How Does Abscisic Acid Control Fruit Quality as a Plant Bioregulator?

Abstract

Various attempts have been made to use abscisic acid (ABA) as a plant bioregulator (PBR). Recently, a new ABA formulation, produced through microbial fermentation, has been commercialized in Japan as a PBR for improving grape peel color. Nonetheless, the horticultural application of ABA remains limited compared to other plant hormones. Generally, the vital functions of ABA include the regulation of abiotic stress tolerance and plant dormancy via metabolic changes associated with the antioxidant system and the modulation of sugar biosynthesis/translocation, respectively. These metabolic changes are crucial for the quality of fruit, suggesting the potential of ABA for promoting the production of high-quality fruit. In non-climacteric fruit, ABA plays a pivotal role in anthocyanin pigmentation, a significant component of the antioxidant machinery. Studies in grapes and strawberries have shown that the responses to ABA differ depending on the type of ABA agonist used and the specific organs to which it is applied. Herein, the influence of ABA on climacteric fruit exhibiting ethylene-regulated ripening is discussed. ABA-mediated ethylene induction followed by ripening suggests a shared regulatory mechanism that underlies ripening in both climacteric and non-climacteric fruits that involves crosstalk between ABA and ethylene. This review firstly summarizes the historical challenges with ABA and its agonist for application as PBRs and discusses the role of ABA in the ripening of non-climacteric fruit, particularly grapes. Subsequently, the molecular background of ABA in both climacteric and non-climacteric fruit ripening is explained, with a focus on peel coloration, sugar synthesis, and aroma volatile synthesis.

Introduction

Abscisic acid (ABA) was initially isolated as a substance that accelerated cotton (Gossypium hirsutum L.) fruit abscission (Liu and Carnsdagger, 1961). In sycamore leaves (Platanus occidentalis L.), ABA significantly contributes to photoperiodic-controlled bud dormancy (Cornforth et al., 1965). In various plant species, its versatile functions in stomatal regulation, seed dormancy, and responses to environmental stresses have been demonstrated. For instance, several researchers have proposed ABA as a decisive factor in seed maturation, dormancy, and germination. An increased ABA level arrests the cell cycle and prevents premature germination, while it decreases during imbibition, promoting germination after dormancy (Ali et al., 2022; Finkelstein, 2013; Tuan et al., 2018). The relationship between ABA levels and seed dormancy has been well established; it has been simulated and modeled as an ordinary differential equation (Penfield et al., 2008). Particularly, ABA signaling closely interacts with glucose signaling, which arrests embryonic hypocotyl development in Arabidopsis (Dekkers et al., 2008). Glucose serves as a fuel for hypocotyl development during seed germination in Arabidopsis (Finkelstein and Lynch, 2000). Recent studies in Arabidopsis have validated the effects of ABA on sugar allocation and metabolism during embryonic hypocotyl development (Xue et al., 2021). ABA impairs glucose influx across the plasma membrane via the suppression of sugar transporter genes. Similarly, ABA is involved in the maintenance of potato (Solanum tuberosum L.) tuber dormancy; ABA accumulation in dormant buds induces plasmodesmatal closure, preventing sugar transportation from the tuber to the buds (Danieli et al., 2023). Furthermore, glucose levels are limited by the suppression of sucrose cleavage and the enhancement of sucrose synthesis. Similar to seed and tuber dormancy, the winter bud dormancy of fruit crops is associated with ABA (Hernandez et al., 2021; Rubio et al., 2019; Zhang et al., 2018). In grapevine (Vitis vinifera L.), ABA promotes starch accumulation by repressing sucrose degradation. These observations validate the vital role of ABA in sugar metabolism and translocation.

ABA is closely associated with abiotic stresses such as drought, cold, exposure to heavy metals, salinity, and ultraviolet irradiation (Finkelstein, 2013; Finkelstein and Lynch, 2000; Hewage et al., 2020). ABA is synthesized in the vascular tissues of roots exposed to drought and is transported to the shoots; at the same time, ABA biosynthesis is activated in the leaves during drought stress. Signaling cascades associated with local biosynthesized and root-emitted ABA integrate and induce stomatal closure, leading to reduced transpiration and water loss. In addition to the abovementioned mechanical response to drought stress, a biochemical response was reported, particularly an increase in antioxidant levels that typically protects cells against reactive oxygen species (ROS) generated following drought stress. In olive (Olea europaea L.) leaves, the phenylpropanoid pathway is stimulated, and phenolic compounds such as oleuropein, verbascoside, luteolin 7-O-glucoside, and apigenin 7-O-glucoside, accumulate under long complete water depletion conditions (Mechri et al., 2020). Furthermore, a recent omics-based analysis demonstrated a global transcriptional change in antioxidant-related genes during the development of drought tolerance in wild soybeans (Glycine soja Sieb. and Zucc.) (Aleem et al., 2021). This activation of the antioxidant system involves phenolic compounds, carotenoids, vitamin C, and flavonoids (Sarker and Oba, 2018). In addition to drought, various other stress conditions induce the development of antioxidant systems. In watermelons (Citrullus lanatus Thunb.) and peaches (Prunus persica L.), cold injury-associated oxidative damage is alleviated by the promotion of antioxidant enzymes via increased levels of internal ABA or the application of exogenous ABA (Guo et al., 2021; Tang et al., 2022). Furthermore, ABA regulates the antioxidant system under salinity stress and exposure to heavy metals such as cadmium, and UV-C irradiation in tomato (Solanum Lycopersicum L.), flowering stalks (Brassica campestris L.), and strawberries (Fragaria × ananassa Duch.), respectively (Hu et al., 2021; Shen et al., 2017; Xu et al., 2019). Understanding the mechanisms underlying the ABA-regulated antioxidant system is essential for modulating plant metabolism.

