Guy 2) interacts with RD21 and acts as a positive regulator of ABA signaling, promoting UPS-dependent degradation of ABI5 and other bZIP TFs downstream [78,79] (Table 5). ABI3 can be degraded by the 26S proteasome, and AIP2 (ABI3-Interacting Protein2) interacts with ABI3 and FUS3 (FUSCA3), mediating the ubiquitination of ABI3 both in vivo and in vitro, thus negatively regulating ABA signaling [80,81,82]. The accumulation of AtMBP-1 is limited by ubiquitin-dependent instability, which is regulated by interaction with AtSAP5. The E3 ubiquitin ligase AtSAP5 promotes UPS degradation of AtMBP-1 upstream of ABI5, ABI3, and ABI4 [83]. Arabidopsis ATLs comprise a special group of RING-type E3 ubiquitin ligases involved in abiotic stress responses. The transcription of ATL78 is regulated by ABA as well as drought, salt, and cold stress. ATL78 modulates ABA-dependent stomatal closure and the accumulation of reactive oxygen species (ROS) during drought stress, positively regulating the ABA signaling pathway [84,85]. SDIR1 is an endoplasmic reticulum membrane-localized ABA-positive regulator that interacts with SDIRIP1 (SDIR1-interacting protein 1) and ubiquitinates it, and then regulates the stability of SDIRIP1 via the UPP [86]. Moreover, SDIRIP1 can be ubiquitinated by AIRP2 as a target, further positively responding to ABA signaling [87]. In wild-type Arabidopsis, the E3 ubiquitin ligase AtAIRP5/GARU plays a role as a positive regulator of ABA-mediated drought response by promoting the degradation of AtSCPL1 (serine carboxypeptidase-like1) [88]. The protein kinase CIPK26 serves as a ubiquitination substrate of the E3 ubiquitin ligase KEG (keep on going), which negatively regulates the ABA signal by mediating the degradation of CIPK26 via the proteasome pathway [89]. Moreover, KEG may also mediate the ubiquitination degradation of bZIP TFs ABI5, ABF1, and ABF3 [90]. MYB96 can directly regulate the expression of ABI4, while MIEL1 negatively regulates ABA sensitivity by promoting the turnover of MYB96 [91,92]. MIEL1 also directly mediates the proteasomal degradation of ABI5 and inhibits its activity by releasing its target protein MYB30, thus precisely controlling ABA signal transduction during seed germination and seedling establishment [93]. Moreover, in Arabidopsis, there exists a E3 ubiquitin ligase SINA2 (SEVEN IN ABSENTIA 2), lacking the classical RING domain but containing a B-box domain, which interacts with a nuclear protein CDKG1 (cyclin-dependent kinase G1) and positively regulates plant response to ABA and osmotic stress [94].
In addition to Arabidopsis, E3 ubiquitin ligase has also been reported to be involved in regulating the ABA pathway in other plants. In rice, the RING-type E3 ligase OsCTR1 mediates drought tolerance by targeting the degradation of OsCP12 and OsRP1 and regulating their subcellular transport in an ABA-dependent manner [95]. In wheat, the RING-HC zinc finger protein TaDIS1 mediates the drought stress response by interacting with TaSTP, and the overexpression of TaDIS1 leads to increased sensitivity to ABA [96]. TaSDIR1-4A encodes a C3H2C3-type RING E3 ligase that mediates the C-terminal ubiquitination and proteolysis of TaWRKY29, transporting it from the plasma membrane to the nucleus. Activated TaWRKY29 binds to the TaABI5 promoter, stimulating its expression, positively regulating the ABA signaling pathway and drought response [97]. In chili pepper, CaASRF1 positively regulates ABA signal transduction and drought stress response by modulating the stability of CaAIBZ1 and CaATBZ1 [98,99]. Furthermore, the stability of CaATBZ1 mediated by CaATIR1 plays a crucial role in drought stress signal transduction. By degrading CaAIBZ1 and CaATBZ1, it positively regulates ABA signal transduction and enhances drought tolerance [90]. In maize, the RING-H2 type E3 ubiquitin ligase ZmWIPF2 interacts with ZmCCT, negatively regulating ABA signaling [100].

4.5.2. U-Box Type

In Arabidopsis, U-box E3 ligase AtPUB9 is a nucleus-localized negative regulator of ABA and plays a role upstream of ABI3 [101]. PUB8 interacts with ABI3 and ABI5 and negatively regulates ABA responses during early growth of Arabidopsis seedling [102]. In rice, MODD (Mediator of OsbZIP46 deactivation and degradation) interacts with the OsPUB70 to promote the degradation of OsbZIP46 and inhibit the expression of OsbZIP46 target genes, negatively regulating ABA signal transduction and drought resistance [103]. On the other hand, OsHUB2, an E3 ligase for H2Bub1, interacts with OsbZIP46 as a positive regulator of ABA signal transduction and drought response [104]. Apple MdABI5, through the MdABI5-MdbHLH93-MdSAG18 regulatory module, accelerates leaf senescence, while U-box-type E3 ubiquitin ligase MdPUB23 interacts with MdABI5 to delay leaf senescence triggered by ABA [50]. In addition, CaPUB24 in chili negatively regulates drought stress response in an ABA-dependent manner, but the specific genes in the ABA signaling pathway it regulates are not known [105].

4.5.3. HECT Type

The RING-type E3 ligases have been extensively studied in different stages of ABA signaling, while HECT-type E3 ligases have been least studied in various stages of ABA signaling. In Arabidopsis, the HECT-type UPL1 and UPL4, as well as the RING-type KEG, can ubiquitinate MAPKKK17/18 and promote their degradation, negatively regulating the ABA signal [106].

4.5.4. CRLs Type

Arabidopsis DWA1/DWA2 (DWD is allergic to ABA1/2) encodes a substrate receptor for CUL4 type E3 ligase, interacts with ABI5 in vivo, and targets its degradation, thereby negatively regulating ABA signaling [107]. ABD1 (ABA-hypersensitive DCAF1), a component of the DCAF-CUL4-type E3 ubiquitin ligase complex, directly binds to ABI5 and influences its stability in the nucleus, negatively modulating Arabidopsis ABA signaling [108]. MATH-BTB proteins are substrate-binding receptors for Cullin3-based E3 ubiquitin ligases. MATH-BTB proteins directly interact with the transcription factor ATHB6, targeting it for proteasomal degradation and positively regulating ABA signaling [109].
There are numerous E3 ubiquitin ligases in the plant genome, and the different types of E3 mentioned above regulate ABA signaling by affecting the expression of related genes at different stages of the ABA signaling pathway (Figure 2), which helps plants to better adapt to the adverse environment and maintain normal growth and development.

