Next Article in Journal
Beneficial Impact of Inhaled 25(OH)-Vitamin D3 and 1,25(OH)2-Vitamin D3 on Pulmonary Response in the Murine Model of Hypersensitivity Pneumonitis
Previous Article in Journal
Exogenous Application of dsRNA—Inducing Silencing of the Fusarium oxysporum Tup1 Gene and Reducing Its Virulence
 
 
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 19
10.3390/ijms251910283
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

Development History, Structure, and Function of ASR (Abscisic Acid-Stress-Ripening) Transcription Factor

by
Yue Zhang
3,†,
Mengfan Wang
3,†,
Andery V. Kitashov
1,4 and
Ling Yang
1,2,3,*
1
Department of Biology, Shenzhen MSU-BIT University, Shenzhen 518172, China
2
College of Forestry, Beijing Forestry University, Beijing 100083, China
3
State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China
4
Biological Faculty, Lomonosov Moscow State University, Moscow 119991, Russia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2024, 25(19), 10283; https://doi.org/10.3390/ijms251910283
Submission received: 14 August 2024 / Revised: 18 September 2024 / Accepted: 20 September 2024 / Published: 24 September 2024
(This article belongs to the Section Molecular Biology)
Browse Figure
Review Reports Versions Notes

Abstract

:
Abiotic and biotic stress factors seriously affect plant growth and development. The process of plant response to abiotic stress involves the synergistic action of multiple resistance genes. The ASR (Abscisic acid stress-ripening) gene is a plant-specific transcription factor that plays a central role in regulating plant senescence, fruit ripening, and response to abiotic stress. ASR family members are highly conserved in plant evolution and contain ABA/WBS domains. ASR was first identified and characterized in tomatoes (Solanum lycopersicum L.). Subsequently, the ASR gene has been reported in many plant species, extending from gymnosperms to monocots and dicots, but lacks orthologues in Arabidopsis (Arabidopsis thaliana). The promoter regions of ASR genes in most species contain light-responsive elements, phytohormone-responsive elements, and abiotic stress-responsive elements. In addition, ASR genes can respond to biotic stresses via regulating the expression of defense genes in various plants. This review comprehensively summarizes the evolutionary history, gene and protein structures, and functions of the ASR gene family members in plant responses to salt stress, low temperature stress, pathogen stress, drought stress, and metal ions, which will provide valuable references for breeding high-yielding and stress-resistant plant varieties.

1. Introduction

The natural environment in which plants exist is dynamic, with stress conditions such as extreme temperatures, drought, salinization, fungi, and other biotic stress factors significantly impacting plant growth and development [1]. Plant hormones play a crucial role in regulating plant growth, development, and stress responses, enhancing plant tolerance to various stresses [2]. This regulatory effect is not the result of a single action, but is mostly linked through some common elements, commonly referred to as hubs or links of crosstalk [3]. ABA (abscisic acid) is a significant plant hormone that regulates plant growth, development, and stress responses when interacting with other plant hormones [4]. The crosstalk between ABA and GA (gibberellin) can modulate seed dormancy, germination, maturation, root growth, and flowering time [5]. ABA can also influence the expression of IAA (auxin) response factors ARF5, ARF6, and ARF10 through ubiquitination responses, thereby controlling the IAA signaling pathway and enhancing plant tolerance to salt stress [6]. Additionally, ABA is involved in promoting fruit ripening [7] and increasing fruit yield [8]. The interaction between ABA and CKs (cytokinin) is particularly evident in breaking seed dormancy [9], inhibiting bud dormancy and leaf senescence [10], as well as enhancing drought tolerance in plants [11,12]. The relationship between ABA and ETH (ethylene) can be both positive and negative, depending on the specific developmental process. ABA can regulate ETH biosynthesis and signaling through controlling the expression of ethylene response factor 11, NCED, and acyl-CoA. For example, ABA can induce ETH biosynthesis in the regulation of photoperiod, fruit ripening, and leaf senescence [13]. Conversely, in the case of long-term darkness, ABA inhibits flowering via suppressing ETH biosynthesis [14]. Additionally, the interaction between ABA and SA (salicylic acid) is particularly significant in responses to drought stress, heavy metal stress, and biotic stress [15,16,17]. The role of JA (jasmonic acid) in the stress response is similar to that of ABA, with their interaction mainly reflected in processes such as triggering stomatal closure and leaf senescence to regulate plant tolerance to drought and low temperatures [18,19]. Furthermore, the stomatal closure promoted by ABA is antagonistically regulated by brassinosteroids and SA, while promoting leaf senescence via counteracting the effects of melatonin and CKs [20].
ASR genes, plant-specific TFs (transcription factors), are crucial in regulating plant senescence, fruit ripening, and response to abiotic stress [21]. These genes are expressed in plant organs and growth stages, playing a significant role in plant response to developmental and environmental conditions, particularly involving ABA signaling [22,23,24,25,26,27]. ASR proteins exhibit strong hydrophilicity, indicating a potential role in drought stress response. Since the first ASR gene was identified in tomatoes, ASR genes have been identified in various monocotyledonous and dicotyledonous plants. However, they have not been found in the model plant Arabidopsis [28]. Studies have shown that ASR proteins typically function as molecular chaperones, osmoregulatory proteins, metal-binding proteins, and antioxidant or detoxification proteins [29,30,31]. Some ASRs also act as unique transcription factors [32]. Therefore, exploring the functions of ASRs in plant growth, development, fruit ripening, and stress responses is crucial for enhancing economic production.

2. The Role of ABA in Plant Growth and Stress Response

Plant growth and development can be influenced by various stress factors in the natural environment. These factors include abiotic stress such as temperature fluctuations, lack of water and nutrients, and soil salinization, as well as biotic stress factors such as infestation via fungi, bacteria, and herbivores. Investigating the mechanism of stress tolerance in plants is crucial. Studies have shown that biotic and abiotic stresses usually occur simultaneously in nature and that there is crosstalk in the plant responses to these stresses, with ABA being the central component of this crosstalk [3,33,34].
ABA was first identified and defined as a plant growth inhibitor in the 1860s. ABA plays an important role in the regulation of plant growth, stress response, and various physiological processes, including seed dormancy and germination [35,36,37,38,39], stomatal movement [40,41,42], fruit development [43,44,45,46], and the response to biotic and abiotic stress factors [47,48,49,50]. Seed dormancy is the main mechanism for plants to overcome stress [51], and ABA plays a significant role in seed dormancy and development. ABA induces seed dormancy and maturation and inhibits seed germination via regulating the activity of transcription factors such as LEC1 (Leafy Cotyledon1) and LEC2 (Leafy Cotyledon2). Excessive accumulation of FUSCA3 and ABI3 (Abscisic Acid Insensitive3) can also inhibit seed germination [52,53]. Additionally, it has been shown that ABA synthesis in the endosperm is the main reason for seed dormancy [37,54]. It was found that the interaction between ODR1 and bHLH57 prevented binding to the NCED6 and NCED9 promoters, which in turn affected ABA biosynthesis and downregulated the transcription of ABI4. During seed maturation, binding of ABI3 to the ODR1 promoter represses its expression and releases the repressive effects of bHLH57, thereby promoting ABA biosynthesis and seed dormancy [54]. ABA inhibits seed germination through preventing seed cracking and endosperm rupture [35]. ABA also influences the growth of plant roots. It was found that reduced endodermal ABA signaling decreased miR165 levels and led to a significant increase in ATHB8 and REV transcript levels, which in turn affected xylem development [55]. Besides forming xylem through microRNA and its target transcription factors, ABA is a key signaling molecule for plants to establish a hydrophobic suberin protein barrier to prevent water and nutrient outflow [56], and it supports the transport of nutrients and water from the xylem to the buds. Furthermore, ABA can promote the growth of primary roots via reducing the biosynthesis of ETH, playing a role in maintaining the root meristem during primary root growth [57]. Exogenous ABA has been shown to promote the ripening of plants such as tomatoes, bananas, peaches, mangoes, and melons through regulating several physiological mechanisms associated with ripening [58,59,60,61]. As an upstream regulator of ETH biosynthesis and signal transduction, ABA positively regulates ETH synthesis during fruit ripening [62,63]. The endogenous ethylene induces the expression of VvNCED1, encoding 9-cis-epoxycarotenoid dioxygenase (NCED) and VvGT, thereby encoding an ABA glucosyltransferase; both increased rapidly during grape ripening. When the level of ABA reaches the peak value, part of it will be stored in the form of ABA-GE. Their interaction thus initiates the berry ripening process [62]. The exogenous addition of ABA also promotes ETH synthesis and accelerates the plant respiration rate to promote fruit ripening. However, another study showed that the ETH production of the ABA-deficient mutant flc was significantly higher than that of the wild type. This indicates that ABA can inhibit the production of excess ETH, suggesting that ABA’s regulation of ETH can be positive or negative depending on the tissue type or developmental stage [64]. In addition, ABA levels were negatively correlated with stomatal density and index. ABA function deficiency mutants (aba1, aba2, aba3, nced3, nced5, atbg1, and atbg2) of Arabidopsis showed an increase in stomatal density and stomatal pressure. In contrast, cyp707a1 and cyp707a3 mutants, which lack the catabolic function of ABA, showed a decrease in stomatal density and index [65,66,67,68]. ABA can also reduce the size of guard cells, thus affecting the size of plant epidermal cells [66,69]. This suggests that ABA is involved in the process of plant stress response through influencing the development of stomata and guard cells.
The most studied function of ABA is its role in abiotic stress responses such as salt, drought, and low temperature. Especially under drought stress, plant cells rapidly accumulate a large amount of ABA. Under drought stress, the ABA content in the leaves increases tenfold or more [70]. Even under long-term drought stress, the synthesis and catabolism rates of ABA in Arabidopsis and soybean (Glycine max) are still high. Moreover, ABA accumulated in guard cells under drought stress promotes stomatal closure and inhibits stomatal opening to reduce transpiration-induced water loss [71,72,73]. ABA can also cause a transient increase in intracellular calcium levels, thereby activating slow-activating (S-type) and fast-activating (R-type) anion channels at the plasma membrane [74]. This suggests that the rapid renewal and accumulation of ABA are the most important mechanisms for plants to cope with drought stress. Moreover, ABA content in plants is also significantly increased under a low temperature and salt stress [75,76,77,78,79,80], and the exogenous application of ABA can improve plant resistance to abiotic stresses such as drought [81,82,83], high salinity [84,85,86], and low temperatures [87,88]. ABA regulates the expression of many genes in plants in response to abiotic stresses such as drought, high salinity, and low temperatures, with several types of transcription factors involved in the ABA-mediated regulation of gene expression. For example, CaSnRK2.4 interacted with and phosphorylated CaNAC035 in vitro and in vivo. In addition, the expression of two ABA biosynthesis-related genes (CaAAO3 and CaNCED3) was significantly upregulated in transgenic pepper (Capsicum annuum) lines with high expression of CaNAC035, which enhanced tolerance to cold stress [87]. These transcription factors interact with cis-acting elements in the promoter region of ABA-induced genes to activate their expression. The cis-acting element ABRE and the dehydration-responsive element DRE are the major stress response elements that play a role in ABA-dependent and ABA-independent gene expression, respectively. In Arabidopsis, NCED3 is considered the major determinant of ABA accumulation under drought stress [89], promoting ABA accumulation and stomatal closure [90]. Additionally, the ABA-responsive genes RD29A, RD29B, AREB1/ABF2, ABF3, and AREB/ABF4 also play an important role in plant drought tolerance [91]. LT178, COR78, RD29A, and NACs are significantly induced under high salinity, drought, and low-temperature stress, which are essential for the abiotic stress responses in the plants [92]. Heat shock factor HSFA6b is activated by ABA-mediated AREB1 and positively regulates drought and high-temperature stress [93]. Furthermore, RD26 is the main signal molecule for plant response to low-temperature stress [92].