ABA activity has also been associated with anthocyanin content. Anthocyanins are key compounds involved in plant antioxidant machinery and are synthesized via the flavonoid pathway (Holton and Cornish, 1995). Anthocyanin biosynthesis begins with the addition of three malonyl-CoAs to p-coumaroyl-CoA by chalcone synthase (CHS), followed by step-by-step enzymatic modification via chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), dihydroflavonol reductase (DFR), anthocyanidin synthase (ANS), and UDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT) finally synthesized anthocyanins in three different chemical structures including pelargonidin, cyanidin, and delphinidin. These compounds play important biological roles, including involvement in plant pigmentation, resulting in a variety of colors ranging from red to blue and varying levels of antioxidant activity. For instance, delphinidin is the most potent antioxidant, whereas pelargonidin is the weakest (Noda et al., 2002). Therefore, in bread wheat (Triticum aestivum L.), the cadmium toxicity-tolerant genotype exhibits a darker purple coleoptile than the less-tolerant genotype (Shoeva and Khlestkina, 2018). Transcriptional changes in UFGT in response to salinity stress and exogenous ABA treatment have also been analyzed in strawberries and Arabidopsis (Crizel et al., 2020; Shi et al., 2022). ABA-dependent transcriptional regulation of UFGT was reported in the maqui berry (Aristotelia chilensis [Mol.] Stuntz) exposed to drought (González-Villagra et al., 2019). RNA-seq analysis under various abiotic stress conditions revealed the involvement of ABA in the expression of genes such as DFR and ANS, encoding anthocyanin biosynthetic enzymes (Li et al., 2015; Shi et al., 2022; Zhang et al., 2019). Moreover, the transcriptional modulation of DFR, ANS, and UFGT during ABA-stimulated drought tolerance is mediated via miRNA156, which directly binds to and cleaves the mRNA encoded by the SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family, a negative regulator of anthocyanin biosynthesis (González-Villagra et al., 2017; Li et al., 2021). The interaction of ABA with anthocyanins under abiotic stress conditions can be further validated from a molecular viewpoint.

Our journey in this review started with a basal understanding of the metabolic changes induced by ABA in abiotic stress tolerance. Changes in sugar metabolism, antioxidant activity, and anthocyanin content are regarded as determinants of horticultural crop quality. This review examines the potential prospective applications of ABA as a plant bioregulator (PBR) in horticulture and its chemical design. It also discusses the use of ABA to regulate fruit ripening, providing insights into new ABA-based PBR.

Biosynthesis and Associated Cellular Signals—A Potential Target for the Development of PBRs

Understanding the target protein and ligand-protein interaction is the first step in designing drugs (Brogi et al., 2020; Sabe et al., 2021). Comprehensive knowledge of the target protein is crucial for computer-aided drug design; for instance, the antiCOVID-19 drug remdesivir was designed to target SARS-CoV-2 RNA-dependent RNA polymerase (Gao et al., 2020; Yin et al., 2020). The inhibition of protein-related plant hormone biosynthesis is a popular strategy represented by paclobutrazol, an inhibitor of gibberellic acid biosynthesis enzyme ent-kaurene oxidase (Hedden and Graebe, 1985).