5. Conclusions and Outlook

Throughout their lifecycle, plants constantly face abiotic stresses. To cope with a range of stress responses, plants have evolved corresponding defense mechanisms to maintain normal growth and development. E3 ubiquitin ligases, as vital components of the ubiquitin–proteasome pathway, comprise a large and functionally complex family. They are currently a focal point in the study of plant growth, development, and stress response mechanisms. ABA is a crucial phytohormone in plants for combating environmental stresses. While the core signaling pathway model of ABA has been established, the ABA signaling transduction network is quite complex, and the response mechanisms of its signal pathways still need refinement. To further unravel the defense mechanisms of plants against abiotic stresses, research on E3 ubiquitin ligases in the ABA signaling pathway is indispensable. While a significant number of E3 ubiquitin ligases have been found to play important roles in the ABA pathway, only a few have been fully elucidated. Many functions and mechanisms of E3 ligases remain unclear, especially for non-RING types, which have been less studied. Future research will continue to explore various aspects of this field. With the in-depth study of the ABA signaling pathway, it is believed that more E3 ubiquitin ligases will be discovered and analyzed in depth. We still need to employ a plethora of methods such as molecular biology, genetics, protein–protein interactions, and omics to uncover the specific targets and regulatory mechanisms of different types of E3 ubiquitin ligases in the ABA signaling pathway. This analysis aims to elucidate their roles in plant growth, development, and response to environmental stresses, laying the groundwork for the development of crops with higher tolerance to environmental stress.
Additionally, E3 ubiquitin ligases can also regulate other endogenous hormone pathways, contributing to plant defense against abiotic stresses by modulating the interactions between other endogenous hormones and ABA. Current research has reported on E3 ubiquitin ligases regulating the interaction between ABA and JA (jasmonic acid) [53] and GA (gibberellic acid) [110] in plant biological processes, but the functional and mechanistic analyses are still incomplete. In future studies, we should strengthen research in this area using new tools and methods. Simultaneously, the development of new drugs targeting plant E3 ubiquitin ligases can be explored to regulate plant growth, development, and stress resistance, providing new strategies to enhance plant stress resilience and improve crop yield and quality. In conclusion, future research will further reveal the important role of plant E3 ubiquitin ligases in the ABA pathway, providing new insights into understanding plant growth, development, and adaptation to the environment, and offering innovative solutions for agricultural production.