3. The Development History of ASR Gene Family Members

ASR gene members contain a conserved ABA/WDS structural domain. ASR genes encode small, plant-specific hydrophilic proteins that are not only involved in plant responses to drought, high salinity, low temperature, and ABA stresses and are closely related to the ABA signaling pathway, but also play a role in many plants’ metabolic processes, such as fruit ripening and sugar metabolism. The first ASR gene, ASR1, was first identified in tomatoes (Solanum lycopersicum L.) in 1993 via screening differential genes in tomato leaves and ripe fruits under drought stress [94]. In 1994, another ASR gene with high sequence similarity to ASR1 was cloned and named ASR2 [95]. Further studies revealed that ASR1 and ASR2 are part of a gene family with at least three members, namely ASR1, ASR2, and ASR3, which are clustered on chromosome 4 of tomatoes [96]. Subsequently, ASR genes have been found in papayas (Pseudocydonia sinensis), tobacco (Nicotiana tabacum L.), and potatoes (Solanum tuberosum L.) [97]. In 2006, the fourth ASR gene was identified and named ASR4. This gene is highly similar in structure to the previously identified ASR gene but contains a specialized structural domain and positively responds to drought stress [98]. The fifth ASR gene, ASR5, was identified in 2011. ASR5 and ASR3 have highly similar coding regions, but their intron sequences are very different. This study also showed that individual members of the ASR gene family exhibited diverse evolutionary histories [99]. Meanwhile, ASR genes have also been identified and cloned in various species, including the potato [100], maize (Zea mays L.) [101], pummelo (Citrus maxima) [102], loblolly pine (Pinus taeda) [103], lily (Lilium longiflorum Thunb. cv.) [104], rice (Oryza sativa L.) [105], grape (Vitis vinifera L.) [106], apple (Malus × domestica) [107], chickpea (Cicer arietinum L.) [108], cucumber (Cucumis sativus) [109], and peach (Prunus persica f. atropurpurea) [110]. Functional analysis of the ASR gene has demonstrated their association with biological processes such as seed dormancy and germination [111], fruit development and ripening [112], and stress response [107,108]. Currently, ASR genes have been identified and characterized in many species through whole genomes, including 6 members in rice [113], 5 members in tomato [98], 4 members in loblolly pine [103], 9 members in maize [101], 33 members in wheat (Triticum aestivum L.) [114], 5 members in Brachypodium (Brachypodium distachyon) [115], 10 members in bay bean [116], 5 members in apple [107], and 4 members in banana (Musa nana Lour.) [117]. There is 1 member in grape [106] and 27 members in 8 Rosaceae (Table 1) [118]. However, no homology to the ASR gene was found in the model plant Arabidopsis, making it difficult to study the function of the ASR gene using Arabidopsis mutants [119].

4. Structure, Physicochemical Properties, and Expression Patterns of ASR

The ASR genes of most species, including wheat [114], tomato [123], banana [117], maize [121], bay bean [116], and apple [107], contain two exons (Table 1), while the exons of ASR genes in Rosaceae plants’ exons usually number between one and four [118]. The promoter elements of ASR genes in most species contain light-response elements, ABA-response elements, GA-response elements, MeJA (methyl jasmonate)-response elements, IAA-response elements, SA-response elements, drought-response elements, and low-temperature-response elements [114,116,118,121]. This suggests that ASR may interact with hormone signaling networks to regulate plant growth and stress response. In addition, the results of subcellular localization showed that all ASR genes are localized in the nucleus [114,115,116,121,124]. Duplication is the main driver of gene expansion during the evolution of species. Five types of gene duplication can occur during evolution, including singleton, dispersed, tandem, proximal, and segmental duplication. The results showed that among the 29 ASR genes in wheat, 29 pairs of tandem duplication and 12 pairs of segmental duplication had emerged, indicating that tandem duplication and segmental duplication were the main driving forces of ASR evolution. In addition, Ka/Ks can be used to determine whether selective pressure is acting on protein-coding genes (Ka/Ks < 1 for purifying selection, Ka/Ks = 1 for neutral selection, and Ka/Ks > 1 for positive selection). The ASR genes of different species were subject to different environmental selections during the evolutionary process. For example, ASR1 of the tomato was subject to environmental purifying selection while ASR2 was subject to positive selection, and ASR1, ASR2, and ASR3 of the apple were subject to environmental purifying selection while ASR4 and ASR5 were subject to positive selection. These results indicate that the ASR genes in tomatoes and apples have evolved mainly to adapt to the environment. In contrast, all ASR genes in Rosaceae were subject to purifying selection by the environment, suggesting that the ASR genes in Rosaceae are highly conserved during evolution [107,118,125]. Furthermore, the ASRs of all species contain conserved ABA/WDS protein domains and are hydrophilic proteins. The stability of ASR proteins differs between species. For example, the ASR proteins of beans and Rosaceae were thermally stable [116,118], while the ASR proteins of apples were unstable [107].
ASR has been shown to be essential for plant growth and stress response, and the roles of different ASR members are quite diverse. SlASR1 was highly expressed in tomato roots and stems and promoted the development of nutrient organs [123]. The expression levels of ASR3 and ASR5 were highest in tomato cotyledons, while ASR4 was highest in mature leaves [123]. Similar to the tomato, most ASR genes in Rosaceae have the highest expression levels in leaves and fruits [118]. Of the 33 ASR genes in wheat, 24 were expressed in roots, stems, leaves, flowers, and fruits [114]. Five ASR genes of bay bean were expressed in all plant tissues, indicating that ASR genes are essential for plant growth and development [115]. In addition, the ASR genes responded to salt stress, drought stress, low-temperature stress, high-temperature stress, and pathogen infection [107,114,115,116,121,123], and were significantly upregulated after treatment with the phytohormone ABA [123]. Similar to the results of the promoter element analysis, this suggests that ASR is linked to the ABA signaling network to regulate plant growth and development as well as the stress response process.

5. ASR Regulates Fruit Ripening

ASR plays a crucial role in fruit ripening through modulating the synthesis and metabolism of glucose, cell wall components, amino acids, ABA, and carotenoids. Studies have shown that ASR is situated within the signaling cascade involving glucose, ABA, and GA. Reduction in ASR protein levels results in the diminished activity of tobacco HK1 (Hexokinase1), impacting glucose metabolism, photosynthesis, and respiration. This reduction also leads to decreased levels of ABA and GA, contributing to plant dwarfism and hastening leaf senescence (Table 2) [125].
Overexpression of plum PpASR1 in tomatoes has been shown to regulate the metabolic processes of the tomato cell wall, leading to a significant increase in the levels of anthocyanin and lycopene [110]. Similarly, overexpression of ASR1 in strawberries significantly increased the expression levels of anthocyanin biosynthesis-related genes CHS (chalcone synthase), CHI (chalcone isomerase), ANS (anthocyanin synthase), and the ABA biosynthesis gene NCED in strawberries and tomatoes. This promotion of anthocyanin and ABA synthesis further enhances the ripening and softening processes in both strawberry and tomato fruits [126]. ASR can also regulate fruit ripening through regulating amino acid metabolism. ZmASR1 has been shown to impact the biosynthesis of BCAA (branched-chain amino acid) and regulate maize grain yield [101]. Tomato ASR1 has been found to enhance the accumulation of proline, methionine, valine, and isoleucine in fruits, thereby promoting fruit development [21,124]. Furthermore, acting as a downstream component of the ABA signaling pathway, ASR has been implicated in the regulation of strawberry fruit ripening and firmness by modulating ABA levels. It has also been linked to an increase in the number of tillers and grain yield in rice [21]. Recent transcriptome and metabolomics analyses have revealed that ASR1 can affect plant photosynthesis, tricarboxylic acid cycle (citrate and succinate), lipid metabolism (phenylalanine and glycerol), and isoprene synthesis (β-carotene and lycopene) pathways, which are also closely related to plant growth and fruit ripening [21].

6. Response of ASR to Low-Temperature Stress

Currently, a large number of studies focus on the mechanism of ASR response to low-temperature stress, including the functions of ASR genes in rice, maize, and lily. The results showed that low-temperature stress significantly induced the expression of OsASR1 in the vegetative and reproductive organs of rice, and overexpression of OsASR1 significantly increased the photosynthetic efficiency (Fv/Fm) of rice leaves under low-temperature stress (Figure 1) [127].

7. Response of ASR to Metal Ions

Overexpression of OsASR3 can also enhance the tolerance of rice to low-temperature stress [128]. Similarly, overexpression of ZmASR1 in maize has been shown to improve photosynthesis efficiency, reduce lipid peroxidation levels, and increase the activities of antioxidant enzymes under low-temperature stress (Figure 1) [129]. Heterologous expression of the ASR family member LLA23 in Arabidopsis promoted the growth of stems and roots via preventing electrolyte leakage, inducing the expression of genes related to low-temperature stress and enhancing the activity of cryoprotective enzymes MDH and LDH (Figure 1) [130]. Furthermore, TtASR1 in E. coli also improved the tolerance of E. coli to low-temperature stress [112]. The expression profile of ASR genes under low-temperature stress has also been characterized in many species. In rice, for instance, the expression of all ASR family members OsASR1–6 was found to be significantly upregulated in response to low-temperature stress [131]. BdASR4, BdASR1, BdASR2, BdASR3, and BdASR5 exhibited positive responses to low-temperature stress [115]. Among the 29 ASR genes in wheat, 11 ASR genes showed a positive response to low-temperature stress [122]. Conversely, the expression level of DiASR1 in the dove tree was significantly downregulated under low-temperature stress, indicating that the function of ASR genes in response to low temperatures varies among different species (Figure 1) [132]. Furthermore, the ABA/WDS domain may play a crucial role in the response of ASR genes to low-temperature stress and other abiotic stresses [133].
Metal ions have a negative impact on plant growth and development (Figure 1) [134,135]. The structure and function of ASR proteins can be regulated through binding to metal ions. Most ASR proteins contain a Zn2+ binding domain. As a chaperone-like protein in the cytoplasm, tomato SlASR1 has a Zn2+-dependent binding activity. Binding to Zn2+ led to the transformation of the protein structure of SlASR1 from an unfolded, disordered state to a folded, ordered state and induced the DNA-binding activity of SlASR1 [136,137]. Under abiotic stress, SlASR1 binds to Zn2+ in the cytoplasm and excretes Zn2+ out of the cell (Figure 1) [138]. Similar to tomato SlASR1, the protein structure of TtASR1 and HvASR1 also changed from an unfolded, disordered state to a folded, ordered state after Zn2+ treatment (Figure 1) [138]. Rice exhibits the highest tolerance to aluminum toxicity among all cereal plants. The expression level of the OsASR5 gene is notably higher when compared with aluminum-sensitive rice genotypes. After 4 to 8 h of aluminum stress, the expression levels of OsASR1–6 varied in their degrees of increase. OsASR5 RNAi rice demonstrated significantly higher aluminum sensitivity than wild-type rice, resulting in delayed flowering, abnormal panicle shape development, and grain loss (Figure 1) [139]. OsASR5 and OsASR1 have complementary functions in response to aluminum stress. OsASR5 regulates the expression of 36 aluminum response genes, including STAR1 and STAR2. This suggests that under aluminum stress, the transcript levels of OsASR5 are significantly elevated, leading to a positive regulation of OsASR1 expression. Additionally, the STAR1/STAR2 complex, along with OsASR1, works together to cover the aluminum binding sites in the cell wall [140,141]. The expression level of ZmASR1 in the roots, stems, and leaves of maize was significantly increased under cadmium stress, and tobacco and yeast overexpressing ZmASR1 were found to be tolerant to cadmium stress (Figure 1) [140]. It has been shown that GmASR proteins in soybean with Fe3+, Ni2+, Cu2+, and Zn2+ binding sites could prevent oxidative damage through buffering metal ions, thus alleviating metal toxicity in plant cells under stress conditions (Figure 1) [142].