ABA is a weakly acidic C15 sesquiterpenoid, naturally synthesized in the form of S-(+)-ABA (Finkelstein, 2013). The initial step of ABA biosynthesis is associated with carotenoid biosynthesis via the MEP pathway, and its biosynthesis pathway is branched from β-carotene, which is found in plastids. The hydroxylation of β-carotene forms xanthophylls, especially zeaxanthin, the precursor of ABA. A lack of zeaxanthin epoxidase, which epoxidates zeaxanthin and forms trans-violaxanthin, resulted in an ABA deficiency in Arabidopsis mutants (aba1) (Rock and Zeevaart, 1991). Analysis of the ABA-deficient mutant aba4 demonstrated that part of trans-violaxanthin is converted to trans-neoxanthin via neoxanthin synthases (ABA4) (North et al., 2007). Both trans-violaxanthin and trans-neoxanthin are isomerized to 9-cis-violaxanthin and 9-cis-neoxanthin, respectively, by an unknown cofactor that interacts with ABA4 (Perreau et al., 2020). Moreover, 9'-cis-epoxycarotenoid dioxygenase (NCED) cleaves these intermediates to form xanthoxin, which is transported to the cytoplasm as a final ABA precursor. Analyses using Arabidopsis mutants aba2 and aba3 confirmed that after enzymatic modification by ABA2 and abscisic aldehyde oxidase, xanthoxin is converted to abscisic aldehyde, followed by S-(+)-ABA (Schwartz et al., 1997; Seo et al., 2000). Although the contribution of the aforementioned enzymes to ABA biosynthesis is well understood, NCED is considered to be the rate-limiting enzyme due to the abundance of violaxanthin in green tissues and the concomitant increases in transcription of NCED with endogenous ABA levels under dehydration stress (Qin and Zeevaart, 1999; Thompson et al., 2004). Recent findings in rice (Oryza sativa L.) have shown that the increase in the chloroplastic β-glucosidase (BGLU) isoenzyme, specifically Os3BGLU6 activity for hydrolyzing glucose-conjugated ABA (ABA-GE) and modulating cellular ABA concentrations, occurs under drought stress (Wang et al., 2020). However, in Arabidopsis, the cellular localization of ABA-GE, particularly in the endoplasmic reticulum, is considered more important than the enzyme activity of BGLU18 (Han et al., 2020). Although the role of ABA release from ABA-GE for internal ABA levels is still a topic of debate (Liang et al., 2020), its importance should not be disregarded. Noticeably, a balance between ABA synthesis and catabolism determines the local ABA levels. In particular, ABA-8'-hydroxylase (CYP707A)-induced turnover of ABA to phaseic acid is an important step in the inactivation of ABA (Kushiro et al., 2004). The importance of plant hormone degradation in PBRs is well understood; forchlorfenuron, an inhibitor of the cytokinin degradation enzyme, has been commercialized.

The strategy of deceiving plant hormone receptor proteins with analogs, such as indole-3-acetic acid analogs, 1-naphthalene acetic acid for auxin receptors, and 1-methylcyclopropene (1-MCP) for ethylene receptors, has been widely adopted while designing PBRs. A pioneering study on ABA receptors focused on the plasma membrane-localized protein known as the G-protein in Arabidopsis (Liu et al., 2007; Pandey et al., 2009). Considering that the initial response to ABA in guard cells is required within one minute under drought stress, it is reasonable to expect the localization of the ABA receptor at the plasma membrane (Pei and Kuchitsu, 2005). However, based on ABA-mimicking chemicals and the ABA-insensitive (ABI) mutant abi2–1 of Arabidopsis, two independent studies reported the PYR/PYL/RCAR protein, setting milestones in ABA receptor studies (Ma et al., 2009; Park et al., 2009). Direct binding of ABA to the internal cavity of the PYR/PYL/RCAR protein suggested the role of PYR/PYL/RCAR protein as a bona fide receptor of ABA in Arabidopsis (Melcher et al., 2009; Miyakawa et al., 2013). When ABA interacts with the cavity of PYR/PYL/RCAR protein, the two unique amino acid residues forming the “gate loop” and the “latch loop” conformationally shift and close the ABA-occupied cavity, which facilitates ABA-binding affinity. The ABA-bound PYR/PYL/RCAR complex sequentially docks to protein phosphatase 2Cs (PP2Cs) via the gate-latch-lock mechanism and functions as a co-receptor to elevate ABA binding to PYR/PYL/RCAR. PP2Cs, identified in abi1 and abi2 mutants of Arabidopsis, dephosphorylate other kinases and are deactivated when ABA binds to the PYR/PYL/RCAR complex (Ma et al., 2009; Yang et al., 2006). Among the target kinases of PP2Cs, SNF1-related kinase2 (SnRK2) plays a vital role in ABA signal transduction in Arabidopsis (Furihata et al., 2006; Umezawa et al., 2009). PP2Cs sustainably bind to SnRK2 in the absence of ABA; however, PYR/PYL/RCAR-ABA-PP2Cs complex formation induces SnRK2-mediated phosphorylation of the ABA-RESPONSIVE ELEMENT-BINDING PROTEIN/ABRE-BINDING FACTORS (AREB/ABF), which activates ABA signaling networks. Additionally, this signaling stimulates the transcription of ABFs, and ABF molecules are accumulated via ABA perception in Arabidopsis (Wang et al., 2019a). Recently, tyrosyl protein sulfotransferase was reported to interact with and break down SnRK2 via post-translational modification of tyrosine sulfation in Arabidopsis (Wang et al., 2023a). However, the specific chemicals targeted in signal transduction have not been reported. The key genes of gibberellic acid signal transduction are known to be involved in the “Green Revolution” as a dwarfing trait (Hedden, 2003), suggesting that signal transduction cascades should be highlighted in future research on PBRs.

Modulation of Internal ABA for Horticultural Application

The use of ABA in horticulture, including its analogs (Fig. 1), has not been commercially available due to a lack of stable and cost-efficient chemical synthesis, which distinguishes it from other hormones (Runkle, 2009). However, in the last 15 years, new formulations produced through microbial fermentation have been developed and released on the market as ProTone, InGrain, and BioNik by Valent BioSciences and Sumitomo Chemical Co., Ltd. (Long Grove, IL, USA). In Japan, S-(+)-ABA, named ABSUP by these companies, was registered as a PBR for table grapes and released in 2023.