Author Contributions

This review was organized by H.K. and X.Z., J.J., M.X., J.W., L.M. and A.M.B. helped with the collection of materials and manuscript revision. H.K. wrote the draft. X.S. and X.Z. conceived the study and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (32372181), the Agricultural Seed Projects of Shandong Province (2023LZGC007), the Modern Agro-industry Technology Research System of Shandong Province (SDAIT-03-04/06), and the Natural Science Foundation of Shandong Province (ZR2023QC049).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors thank the National Center of Technology Innovation for Comprehensive Utilization of Saline-Alkali Land for providing research platform, Dongying, China, which made equal contribution to this work as Shandong Agricultural University.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Knight, H.; Knight, M.R. Abiotic stress signalling pathways: Specificity and cross-talk. Trends Plant Sci. 2001, 6, 262–267. [Google Scholar] [CrossRef] [PubMed]
  2. Saharan, B.S.; Brar, B.; Duhan, J.S.; Kumar, R.; Marwaha, S.; Rajput, V.D.; Minkina, T. Molecular and Physiological Mechanisms to Mitigate Abiotic Stress Conditions in Plants. Life 2022, 12, 1634. [Google Scholar] [CrossRef] [PubMed]
  3. Xu, F.-Q.; Xue, H.-W. The ubiquitin-proteasome system in plant responses to environments. Plant Cell Environ. 2019, 42, 2931–2944. [Google Scholar] [CrossRef] [PubMed]
  4. Isono, E.; Nagel, M.-K. Deubiquitylating enzymes and their emerging role in plant biology. Front. Plant Sci. 2014, 5, 56. [Google Scholar] [CrossRef] [PubMed]
  5. Yang, Q.; Zhao, J.; Chen, D.; Wang, Y. E3 ubiquitin ligases: Styles, structures and functions. Mol. Biomed. 2021, 2, 1–17. [Google Scholar] [CrossRef] [PubMed]
  6. Ying, W.; Liao, L.; Wei, H.; Gao, Y.; Liu, X.; Sun, L. Structural basis for abscisic acid efflux mediated by ABCG25 in Arabidopsis thaliana. Nat. Plants 2023, 9, 1697–1708. [Google Scholar] [CrossRef]
  7. Park, S.-Y.; Fung, P.; Nishimura, N.; Jensen, D.R.; Fujii, H.; Zhao, Y.; Lumba, S.; Santiago, J.; Rodrigues, A.; Chow, T.-F.F.; et al. Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science 2009, 324, 1068–1071. [Google Scholar] [CrossRef]
  8. Irigoyen, M.L.; Iniesto, E.; Rodriguez, L.; Puga, M.I.; Yanagawa, Y.; Pick, E.; Strickland, E.; Paz-Ares, J.; Wei, N.; De Jaeger, G.; et al. Correction to: Targeted Degradation of Abscisic Acid Receptors Is Mediated by the Ubiquitin Ligase Substrate Adaptor DDA1 in Arabidopsis. Plant Cell 2022, 34, 2807–2808. [Google Scholar] [CrossRef] [PubMed]
  9. Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef]
  10. Marshall, R.S.; Vierstra, R.D. Dynamic Regulation of the 26S Proteasome: From Synthesis to Degradation. Front. Mol. Biosci. 2019, 6, 40. [Google Scholar] [CrossRef]
  11. Kwon, Y.T.; Ciechanover, A. The Ubiquitin Code in the Ubiquitin-Proteasome System and Autophagy. Trends Biochem. Sci. 2017, 42, 873–886. [Google Scholar] [CrossRef] [PubMed]
  12. Morreale, F.E.; Walden, H. Types of ubiquitin ligases. Cell 2016, 165, 248–248.e1. [Google Scholar] [CrossRef] [PubMed]
  13. Stone, S.L. Role of the ubiquitin proteasome system in plant response to abiotic stress. Int. Rev. Cell Mol. Biol. 2019, 343, 65–110. [Google Scholar]
  14. Vierstra, R.D. The ubiquitin–26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 2009, 10, 385–397. [Google Scholar] [CrossRef] [PubMed]
  15. Chen, R.-H.; Chen, Y.-H.; Huang, T.-Y. Ubiquitin-mediated regulation of autophagy. J. Biomed. Sci. 2019, 26, 1–12. [Google Scholar] [CrossRef] [PubMed]
  16. Nagels Durand, A.; Pauwels, L.; Goossens, A. The ubiquitin uystem and jasmonate Signaling. Plants 2016, 5, 6. [Google Scholar] [CrossRef] [PubMed]
  17. Vierstra, R.D. The Expanding Universe of Ubiquitin and Ubiquitin-Like Modifiers. Plant Physiol. 2012, 160, 2–14. [Google Scholar] [CrossRef] [PubMed]
  18. Al-Saharin, R.; Mooney, S.; Dissmeyer, N.; Hellmann, H. Using CRL3BPM E3 ligase substrate recognition sites as tools to impact plant development and stress tolerance in Arabidopsis thaliana. Plant Direct 2022, 6, e474. [Google Scholar] [CrossRef] [PubMed]
  19. Callis, J. The Ubiquitination Machinery of the Ubiquitin System. Arab. Book 2014, 12, e0174. [Google Scholar] [CrossRef] [PubMed]
  20. Yang, L.; Zhao, M.; Zhang, X.; Jiang, J.; Fei, N.; Ji, W.; Ye, Y.; Guan, W.; Yang, Y.; Zhao, T. Acidovorax citrulli type III effector AopU interferes with plant immune responses and interacts with a watermelon E3 ubiquitin ligase. Front. Microbiol. 2023, 14, 1275032. [Google Scholar] [CrossRef]
  21. Han, P.-L.; Dong, Y.-H.; Gu, K.-D.; Yu, J.-Q.; Hu, D.-G.; Hao, Y.-J. The apple U-box E3 ubiquitin ligase MdPUB29 con-tributes to activate plant immune response to the fungal pathogen Botryosphaeria dothidea. Planta 2019, 249, 1177–1188. [Google Scholar] [CrossRef] [PubMed]
  22. Tian, A.; Yu, H.; Cui, Z. Functional characterization of E3 ubiquity ligase Bra015092 in pollen development of Brassica campestris ssp. Chinensis. Physiol. Plant. 2022, 174, e13808. [Google Scholar] [CrossRef] [PubMed]
  23. Cao, H.; Li, X.; Wang, Z.; Ding, M.; Sun, Y.; Dong, F.; Chen, F.; Liu, L.; Doughty, J.; Li, Y.; et al. Histone H2B Monoubiquitination Mediated by HISTONE MONOUBIQUITINATION1 and HISTONE MONOUBIQUITINATION2 Is Involved in Anther Development by Regulating Tapetum Degradation-Related Genes in Rice. Plant Physiol. 2015, 168, 1389–1405. [Google Scholar] [CrossRef] [PubMed]