8. Response of ASR to Salt Stress

Under salt stress, the excessive accumulation of Na+ can lead to ion imbalance, oxidative stress, nutrient deficiency, growth retardation, and cell death [143]. Studies have demonstrated that ASR responds to salt stress via eliminating excess ROS, activating stress response genes, and regulating intracellular Na+/K+. The expression level of the ThASR3 gene in Tamarix hispida was significantly increased, which was similar to the expression patterns of OsASR6 in rice, CrASR in bay bean, HvASR5 in barley, and TaASR1-D in wheat, indicating that a conserved role in ASR family members across different species is in their salt response (Figure 1) [116,144,145,146]. Salt stress triggered a surge in ROS levels within cells, disrupting the redox balance. Overexpression of ASR genes can boost antioxidant enzyme activity, enhance the accumulation of osmotic regulators like proline and glycine betaine, reduce intracellular MDA content and electrolyte permeability, improve ROS scavenging capacity, stimulate root, stem, leaf, and fruit development, and ultimately increase the yield of plants [144,146,147,148]. ASR can also enhance salt stress resistance via upregulating the expression of salt-responsive genes. Overexpression of BdASR2 in Brachypodium resulted in increased expression levels of BdWRKY36, BdSOS2, and BdHKT7, as well as antioxidant enzyme genes BdCAT, BdAPX2 and BdMn-SOD [148]. Similarly, the expression of antioxidant enzyme genes APX2, FSD1, CSD1, and CAT1 was also significantly induced in Arabidopsis heterologously expressing IpASR (Figure 1) [147], suggesting that ASR responded to salt stress via controlling ROS homeostasis and regulating the expression of stress-related genes. Banana MaASR1 was found to improve salt tolerance in Arabidopsis through downregulating the ABA-dependent stress response genes, while leaving the ABA-independent genes and ABA biosynthesis pathway genes unaffected (Figure 1) [149]. Moreover, ASR can reduce the Na+/K+ ratio via reducing Na+ uptake and eliminating excess Na+ from cells [150]. For instance, overexpression of OsASR6 in rice and TaASR1-D in wheat led to a significant reduction in Na+/K+ levels in leaf cells and seedlings, respectively, indicating that ASR plays a crucial role in maintaining ion homeostasis both internally and externally (Figure 1) [26,144]. In addition, studies have demonstrated that heterologous expression of the ASR genes enhanced salt stress tolerance in yeast and E. coli [109,112,116,151]. A recent study has demonstrated that ASR was mainly involved in chitin catabolism, redox balance, cell wall modification, defense response to fungi, defense response to low-temperature stress, and transcriptional regulation [145].

9. Response of ASR to Drought Stress

Drought stress significantly affects plant growth and reduces crop yield. Plants have evolved complex mechanisms to cope with drought stress. Studies have shown that ASR responds to drought stress via scavenging excessive ROS in cells, inducing stress-responsive gene expression, promoting compatible solute accumulation, and regulating stomatal morphology. Similarly, drought stress also leads to a high accumulation of intracellular ROS and disrupts the redox balance. Overexpression of ASR genes can increase the activities of antioxidant enzymes, such as SOD, POD, CAT, and GSH, and scavenge excessive H2O2 and MDA in cells to maintain the redox balance [111,113,115,151,152,153]. ASR can also promote the accumulation of free amino acids such as proline in tissues to resist drought stress [110,151]. Drought stress can result in damage to cell membrane and cell wall structures, leading to the outflow of cell solutes. Heterologous expression of PpASR gene in tobacco significantly reduced the ion outflow of tobacco cells, which was essential for the stability of cell structure under drought stress [110]. SiASR1 from foxtail millet (Setaria italica), TaASR1 from wheat, and OsASR6 from rice were also shown to reduce cell outflow (Figure 1) [111,113,151]. Drought stress is recognized for triggering the activation of stress response genes. Heterologous expression of Brachypodium BdASR1 in tobacco led to a significant increase in the expression of stress-related genes such as NtEDR10C, NtEDR10D, NtLTP1, and NtDREB3, as well as genes related to the synthesis of antioxidant enzymes such as NtSOD, NtPOX, and NtCAT (Figure 1) [115]. Similarly, heterologous expression of SiASR1 from Setaria italica in tobacco also resulted in significantly increased expression levels of the antioxidant enzyme synthesis genes SOD, POD, and CAT (Figure 1) [113]. The heterologous expression of ZmASR3 from maize in Arabidopsis led to a significant induction of the stress-resistant genes AtCOR2 and AtDREB15A (Figure 1) [153]. The expression of stress-responsive genes such as CBF1, CBF2, CBF3, DREB2A, RAB16, WRKY36, AREB, LEA, NCED2, and P5CS1 was also shown to be positively regulated in wheat TaASR2D and moso bamboo PheASR2 (Figure 1) [152,154]. This suggests that ASR responds to drought stress via controlling ROS homeostasis and regulating the expression of stress-related genes. Furthermore, it was found that the positive regulation of ASR during drought stress can be counterbalanced by exogenous ABA. Overexpression of ZmASR3 in plants led to an increased accumulation of ABA in leaves, resulting in a significant increase in the expression levels of ABA-dependent genes including NCED3, AAO3, EDR1, RAB18, and SnRK2.6 [152,153,154]. Drought stress typically causes changes in stomatal structure and density. ASR has been found to decrease stomatal opening, stomatal density, and stomatal conductance in leaves under drought conditions, ultimately reducing leaf water loss. This process is closely related to the ABA signaling pathway and is finely regulated by ABA. These findings suggest that ASR modulates stomatal structure and density through an ABA-dependent signaling pathway, playing a crucial role in plant responses to drought stress [30,146,153].

10. Response of ASR to Pathogen Infection

The role of ASR in abiotic stress has been extensively studied, but there are few reports on its role in biotic stress. Studies have shown that the expression of OsASR6 in rice was significantly induced after Xoo (Xanthomonas oryzae pv. oryzae) and Xoc (Xanthomonas oryzae pv. oryzicola) treatments. The expression levels of MpASR in plantain (Musa paradisiaca) increased significantly after treatment with Fusarium oxysporum f. sp. Cubense, suggesting that they may act as positive regulators in response to pathogens (Figure 1) [155,156]. The expression levels of MdASR2, MdASR3, and MdASR6 were consistently downregulated after inoculation. This indicates that they respond to the negative regulator of Alternaria alternata f. sp. Mali (Figure 1) [107]. The ASR gene has been shown to respond to biotic stress via regulating the expression of defense genes. Specifically, OsASR2 was found to regulate the activity of the GT-1 element in the promoter of Os2H16 and enhance the resistance to Xoo and Rhizoctonia solani (Figure 1) [157]. Interestingly, OsASR6, another member of the rice ASR family, regulates the expression of target genes PibHs, ASN1, WRKYs, and CIPKs, thereby affecting rice resistance to Xoo and Xoc [156], suggesting that different members of the ASR family within the same species may have varying functions in response to stress. Furthermore, tomato ASR1 positively influences the infection of the necrotrophic fungus Botrytis cinerea [21]. In addition to regulating the expression of defense genes, ASR enhances resistance to pathogens through promoting the activity of antioxidant enzymes and defense-related enzymes PPO and PAL, as well as through reducing ROS accumulation [107]. A recent study has demonstrated that pepper CaASR1 can enhance pepper resistance to Capsicum annuum through promoting SA-dependent signal transduction and inhibiting JA-dependent signal transduction. These findings suggest that the SA pathway may serve as the central pathway for ASR-mediated pathogen response (Figure 1) [158].

11. Conclusions

ASR plays a crucial role in promoting plant growth and fruit ripening through regulating the biosynthesis and metabolism of various compounds such as glucose, cell wall components, amino acids, ABA, and carotenoids, ultimately leading to increased fruit and grain yield. Currently, research on ASR promoting fruit ripening mainly focuses on Rosaceae and Solanaceae, as well as cereal crops.
Plant responses to abiotic stresses can be attributed to reducing the damage caused by osmotic stress, such as through promoting the activity of antioxidant enzymes, accelerating intracellular Na+ efflux, scavenging excessive ROS, inducing the expression of antioxidant enzyme genes, and promoting the accumulation of osmotic protectants and free amino acids. Additionally, this response is closely related to the ABA signal transduction pathway. ASR responds to biotic stress through controlling ROS homeostasis and inducing the expression of downstream stress-related genes. Among these, the SA pathway may be the core pathway of the ASR-mediated biotic stress response.
Although the role of ASR in fruit ripening and abiotic stress has been extensively studied, its role in biotic stress has rarely been reported. Considering the importance of cereal crops in the development of national economy and the susceptibility of cereal pathogens under natural conditions, exploring the mechanism of the ASR gene response to biotic stress should be the main direction of ASR functional analyses.