Fig. 1

The chemical structures of ABA (1) and ABA analogs; 5-(1,2-epoxy-2,6,6-trimethyl-1-cyclohexyl)-3-methyl-cis, trans-2,4-pentadienoic acid (2), (+)-3'-butyl ABA (3), 1',4'-dihydroxy-γ-ionylideneacetic acid (4), 7'-hydroxy ABA (5), 8'-methylene ABA (6), methylidyne ABA (7), (+)-9'-acetylene ABA (8), (+)-(2Z,4E)-5-(l',4'-dihydroxy-6',6'-dimethyl-2'-methylenecyclohexyl)-3-methyl-2,4-pentadienoic acid (9), 8'-methylene ABA methyl ester (PBI-365) (10), 8'-acethylene ABA methyl ester (PBI-429) (11), acetylenic divinyl methyl-ABA (12); the structure from Chen and MacTaggart (1986) (13), the structure from Kim et al. (1992) (14), 2',3'-iso-PhABA (15), LAB 144143 (16), LAB 17 3711 (17), 2-fluoro epoxy-β-ionylideneacetic acids (18), 2-methoxycarbonyl epoxy-β-ionylideneacetic acids (19), Abz-E3M (20), and Abz-E2B (21).

The historical background of various ABA (1) analogs includes both commercial and experimental purposes. For instance, 5-(1,2-epoxy-2,6,6-trimethyl-1-cyclohexyl)-3-methyl-cis, trans-2,4-pentadienoic acid (2) was synthesized as an ABA analog, which was structurally different from ABA owing to the C1'-dehydration and C4'-methylation in a cyclohexane ring, exhibiting a growth inhibitory effect in lettuce (Lactuca sativa L.) seedlings (Tamura and Nagao, 1969). Similarly, the cyclohexane ring is considered an important site for designing ABA analogs, as observed in C3'- (3) and 7'- (4–5) derivatives of ABA (Oritani et al., 1984; Song et al., 2020; Walker-Simmons et al., 1997; Yoshida et al., 2019). Among them, an analog created by modification of C8' showed a wide variety. 8'-methylene (6) and methylidyne (7) ABA showed a more substantial inhibitory effect on wheat embryo germination and rice elongation, respectively, than ABA (Abrams et al., 1997; Todoroki et al., 1997). 9'-vinylation (8) was demonstrated as a similarly positioned carbon modification (Mizutani and Todoroki, 2006). Moreover, a side-chain-modified structure was presented as an ABA analog. The methyl-esterified carboxy group at C1, the hydroxy ester of (+)-(2Z,4E)-5-(l',4'-dihydroxy-6',6'-dimethyl-2'-methylenecyclohexyl)-3-methyl-2,4-pentadienoic acid (9), was isolated as a natural ABA analog from the fungus Cercospora cruenta, which inhibited the growth of rice seedlings (Oritani et al., 1984). Various side-chain modifications, in addition to esterification (10–11), have been attempted, such as vinyl acetylation (12) and conjugation of the benzene ring (13–14) (Asami et al., 1998; Chen and MacTaggart, 1986; Kim et al., 1992; Wilen et al., 1994). Other artificially synthesized ABA analogs derived from different chemicals include iso-PhABA and APAn (15) (from 1-tetralone) (Che et al., 2020; Han et al., 2017; Nyangulu et al., 2006), LAB 144143 (16)/LAB 17 3711 (17) (from terpenoid) (Flores et al., 1988), and 2-fluoro (18) and 2-methoxycarbonyl epoxy-β-ionylideneacetic acids (19) (from epoxy-β-ionylideneacetic acid) (Kiyota et al., 1996). A novel ABA synthesis method has been developed, and S-(+)-ABA-containing PBRs have been commercialized for the last 15 years; however, the problem of rapid inactivation of ABA via biodegradation remains. Therefore, the development of new ABA analogs is ongoing.

The mechanism by which ABA analogs influence plant growth has been discussed in terms of the inhibition of ABA degradation enzymes. The C8' acetylated ABA and its methyl ester (PBI 429) irreversibly inhibit CYP701A activity and change the stomatal conductance of apple (Malus × domestica Borkh.) and pansies (Viola × wittrockiana Gams.) (McArtney et al., 2014; Weaver and van Iersel, 2014). Classically, uniconazole and its derivatives, such as diniconazole, IMI-OH, and UT4, are well documented (Kitahata et al., 2005; Todoroki et al., 2008, 2009a); Uniconazole functions in a cytochrome P450-dependent manner and also affects CYP701A in the gibberellin synthesis pathway (Izumi et al., 1988). Thus, although uniconazole enhances drought tolerance in rice seedlings, elongation is strongly suppressed (Todoroki et al., 2009b). Abscinazoles (Abz), a specific inhibitor of ABA 8'-hydroxylase, was developed through a series of studies on uniconazole-based chemicals (Okazaki et al., 2012; Takeuchi et al., 2016; Todoroki et al., 2009b). The strongest Abz, Abz-E3M (20), stimulated stomatal closure and drought tolerance without gibberellin-associated dwarfing, suggesting that Abz-E3M can specifically inhibit ABA 8'-hydroxylase activity in rice. The practical application of Abz in other horticultural crops, including maize and apple seedlings, was reported (Kondo et al., 2012). Previously, we reported a protective effect of Abz-E2B (21) against salt tolerance beyond the experimental period (16 days). Therefore, the application of an ABA 8'-hydroxylase inhibitor is considered a long-lasting environmental stress mitigation, which is more effective than ABA (Sales et al., 2017).