  24. Zhao, J.; Zhao, L.; Zhang, M.; Zafar, S.A.; Fang, J.; Li, M.; Zhang, W.; Li, X. Arabidopsis E3 Ubiquitin Ligases PUB22 and PUB23 Negatively Regulate Drought Tolerance by Targeting ABA Receptor PYL9 for Degradation. Int. J. Mol. Sci. 2017, 18, 1841. [Google Scholar] [CrossRef]
  25. Yang, L.; Liu, Q.; Liu, Z.; Yang, H.; Wang, J.; Li, X.; Yang, Y. Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling. J. Integr. Plant Biol. 2015, 58, 67–80. [Google Scholar] [CrossRef] [PubMed]
  26. Xia, Z.; Liu, Q.; Wu, J.; Ding, J. ZmRFP1, the putative ortholog of SDIR1, encodes a RING-H2 E3 ubiquitin ligase and responds to drought stress in an ABA-dependent manner in maize. Gene 2011, 495, 146–153. [Google Scholar] [CrossRef] [PubMed]
  27. Yang, L.; Wu, L.; Chang, W.; Li, Z.; Miao, M.; Li, Y.; Yang, J.; Liu, Z.; Tan, J. Overexpression of the maize E3 ubiquitin ligase gene ZmAIRP4 enhances drought stress tolerance in Arabidopsis. Plant Physiol. Biochem. 2018, 123, 34–42. [Google Scholar] [CrossRef]
  28. Du, B.; Nie, N.; Sun, S.; Hu, Y.; Bai, Y.; He, S.; Zhao, N.; Liu, Q.; Zhai, H. A novel sweetpotato RING-H2 type E3 ubiquitin ligase gene IbATL38 enhances salt tolerance in transgenic Arabidopsis. Plant Sci. 2021, 304, 110802. [Google Scholar] [CrossRef] [PubMed]
  29. Wang, W.; Wang, W.; Wu, Y.; Li, Q.; Zhang, G.; Shi, R.; Yang, J.; Wang, Y.; Wang, W. The involvement of wheat U-box E3 ubiquitin ligase TaPUB1 in salt stress tolerance. J. Integr. Plant Biol. 2019, 62, 631–651. [Google Scholar] [CrossRef]
  30. Jiang, B.; Shi, Y.; Peng, Y.; Jia, Y.; Yan, Y.; Dong, X.; Li, H.; Dong, J.; Li, J.; Gong, Z.; et al. Cold-Induced CBF–PIF3 Interaction Enhances Freezing Tolerance by Stabilizing the phyB Thermosensor in Arabidopsis. Mol. Plant 2020, 13, 894–906. [Google Scholar] [CrossRef]
  31. Min, H.J.; Jung, Y.J.; Kang, B.G.; Kim, W.T. CaPUB1, a hot pepper U-box E3 ubiquitin ligase, confers enhanced cold stress tolerance and decreased drought stress tolerance in transgenicrice (Oryza sativa L.). Mol. Cells 2016, 39, 250–257. [Google Scholar] [CrossRef] [PubMed]
  32. Peng, L.; Wan, X.; Huang, K.; Pei, L.; Xiong, J.; Li, X.; Wang, J. AtPUB48 E3 ligase plays a crucial role in the thermotolerance of Arabidopsis. Biochem. Biophys. Res. Commun. 2018, 509, 281–286. [Google Scholar] [CrossRef]
  33. Li, Q.; Wang, W.; Wang, W.; Zhang, G.; Liu, Y.; Wang, Y.; Wang, W. Wheat F-box protein gene TaFBA1 is involved in plant tolerance to heat stress. Front. Plant Sci. 2018, 9, 521. [Google Scholar] [CrossRef]
  34. Waadt, R.; Seller, C.A.; Hsu, P.-K.; Takahashi, Y.; Munemasa, S.; Schroeder, J.I. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 2022, 23, 680–694. [Google Scholar] [CrossRef] [PubMed]
  35. Sah, S.K.; Reddy, K.R.; Li, J. Abscisic Acid and Abiotic Stress Tolerance in Crop Plants. Front. Plant Sci. 2016, 7, 571. [Google Scholar] [CrossRef] [PubMed]
  36. Yao, C.; Zhang, F.; Sun, X.; Shang, D.; He, F.; Li, X.; Zhang, J.; Jiang, X. Effects of S-abscisic acid (S-ABA) on seed germi-nation, seedling growth, and Asr1 gene expression under drought stress in maize. J. Plant Growth Regul. 2019, 38, 1300–1313. [Google Scholar] [CrossRef]
  37. Ohkuma, K.; Lyon, J.L.; Addicott, F.T.; Smith, O.E. Abscisin II, an Abscission-Accelerating Substance from Young Cotton Fruit. Science 1963, 142, 1592–1593. [Google Scholar] [CrossRef] [PubMed]
  38. Shu, K.; Liu, X.-D.; Xie, Q.; He, Z.-H. Two Faces of One Seed: Hormonal Regulation of Dormancy and Germination. Mol. Plant 2015, 9, 34–45. [Google Scholar] [CrossRef] [PubMed]
  39. Han, X.; Kahmann, R. Manipulation of Phytohormone Pathways by Effectors of Filamentous Plant Pathogens. Front. Plant Sci. 2019, 10, 822. [Google Scholar] [CrossRef]
  40. Aslam, M.M.; Waseem, M.; Jakada, B.H.; Okal, E.J.; Lei, Z.; Saqib, H.S.A.; Yuan, W.; Xu, W.; Zhang, Q. Mechanisms of Abscisic Acid-Mediated Drought Stress Responses in Plants. Int. J. Mol. Sci. 2022, 23, 1084. [Google Scholar] [CrossRef]
  41. Bharath, P.; Gahir, S.; Raghavendra, A.S. Abscisic Acid-Induced Stomatal Closure: An Important Component of Plant Defense Against Abiotic and Biotic Stress. Front. Plant Sci. 2021, 12, 615114. [Google Scholar] [CrossRef]
  42. Ma, Y.; Szostkiewicz, I.; Korte, A.; Moes, D.; Yang, Y.; Christmann, A.; Grill, E. Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors. Science 2009, 324, 1064–1068. [Google Scholar] [CrossRef]
  43. Gonzalez-Guzman, M.; Pizzio, G.A.; Antoni, R.; Vera-Sirera, F.; Merilo, E.; Bassel, G.W.; Fernández, M.A.; Holdsworth, M.J.; Perez-Amador, M.A.; Kollist, H.; et al. Arabidopsis PYR/PYL/RCAR receptors play a major role in quan-titative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 2012, 24, 2483–2496. [Google Scholar] [CrossRef] [PubMed]
  44. Hong, Y.; Yao, J.; Shi, H.; Chen, Y.; Zhu, J.-K.; Wang, Z. The Arabidopsis spliceosomal protein SmEb modulates ABA responses by maintaining proper alternative splicing of HAB1. Stress Biol. 2021, 1, 4. [Google Scholar] [CrossRef] [PubMed]
  45. Zhao, H.; Nie, K.; Zhou, H.; Yan, X.; Zhan, Q.; Zheng, Y.; Song, C.-P. ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes. New Phytol. 2020, 228, 596–608. [Google Scholar] [CrossRef]
  46. Dittrich, M.; Mueller, H.M.; Bauer, H.; Peirats-Llobet, M.; Rodriguez, P.L.; Geilfus, C.-M.; Carpentier, S.C.; Al Rasheid, K.A.S.; Kollist, H.; Merilo, E.; et al. The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nat. Plants 2019, 5, 1002–1011. [Google Scholar] [CrossRef] [PubMed]