Author Contributions

L.Y. and Y.Z. made the research plan, Y.Z. wrote the main manuscript text and prepared the figures, M.W. reviewed and edited. A.V.K. and L.Y. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work is supported by the National Natural Science Foundation of China (Grant No. 32071757).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the editors and reviewers for their careful reading and valuable comments. We also acknowledge the Kombi Kaviriri David of Northeast Forestry University for the proofreading.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Guo, S.X.; He, F.; Song, B.A.; Wu, J. Future direction of agrochemical development for plant disease in China. Food Energy Secur. 2021, 10, e293. [Google Scholar] [CrossRef]
  2. Waadt, R.; Seller, C.A.; Hsu, P.K.; Takahashi, Y.; Munemasa, S.; Schroeder, J. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 2022, 23, 680–694. [Google Scholar] [CrossRef] [PubMed]
  3. Singh, A.; Roychoudhury, A. Abscisic acid in plants under abiotic stress: Crosstalk with major phytohormones. Plant Cell Rep. 2023, 42, 961–974. [Google Scholar] [CrossRef] [PubMed]
  4. Yoshida, T.; Christmann, A.; Yamaguchi-Shinozaki, K.; Grill, E.; Fernie, A.R. Revisiting the Basal Role of ABA—Roles Outside of Stress. Trends Plant Sci. 2019, 24, 625–635. [Google Scholar] [CrossRef] [PubMed]
  5. Shu, K.; Chen, Q.; Wu, Y.R.; Liu, R.J.; Zhang, H.W.; Wang, P.F.; Li, Y.L.; Wang, S.F.; Tang, S.Y.; Liu, C.Y.; et al. ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. Plant J. 2016, 85, 348–361. [Google Scholar] [CrossRef] [PubMed]
  6. Ding, Z.J.; Yan, J.Y.; Li, C.X.; Li, G.X.; Wu, Y.R.; Zheng, S.J. Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J. 2015, 84, 56–69. [Google Scholar] [CrossRef] [PubMed]
  7. Breitel, D.A.; Chappell-Maor, L.; Meir, S.; Panizel, I.; Puig, C.P.; Hao, Y.W.; Yifhar, T.; Yasuor, H.; Zouine, M.; Bouzayen, M.; et al. AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening. PLoS Genet. 2016, 12, e1005903. [Google Scholar] [CrossRef]
  8. Promchuea, S.; Zhu, Y.J.; Chen, Z.Z.; Zhang, J.; Gong, Z.Z. ARF2 coordinates with PLETHORAs and PINs to orchestrate ABA-mediated root meristem activity in Arabidopsis. J. Integr. Plant Biol. 2017, 59, 30–43. [Google Scholar] [CrossRef]
  9. Corot, A.; Roman, H.; Douillet, O.; Autret, H.; Perez-Garcia, M.D.; Citerne, S.; Bertheloot, J.; Sakr, S.; Leduc, N.; Demotes-Mainard, S. Cytokinins and Abscisic Acid Act Antagonistically in the Regulation of the Bud Outgrowth Pattern by Light Intensity. Front. Plant Sci. 2017, 8, 1724. [Google Scholar] [CrossRef]
  10. Sirko, A.; Wawrzynska, A.; Brzywczy, J.; Sienko, M. Control of ABA Signaling and Crosstalk with Other Hormones by the Selective Degradation of Pathway Components. Int. J. Mol. Sci. 2021, 22, 4638. [Google Scholar] [CrossRef]
  11. Chandrasekaran, U.; Luo, X.F.; Zhou, W.G.; Shu, K. Multifaceted Signaling Networks Mediated by Abscisic Acid Insensitive 4. Plant Commun. 2020, 1, 100040. [Google Scholar] [CrossRef] [PubMed]
  12. Huang, X.Z.; Zhang, X.Y.; Gong, Z.Z.; Yang, S.H.; Shi, Y.T. ABI4 represses the expression of type-A ARRs to inhibit seed germination in Arabidopsis. Plant J. 2017, 89, 354–365. [Google Scholar] [CrossRef]
  13. Jakubowicz, M.; Nowak, W.; Galganski, L.; Babula-Skowronska, D.; Kubiak, P. Expression profiling of the genes encoding ABA route components and the ACC oxidase isozymes in the senescing leaves of Populus tremula. J. Plant Physiol. 2020, 248, 153143. [Google Scholar] [CrossRef] [PubMed]
  14. Wilmowicz, E.; Frankowski, K.; Kucko, A.; Kesy, J.; Kopcewicz, J. Involvement of IAA regulated ACC oxidase gene PNACO3 in Pharbitis nil flower inhibition. Acta Biol. Cracoviensia Ser. Bot. 2014, 56, 90–96. [Google Scholar] [CrossRef]
  15. Chojak-Kozniewska, J.; Linkiewicz, A.; Sowa, S.; Radzioch, M.A.; Kuzniak, E. Interactive effects of salt stress and Pseudomonas syringae pv.lachrymans infection in cucumber: Involvement of antioxidant enzymes, abscisic acid and salicylic acid. Environ. Exp. Bot. 2017, 136, 9–20. [Google Scholar] [CrossRef]
  16. López-Orenes, A.; Alba, J.M.; Kant, M.R.; Calderón, A.A.; Ferrer, M.A. OPDA and ABA accumulation in Pb-stressed Zygophyllum fabago can be primed by salicylic acid and coincides with organ-specific differences in accumulation of phenolics. Plant Physiol. Biochem. 2020, 154, 612–621. [Google Scholar] [CrossRef] [PubMed]
  17. Prodhan, M.Y.; Munemasa, S.; Nahar, M.; Nakamura, Y.; Murata, Y. Guard Cell Salicylic Acid Signaling Is Integrated into Abscisic Acid Signaling via the Ca2+/CPK-Dependent Pathway. Plant Physiol. 2018, 178, 441–450. [Google Scholar] [CrossRef] [PubMed]
  18. Wang, X.; Li, Q.; Xie, J.J.; Huang, M.; Cai, J.; Zhou, Q.; Dai, T.B.; Jiang, D. Abscisic acid and jasmonic acid are involved in drought priming-induced tolerance to drought in wheat. Crop J. 2021, 9, 120–132. [Google Scholar] [CrossRef]
  19. Wang, F.; Guo, Z.X.; Li, H.Z.; Wang, M.M.; Onac, E.; Zhou, J.; Xia, X.J.; Shi, K.; Yu, J.Q.; Zhou, Y.H. Phytochrome A and B Function Antagonistically to Regulate Cold Tolerance via Abscisic Acid-Dependent Jasmonate Signaling. Plant Physiol. 2016, 170, 459–471. [Google Scholar] [CrossRef]
  20. Ha, Y.M.; Shang, Y.; Yang, D.; Nam, K.H. Brassinosteroid reduces ABA accumulation leading to the inhibition of ABA-induced stomatal closure. Biochem. Biophys. Res. Commun. 2018, 504, 143–148. [Google Scholar] [CrossRef]
  21. Dominguez, P.G.; Conti, G.; Duffy, T.; Insani, M.; Alseekh, S.; Asurmendi, S.; Fernie, A.R.; Carrari, F. Multiomics analyses reveal the roles of the ASR1 transcription factor in tomato fruits. J. Exp. Bot. 2021, 72, 6490–6509. [Google Scholar] [CrossRef] [PubMed]
  22. Liu, H.; Ding, Q.Q.; Cao, L.S.; Huang, Z.W.; Wang, Z.F.; Zhang, M.; Jian, S.G. Identification of the Abscisic Acid-, Stress-, and Ripening-Induced (ASR) Family Involved in the Adaptation of Tetragonia tetragonoides (Pall.) Kuntze to Saline-Alkaline and Drought Habitats. Int. J. Mol. Sci. 2023, 24, 15815. [Google Scholar] [CrossRef] [PubMed]
  23. Huang, X.; Wei, J.M.; Feng, W.Z.; Luo, Q.; Tan, G.F.; Li, Y.Z. Interaction between SlMAPK3 and SlASR4 regulates drought resistance in tomato (Solanum lycopersicum L.). Mol. Breed. 2023, 43, 73. [Google Scholar] [CrossRef] [PubMed]
  24. Zheng, P.J.; Liu, M.X.; Pang, L.J.; Sun, R.Y.; Yao, M.H.; Wang, X.J.; Kang, Z.S.; Liu, J. Stripe rust effector Pst21674 compromises wheat resistance by targeting transcription factor TaASR3. Plant Physiol. 2023, 193, 2806–2824. [Google Scholar] [CrossRef]
  25. Zhang, Y.; Ma, H.J.; Zhou, T.C.; Zhu, Z.Y.; Zhang, Y.; Zhao, X.; Wang, C. ThASR3 confers salt and osmotic stress tolerances in transgenic Tamarix and Arabidopsis. BMC Plant Biol. 2022, 22, 586. [Google Scholar] [CrossRef] [PubMed]
  26. Zhang, Q.; Liu, Y.Q.; Jiang, Y.L.; Li, A.Q.; Cheng, B.J.; Wu, J.D. OsASR6 Enhances Salt Stress Tolerance in Rice. Int. J. Mol. Sci. 2022, 23, 9340. [Google Scholar] [CrossRef]
  27. Yacoubi, I.; Gadaleta, A.; Mathlouthi, N.; Hamdi, K.; Giancaspro, A. Abscisic Acid-Stress-Ripening Genes Involved in Plant Response to High Salinity and Water Deficit in Durum and Common Wheat. Front. Plant Sci. 2022, 13, 789701. [Google Scholar] [CrossRef]
  28. González, R.M.; Iusem, N.D. Twenty years of research on Asr (ABA-stress-ripening) genes and proteins. Planta 2014, 239, 941–949. [Google Scholar] [CrossRef]
  29. Zhang, J.; Zhu, Q.S.; Yu, H.J.; Li, L.; Zhang, G.Q.; Chen, X.; Jiang, M.Y.; Tan, M. Comprehensive Analysis of the Cadmium Tolerance of Abscisic Acid-, Stress- and Ripening-Induced Proteins (ASRs) in Maize. Int. J. Mol. Sci. 2019, 20, 133. [Google Scholar] [CrossRef]
  30. Li, J.J.; Li, Y.; Yin, Z.G.; Jiang, J.H.; Zhang, M.H.; Guo, X.; Ye, Z.J.; Zhao, Y.; Xiong, H.Y.; Zhang, Z.Y.; et al. OsASR5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H2O2 signalling in rice. Plant Biotechnol. J. 2017, 15, 183–196. [Google Scholar] [CrossRef]
  31. Ye, Y.Y.; Lin, R.Y.; Su, H.X.; Chen, H.F.; Luo, M.; Yang, L.X.; Zhang, M. The functional identification of glycine-rich TtASR from Tetragonia tetragonoides (Pall.) Kuntze involving in plant abiotic stress tolerance. Plant Physiol. Biochem. 2019, 143, 212–223. [Google Scholar] [CrossRef] [PubMed]
  32. Barros, N.L.F.; Siqueira, A.S.; Arenhart, R.A.; Margis-Pinheiro, M. Modeling the zinc effect on OsASR5-STAR1 promoter interaction by molecular dynamics. Proteins-Struct. Funct. Bioinform. 2023, 91, 944–955. [Google Scholar] [CrossRef] [PubMed]
  33. Fujita, M.; Fujita, Y.; Noutoshi, Y.; Takahashi, F.; Narusaka, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9, 436–442. [Google Scholar] [CrossRef] [PubMed]
  34. Rachappanavar, V.; Padiyal, A.; Sharma, J.K.; Gupta, S.K. Plant hormone-mediated stress regulation responses in fruit crops—A review. Sci. Hortic. 2022, 304, 111302. [Google Scholar] [CrossRef]
  35. Finch-Savage, W.E.; Leubner-Metzger, G. Seed dormancy and the control of germination. New Phytol. 2006, 171, 501–523. [Google Scholar] [CrossRef]
  36. Chen, S.Y.; Kuo, S.R.; Chien, C.T. Roles of gibberellins and abscisic acid in dormancy and germination of red bayberry (Myrica rubra) seeds. Tree Physiol. 2008, 28, 1431–1439. [Google Scholar] [CrossRef]
  37. Lefebvre, V.; North, H.; Frey, A.; Sotta, B.; Seo, M.; Okamoto, M.; Nambara, E.; Marion-Poll, A. Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J. 2006, 45, 309–319. [Google Scholar] [CrossRef]
  38. Manz, B.; Muller, K.; Kucera, B.; Volke, F.; Leubner-Metzger, G. Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiol. 2005, 138, 1538–1551. [Google Scholar] [CrossRef]
  39. Ali, F.; Qanmber, G.; Li, F.G.; Wang, Z. Updated role of ABA in seed maturation, dormancy, and germination. J. Adv. Res. 2022, 35, 199–214. [Google Scholar] [CrossRef]
  40. Kudoyarova, G.; Veselova, S.; Hartung, W.; Farhutdinov, R.; Veselov, D.; Sharipova, G. Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporative demand. Planta 2011, 233, 87–94. [Google Scholar] [CrossRef]
  41. Du, H.; Wu, N.; Chang, Y.; Li, X.H.; Xiao, J.H.; Xiong, L.Z. Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol. Biol. 2013, 83, 475–488. [Google Scholar] [CrossRef] [PubMed]
  42. Mukherjee, A.; Dwivedi, S.; Bhagavatula, L.; Datta, S. Integration of light and ABA signaling pathways to combat drought stress in plants. Plant Cell Rep. 2023, 42, 829–841. [Google Scholar] [CrossRef] [PubMed]
  43. Zaharah, S.S.; Singh, Z.; Symons, G.M.; Reid, J.B. Role of Brassinosteroids, Ethylene, Abscisic Acid, and Indole-3-Acetic Acid in Mango Fruit Ripening. J. Plant Growth Regul. 2012, 31, 363–372. [Google Scholar] [CrossRef]
  44. Giovannoni, J. Molecular biology of fruit maturation and ripening. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 725–749. [Google Scholar] [CrossRef] [PubMed]
  45. Wu, W.; Cao, S.F.; Shi, L.Y.; Chen, W.; Yin, X.R.; Yang, Z.F. Abscisic acid biosynthesis, metabolism and signaling in ripening fruit. Front. Plant Sci. 2023, 14, 1279031. [Google Scholar] [CrossRef]
  46. Gupta, K.; Wani, S.H.; Razzaq, A.; Skalicky, M.; Samantara, K.; Gupta, S.; Pandita, D.; Goel, S.; Grewal, S.; Hejnak, V.; et al. Abscisic Acid: Role in Fruit Development and Ripening. Front. Plant Sci. 2022, 13, 817500. [Google Scholar] [CrossRef]
  47. Zhu, J.K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002, 53, 247–273. [Google Scholar] [CrossRef]
  48. Chernys, J.T.; Zeevaart, J.A.D. Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol. 2000, 124, 343–353. [Google Scholar] [CrossRef]
  49. Basso, M.F.; Contaldi, F.; Lo Celso, F.; Karalija, E.; Paz-Carrasco, L.C.; Barone, G.; Ferrante, A.; Martinelli, F. Expression profile of the NCED/CCD genes in chickpea and lentil during abiotic stress reveals a positive correlation with increased plant tolerance. Plant Sci. 2023, 336, 111817. [Google Scholar] [CrossRef]
  50. Hewage, K.A.H.; Yang, J.F.; Wang, D.; Hao, G.F.; Yang, G.F.; Zhu, J.K. Chemical Manipulation of Abscisic Acid Signaling: A New Approach to Abiotic and Biotic Stress Management in Agriculture. Adv. Sci. 2020, 7, 2001265. [Google Scholar] [CrossRef]
  51. Yan, A.; Chen, Z. The Control of Seed Dormancy and Germination by Temperature, Light and Nitrate. Bot. Rev. 2020, 86, 39–75. [Google Scholar] [CrossRef]
  52. Yan, A.; Chen, Z. The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep. 2017, 36, 689–703. [Google Scholar] [CrossRef] [PubMed]
  53. Monke, G.; Seifert, M.; Keilwagen, J.; Mohr, M.; Grosse, I.; Hahnel, U.; Junker, A.; Weisshaar, B.; Conrad, U.; Baumlein, H.; et al. Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res. 2012, 40, 8240–8254. [Google Scholar] [CrossRef] [PubMed]
  54. Sano, N.; Marion-Poll, A. ABA Metabolism and Homeostasis in Seed Dormancy and Germination. Int. J. Mol. Sci. 2021, 22, 5069. [Google Scholar] [CrossRef]
  55. Ramachandran, P.; Wang, G.D.; Augstein, F.; Annelie, J.D.; Carlsbecker, A. Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165. Development 2018, 145, dev159202. [Google Scholar] [CrossRef] [PubMed]
  56. Barberon, M.; Vermeer, J.E.M.; De Bellis, D.; Wang, P.; Naseer, S.; Andersen, T.G.; Humbel, B.M.; Nawrath, C.; Takano, J.; Salt, D.E.; et al. Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation. Cell 2016, 164, 447–459. [Google Scholar] [CrossRef]
  57. Li, Z.F.; Zhang, L.X.; Yu, Y.W.; Quan, R.D.; Zhang, Z.J.; Zhang, H.W.; Huang, R.F. The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J. 2011, 68, 88–99. [Google Scholar] [CrossRef]
  58. Mou, W.S.; Li, D.D.; Bu, J.W.; Jiang, Y.Y.; Khan, Z.U.; Luo, Z.S.; Mao, L.C.; Ying, T.J. Comprehensive Analysis of ABA Effects on Ethylene Biosynthesis and Signaling during Tomato Fruit Ripening. PLoS ONE 2016, 11, e0154072. [Google Scholar] [CrossRef]
  59. Chen, P.; Sun, Y.F.; Kai, W.B.; Liang, B.; Zhang, Y.S.; Zhai, X.W.; Jiang, L.; Du, Y.W.; Leng, P. Interactions of ABA signaling core components (SlPYLs, SlPP2Cs, and SlSnRK2s) in tomato (Solanum lycopersicon). J. Plant Physiol. 2016, 205, 67–74. [Google Scholar] [CrossRef]
  60. Zaharah, S.S.; Singh, Z.; Symons, G.M.; Reid, J.B. Mode of action of abscisic acid in triggering ethylene biosynthesis and softening during ripening in mango fruit. Postharvest Biol. Technol. 2013, 75, 37–44. [Google Scholar] [CrossRef]
  61. Zhang, M.; Leng, P.; Zhang, G.L.; Li, X.X. Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J. Plant Physiol. 2009, 166, 1241–1252. [Google Scholar] [CrossRef] [PubMed]
  62. Sun, L.A.; Zhang, M.; Ren, J.; Qi, J.X.; Zhang, G.J.; Leng, P. Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biol. 2010, 10, 257. [Google Scholar] [CrossRef]
  63. Wang, P.P.; Yu, A.S.; Ji, X.L.; Mu, Q.; Haider, M.S.; Wei, R.A.; Leng, X.P.; Fang, J.G. Transcriptome and metabolite integrated analysis reveals that exogenous ethylene controls berry ripening processes in grapevine. Food Res. Int. 2022, 155, 111084. [Google Scholar] [CrossRef] [PubMed]
  64. Nitsch, L.; Kohen, W.; Oplaat, C.; Charnikhova, T.; Cristescu, S.; Michieli, P.; Wolters-Arts, M.; Bouwmeester, H.; Mariani, C.; Vriezen, W.H.; et al. ABA-deficiency results in reduced plant and fruit size in tomato. J. Plant Physiol. 2012, 169, 878–883. [Google Scholar] [CrossRef] [PubMed]
  65. Allen, J.; Guo, K.; Zhang, D.X.; Ince, M.; Jammes, F. ABA-glucose ester hydrolyzing enzyme ATBG1 and PHYB antagonistically regulate stomatal development. PLoS ONE 2019, 14, e0218605. [Google Scholar] [CrossRef] [PubMed]
  66. Tanaka, Y.; Nose, T.; Jikumaru, Y.; Kamiya, Y. ABA inhibits entry into stomatal-lineage development in Arabidopsis leaves. Plant J. 2013, 74, 448–457. [Google Scholar] [CrossRef]
  67. Yoshida, T.; Obata, T.; Feil, R.; Lunn, J.E.; Fujita, Y.; Yamaguchi-Shinozaki, K.; Fernie, A.R. The Role of Abscisic Acid Signaling in Maintaining the Metabolic Balance Required for Arabidopsis Growth under Nonstress Conditions. Plant Cell 2019, 31, 84–105. [Google Scholar] [CrossRef] [PubMed]
  68. Lake, J.A.; Woodward, F.I. Response of stomatal numbers to CO2 and humidity: Control by transpiration rate and abscisic acid. New Phytol. 2008, 179, 397–404. [Google Scholar] [CrossRef]
  69. Seller, C.A.; Schroeder, J.I. Distinct guard cell-specific remodeling of chromatin accessibility during abscisic acid- and CO2-dependent stomatal regulation. Proc. Natl. Acad. Sci. USA 2023, 120, e2310670120. [Google Scholar] [CrossRef]
  70. Seiler, C.; Harshavardhan, V.T.; Rajesh, K.; Reddy, P.S.; Strickert, M.; Rolletschek, H.; Scholz, U.; Wobus, U.; Sreenivasulu, N. ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. J. Exp. Bot. 2011, 62, 2615–2632. [Google Scholar] [CrossRef]
  71. Kim, T.H.; Bohmer, M.; Hu, H.H.; Nishimura, N.; Schroeder, J.I. Guard Cell Signal Transduction Network: Advances in Understanding Abscisic Acid, CO2, and Ca2+ Signaling. In Annual Review of Plant Biology; Merchant, S., Briggs, W.R., Ort, D., Eds.; Annual Review of Plant Biology; Annual Reviews: Palo Alto, CA, USA, 2010; Volume 61, pp. 561–591. [Google Scholar]
  72. Zhang, Y.; He, Y.; Zhao, H.Y.; Zhang, Y.; Yang, J.; Ou, X.Q.; Zhang, J.L.; Zhu, Q.D.; Devlin, P. A 14-3-3 Protein-Encoding Gene, BdGF14g, Confers Better Drought Tolerance by Regulating ABA Biosynthesis and Signaling. Plants 2023, 12, 3975. [Google Scholar] [CrossRef] [PubMed]
  73. Zlobin, I.E.; Vankova, R.; Dobrev, P.I.; Gaudinova, A.; Kartashov, A.V.; Ivanov, Y.V.; Ivanova, A.I.; Kuznetsov, V.V. Abscisic Acid and Cytokinins Are Not Involved in the Regulation of Stomatal Conductance of Scots Pine Saplings during Post-Drought Recovery. Biomolecules 2023, 13, 523. [Google Scholar] [CrossRef] [PubMed]
  74. Sanchez, J.P.; Chua, N.H. Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 2001, 13, 1143–1154. [Google Scholar] [CrossRef] [PubMed]
  75. Singh, N.K.; Larosa, P.C.; Handa, A.K.; Hasegawa, P.M.; Bressan, R.A. Hormonal regulation of protein of protein synthesis with tolerance in plant cells. Proc. Natl. Acad. Sci. USA 1987, 84, 739–743. [Google Scholar] [CrossRef]
  76. Eze, J.M.O.; Dumbroff, E.B.; Thompson, J.E. Effects of temperature and moisture stress on the accumulation of abscisis acid in bean. Physiol. Plant. 1983, 58, 179–183. [Google Scholar] [CrossRef]
  77. Daie, J.; Campbell, W.F. Response of tomato plants to stressful temperatures increase in abscisic acid concentrations. Plant Physiol. 1981, 67, 26–29. [Google Scholar] [CrossRef]
  78. Wang, D.; Yang, Z.J.; Feng, M.Y.; Yang, W.W.; Qu, R.; Nie, S.M. The overexpression of SlBRI1 driven by Atrd29A promoter-transgenic plants improves the chilling stress tolerance of tomato. Planta 2024, 259, 11. [Google Scholar] [CrossRef]
  79. Xu, C.; Wang, Y.; Yang, H.; Tang, Y.; Liu, B.; Hu, X.; Hu, Z. Cold acclimation alleviates photosynthetic inhibition and oxidative damage induced by cold stress in citrus seedlings. Plant Signal. Behav. 2023, 18, 2285169. [Google Scholar] [CrossRef]
  80. Yao, Y.D.; Yang, Y.; Pan, Y.; Liu, Z.S.; Hou, X.M.; Li, Y.H.; Zhang, H.S.; Wang, C.L.; Liao, W.B. Crucial roles of trehalose and 5-azacytidine in alleviating salt stress in tomato: Both synergistically and independently. Plant Physiol. Biochem. 2023, 203, 108075. [Google Scholar] [CrossRef]
  81. Wei, L.T.; Wang, L.N.; Yang, Y.; Wang, P.F.; Guol, T.C.; Kang, G.Z. Abscisic acid enhances tolerance of wheat seedlings to drought and regulates transcript levels of genes encoding ascorbate-glutathione biosynthesis. Front. Plant Sci. 2015, 6, 00458. [Google Scholar] [CrossRef]
  82. Waterland, N.L.; Campbell, C.A.; Finer, J.J.; Jones, M.L. Abscisic Acid Application Enhances Drought Stress Tolerance in Bedding Plants. Hortscience 2010, 45, 409–413. [Google Scholar] [CrossRef]
  83. Habibpourmehraban, F.; Masoomi-Aladizgeh, F.; Haynes, P.A. Effect of ABA Pre-Treatment on Rice Plant Transcriptome Response to Multiple Abiotic Stress. Biomolecules 2023, 13, 1554. [Google Scholar] [CrossRef] [PubMed]
  84. Etehadnia, M.; Waterer, D.R.; Tanino, K.K. The Method of ABA Application Affects Salt Stress Responses in Resistant and Sensitive Potato Lines. J. Plant Growth Regul. 2008, 27, 331–341. [Google Scholar] [CrossRef]
  85. Khadri, M.; Tejera, N.A.; Lluch, C. Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J. Plant Growth Regul. 2006, 25, 110–119. [Google Scholar] [CrossRef]
  86. Ruan, M.J.; He, W.L.; He, R.; Wang, X.X.; Wei, J.X.; Zhu, Y.J.; Li, R.L.; Jiang, Z.J.; Na, X.F.; Wang, X.M.; et al. Alternative oxidase 2 influences Arabidopsis seed germination under salt stress by modulating ABA signalling and ROS homeostasis. Environ. Exp. Bot. 2024, 217. [Google Scholar] [CrossRef]
  87. Zhang, H.F.; Pei, Y.P.; Zhu, F.L.; He, Q.; Zhou, Y.Y.; Ma, B.H.; Chen, X.Q.; Guo, J.B.; Khan, A.; Jahangir, M.; et al. CaSnRK2.4-mediated phosphorylation of CaNAC035 regulates abscisic acid synthesis in pepper (Capsicum annuum L.) responding to cold stress. Plant J. 2023, 117, 1377–1391. [Google Scholar] [CrossRef]
  88. Wang, Q.; Zhu, M.T.; Zhang, L.L.; Liu, Y. Abscisic acid increases the viability of cryopreserved shoot tips of Lilium pumilum by regulating the osmotic stress and programmed cell death. Plant Cell Tissue Organ Cult. 2023, 155, 731–741. [Google Scholar] [CrossRef]
  89. Bader, Z.E.; Bae, M.J.; Ali, A.; Park, J.; Baek, D.; Yun, D.J. GIGANTEA-ENHANCED EM LEVEL complex initiates drought escape response via dual function of ABA synthesis and flowering promotion. Plant Signal. Behav. 2023, 18, 2180056. [Google Scholar] [CrossRef]
  90. Malcheska, F.; Ahmad, A.; Batool, S.; Muller, H.M.; Ludwig-Mueller, J.; Kreuzwieser, J.; Randewig, D.; Hansch, R.; Mendel, R.R.; Hell, R.; et al. Drought-Enhanced Xylem Sap Sulfate Closes Stomata by Affecting ALMT12 and Guard Cell ABA Synthesis. Plant Physiol. 2017, 174, 798–814. [Google Scholar] [CrossRef]
  91. Jaradat, M.R.; Feurtado, J.A.; Huang, D.Q.; Lu, Y.Q.; Cutler, A.J. Multiple roles of the transcription factor AtMYBR1/AtMYB44 in ABA signaling, stress responses, and leaf senescence. BMC Plant Biol. 2013, 13, 192. [Google Scholar] [CrossRef]
  92. Fujii, H.; Verslues, P.E.; Zhu, J.K. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl. Acad. Sci. USA 2011, 108, 1717–1722. [Google Scholar] [CrossRef] [PubMed]
  93. Huang, Y.C.; Niu, C.Y.; Yang, C.R.; Jinn, T.L. The Heat Stress Factor HSFA6b Connects ABA Signaling and ABA-Mediated Heat Responses. Plant Physiol. 2016, 172, 1182–1199. [Google Scholar] [CrossRef] [PubMed]
  94. Iusem, N.D.; Bartholomew, D.M.; Hitz, W.D.; Scolnik, P.A. Tomato (Lycopersicon esculentum) trancript induced by water-deficit and ripening. Plant Physiol. 1993, 102, 1353–1354. [Google Scholar] [CrossRef] [PubMed]
  95. Rossi, M.; Iusem, N.D. Tomato (Lycopersicon esculentum) genomic clone homologous to a gene encoding an abcisic acid-induced protein. Plant Physiol. 1994, 104, 1073–1074. [Google Scholar] [CrossRef]
  96. Rossi, M.; Lijavetzky, D.; Bernacchi, D.; Hopp, H.E.; Iusem, N. Asr genes belong to a gene family comprising at least three closely linked loci on chromosome 4 in tomato. Mol. Gen. Genet. 1996, 252, 489–492. [Google Scholar] [CrossRef]
  97. Rossi, M.; Carrari, F.; Cabrera-Ponce, J.L.; Vazquez-Rovere, C.; Herrera-Estrella, L.; Gudesblat, G.; Iusem, N.D. Analysis of an abscisic acid (ABA)-responsive gene promoter belonging to the Asr gene family from tomato in homologous and heterologous systems. Mol. Gen. Genet. 1998, 258, 1–8. [Google Scholar] [CrossRef]
  98. Frankel, N.; Carrari, F.; Hasson, E.; Iusem, N.D. Evolutionary history of the Asr gene family. Gene 2006, 378, 74–83. [Google Scholar] [CrossRef]
  99. Fischer, I.; Camus-Kulandaivelu, L.; Allal, F.; Stephan, W. Adaptation to drought in two wild tomato species: The evolution of the Asr gene family. New Phytol. 2011, 190, 1032–1044. [Google Scholar] [CrossRef]
  100. Schneider, A.; Salamini, F.; Gebhardt, C. Expression patterns and promoter activity of the cold-regulated gene ci21A of potato. Plant Physiol. 1997, 113, 335–345. [Google Scholar] [CrossRef]
  101. Virlouvet, L.; Jacquemot, M.P.; Gerentes, D.; Corti, H.; Bouton, S.; Gilard, F.; Valot, B.; Trouverie, J.; Tcherkez, G.; Falque, M.; et al. The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions. Plant Physiol. 2011, 157, 917–936. [Google Scholar] [CrossRef]
  102. Canel, C.; Baileyserres, J.N.; Roose, M.L. Pomelo fruit transcript homologous to ripening-induced genes. Plant Physiol. 1995, 108, 1323–1324. [Google Scholar] [CrossRef]
  103. Chang, S.J.; Puryear, J.D.; Dias, M.; Funkhouser, E.A.; Newton, R.J.; Cairney, J. Gene expression under water deficit in loblolly pine (Pinus taeda): Isolation and characterization of cDNA clones. Physiol. Plant. 1996, 97, 139–148. [Google Scholar] [CrossRef]
  104. Wang, C.S.; Liau, Y.E.; Huang, J.C.; Wu, T.D.; Su, C.C.; Lin, C.H. Characterization of a desiccation-related protein in lily pollen during development and stress. Plant Cell Physiol. 1998, 39, 1307–1314. [Google Scholar] [CrossRef]
  105. Vaidyanathan, R.; Kuruvilla, S.; Thomas, G. Characterization and expression pattern of an abscisic acid and osmotic stress responsive gene from rice. Plant Sci. 1999, 140, 21–30. [Google Scholar] [CrossRef]
  106. Cakir, B.; Agasse, A.; Gaillard, C.; Saumonneau, A.; Delrot, S.; Atanassova, R. A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 2003, 15, 2165–2180. [Google Scholar] [CrossRef] [PubMed]
  107. Huang, K.H.; Zhong, Y.; Li, Y.J.; Zheng, D.; Cheng, Z.M. Genome-wide identification and expression analysis of the apple ASR gene family in response to Alternaria alternata f. sp mali. Genome 2016, 59, 866–878. [Google Scholar] [CrossRef] [PubMed]
  108. Sachdeva, S.; Bharadwaj, C.; Singh, R.K.; Jain, P.K.; Patil, B.S.; Roorkiwal, M.; Varshney, R. Characterization of ASR gene and its role in drought tolerance in chickpea (Cicer arietinum L.). PLoS ONE 2020, 15, e0234550. [Google Scholar] [CrossRef] [PubMed]
  109. Zhou, Y.; Hu, L.F.; Jiang, L.W.; Liu, H.J.; Liu, S.Q. Molecular cloning and characterization of an ASR gene from Cucumis sativus. Plant Cell Tissue Organ Cult. 2017, 130, 553–565. [Google Scholar] [CrossRef]
  110. Wei, J.X.; Hu, F.; Jiang, W.B.; Chen, H.M. Functional Analysis of Abscisic Acid-Stress Ripening Transcription Factor in Prunus persica f. atropurpurea. J. Plant Growth Regul. 2018, 37, 85–100. [Google Scholar] [CrossRef]
  111. Hu, W.; Huang, C.; Deng, X.M.; Zhou, S.Y.; Chen, L.H.; Li, Y.; Wang, C.; Ma, Z.B.; Yuan, Q.Q.; Wang, Y.; et al. TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ. 2013, 36, 1449–1464. [Google Scholar] [CrossRef]
  112. Hamdi, K.; Brini, F.; Kharrat, N.; Masmoudi, K.; Yakoubi, I. Abscisic Acid, Stress, and Ripening (TtASR1) Gene as a Functional Marker for Salt Tolerance in Durum Wheat. Biomed Res. Int. 2020, 2020, 7876357. [Google Scholar] [CrossRef] [PubMed]
  113. Feng, Z.J.; Xu, Z.S.; Sun, J.T.; Li, L.C.; Chen, M.; Yang, G.X.; He, G.Y.; Ma, Y.Z. Investigation of the ASR family in foxtail millet and the role of ASR1 in drought/oxidative stress tolerance. Plant Cell Rep. 2016, 35, 115–128. [Google Scholar] [CrossRef] [PubMed]
  114. Li, H.W.; Guan, H.Y.; Zhuo, Q.C.; Wang, Z.S.; Li, S.D.; Si, J.S.; Zhang, B.; Feng, B.; Kong, L.A.; Wang, F.H.; et al. Genome-wide characterization of the abscisic acid-, stress- and ripening-induced (ASR) gene family in wheat (Triticum aestivum L.). Biol. Res. 2020, 53, 23. [Google Scholar] [CrossRef] [PubMed]
  115. Wang, L.Z.; Hu, W.; Feng, J.L.; Yang, X.Y.; Huang, Q.J.; Xiao, J.J.; Liu, Y.; Yang, G.X.; He, G.Y. Identification of the ASR gene family from Brachypodium distachyon and functional characterization of BdASR1 in response to drought stress. Plant Cell Rep. 2016, 35, 1221–1234. [Google Scholar] [CrossRef] [PubMed]
  116. Lin, R.Y.; Zou, T.; Mei, Q.M.; Wang, Z.F.; Zhang, M.; Jian, S.U. Genome-Wide Analysis of the Late Embryogenesis Abundant (LEA) and Abscisic Acid-, Stress-, and Ripening-Induced (ASR) Gene Superfamily from Canavalia rosea and Their Roles in Salinity/Alkaline and Drought Tolerance. Int. J. Mol. Sci. 2021, 22, 4554. [Google Scholar] [CrossRef]
  117. Henry, I.M.; Carpentier, S.C.; Pampurova, S.; Van Hoylandt, A.; Panis, B.; Swennen, R.; Remy, S. Structure and regulation of the Asr gene family in banana. Planta 2011, 234, 785–798. [Google Scholar] [CrossRef]
  118. Zhao, B.Y.; Yi, X.R.; Qiao, X.; Tang, Y.; Xu, Z.M.; Liu, S.T.; Zhang, S.L. Genome-Wide Identification and Comparative Analysis of the ASR Gene Family in the Rosaceae and Expression Analysis of PbrASRs During Fruit Development. Front. Genet. 2021, 12, 792250. [Google Scholar] [CrossRef]
  119. Carrari, F.; Fernie, A.R.; Iusem, N.D. Heard it through the grapevine? ABA and sugar cross-talk: The ASR story. Trends Plant Sci. 2004, 9, 57–59. [Google Scholar] [CrossRef]
  120. Philippe, R.; Courtois, B.; McNally, K.L.; Mournet, P.; El-Malki, R.; Le Paslier, M.C.; Fabre, D.; Billot, C.; Brunel, D.; Glaszmann, J.C.; et al. Structure, allelic diversity and selection of Asr genes, candidate for drought tolerance, in Oryza sativa L. and wild relatives. Theor. Appl. Genet. 2010, 121, 769–787. [Google Scholar] [CrossRef]
  121. Zhang, L.L.; Yi, X.P.; Guo, J.Y.; Zhao, H.; Xia, Q.Y.; He, P.P.; Huo, S.S.; Qu, J.; Cao, Y.; Tan, Y.H.; et al. Expression patterns of the ZmASR family during simulated drought stress in maize. Agron. J. 2021, 113, 894–905. [Google Scholar] [CrossRef]
  122. Zan, T.; Li, L.Q.; Xie, T.T.; Zhang, L.; Li, X.J. Genome-wide identification and abiotic stress response patterns of abscisic acid stress ripening protein family members in Triticum aestivum L. Genomics 2020, 112, 3794–3802. [Google Scholar] [CrossRef]
  123. Golan, I.; Dominguez, P.G.; Konrad, Z.; Shkolnik-Inbar, D.; Carrari, F.; Bar-Zvi, D. Tomato ABSCISIC ACID STRESS RIPENING (ASR) Gene Family Revisited. PLoS ONE 2014, 9, e0107117. [Google Scholar] [CrossRef] [PubMed]
  124. Chen, J.Y.; Liu, D.J.; Jiang, Y.M.; Zhao, M.L.; Shan, W.; Kuang, J.F.; Lu, W.J. Molecular Characterization of a Strawberry FaASR Gene in Relation to Fruit Ripening. PLoS ONE 2011, 6, e0024649. [Google Scholar] [CrossRef] [PubMed]
  125. Dominguez, P.G.; Frankel, N.; Mazuch, J.; Balbo, I.; Iusem, N.; Fernie, A.R.; Carrari, F. ASR1 Mediates Glucose-Hormone Cross Talk by Affecting Sugar Trafficking in Tobacco Plants. Plant Physiol. 2013, 161, 1486–1500. [Google Scholar] [CrossRef] [PubMed]
  126. Jia, H.F.; Jiu, S.T.; Zhang, C.; Wang, C.; Tariq, P.; Liu, Z.J.; Wang, B.J.; Cui, L.W.; Fang, J.G. Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol. J. 2016, 14, 2045–2065. [Google Scholar] [CrossRef] [PubMed]
  127. Kim, S.J.; Lee, S.C.; Hong, S.K.; An, K.; An, G.; Kim, S.R. Ectopic expression of a cold-responsive OsAsr1 cDNA gives enhanced cold tolerance in transgenic rice plants. Mol. Cells 2009, 27, 449–458. [Google Scholar] [CrossRef]
  128. Joo, J.; Lee, Y.H.; Kim, Y.K.; Nahm, B.H.; Song, S.I. Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue-dependent sugar and hormone-sensitivities. Mol. Cells 2013, 35, 421–435. [Google Scholar] [CrossRef]
  129. Li, X.Y.; Li, L.J.; Zuo, S.Y.; Li, J.; Wei, S. Differentially expressed ZmASR genes associated with chilling tolerance in maize (Zea mays) varieties. Funct. Plant Biol. 2018, 45, 1173–1180. [Google Scholar] [CrossRef]
  130. Hsu, Y.F.; Yu, S.C.; Yang, C.Y.; Wang, C.S. Lily ASR protein-conferred cold and freezing resistance in Arabidopsis. Plant Physiol. Biochem. 2011, 49, 937–945. [Google Scholar] [CrossRef]
  131. Perez-Diaz, J.; Wu, T.M.; Perez-Diaz, R.; Ruiz-Lara, S.; Hong, C.Y.; Casaretto, J.A. Organ- and stress-specific expression of the ASR genes in rice. Plant Cell Rep. 2014, 33, 61–73. [Google Scholar] [CrossRef]
  132. Wu, X.M.; Gao, R.X.; Mao, R.J.; Lin, Y.; Yang, Z.M.; Li, J.; Cao, F.X.; Li, M. Inducing bract-like leaves in Arabidopsis through ectopically expressing an ASR gene from the dove tree. Ind. Crops Prod. 2022, 180, 114796. [Google Scholar] [CrossRef]
  133. Yacoubi, I.; Hamdi, K.; Fourquet, P.; Bignon, C.; Longhi, S. Structural and Functional Characterization of the ABA-Water Deficit Stress Domain from Wheat and Barley: An Intrinsically Disordered Domain behind the Versatile Functions of the Plant Abscissic Acid, Stress and Ripening Protein Family. Int. J. Mol. Sci. 2021, 22, 2314. [Google Scholar] [CrossRef] [PubMed]
  134. Clemens, S.; Ma, J.F. Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods. In Annual Review of Plant Biology; Merchant, S.S., Ed.; Annual Review of Plant Biology; Annual Reviews: Palo Alto, CA, USA, 2016; Volume 67, pp. 489–512. [Google Scholar]
  135. Elazab, D.; Lambardi, M.; Capuana, M. In Vitro Culture Studies for the Mitigation of Heavy Metal Stress in Plants. Plants 2023, 12, 3387. [Google Scholar] [CrossRef]
  136. Konrad, Z.; Bar-Zvi, D. Synergism between the chaperone-like activity of the stress regulated ASR1 protein and the osmolyte glycine-betaine. Planta 2008, 227, 1213–1219. [Google Scholar] [CrossRef] [PubMed]
  137. Goldgur, Y.; Rom, S.; Ghirlando, R.; Shkolnik, D.; Shadrin, N.; Konrad, Z.; Bar-Zvi, D. Desiccation and zinc binding induce transition of tomato abscisic acid stress ripening 1, a water stress- and salt stress-regulated plant-specific protein, from unfolded to folded state. Plant Physiol. 2007, 143, 617–628. [Google Scholar] [CrossRef] [PubMed]
  138. Wetzler, D.E.; Wightman, F.F.; Bucci, H.A.; Rinaldi, J.; Caramelo, J.J.; Iusem, N.D.; Ricardi, M.M. Conformational plasticity of the intrinsically disordered protein ASR1 modulates its function as a drought stress-responsive gene. PLoS ONE 2018, 13, e0202808. [Google Scholar] [CrossRef]
  139. Arenhart, R.A.; De Lima, J.C.; Pedron, M.; Carvalho, F.E.L.; Da Silveira, J.A.G.; Rosa, S.B.; Caverzan, A.; Andrade, C.M.B.; Schunemann, M.; Margis, R.; et al. Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ. 2013, 36, 52–67. [Google Scholar] [CrossRef]
  140. Arenhart, R.A.; Bai, Y.; de Oliveira, L.F.V.; Neto, L.B.; Schunemann, M.; Maraschin, F.D.; Mariath, J.; Silverio, A.; Sachetto-Martins, G.; Margis, R.; et al. New Insights into Aluminum Tolerance in Rice: The ASR5 Protein Binds the STAR1 Promoter and Other Aluminum-Responsive Genes. Mol. Plant 2014, 7, 709–721. [Google Scholar] [CrossRef]
  141. Arenhart, R.A.; Schunemann, M.; Neto, L.B.; Margis, R.; Wang, Z.Y.; Margis-Pinheiro, M. Rice ASR1 and ASR5 are complementary transcription factors regulating aluminium responsive genes. Plant Cell Environ. 2016, 39, 645–651. [Google Scholar] [CrossRef]
  142. Li, R.H.; Liu, G.B.; Wang, H.; Zheng, Y.Z. Effects of Fe3+ and Zn2+ on the Structural and Thermodynamic Properties of a Soybean ASR Protein. Biosci. Biotechnol. Biochem. 2013, 77, 475–481. [Google Scholar] [CrossRef]
  143. Ahanger, M.A.; Agarwal, R.M. Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L.) as influenced by potassium supplementation. Plant Physiol. Biochem. 2017, 115, 449–460. [Google Scholar] [CrossRef]
  144. Qiu, D.; Hu, W.; Zhou, Y.; Xiao, J.; Hu, R.; Wei, Q.H.; Zhang, Y.; Feng, J.L.; Sun, F.S.; Sun, J.T.; et al. TaASR1-D confers abiotic stress resistance by affecting ROS accumulation and ABA signalling in transgenic wheat. Plant Biotechnol. J. 2021, 19, 1588–1601. [Google Scholar] [CrossRef] [PubMed]
  145. Perez-Diaz, J.; Perez-Diaz, J.R.; Medeiros, D.B.; Zuther, E.; Hong, C.Y.; Nunes-Nesi, A.; Hincha, D.K.; Ruiz-Lara, S.; Casaretto, J.A. Transcriptome analysis reveals potential roles of a barley ASR gene that confers stress tolerance in transgenic rice. J. Plant Physiol. 2019, 238, 29–39. [Google Scholar] [CrossRef]
  146. Yang, C.Y.; Chen, Y.C.; Jauh, G.Y.; Wang, C.S. A lily ASR protein involves abscisic acid signaling and confers drought and salt resistance in Arabidopsis. Plant Physiol. 2005, 139, 836–846. [Google Scholar] [CrossRef] [PubMed]
  147. Zheng, J.X.; Zhang, H.; Su, H.X.; Xia, K.F.; Jian, S.G.; Zhang, M. Ipomoea pes-caprae IpASR Improves Salinity and Drought Tolerance in Transgenic Escherichia coli and Arabidopsis. Int. J. Mol. Sci. 2018, 19, 2252. [Google Scholar] [CrossRef] [PubMed]
  148. Yoon, J.S.; Flores, P.C.; Seo, Y.W. Overexpression of BdASR2 Plays a Positive Role in Response to Salt Tolerance in Brachypodium distachyon. J. Plant Biol. 2022, 65, 111–119. [Google Scholar] [CrossRef]
  149. Miao, H.X.; Wang, Y.; Liu, J.H.; Jia, C.H.; Hu, W.; Sun, P.G.; Jin, Z.Q.; Xu, B.Y. Molecular cloning and expression analysis of the MaASR1 gene in banana and functional characterization under salt stress. Electron. J. Biotechnol. 2014, 17, 287–295. [Google Scholar] [CrossRef]
  150. Yildirim, E.; Ekinci, M.; Turan, M.; Dursun, A.; Kul, R.; Parlakova, F. Roles of glycine betaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.). Arch. Agron. Soil Sci. 2015, 61, 1673–1689. [Google Scholar] [CrossRef]
  151. Srivastava, D.; Verma, G.; Chawda, K.; Chauhan, A.S.; Pande, V.; Chakrabarty, D. Overexpression of Asr6, abscisic acid stress-ripening protein, enhances drought tolerance and modulates gene expression in rice (Oryza sativa L.). Environ. Exp. Bot. 2022, 202, 105005. [Google Scholar] [CrossRef]
  152. Wu, M.; Liu, R.; Gao, Y.M.; Xiong, R.; Shi, Y.N.; Xiang, Y. PheASR2, a novel stress-responsive transcription factor from moso bamboo (Phyllostachys edulis), enhances drought tolerance in transgenic rice via increased sensitivity to abscisic acid. Plant Physiol. Biochem. 2020, 154, 184–194. [Google Scholar] [CrossRef]
  153. Liang, Y.N.; Jiang, Y.L.; Du, M.; Li, B.Y.; Chen, L.; Chen, M.C.; Jin, D.M.; Wu, J.D. ZmASR3 from the Maize ASR Gene Family Positively Regulates Drought Tolerance in Transgenic Arabidopsis. Int. J. Mol. Sci. 2019, 20, 2278. [Google Scholar] [CrossRef] [PubMed]
  154. Yoon, J.S.; Kim, J.Y.; Kim, D.Y.; Seo, Y.W. A novel wheat ASR gene, TaASR2D, enhances drought tolerance in Brachypodium distachyon. Plant Physiol. Biochem. 2021, 159, 400–414. [Google Scholar] [CrossRef] [PubMed]
  155. Liu, H.Y.; Dai, J.R.; Feng, D.R.; Liu, B.; Wang, H.B.; Wang, J.F. Characterization of a Novel Plantain Asr Gene, MpAsr, that is Regulated in Response to Infection of Fusarium oxysporum f. sp cubense and Abiotic Stresses. J. Integr. Plant Biol. 2010, 52, 315–323. [Google Scholar] [CrossRef] [PubMed]
  156. Guo, W.Y.; Chen, S.Y.; Xu, Y.P.; Cai, X.Z. OsASR6 Alleviates Rice Resistance to Xanthomonas oryzae via Transcriptional Suppression of OsCIPK15. Int. J. Mol. Sci. 2022, 23, 6622. [Google Scholar] [CrossRef]
  157. Li, N.; Wei, S.T.; Chen, J.; Yang, F.F.; Kong, L.G.; Chen, C.X.; Ding, X.H.; Chu, Z.H. OsASR2 regulates the expression of a defence-related gene, Os2H16, by targeting the GT-1 cis-element. Plant Biotechnol. J. 2018, 16, 771–783. [Google Scholar] [CrossRef]
  158. Huang, J.F.; Shen, L.; Yang, S.; Guan, D.Y.; He, S.L. CaASR1 promotes salicylic acid- but represses jasmonic acid-dependent signaling to enhance the resistance of Capsicum annuum to bacterial wilt by modulating CabZIP63. J. Exp. Bot. 2020, 71, 6538–6554. [Google Scholar] [CrossRef]
Ijms 25 10283 g001
Figure 1. ASR genes responding to low-temperature stress, drought stress, pathogen stress and metal ions, and as well as being involved in plant growth. The external pink areas represents plant growth and response to different stress conditions. The internal yellow areas represent ASR genes in different species.
Figure 1. ASR genes responding to low-temperature stress, drought stress, pathogen stress and metal ions, and as well as being involved in plant growth. The external pink areas represents plant growth and response to different stress conditions. The internal yellow areas represent ASR genes in different species.
Ijms 25 10283 g001
Table 1. Gene structure, subcellular localization, and protein physicochemical properties of ASRs from different species. References: [107,113,115,116,118,120,121,122].
Table 1. Gene structure, subcellular localization, and protein physicochemical properties of ASRs from different species. References: [107,113,115,116,118,120,121,122].
SpeciesGene IDExonsIntronsLength (aa)Mw (kD)PIGravySubcellular Localization
Canavalia roseaCrASR12123525.925.79−1.449Nucleus,
Cytoplasm
CrASR22113014.986.34−1.321Nucleus,
Cytoplasm,
Mitochondria
CrASR32111413.096.41−1.341Nucleus,
Cytoplasm, Mitochondria
Triticum
aestivum		TaASR12113715.36.06−1.2Nucleus
TaASR22126428.835.19−1.76Nucleus
TaASR32111012.349.89−1.29Nucleus,
Cytoplasm
TaASR4219710.769.99−1.33Nucleus
TaASR52111012.349.89−1.29Nucleus
TaASR6219410.399.82−1.23Nucleus
TaASR72121923.186.25−0.98Nucleus
TaASR82121823.216.24−0.93Nucleus
TaASR92121923.686.16−1.07Nucleus
TaASR102123024.917.79−0.99Nucleus
TaASR112111012.349.89−1.29Nucleus
TaASR1232134156.11−1.04Nucleus,
Cytoplasm
TaASR132127930.344.97−1.76Nucleus
TaASR142110011.049.99−1.35Nucleus,
Cytoplasm
TaASR152122724.396.27−1.09Nucleus,
Cytoplasm
TaASR162122123.456.1−0.95Nucleus,
Cytoplasm
TaASR172121923.146.03−0.96Nucleus
TaASR18219710.849.99−1.33Nucleus
TaASR192113815.466.14−1.2Nucleus
TaASR202126228.655.2−1.74Nucleus,
Cytoplasm
TaASR213217518.866.51−1.11Nucleus
TaASR222121823.26.24−0.92Nucleus,
Cytoplasm
TaASR232122023.256.19−0.99Nucleus,
Cytoplasm
TaASR24219410.449.7−1.22Nucleus,
Cytoplasm
TaASR25219110.19.87−1.21Nucleus
TaASR26219410.379.74−1.23Nucleus,
Cytoplasm
TaASR27219710.8110.04−1.37Nucleus,
Cytoplasm
TaASR282110011.1610.14−1.33Nucleus,
Cytoplasm
TaASR292111012.349.89−1.29Nucleus
Setaria italicaSiASR11220022.56.3−1.190Nucleus
SiASR21113715.46.2−1.277Nucleus
SiASR32110511.79.7−1.147Nucleus
SiASR43210211.59.3−1.417Nucleus
SiASR51117319.46.3−1.366Nucleus
SiASR62110111.56.8−1.636Nucleus
Brachypodium distachyonBdASR12120121.826.18−1.061Nucleus
BdASR22111112.279.84−1.155Whole cells
BdASR32110211.059.82−1.208Whole cells
BdASR42113915.376.17−1.025Whole cells
BdASR52124025.975.11−1.641Whole cells
Pyrus bretschneideriPbrASR12120322.355.63−1.426Nucleus
PbrASR22118219.815.96−1.387Nucleus
PbrASR32113415.296.1−1.439Nucleus,
Cytoplasm
Fragaria vescaFvASR12119221.026.03−1.278Nucleus
Malus × domesticaMdASR12120222.125.74−1.421Nucleus
MdASR22113312.056.17−1.276Nucleus
MdASR32111913.519.69−0.639Nucleus
Prunus aviumPavvASR12113516.415.36−1.082Nucleus
PavvASR22128329.995.39−1.54Nucleus
PavvASR32127729.355.53−1.537Nucleus
PavvASR42126928.065.53−1.271Nucleus
PavvASR52127629.155.13−1.523Nucleus
PavvASR621667.76.18−1.432Nucleus
PavvASR721667.736.24−1.538Nucleus
PavvASR82111012.576.26−1.328Nucleus
Pyrus
communis		PcoASR12120222.055.7−1.367Nucleus
PcoASR22113415.276.1−1.436Nucleus
PcoASR32113515.466.48−1.393Nucleus
Prunus mumePmASR11114815.185−1.105Nucleus
PmASR22114115.946.19−1.293Nucleus
PmASR33222323.855.66−1.312Nucleus
PmASR44323426.035.66−0.978Nucleus
PmASR521667.666.2−1.438Nucleus
Prunus persicaPryASR1219811.036.4−1.364Nucleus
PryASR22119320.765.68−1.335Nucleus
PryASR32131133.225.62−1.374Nucleus
Rubus occidentalisRocASR12119221.095.77−1.319Nucleus
Malus × domesticaMdASR12120222.135.74−1.421Nucleus
MdASR22113315.086.41−1.162Nucleus
MdASR32112013.225.48−1.171Nucleus
MdASR42118219.86−1.462Nucleus
MdASR52120022.275.91−1.433Nucleus
Zea maysZmASR12113815.545.89−1.264Nucleus
ZmASR22113114.96.15−1.373Nucleus
ZmASR32126927.785.07−1.49Nucleus
ZmASR42118120.436.3−1.28Nucleus
ZmASR52110411.796.65−1.319Nucleus,
Cytoplasm
ZmASR62110611.548.05−1.125Nucleus
ZmASR71110612.0810.56−1.301Nucleus
ZmASR81110211.469.66−1.19Nucleus
ZmASR91110211.419.78−1.205Nucleus
Oryza sativaOsASR1219610.579.62−1.222Nucleus
OsASR22110511.689.66−1.212Nucleus
OsASR32110511.686.76−1.112Nucleus
OsASR42113815.466.20−1.243Nucleus
OsASR52122924.469.49−1.313Nucleus
OsASR62113615.506.48−1.113Chloroplast, Cytoplasm, Nucleus
Table 2. The functions of ASRs in different plants in regulating fruit ripening process. References: [21,101,110,124,126,127].
Table 2. The functions of ASRs in different plants in regulating fruit ripening process. References: [21,101,110,124,126,127].
SpeciesGene NameDescription of Biological Functions
Nicotiana tabacumNtASR1Transgenic lines with reduced ASR1 protein levels in tobacco show impaired glucose metabolism and altered levels of ABA and GA, which in turn regulate leaf Glc signaling and carbon partitioning.
Prunus persica f.
atropurpurea		PpASR1Transient expression of PpASR in tomato promotes fruit softening and ripening in cross-signaling between ABA and sucrose.
Fragaria ananassa
Duch.		FaASR1Overexpression of ASR1 significantly increases the expression levels of anthocyanin biosynthesis and ABA biosynthesis genes in strawberry and further enhances the ripening and softening process of the strawberry fruit.
Zea mays L.ZmASR1The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions.
Solanum lycopersicum L.SlASR1SlASR1 enhances the accumulation of proline, methionine, valine, and isoleucine in tomato, thereby promoting fruit development.
Oryza sativa L.OsASRAs a downstream component of the ABA signaling pathway, OsASR also increases the number of tillers and grain yield in rice via regulating ABA levels.
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

Zhang, Y.; Wang, M.; Kitashov, A.V.; Yang, L. Development History, Structure, and Function of ASR (Abscisic Acid-Stress-Ripening) Transcription Factor. Int. J. Mol. Sci. 2024, 25, 10283. https://doi.org/10.3390/ijms251910283

AMA Style

Zhang Y, Wang M, Kitashov AV, Yang L. Development History, Structure, and Function of ASR (Abscisic Acid-Stress-Ripening) Transcription Factor. International Journal of Molecular Sciences. 2024; 25(19):10283. https://doi.org/10.3390/ijms251910283

Chicago/Turabian Style

Zhang, Yue, Mengfan Wang, Andery V. Kitashov, and Ling Yang. 2024. "Development History, Structure, and Function of ASR (Abscisic Acid-Stress-Ripening) Transcription Factor" International Journal of Molecular Sciences 25, no. 19: 10283. https://doi.org/10.3390/ijms251910283

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