Other aspects of ABA involve the role of chemicals such as the PBR in relation to the removal of ABA, as the germination rate of seeds is influenced by the abundance of ABA. Chemicals that disturb ABA biosynthesis have been reported; for instance, nordihydroguaiaretic acid (NDGA) (22) and abamine SG (23) inhibit NCED, and fluridone and norflurazon target carotenoid biosynthesis (Bartels and Watson, 1978; Han et al., 2004) (Fig. 2). Although high target enzyme-specificity was observed in abamine SG, NDGA and fluridone (24)/norflurazon (25) caused morphological changes by blocking lipid metabolism and decolorization due to a lack of carotenoids, respectively. The determination of PYR/PYL/RCAR proteins significantly influenced the design of ABA-specific inhibitors in terms of receptor competitors. The PYR/PYL/RCAR receptor was identified while studying pyrabactin (26), which occupies the ABA-binding pocket; however, it does not interact with the gate loop, forming an unclosed conformation that does not interfere with PP2Cs activity (Melcher et al., 2010). Recently developed ABA antagonists, such as AS-6 (27), PAN-Me (28), and antabactin, interact with the gate loop, but show a noncanonical closed-gate receptor conformer (Takeuchi et al., 2014, 2018; Vaidya et al., 2021). Noticeably, 13 ABA receptors (PYR1 and PYL1-12) have been reported in Arabidopsis, and the specificity spectrum of these antagonists against the receptors varies. AA1 (29), an agonist specific to all ABA receptors, has also been designed (Ye et al., 2017).

Fig. 2

The structures of chemicals synthesized as ABA inhibitors; nordihydroguaiaretic acid (22), abamine SG (23), fluridone (24), norflurazon (25), pyrabactin (26), AS-6 (27), PAN-Me (28), AA1 (29).

ABA-mediated Fruit Quality Control in Non-climacteric Fruit

Based on the ripening process, fleshy fruits are conventionally categorized into two types: climacteric and non-climacteric; the differences between them have been reviewed and explored (Cherian et al., 2014; Paul et al., 2012; Perotti et al., 2023; Pujol and Garcia-Mas, 2023). The two types of fruit ripening are defined by distinct respiratory patterns. Climacteric fruits, such as apples, bananas (Musa spp.), and tomatoes, exhibit a burst of respiration at the initial stage of ripening. Moreover, the critical role of ethylene in increasing respiration, which coordinates fruit softening, conversion of starch into sugar, production of aromatic volatiles, and other biological processes related to ripening of climacteric fruit, has been well demonstrated. In contrast, during the ripening of non-climacteric fruits such as grapes, sweet cherries (Prunus avium L.), and strawberries, major changes in respiration and ethylene production are generally undetectable. Unlike climacteric fruit that exhibit rapidly promoted ripening at the end of the growth stage, non-climacteric fruit gradually mature, and the underlying hormonal regulatory mechanism remains unclear. However, various studies in grapes and strawberries have suggested the possible management of non-climacteric fruits using ABA.