  47. Takahashi, Y.; Zhang, J.; Hsu, P.-K.; Ceciliato, P.H.O.; Zhang, L.; Dubeaux, G.; Munemasa, S.; Ge, C.; Zhao, Y.; Hauser, F.; et al. MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat. Commun. 2020, 11, 12. [Google Scholar] [CrossRef]
  48. Lumba, S.; Toh, S.; Handfield, L.-F.; Swan, M.; Liu, R.; Youn, J.-Y.; Cutler, S.R.; Subramaniam, R.; Provart, N.; Moses, A.; et al. A Mesoscale Abscisic Acid Hormone Interactome Reveals a Dynamic Signaling Landscape in Arabidopsis. Dev. Cell 2014, 29, 360–372. [Google Scholar] [CrossRef] [PubMed]
  49. Xing, W.; Pi, Z.; Liu, J.; Li, X.; Zou, Y.; Wang, M.; Liu, D.; Wang, Q.; Wu, Z. Comparative transcriptome analysis reveals an ABA-responsive regulation network associated with cell wall organization and oxidation reduction in sugar beet. Plant Growth Regul. 2020, 91, 127–141. [Google Scholar] [CrossRef]
  50. Yang, F.; Zhao, L.-L.; Song, L.-Q.; Han, Y.; You, C.-X.; An, J.-P. Apple E3 ligase MdPUB23 mediates ubiquitin-dependent degradation of MdABI5 to delay ABA-triggered leaf senescence. Hortic. Res. 2024, 11, uhae029. [Google Scholar] [CrossRef]
  51. Guo, L.; Cao, M.; Li, Y.; Wang, J.; He, L.; Li, P.; Lin, X.; Li, X.; Yuan, X.; Zhao, B.; et al. RING finger ubiquitin E3 ligase CsCHYR1 targets CsATAF1 for degradation to modulate the drought stress response of cucumber through the ABA-dependent pathway. Plant Physiol. Biochem. 2023, 202, 107928. [Google Scholar] [CrossRef] [PubMed]
  52. Yu, F.; Cao, X.; Liu, G.; Wang, Q.; Xia, R.; Zhang, X.; Xie, Q. ESCRT-I Component VPS23A Is Targeted by E3 Ubiquitin Ligase XBAT35 for Proteasome-Mediated Degradation in Modulating ABA Signaling. Mol. Plant 2020, 13, 1556–1569. [Google Scholar] [CrossRef] [PubMed]
  53. Koh, H.; Joo, H.; Lim, C.W.; Lee, S.C. Roles of the pepper JAZ protein CaJAZ1-03 and its interacting partner RING-type E3 ligase CaASRF1 in regulating ABA signaling and drought responses. Plant Cell Environ. 2023, 46, 3242–3257. [Google Scholar] [CrossRef] [PubMed]
  54. Endo, A.; Okamoto, M.; Koshiba, T. ABA biosynthetic and catabolic pathways. In Abscisic Acid: Metabolism, Transport and Signaling; Springer: Dordrecht, The Netherlands, 2014; pp. 21–45. [Google Scholar]
  55. Xiong, L.; Zhu, J.-K. Regulation of Abscisic Acid Biosynthesis. Plant Physiol. 2003, 133, 29–36. [Google Scholar] [CrossRef] [PubMed]
  56. Dejonghe, W.; Okamoto, M.; Cutler, S.R. Small Molecule Probes of ABA Biosynthesis and Signaling. Plant Cell Physiol. 2018, 59, 1490–1499. [Google Scholar] [CrossRef] [PubMed]
  57. Zeng, D.-E.; Hou, P.; Xiao, F.; Liu, Y. Overexpressing a novel RING-H2 finger protein gene, OsRHP1, enhances drought and salt tolerance in rice (Oryza sativa L.). J. Plant Biol. 2014, 57, 357–365. [Google Scholar] [CrossRef]
  58. Ko, J.; Yang, S.H.; Han, K. Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. 2006, 47, 343–355. [Google Scholar] [CrossRef] [PubMed]
  59. Raab, S.; Drechsel, G.; Zarepour, M.; Hartung, W.; Koshiba, T.; Bittner, F.; Hoth, S. Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J. 2009, 59, 39–51. [Google Scholar] [CrossRef]
  60. Brugière, N.; Zhang, W.; Xu, Q.; Scolaro, E.J.; Lu, C.; Kahsay, R.Y.; Kise, R.; Trecker, L.; Williams, R.W.; Hakimi, S.; et al. Overexpression of RING Domain E3 Ligase ZmXerico1 Confers Drought Tolerance through Regulation of ABA Homeostasis. Plant Physiol. 2017, 175, 1350–1369. [Google Scholar] [CrossRef]
  61. Belda-Palazon, B.; Rodriguez, L.; Fernandez, M.A.; Castillo, M.-C.; Anderson, E.M.; Gao, C.; Gonzalez-Guzman, M.; Pei-rats-Llobet, M.; Zhao, Q.; De Winne, N.; et al. FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant Cell 2016, 28, 2291–2311. [Google Scholar] [CrossRef]
  62. Chen, X.; Wang, T.; Rehman, A.U.; Wang, Y.; Qi, J.; Li, Z.; Song, C.; Wang, B.; Yang, S.; Gong, Z. Arabidopsis U-box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7. J. Integr. Plant Biol. 2021, 63, 494–509. [Google Scholar] [CrossRef] [PubMed]
  63. Fernandez, M.A.; Belda-Palazon, B.; Julian, J.; Coego, A.; Lozano-Juste, J.; Iñigo, S.; Rodriguez, L.; Bueso, E.; Goossens, A.; Rodriguez, P.L. RBR-Type E3 Ligases and the Ubiquitin-Conjugating Enzyme UBC26 Regulate Abscisic Acid Receptor Levels and Signaling. Plant Physiol. 2019, 182, 1723–1742. [Google Scholar] [CrossRef]
  64. Li, Y.; Zhang, L.; Li, D.; Liu, Z.; Wang, J.; Li, X.; Yang, Y. The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signalling by facilitating ABA receptor RCAR3 degradation. Plant Cell Environ. 2015, 39, 571–582. [Google Scholar] [CrossRef]
  65. Li, D.; Zhang, L.; Li, X.; Kong, X.; Wang, X.; Li, Y.; Liu, Z.; Wang, J.; Li, X.; Yang, Y. AtRAE1 is involved in degradation of ABA receptor RCAR1 and negatively regulates ABA signalling in Arabidopsis. Plant Cell Environ. 2017, 41, 231–244. [Google Scholar] [CrossRef]
  66. Coego, A.; Julian, J.; Lozano-Juste, J.; Pizzio, G.A.; Alrefaei, A.F.; Rodriguez, P.L. Ubiquitylation of ABA Receptors and Protein Phosphatase 2C Coreceptors to Modulate ABA Signaling and Stress Response. Int. J. Mol. Sci. 2021, 22, 7103. [Google Scholar] [CrossRef]
  67. Kong, L.; Cheng, J.; Zhu, Y.; Ding, Y.; Meng, J.; Chen, Z.; Xie, Q.; Guo, Y.; Li, J.; Yang, S.; et al. Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat. Commun. 2015, 6, 8630. [Google Scholar] [CrossRef]
  68. Belda-Palazon, B.; Julian, J.; Coego, A.; Wu, Q.; Zhang, X.; Batistic, O.; Alquraishi, S.A.; Kudla, J.; An, C.; Rodriguez, P.L. ABA inhibits myristoylation and induces shuttling of the RGLG1 E3 ligase to promote nuclear degradation of PP2CA. Plant J. 2019, 98, 813–825. [Google Scholar] [CrossRef] [PubMed]
  69. Wu, Q.; Zhang, X.; Peirats-Llobet, M.; Belda-Palazon, B.; Wang, X.; Cui, S.; Yu, X.; Rodriguez, P.L.; An, C. Ubiquitin Ligases RGLG1 and RGLG5 Regulate Abscisic Acid Signaling by Controlling the Turnover of Phosphatase PP2CA. Plant Cell 2016, 28, 2178–2196. [Google Scholar] [CrossRef] [PubMed]
  70. Baek, W.; Lim, C.W.; Luan, S.; Lee, S.C. The RING finger E3 ligases PIR1 and PIR2 mediate PP2CA degradation to enhance abscisic acid response in Arabidopsis. Plant J. 2019, 100, 473–486. [Google Scholar] [CrossRef]
  71. Pan, W.; Lin, B.; Yang, X.; Liu, L.; Xia, R.; Li, J.; Wu, Y.; Xie, Q. The UBC27–AIRP3 ubiquitination complex modulates ABA signaling by promoting the degradation of ABI1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 2020, 117, 27694–27702. [Google Scholar] [CrossRef]
  72. Chen, Q.; Bai, L.; Wang, W.; Shi, H.; Botella, J.R.; Zhan, Q.; Liu, K.; Yang, H.; Song, C. COP1 promotes ABA-induced stomatal closure by modulating the abundance of ABI/HAB and AHG3 phosphatases. New Phytol. 2020, 229, 2035–2049. [Google Scholar] [CrossRef] [PubMed]
  73. Lim, C.W.; Baek, W.; Lee, S.C. The Pepper RING-Type E3 Ligase CaAIRF1 Regulates ABA and Drought Signaling via CaADIP1 Protein Phosphatase Degradation. Plant Physiol. 2017, 173, 2323–2339. [Google Scholar] [CrossRef] [PubMed]
  74. Kim, S.; Park, S.-I.; Kwon, H.; Cho, M.H.; Kim, B.-G.; Chung, J.H.; Nam, M.H.; Song, J.S.; Kim, K.-H.; Yoon, I.S. The rice abscisic acid-responsive RING finger E3 ligase OsRF1 targets OsPP2C09 for degradation and donfers drought and salinity tolerance in rice. Front. Plant Sci. 2021, 12, 797940. [Google Scholar]
  75. Cheng, C.; Wang, Z.; Ren, Z.; Zhi, L.; Yao, B.; Su, C.; Liu, L.; Li, X. SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet. 2017, 13, e1006947. [Google Scholar] [CrossRef] [PubMed]
  76. Ali, A.; Kim, J.K.; Jan, M.; Khan, H.A.; Khan, I.U.; Shen, M.; Park, J.; Lim, C.J.; Hussain, S.; Baek, D.; et al. Rheostatic Control of ABA Signaling through HOS15-Mediated OST1 Degradation. Mol. Plant 2019, 12, 1447–1462. [Google Scholar] [CrossRef] [PubMed]
  77. Raghavendra, A.S.; Gonugunta, V.K.; Christmann, A.; Grill, E. ABA perception and signalling. Trends Plant Sci. 2010, 15, 395–401. [Google Scholar] [CrossRef] [PubMed]
  78. Kim, J.H.; Kim, W.T. The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol. 2013, 162, 1733–1749. [Google Scholar] [CrossRef] [PubMed]
  79. Koizumi, M.; Yamaguchi-Shinozaki, K.; Tsuji, H.; Shinozaki, K. Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 1993, 129, 175–182. [Google Scholar] [CrossRef] [PubMed]
  80. Duong, S.; Vonapartis, E.; Li, C.-Y.; Patel, S.; Gazzarrini, S. The E3 ligase ABI3-INTERACTING PROTEIN2 negatively regulates FUSCA3 and plays a role in cotyledon development in Arabidopsis thaliana. J. Exp. Bot. 2017, 68, 1555–1567. [Google Scholar] [CrossRef]
  81. Zhang, X.; Garreton, V.; Chua, N.-H. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev. 2005, 19, 1532–1543. [Google Scholar] [CrossRef]
  82. Kurup, S.; Jones, H.D.; Holdsworth, M.J. Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J. 2000, 21, 143–155. [Google Scholar] [CrossRef] [PubMed]
  83. Kang, M.; Abdelmageed, H.; Lee, S.; Reichert, A.; Mysore, K.S.; Allen, R.D. AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. Plant J. 2013, 76, 481–493. [Google Scholar] [CrossRef] [PubMed]
  84. Suh, J.Y.; Kim, S.J.; Oh, T.R.; Cho, S.K.; Yang, S.W.; Kim, W.T. Arabidopsis Tóxicos en Levadura 78 (AtATL78) mediates ABA-dependent ROS signaling in response to drought stress. Biochem. Biophys. Res. Commun. 2016, 469, 8–14. [Google Scholar] [CrossRef] [PubMed]
  85. Kim, S.J.; Kim, W.T. Suppression of Arabidopsis RING E3 ubiquitin ligase AtATL78 increases tolerance to cold stress and decreases tolerance to drought stress. FEBS Lett. 2013, 587, 2584–2590. [Google Scholar] [CrossRef] [PubMed]
  86. Zhang, H.; Cui, F.; Wu, Y.; Lou, L.; Liu, L.; Tian, M.; Ning, Y.; Shu, K.; Tang, S.; Xie, Q. The RING Finger Ubiquitin E3 Ligase SDIR1 Targets SDIR1-INTERACTING PROTEIN1 for Degradation to Modulate the Salt Stress Response and ABA Signaling in Arabidopsis. Plant Cell 2015, 27, 214–227. [Google Scholar] [CrossRef] [PubMed]
  87. Oh, T.R.; Kim, J.H.; Cho, S.K.; Ryu, M.Y.; Yang, S.W.; Kim, W.T. AtAIRP2 E3 ligase affects ABA and high-salinity responses by stimulating its ATP1/SDIRIP1 substrate turnover. Plant Physiol. 2017, 174, 2515–2531. [Google Scholar] [CrossRef]
  88. Cho, N.H.; Woo, O.-G.; Kim, E.Y.; Park, K.; Seo, D.H.; Yu, S.G.; Choi, Y.A.; Lee, J.H.; Lee, J.-H.; Kim, W.T. E3 ligase AtAIRP5/GARU regulates drought stress response by stimulating SERINE CARBOXYPEPTIDASE-LIKE1 turnover. Plant Physiol. 2022, 190, 898–919. [Google Scholar] [CrossRef] [PubMed]
  89. Lyzenga, W.J.; Liu, H.; Schofield, A.; Muise-Hennessey, A.; Stone, S.L. Arabidopsis CIPK26 interacts with KEG, compo-nents of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J. Exp. Bot. 2013, 64, 2779–2791. [Google Scholar] [CrossRef] [PubMed]
  90. Joo, H.; Baek, W.; Lim, C.W.; Lee, S.C. Post-translational modifications of bZIP transcription factors in abscisic acid sig-naling and drought responses. Curr. Genom. 2021, 22, 4–15. [Google Scholar] [CrossRef]
  91. Lee, H.G.; Seo, P.J. The Arabidopsis MIEL1 E3 ligase negatively regulates ABA signalling by promoting protein turnover of MYB96. Nat. Commun. 2016, 7, 12525. [Google Scholar] [CrossRef]