Several studies reported increased levels of endogenous ABA and genes, such as NCEDs, that are involved in ABA biosynthesis during berry ripening of both strawberries and grapes (Kondo et al., 2014; Li et al., 2022a, b; Saito et al., 2022). Moreover, the effects of exogenous ABA on the ripening of strawberries and grapes have been reported. A recent report illustrated various effects of exogenous ABA application methods in strawberries; an ABA feed from the stalk was more stimulative than an ABA injection to the receptacle for berry ripening (Li et al., 2022b). The authors demonstrated that stalk feeding induces the transportation of ABA to achenes, which promotes autocatalytic ABA biosynthesis via NCED transcription. The crucial role of ABA and the stabilization of NCED mRNA in berry ripening was indicated (Zhou et al., 2021). N6-methyladenosine (m⁶A methylation), a post-transcriptional modification, was dramatically altered during the ripening of the diploid woodland strawberry (Fragaria vesca). Among the thousands of mRNAs exhibiting ABA-dependent m⁶A hypermethylation, FvNCED5 and FvAREB1 were identified, and it was assumed that high mRNA stability mediated by m⁶A methylation contributes to translational efficiency. In strawberries, ABA induces an increase in total sugar, anthocyanin content, and antioxidant capacity associated with ROS signaling (Zhang et al., 2021). In grapes, an increase in free ABA levels was recorded at the onset of the berry ripening phase called veraison, which is defined as the second phase in the growth cycle of berries (Wang et al., 2022a). In this phase, the softening of berries, accumulation of sugar and anthocyanin, and development of aromatic volatiles are initiated. The effect of exogenous ABA application in grapes was similarly explored to that in strawberries, and a significant improvement in anthocyanin content and related molecular mechanisms, have been widely reviewed (Azuma, 2018; Wang et al., 2023b). The increase in antioxidants, including total phenolic and flavonoid compounds, following exogenous ABA application was similarly shown in ‘Cabernet Sauvignon’, ‘Merlot’, and ‘Red Globe’ (Alenazi et al., 2019; Zhu et al., 2016). Contrastingly, the correlation between exogenous ABA application and altered sugar content in grape berries is complex. Previously, most researchers detected no increase in sugar concentrations after exogenous ABA application (Saito et al., 2022). Another report indicated an increase in sugar content following exogenous ABA application (Hong et al., 2023); however, this group indicated weakened ABA signaling through the reduction of the SnRK1 transcript. Previously, we found different patterns of alterations in ABA and sugar contents under various lighting conditions (Fig. 3). Although irradiation using a blue-light-emitting diode (LED) resulted in higher levels of endogenous ABA compared to that induced by red-LED irradiation, the sugar content showed similar fluctuations between red-LED and blue-LED irradiation (Rodyoung et al., 2016). The variation in the distribution of ABA based on the organ of its application in grapes remains unclear; however, it crucially affects the ripening of non-climacteric fruit, and further elucidation of fruit quality control by ABA application is required.

Fig. 3

The effects of blue- and red-LED irradiation applied at night on endogenous ABA, anthocyanin, and sugar biosynthesis; strong (++) or moderate (+) enhancement of the pathways was detected compared with the control (without irradiation) plants.

Ripening control via suppressed ABA content is another essential aspect of growing non-climacteric fruit. Externally applied fluridone delays strawberry ripening (Jia et al., 2011). In grapes, postharvest treatment by vacuum infiltration of NDGA prevents abscission in berries, promoting an extended shelf life (Zhu et al., 2022). However, in the black grape cultivar ‘Kyoho’, treated with NDGA at veraison, there was a significant interruption in anthocyanin accumulation (Jia et al., 2018; Kondo et al., 2022). ABA plays a vital role in R2R3-MYB transcription factor-mediated signaling, which speeds up the transcription of DFR and UFGT. The inhibition of ABA signaling by virus-induced silencing of the ABI4 gene delayed coloration (Chai and Shen, 2016). In contrast, the application of NDGA in cherries, which are considered non-climacteric fruit, was also examined, and there was difficulty in extending the shelf life, suggesting that NDGA-mediated quality control is limited and dependent on the target fruit species (Luo et al., 2014a). In citrus (Citrus reticulata Blanco), it was demonstrated that NDGA induced an extension of the storage period, and the preservation of peel color was highlighted through the maintenance of chlorophyll content (Wang et al., 2016). The green peel of the ‘Shine Muscat’, a yellow-green grape cultivar bred in Japan and widely cultivated in East Asia, is generally preferred in the market. In ‘Shine Muscat’, NDGA application to berries at veraison suppressed chlorophyll degradation (Lin et al., 2018b). These results suggest that ABA inhibition can aid in controlling the shelf life and preferred appearance of fruits. While exploring an effective treatment method, we developed a foliar NDGA application protocol that exhibited an effect similar to that of conventional dipping and laborless methods (Saito et al., 2022). For instance, a foliar application of NDGA changed both the peel color and the aroma volatile content in ‘Kyoho’. Although the molecular basis underlying the ABA-regulated aroma volatile levels remains unclear, a change in the hypoxic condition and enzymatic activity of aroma volatile biosynthesis (alcohol dehydrogenase, ADH) inside the flesh was assumed (Xiao et al., 2018). Our suggestions about the quality control in non-climacteric fruit using ABA inhibitors can help expand the aroma volatile content in addition to the regulation of peel coloration and antioxidant content.

Next, we focused on various types of ABA-like chemicals or ABA-specific inhibitors, considering the problems of rapid biodegradation of ABA or specificity of NDGA. A study reported an increase in vitamin C content and antioxidant activity by spraying the ABA agonist pyrabactin before ripening (Rubus idaeus L.) (Miret and Munné-Bosch, 2016); however, knowledge regarding fruit quality control using ABA agonists and antagonists remains limited; most analyses using these chemicals focused on seed germination and stomatal closure. We examined the PYR/PYL/RCAR inhibitor AS-6 applied to ‘Kyoho’, which affected anthocyanin accumulation even with normal ABA accumulation, suggesting flexibility in the control of fruit quality by using ABA-related chemicals (Kondo et al., 2022). In particular, the application of Abz in grapes could be a forerunner for newly designed chemicals for controlling fruit quality (Fig. 4). Abz-E3M specifically inhibits ABA degradation by targeting the CYP707A enzyme and enhances berry ripening in ‘Shine Muscat’ (Lin et al., 2018a). Surprisingly, the application of Abz-E3M not only accelerated the ripening process, including berry softening and reducing titratable acid, but also increased sugar content. An enhancement of sugar accumulation mediated by Abz was identified in the ‘Kyoho’ variety (Thunyamada et al., 2023). The involvement of ABA in sugar metabolism is still unclear; however, Abz-E3M application stimulated sugar accumulation in both ‘Kyoho’ and ‘Shine Muscat’ in our study (Lin et al., 2018a; Thunyamada et al., 2023). Although both exogenous ABA and an improved endogenous ABA level with Abz-E3 treatment enhanced the anthocyanin content in ‘Kyoho’, the underlying molecular signal transduction, especially by DNA methylation, varies between these effects (Saito et al., 2018). Thus, we speculate that the method used to regulate ABA levels, such as exogenous ABA application or prevention of ABA degradation, is vital for implementing flexible management of fruit quality. Additionally, it will be necessary to ensure the food and environmental safety of these chemicals in order to commercialize the wide range of ABA-related chemicals.

Fig. 4

The different processes of berry maturation regulated by ABA accumulation via inhibited ABA degradation using Abz-E3M (magenta arrows) and exogenous ABA application (blue arrows).

Can ABA Modulate the Qualities of Climacteric Fruit?

In climacteric fruit, ethylene has been widely accepted as a phytohormone that accelerates the ripening process in both biochemical and physiological aspects. Ethylene is synthesized from S-adenosyl-methionine through the action of the enzymes 1-aminocyclopropane-1-carboxylic acid synthase (ACS) and 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) (Cherian et al., 2014; Paul et al., 2012; Perotti et al., 2023; Pujol and Garcia-Mas, 2023). Conversely, recent findings challenged the general understanding by implying that the ripening of climacteric fruit is not solely controlled by ethylene. The direct interaction of the Arabidopsis ABI4 protein with the promoters of both the ACS2 and ACO4/8 genes negatively regulated the transcription of these genes, resulting in weaker ethylene production (Dong et al., 2016). On the contrary, during Arabidopsis root elongation, ABA is also known to activate calcium-dependent protein kinases and phosphorylate the C-terminus of the ACS6 protein, enhancing the protein stability of ACS6 and increasing ethylene production (Luo et al., 2014b). These observations suggest that the classification of fruits into climacteric and non-climacteric categories may be an over-simplification. The mode of ethylene production is classified as “System 1”, which is auto‐inhibitory and fluctuates at basal levels during normal growth in both climacteric and non-climacteric fruit, and “System 2 (the ethylene burst in climacteric fruit ripening)” (Hewitt and Dhingra, 2020). However, both climacteric and non-climacteric Japanese plum (Prunus salicina Lindl.) originated from a climacteric cultivar through bud sport mutations (Minas et al., 2015). Thus, the evidence that climacteric and non-climacteric fruits share similar ripening pathways and the role of ABA in the ripening of climacteric fruit are still open questions.

The role of ABA in the ripening of climacteric fruit, particularly anthocyanin biosynthesis, has been discussed. It is widely accepted that apple is classified as a climacteric fruit; thus, its anthocyanin content was shown to be promoted by ethylene-driven MdMYB1 expression (Wang et al., 2022b). In contrast, the MdABI5 protein directly binds to the promoter of the MdbHLH3 gene, which codes the transcription factor that modulates MdDFR. This binding stimulates the transcription of the MdbHLH3 gene (An et al., 2021). The authors also showed that the protein complex of MdABI5 enhanced the transcription of MdDFR by interacting with MdMYB1 and MdbHLH3 proteins. Therefore, the influence of exogenous ABA application on apple peel coloration was also demonstrated. The 0–75 μM and 0–100 μM of exogenous ABA applications linearly accumulated the peel anthocyanin content in ‘Red Delicious’ and ‘Fuji’ apples, respectively (An et al., 2018; Liu et al., 2023). Moreover, the importance of ethylene production facilitated by ABA was discussed in apples under postharvest conditions (Fernández-Cancelo et al., 2022). The molecular background of ABA in ethylene production was shown in tomatoes; ABA or NDGA application stimulated or delayed the production of ethylene, respectively, by modulating ethylene biosynthesis at the enzymatic activity level following ethylene production (Mou et al., 2016). Notably, delayed ripening by the application of 1-MCP immediately after ABA exposure was observed, suggesting the essential role of ethylene in ABA triggering ethylene production. In peach, which is classified as a climacteric fruit, the direct binding of ETHYLENE RESPONSE FACTOR (PpERF3) protein to the 5'-upstream region of PpNCED2/3 has been reported, resulting in increased transcription of PpNCED2/3 during ripening (Wang et al., 2019b). A similar interaction between ABA and ethylene was also found in strawberry, which is a typical non-climacteric fruit. Exogenously applied ABA stimulated the ethylene production of strawberries and accelerated the accumulation of anthocyanin content (Jiang and Joyce, 2003). Conversely, dipping treatment with ethephon enhanced the internal ABA level, resulting in an increase in anthocyanin content. In blueberry (Vaccinium ashei Reade), which showed atypical climacteric ripening without autocatalytic system 2 ethylene, the internal ABA level was reportedly increased in response to ethylene (Wang and Nambeesan, 2024). It was also demonstrated that ethylene inhibited the degradation of FaNCED1 mRNA via miRNA (miR161) silencing (Chen et al., 2023). These observations implied a cross-relation between ABA and ethylene and possible fruit quality improvement by ABA treatment, such as fruit coloration, even in climacteric fruit. Actually, we previously discovered that ABA treatment induces ethylene production in apples, and cis-elements for the AREB/ABF were found in the 5'-upstream region of the ethylene biosynthesis genes in the ‘Orin’ apple (Wang et al., 2018).

Our findings in the ‘Orin’ apple further reflected the ABA-mediated modulation of aroma volatile content in climacteric fruit, which is comparable to that observed in grapes. The enhanced level of several esters produces the apple aroma; alcohol acyltransferase (AAT), the key ester synthesis enzyme activity, is driven by exogenous ABA treatment. A similar analysis using climacteric kiwifruit (Actinidia deliciosa A. Chev, ‘Xuxiang’) revealed enhanced activity of enzymes, including AAT, associated with ester biosynthesis after exogenous ABA application (Han et al., 2022). Additionally, multiple cis-elements (ABRE and G-box) were found to be involved in the promoter sequences of genes encoding ester biosynthesis enzymes, such as AAT. In contrast, despite evidence indicating the crucial role of ABA in anthocyanins in both climacteric and non-climacteric fruits, the regulatory machinery of aroma volatiles in climacteric fruits has been discussed specifically in relation to ethylene. The knockdown of MdACS or MdACO in the low ethylene-producing transgenic ‘Green sleeves’ apple caused lower AAT activity, resulting in a suppressed ester content (Defilippi et al., 2005). Previously, we reported the suppression of ester content by 1-MCP, an ethylene biosynthesis inhibitor, in the ‘Orin’ apple (Wang et al., 2018). Therefore, exogenous ABA-induced alteration in the ester content is possibly attributable to the regulation of multiple ABA-related cis-elements and ABA-associated ethylene synthesis. Noticeably, the influence of ADH activity was not demonstrated in transgenic ‘Green sleeves’ lines. ADH is a key enzyme regulating the biosynthesis of alcohols and aldehydes and adds green aromatic notes to the fruit. In ‘Hayward’ kiwifruit, transcriptional changes in AdADH3 were induced by neither ethylene nor 1-MCP treatment (Zhang et al., 2020). The ADH activity of the European pear (Pyrus communis L.) is strongly influenced by low oxygen conditions (Ke et al., 1994), which is comparable to our findings in grapes, indicating altered gene transcription in response to lower oxygen conditions (Saito et al., 2022). In ‘Kyoho’ and ‘Shine muscat’ grapes, we demonstrated reduced hexenol and (E)-2-hexenal (C₆ alcohol and aldehyde, respectively) after applying exogenous NDGA (Jia et al., 2018; Lin et al., 2018b). Collectively, the modulation of volatile aroma content, especially green aromatic notes regulated by alcohol/aldehyde, is possible by treating climacteric fruit with ABA (Fig. 5). Moreover, the molecular machinery for alcohol/aldehyde biosynthesis is considered to be controlled by ABA rather than ethylene, and this may be shared by both climacteric and non-climacteric fruits.

Fig. 5

Estimated model for regulatory pathways associated with aroma volatile biosynthesis, which are shared between climacteric and non-climacteric fruits; ABA- and ethylene-associated fruit ripening/maturation.

Conclusion and Perspectives

The recent establishment of cost-effective ABA synthesis via microbial fermentation is a breakthrough in the commercial application of ABA in PBR. However, the issue of ABA’s rapid inactivation via biodegradation persists. The demonstration of long-lasting salt tolerance in apples through the use of Abz-E2B suggests that it is possible to overcome challenges associated with the biodegradation of ABA analogs. Conversely, antagonistic chemicals, such as PBRs, have been developed based on the precise structure of an ABA receptor, the PYR/PYL/RCAR protein. These observations significantly contribute to understanding the molecular basis of ABA signaling and propose a new avenue for fruit quality control via pre- and postharvest ABA application. We have summarized published information on the roles of ABA in non-climacteric fruits, its effects on fruit quality, such as peel color and aroma volatiles, and the impacts of treatments using various ABA-related chemicals and treatment methods. Moreover, the close connection between ABA and ethylene-driven ripening of climacteric fruits was elucidated, and a potential ABA-based strategy for controlling fruit quality was proposed. On the contrary, the horticultural applications of ABA are limited to improving grape pigmentation, and only one registered ABA-related PBR exists, suggesting that current knowledge is inadequate compared to that of other plant hormones. Therefore, future research goals on the effective application of ABA in horticulture should include the expansion of chemical variation, application methods/organs, and applicable plant species.

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