  92. Lee, K.; Gil Lee, H.; Yoon, S.; Kim, H.U.; Seo, P.J. The Arabidopsis MYB96 Transcription Factor Is a Positive Regulator of ABSCISIC ACID-INSENSITIVE4 in the Control of Seed Germination. Plant Physiol. 2015, 168, 677–689. [Google Scholar] [CrossRef] [PubMed]
  93. Nie, K.; Zhao, H.; Wang, X.; Niu, Y.; Zhou, H.; Zheng, Y. The MIEL1-ABI5/MYB30 regulatory module fine tunes abscisic acid signaling during seed germination. J. Integr. Plant Biol. 2022, 64, 930–941. [Google Scholar] [CrossRef] [PubMed]
  94. Chen, Y.; Fokar, M.; Kang, M.; Chen, N.; Allen, R.D.; Chen, Y. Phosphorylation of Arabidopsis SINA2 by CDKG1 affects its ubiquitin ligase activity. BMC Plant Biol. 2018, 18, 147. [Google Scholar] [CrossRef]
  95. Lim, S.D.; Lee, C.; Jang, C.S. The rice RING E3 ligase, OsCTR1, inhibits trafficking to the chloroplasts of OsCP12 and OsRP1, and its overexpression confers drought tolerance in Arabidopsis. Plant Cell Environ. 2014, 37, 1097–1113. [Google Scholar] [CrossRef] [PubMed]
  96. Lv, Q.; Zhang, L.; Zan, T.; Li, L.; Li, X. Wheat RING E3 ubiquitin ligase TaDIS1 degrade TaSTP via the 26S proteasome pathway. Plant Sci. 2020, 296, 110494. [Google Scholar] [CrossRef]
  97. Meng, Y.; Lv, Q.; Li, L.; Wang, B.; Chen, L.; Yang, W.; Lei, Y.; Xie, Y.; Li, X. E3 ubiquitin ligase TaSDIR1-4A activates membrane-bound transcription factor TaWRKY29 to positively regulate drought resistance. Plant Biotechnol. J. 2023, 22, 987–1000. [Google Scholar] [CrossRef] [PubMed]
  98. Joo, H.; Lim, C.W.; Lee, S.C. Roles of pepper bZIP transcription factor CaATBZ1 and its interacting partner RING-type E3 ligase CaASRF1 in modulation of ABA signalling and drought tolerance. Plant J. 2019, 100, 399–410. [Google Scholar] [CrossRef] [PubMed]
  99. Joo, H.; Lim, C.W.; Lee, S.C. A pepper RING-type E3 ligase, CaASRF1, plays a positive role in drought tolerance via modulation of CaAIBZ1 stability. Plant J. 2018, 98, 5–18. [Google Scholar] [CrossRef] [PubMed]
  100. Zhang, Z.; Qu, J.; Lu, M.; Zhao, X.; Xu, Y.; Wang, L.; Liu, Z.; Shi, Y.; Liu, C.; Li, Y.; et al. The maize transcription factor CCT regulates drought tolerance by interacting with Fra a 1, E3 ligase WIPF2, and auxin response factor Aux/IAA8. J. Exp. Bot. 2023, 75, 103–122. [Google Scholar] [CrossRef]
  101. Samuel, M.A.; Mudgil, Y.; Salt, J.N.; Delmas, F.; Ramachandran, S.; Chilelli, A.; Goring, D.R. Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol. 2008, 147, 2084–2095. [Google Scholar] [CrossRef]
  102. Li, Z.; Li, S.; Jin, D.; Yang, Y.; Pu, Z.; Han, X.; Hu, Y.; Jiang, Y. U-box E3 ubiquitin ligase PUB8 attenuates abscisic acid responses during early seedling growth. Plant Physiol. 2023, 191, 2519–2533. [Google Scholar] [CrossRef]
  103. Tang, N.; Ma, S.; Zong, W.; Yang, N.; Lv, Y.; Yan, C.; Guo, Z.; Li, J.; Li, X.; Xiang, Y.; et al. MODD Mediates Deactivation and Degradation of OsbZIP46 to Negatively Regulate ABA Signaling and Drought Re-sistance in Rice. Plant Cell 2016, 28, 2161–2177. [Google Scholar] [CrossRef] [PubMed]
  104. Ma, S.; Tang, N.; Li, X.; Xie, Y.; Xiang, D.; Fu, J.; Shen, J.; Yang, J.; Tu, H.; Li, X.; et al. Reversible Histone H2B Monoubiquitination Fine-Tunes Abscisic Acid Signaling and Drought Response in Rice. Mol. Plant 2018, 12, 263–277. [Google Scholar] [CrossRef]
  105. Bae, Y.; Cho, J.; Choi, J.; Lim, C.W.; Lee, S.C. Pepper U-Box E3 ubiquitin ligase 24, CaPUB24, negatively regulates drought stress response. Physiol. Plant. 2024, 176, e14240. [Google Scholar] [CrossRef] [PubMed]
  106. Lee, J.-H.; Yoon, H.-J.; Terzaghi, W.; Martinez, C.; Dai, M.; Li, J.; Byun, M.-O.; Deng, X.W. DWA1 and DWA2, two Ara-bidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 2010, 22, 1716–1732. [Google Scholar] [CrossRef] [PubMed]
  107. Seo, K.-I.; Lee, J.-H.; Nezames, C.D.; Zhong, S.; Song, E.; Byun, M.-O.; Deng, X.W. ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell 2014, 26, 695–711. [Google Scholar] [CrossRef]
  108. Lechner, E.; Leonhardt, N.; Eisler, H.; Parmentier, Y.; Alioua, M.; Jacquet, H.; Leung, J.; Genschik, P. MATH/BTB CRL3 Receptors Target the Homeodomain-Leucine Zipper ATHB6 to Modulate Abscisic Acid Signaling. Dev. Cell 2011, 21, 1116–1128. [Google Scholar] [CrossRef]
  109. Tajdel-Zielińska, M.; Janicki, M.; Marczak, M.; Ludwików, A. Arabidopsis HECT and RING-type E3 Ligases Promote MAPKKK18 Degradation to Regulate Abscisic Acid Signaling. Plant Cell Physiol. 2023, 65, 390–404. [Google Scholar] [CrossRef]
  110. Lin, Q.; Wu, F.; Sheng, P.; Zhang, Z.; Zhang, X.; Guo, X.; Wang, J.; Cheng, Z.; Wang, J.; Wang, H.; et al. The SnRK2-APC/C(TE) regulatory module mediates the antagonistic action of gibberellic acid and abscisic acid pathways. Nat. Commun. 2015, 6, 7981. [Google Scholar] [CrossRef]
Ijms 25 07120 g001
Figure 1. Ubiquitin–proteasome system (by Figdraw). Ubiquitin binds to E1 to form the Ub-E1 complex. The Ub-E1 complex transfers Ub to E2 via a thioesterification reaction, forming the Ub-E2 complex. The Ub-E2 complex transfers Ub to the target protein through two pathways. Finally, most of the ubiquitinated target proteins are degraded by the 26S proteasome, releasing ubiquitin for recycling.
Figure 1. Ubiquitin–proteasome system (by Figdraw). Ubiquitin binds to E1 to form the Ub-E1 complex. The Ub-E1 complex transfers Ub to E2 via a thioesterification reaction, forming the Ub-E2 complex. The Ub-E2 complex transfers Ub to the target protein through two pathways. Finally, most of the ubiquitinated target proteins are degraded by the 26S proteasome, releasing ubiquitin for recycling.
Ijms 25 07120 g001
Ijms 25 07120 g002
Figure 2. E3 ubiquitin ligase regulation of the ABA pathway (by Figdraw). NCED, ZEP, and AAO3 are key enzymes in ABA biosynthesis. The pink boxes represent the regulatory effects of different E3 ubiquitin ligases on components such as PYR/PYLs/RCARs, PP2Cs, SnRK2s, and ABIs/ABFs in the ABA pathway. Arrows and vertical bars with horizontal lines represent positive regulation and negative regulation, respectively.
Figure 2. E3 ubiquitin ligase regulation of the ABA pathway (by Figdraw). NCED, ZEP, and AAO3 are key enzymes in ABA biosynthesis. The pink boxes represent the regulatory effects of different E3 ubiquitin ligases on components such as PYR/PYLs/RCARs, PP2Cs, SnRK2s, and ABIs/ABFs in the ABA pathway. Arrows and vertical bars with horizontal lines represent positive regulation and negative regulation, respectively.
Ijms 25 07120 g002
Table 1. E3 ubiquitin ligases regulate ABA biosynthesis and degradation metabolism.
Table 1. E3 ubiquitin ligases regulate ABA biosynthesis and degradation metabolism.
E3 TypeProtein or ComplexTargetsOrganismRegulation of ABAReferences
RING-H2OsRHP1OsZEP, OsNCED, OsAAORicePositive [57]
XERICONCED3ArabidopsisPositive [58]
ZmXerico1ZmABA8ox1a, ZmABA8ox3aMaizePositive [60]
U-boxSAUL1/AtPUB44AAO3ArabidopsisNegative [59]
Table 2. E3 ubiquitin ligases regulate PYR/PYLs/RCARs receptor protein stability.
Table 2. E3 ubiquitin ligases regulate PYR/PYLs/RCARs receptor protein stability.
E3 TypeProtein or ComplexTargetsOrganismRegulation of ABAReferences
RINGRSL1PYR/PYLs/RCARsArabidopsisNegative [61]
XBAT35VPS23AArabidopsisPositive [52]
U-boxPUB22/PUB23PYL9ArabidopsisNegative [24]
PUB11LRR1/KIN7ArabidopsisNegative [62]
RBRRFA1/RFA4PYR1/4/5/8ArabidopsisNegative [63]
CRLsCRL4_DDA1PYL8/RCAR3ArabidopsisNegative [8]
SCF_RIFP1RCAR3ArabidopsisNegative [64]
AtRAE1RCAR1ArabidopsisNegative [65]
Table 3. E3 ubiquitin ligases regulate PP2Cs phosphatase activity.
Table 3. E3 ubiquitin ligases regulate PP2Cs phosphatase activity.
E3 TypeProtein or
Complex		TargetsOrganismRegulation of ABAReferences
U-boxPUB12/PUB13ABI1ArabidopsisPositive [67]
RINGRGLG1PP2CAArabidopsisPositive [68]
RGLG5PP2CAArabidopsisPositive [69]
PIR1/PIR2PP2CAArabidopsisPositive [70]
AIRP3ABI1ArabidopsisPositive [71]
COP1ABI/HAB, AHG3ArabidopsisPositive [72]
CaAIRF1CaADIP1Capsicum annuumPositive [73]
OsRF1OsPP2C09RicePositive [74]
Table 4. E3 ubiquitin ligases regulate SnRK2s kinase activity.
Table 4. E3 ubiquitin ligases regulate SnRK2s kinase activity.
E3 TypeProtein or ComplexTargetsOrganismRegulation of ABAReferences
CRLsSCF_AtPP2-B11SnRK2.3ArabidopsisNegative [75]
CUL4-DDB1-HOS15OST1ArabidopsisNegative [76]
RINGCsCHYR1CsSnRK2.6, CsATAF1CucumberPositive [51]
Table 5. E3 ubiquitin ligases regulate ABIs/ABFs and other downstream response transcription factors.
Table 5. E3 ubiquitin ligases regulate ABIs/ABFs and other downstream response transcription factors.
E3 TypeProtein or ComplexTargetsOrganismRegulation of ABAReferences
RINGAtAIRP3/LOG2RD21ArabidopsisPositive [78]
AIP2ABI3, FUS3ArabidopsisNegative [80]
AtSAP5AtMBP-1ArabidopsisNegative [83]
ATL78CatalasesArabidopsisPositive [85]
SDIR1SDIRIP1ArabidopsisPositive [86]
AIRP2SDIRIP1ArabidopsisPositive [87]
AtAIRP5/GARUAtSCPL1ArabidopsisPositive [88]
KEGCIPK26, bZIP TFsArabidopsisNegative [89]
MIEL1MYB96, ABI5ArabidopsisNegative [91,93]
SINA2CDKG1ArabidopsisPositive [94]
OsCTR1OsCP12, OsRP1RicePositive [95]
TaDIS1TaSTPTriticum aestivumPositive [96]
TaSDIR1-4ATaWRKY29Triticum aestivumPositive [97]
CaASRF1CaAIBZ1, CaATBZ1Capsicum annuumPositive [98,99]
CaATIR1CaAIBZ1, CaATBZ1Capsicum annuumPositive [90]
ZmWIPF2ZmCCTMaizeNegative [100]
U-boxAtPUB9ABI3ArabidopsisNegative [101]
PUB8ABI3, ABI5ArabidopsisNegative [102]
OsPUB70OsbZIP46RiceNegative [103]
OsHUB2OsbZIP46RicePositive [104]
MdPUB23MdABI5AppleNegative [50]
CaPUB24NDCapsicum annuumNegative [105]
HECTUPL1/UPL4MAPKKK17/18ArabidopsisNegative [106]
CRLsDWA1/DWA2ABI5ArabidopsisNegative [107]
ABD1ABI5ArabidopsisNegative [108]
MATH-BTBATHB6ArabidopsisPositive [109]
ND: not detected.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Kou, H.; Zhang, X.; Jia, J.; Xin, M.; Wang, J.; Mao, L.; Baltaevich, A.M.; Song, X. Research Progress in the Regulation of the ABA Signaling Pathway by E3 Ubiquitin Ligases in Plants. Int. J. Mol. Sci. 2024, 25, 7120. https://doi.org/10.3390/ijms25137120

AMA Style

Kou H, Zhang X, Jia J, Xin M, Wang J, Mao L, Baltaevich AM, Song X. Research Progress in the Regulation of the ABA Signaling Pathway by E3 Ubiquitin Ligases in Plants. International Journal of Molecular Sciences. 2024; 25(13):7120. https://doi.org/10.3390/ijms25137120

Chicago/Turabian Style

Kou, Hongyun, Xiaopei Zhang, Jinghao Jia, Ming Xin, Jinhui Wang, Lili Mao, Ahmedov Miraziz Baltaevich, and Xianliang Song. 2024. "Research Progress in the Regulation of the ABA Signaling Pathway by E3 Ubiquitin Ligases in Plants" International Journal of Molecular Sciences 25, no. 13: 7120. https://doi.org/10.3390/ijms25137120

APA Style

Kou, H., Zhang, X., Jia, J., Xin, M., Wang, J., Mao, L., Baltaevich, A. M., & Song, X. (2024). Research Progress in the Regulation of the ABA Signaling Pathway by E3 Ubiquitin Ligases in Plants. International Journal of Molecular Sciences, 25(13), 7120. https://doi.org/10.3390/ijms25137120

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop