TY - JOUR
AU - Guo, Yangdong
AB - Abstract The phytohormone abscisic acid (ABA) plays a crucial role not only in fruit development and ripening, but also in adaptive responses to biotic and abiotic stresses. In these processes, the actions of ABA are under the control of complex regulatory mechanisms involving ABA metabolism, signal transduction, and transport. The endogenous ABA content is determined by the dynamic balance between biosynthesis and catabolism, processes which are regulated by 9-cis-epoxycarotenoid dioxygenase (NCED) and ABA 8′-hydroxylase (CYP707A), respectively. ABA conjugation by cytosolic UDP-glucosyltransferases, or release by β-glucosidases, is also important for maintaining ABA homeostasis. Recently, multiple putative ABA receptors localized at different subcellular sites have been reported. Among these is a major breakthrough in the field of ABA signalling—the identification of a signalling cascade involving the PYR/PYL/RCAR protein family, the type 2C protein phosphatases (PP2Cs), and subfamily 2 of the SNF1-related kinases (SnRK2s). With regard to transport, two ATP-binding cassette (ABC) proteins and two ABA transporters in the nitrate transporter 1/peptide transporter (NRT1/PTR) family have been identified. In this review, we summarize recent research progress on the role of ABA in fruit ripening, stress response, and transcriptional regulation, and also the functional verification of both ABA-responsive and ripening-related genes. In addition, we suggest possible commercial applications of genetic manipulation of ABA signalling to improve fruit quality and yields. ABA, ABA metabolism, ABA signalling, ABA transporter, fruit ripening, stress response, transcriptional regulation. Introduction Fruits are rich sources of vitamins and minerals, both of which are important in human nutrition (DellaPenna and Pogson, 2006). The fleshy fruits have classically been divided into two categories based on their patterns of respiration during fruit maturation and ripening. One group is the climacteric fruits, which includes tomato, apple, pear, peach, and banana, fruits that are characterized by a burst of ethylene release during ripening (Buesa et al., 1994; White, 2002; Hiwasa et al., 2003; Zaharah et al., 2013). In these fruits, ethylene induces the transcription of many ripening-associated genes, and its action results in the specific features of fruit ripeness (Bleecker and Kende, 2000; Giovannoni, 2001, 2004). The second group is the non-climacteric fruits, in which there is no respiration peak or ethylene burst during the ripening process, as shown in grapes (Deytieux et al., 2007; Koyama et al., 2010), strawberry (Trainotti et al., 2005), cherry (Kondo and Inoue, 1997), and orange (Rodrigo et al., 2006). Some fruits such as persimmon (Diospyros kaki Thunb.) are classified as climacteric (Abeles et al., 1992), but, unlike typical climacteric fruits, the amount of ethylene released by the fruits declines as fruit ripening progresses (Fig. 1C). Ethylene released from ripe fruit at the harvest stage is <10% of that released by the immature fruit (Takata et al., 1983; Nakano et al., 2003). Fig. 1. View largeDownload slide Changes in ABA content and ethylene release in fruits of tomato (a climacteric fruit), cucumber (a non-climacteric fruit), and persimmon (an atypical climacteric fruit) during development and ripening. (A) During development of tomato fruit (cv. ‘Jia Bao’), fruits were sampled at the following times after anthesis (stages): 20 DAA (immature green), 35 DAA (mature green), 38 DAA (breaker), 40 DAA (turning), 42 DAA (pink), 43 DAA (harvest red), and 45 DAA (over red) (Sun et al., 2012a, b). (B) Based on the changes in growth parameters (Wang et al., 2012), we defined the growth stages for Jin Qing NO. 1 cucumber fruit. From pollination to 9 days after flowering (DAF) was the immature green stage, 12–15 DAF was the breaker stage, 18–24 DAF was the turning stage, 27–30 DAF was the fully ripe stage, and 35–43 DAF was the senescence stage. (C) Fruit samples were collected from 75 days after full bloom (DAFB) to 165 DAFB. 115 DAFB was the onset of pigmentation, 125 DAFB at the ABA peak value was the turning stage, and 145 DAFB was the harvest stage (Zhao et al., 2012). Fig. 1. View largeDownload slide Changes in ABA content and ethylene release in fruits of tomato (a climacteric fruit), cucumber (a non-climacteric fruit), and persimmon (an atypical climacteric fruit) during development and ripening. (A) During development of tomato fruit (cv. ‘Jia Bao’), fruits were sampled at the following times after anthesis (stages): 20 DAA (immature green), 35 DAA (mature green), 38 DAA (breaker), 40 DAA (turning), 42 DAA (pink), 43 DAA (harvest red), and 45 DAA (over red) (Sun et al., 2012a, b). (B) Based on the changes in growth parameters (Wang et al., 2012), we defined the growth stages for Jin Qing NO. 1 cucumber fruit. From pollination to 9 days after flowering (DAF) was the immature green stage, 12–15 DAF was the breaker stage, 18–24 DAF was the turning stage, 27–30 DAF was the fully ripe stage, and 35–43 DAF was the senescence stage. (C) Fruit samples were collected from 75 days after full bloom (DAFB) to 165 DAFB. 115 DAFB was the onset of pigmentation, 125 DAFB at the ABA peak value was the turning stage, and 145 DAFB was the harvest stage (Zhao et al., 2012). To date, the ripening mechanism of climacteric fruits, especially with respect to the effects of ethylene, has been well studied (Alexander and Grierson, 2002; Klee and Giovannoni, 2011). A high-level regulatory network of transcription factors that control fruit development has been described in tomato (Vrebalov et al., 2002; Srivastava and Handa, 2005; Manning et al., 2006; Seymour et al., 2008, 2013a, 2013b; Itkin et al., 2009; Chung et al., 2010; Jaakola et al., 2010; Karlova et al., 2011; Martel et al., 2011; Lee et al., 2012). In contrast, the mechanisms involved in the ripening of non-climacteric fruits remain unclear. Although the patterns of fruit development and ripening are diverse, they exhibit the same ripening phenomena which usually include cell wall modifications together with associated fruit softening, the synthesis of pigments, the conversion of starch into simple sugars, and the synthesis of volatile compounds that influence fruit taste and aroma (Saladie et al., 2007). Accompanying these biochemical processes, fruits go through a remarkable transformation from something that is unpalatable into an attractive, edible fruit (Barry et al., 2010; Matas et al., 2011). The difference between climacteric and non-climacteric fruits depends only on whether ethylene is released during maturation/ripening or not. In addition, studies on rare tomato mutations such as ripening inhibitor (rin) and non-ripening (nor) have shown that application of exogenous ethylene does not promote fruit ripening, yet it does induce expression of ethylene-regulated ripening genes (Tigchelaar et al., 1978; Yen et al., 1997). These results indicate that in addition to general ethylene biosynthesis and signalling, there may be other ethylene-independent regulatory factors responsible for the control of ripening of both fruit types that are upstream of ethylene. Abscisic acid (ABA) can be considered to be another ripening control factor for the following reasons: (i) as shown in Fig. 1, there is a sharp increase in ABA accumulation during the onset of fruit ripening and/or the ripening process in both climacteric (Buesa et al., 1994) and non-climacteric (Kojima et al., 1995; Kondo and Inoue, 1997) fruits; (ii) ABA accumulates preceding ethylene release in climacteric fruits (Zhang et al., 2009a, b); (iii) the application of exogenous ABA enhances the production of several metabolites involved in fruit ripening, thereby promoting fruit ripening (Chernys and Zeevaart, 2000; Ban et al., 2003; Cakir et al., 2003; Jeong et al., 2004; Giribaldi et al., 2010); (iv) in ABA-deficient tomato mutants, the fruit did not show the normal growth pattern observed in the wild type (Taylor et al., 2000; Galpaz et al., 2008); (v) the de-greening stage began later in ABA-deficient orange mutants (Rodrigo et al., 2003); and (vi) the inhibition of ABA signalling in FaPYL1-RNA interference (RNAi)-silenced strawberry fruit impeded fruit ripening (Jia et al., 2011). ABA was first discovered to function in plant wilting and stomatal closure in the late 1960s (Mittelheuser and Van Steveninck, 1969; Wright and Hiron, 1969). To date, considerable progress has been made in research into the role of ABA in the regulation of fleshy fruit ripening. However, the molecular mechanisms remain to be elucidated. To describe the mechanisms of ABA action at the molecular level, it is necessary to identify all of the components involved in ABA homeostasis, including the functional components in ABA metabolism, signal transduction, and transport. On the other hand, ABA is associated with the plant's response to different kinds of abiotic stresses such as drought, high temperature, chilling, and salinity (Qin and Zeevaart, 2002; Seki et al., 2007). However, research on the involvement of ABA in regulating abiotic stress in fruits has rarely been reported. This review focuses on research progress into the role of ABA in fruit ripening and responses to abiotic stress. Synthesis, catabolism, and reactivation of ABA in fruits In higher plants, the ABA biosynthetic pathway is well understood (Fig. 2), and numerous mutants have been identified at each step in this pathway in Arabidopsis (North et al., 2007; Huo et al., 2013), tomato (Burbidge et al., 1999; Nitsch et al., 2009), and maize (Tan et al., 1997, 2001). ABA is synthesized de novo from a C40 carotenoid. The carotenoid biosynthetic pathway begins with the formation of phytoene from two molecules of geranylgeranyl diphosphate (GGPP) in the central isoprenoid pathway. Four desaturation steps give rise to lycopene; cyclizations at both ends of the lycopene molecule produce α- or β-carotene, which undergo hydroxylation at C3 and C3′ to form the xanthophylls, lutein and zeaxanthin, respectively. An important phase of ABA biosynthesis is initiated in plastids with the hydroxylation and epoxidation of the β-carotene to produce the all-trans-xanthophylls zeaxanthin and violaxanthin. Violaxanthin is then converted into 9-cis-epoxyxanthophylls, which are oxidatively cleaved by 9-cis-epoxycarotenoid dioxygenase (NCED) to yield xanthoxin, the first C15 intermediate of ABA biosynthesis. Xanthoxin exits the plastid into the cytosol where it is oxidized in two further steps to form ABA (Qin and Zeevaart, 1999; Schwartz et al., 2003; Taylor et al., 2005). Overexpression experiments in transgenic plants demonstrated unequivocally that NCED is a key rate-limiting step in ABA biosynthesis (Thompson et al., 2000; Iuchi et al., 2001; Tung et al., 2008). The ABA catabolic pathway has been established through the hydroxylation reaction. In the hydroxylation pathway, among three different methyl groups, C-8′ is the predominant position for the hydroxylation reaction, which is mediated in Arabidopsis by proteins encoded by the CYP707A gene family (Kushiro et al., 2004; Saito et al., 2004). Dihydroxyphaseic acid (DPA) may be the major metabolite of ABA (Setha et al., 2005). Moreover, ABA conjugation by cytosolic UDP-glucosyltransferases (GTs) or release by β-glucosidases (BGs), through intracellular or intertissue transport processes, can also alter ABA homeostasis (Hartung et al., 2002; Sauter et al., 2002; Jiang and Hartung, 2008; Seo and Koshiba, 2011; Burla et al., 2013). Thus, free ABA, phaseic acid, and DPA are present mainly in the extravacuolar compartments. In contrast to these oxidized ABA catabolites, ABA-glucosyl ester has been reported to accumulate in vacuoles and presumably in the endoplasmic reticulum, since AtBG1 is located there (Lee et al., 2006; Xu et al., 2012). Fig. 2. View largeDownload slide ABA metabolism, signal transduction, and reactivation pathways. (A) ABA is synthesized de novo from a C40 carotenoid (Qin and Zeevaart, 1999; Schwartz et al., 2003; Taylor et al., 2005). (B) ABA catabolic pathway (Saito et al., 2004; Kushiro et al., 2004; Setha et al.,2005). (C) ABA–glucose conjugation (Sauter et al., 2002; Seo and Koshiba, 2011; Burla et al., 2013). (D) ABA signal transduction (Ma et al., 2009; Park et al., 2009; Yin et al., 2009; Gonzalez-Guzman et al., 2012). Fig. 2. View largeDownload slide ABA metabolism, signal transduction, and reactivation pathways. (A) ABA is synthesized de novo from a C40 carotenoid (Qin and Zeevaart, 1999; Schwartz et al., 2003; Taylor et al., 2005). (B) ABA catabolic pathway (Saito et al., 2004; Kushiro et al., 2004; Setha et al.,2005). (C) ABA–glucose conjugation (Sauter et al., 2002; Seo and Koshiba, 2011; Burla et al., 2013). (D) ABA signal transduction (Ma et al., 2009; Park et al., 2009; Yin et al., 2009; Gonzalez-Guzman et al., 2012). In fruit, the endogenous ABA content is determined by the dynamic balance of biosynthesis (NCED genes), catabolism (CYP707A genes), and reactivation (BG/GT genes), and the spatio-temporal expression of the genes encoding these proteins is regulated by the ABA pool at the transcriptional level. Therefore, the change in the dynamic balance of these three processes may lead to alterations in the level of ABA. Since the gene encoding NCED, the key ABA biosynthesis enzyme, was first isolated from the maize vp14 mutant (Tan et al., 1997), it has been cloned and characterized from various climacteric fruit species such as apple (Lara and Vendrell, 2000), peach (Alvaro et al., 2013), tomato (Burbidge et al., 1999), and melon (Sun et al., 2013), as well as non-climacteric fruits such as orange (Rodrigo et al., 2006) and grape (Wheeler et al., 2009). At present, at least four NCED genes have been cloned from tomato fruits (Huo et al., 2013). ABA levels in tomato fruit are regulated mainly by SlNCED1 at the transcriptional level, and in response to dehydration (Zhang et al., 2009a). Tomatoes overexpressing SlNCED1 had enhanced ABA accumulation and drought tolerance, and reduced levels of transpiration (Thompson et al., 2000). Tomato fruits from an ABA-deficient mutant showed a decrease in mean fruit weight and did not show the normal development and ripening observed in the wild type (Galpaz et al., 2008). Also, in transgenic tomato fruits expressing a SlNCED1-RNAi construct, as a consequence of silencing the SlNCED1 gene, the reduction in endogenous ABA levels inhibited cell wall degradation, indicating that ABA is indispensable during fruit development and ripening (Sun et al., 2012a, b). On the other hand, the regulation of CYP707A, which encodes ABA 8′-hydroxylase, can alter the dynamic balance of ABA levels (Saito et al., 2004). For example, enhanced expression or loss of function of the CYP707A2 gene can affect ABA levels in Arabidopsis seedlings, which will subsequently change their sensitivity to exogenous glucose (Zhu et al., 2011). The PacCYP707A1 and PacCYP707A3 genes expressed in sweet cherry fruit are up-regulated by water stress and ABA treatment (Ren et al., 2010). It is worth noting that the regulatory mechanisms of CYP707A gene expression in response to ABA and dehydration are somewhat different. Although ABA-responsive elements (ABREs) are present in the CYP707A gene promoter regions, in ABA-deficient (aba2-2 and nced3-2) or ABA-insensitive (abi1-1 and abi2-1) mutants, the responses of CYP707A genes to dehydration are ABA independent, but sometimes depend partly on ABA signalling under dehydration conditions (Umezawa et al., 2006). Besides these main regulatory steps in the ABA metabolic pathway, metabolic steps upstream of ABA metabolism also contribute to the determination of ABA levels. Overexpression of genes encoding regulatory enzymes in the methylerythritol phosphate (MEP) pathway (1-deoxy-d-xylulose 5-phosphate synthase), the carotenoid biosynthesis pathway (phytoene synthase), and the xanthophyll cycle (ZEP) can cause enhanced accumulation of ABA in seeds or seedlings (Frey et al., 1999; Estévez et al., 2001; Lindgren et al., 2003). Taken together, this indicates that the regulation of ABA metabolism is not merely restricted to specific steps in ABA metabolism (i.e. NCED and CYP707A), but is also coordinated with other pathways that are upstream of ABA metabolism. In addition, reactivation of the BG-conjugated/inactive ABA to free/active ABA also affects cellular ABA levels (Price et al., 2003; Burla et al., 2013). Recently, the functions of BGs in the activation of hormone groups in plants, including auxins, ABA, and cytokinins, has been reported (Brzobohaty et al., 1993; Lee et al., 2006). One or more genes in the BG family can have expression patterns that coincide with the variation in ABA accumulation during fruit ripening, which may indicate their roles in co-regulating the ABA pool in these fruits at the transcriptional level (Sun et al., 2010; Zhang et al., 2013). For example, in strawberry fruit, the expression pattern of FaBG3 was coincident with ABA accumulation during fruit ripening, and it has been shown by gene silencing (FaBG3-RNAi plants) that FaBG3 is not only related to fruit ripening, but can also confer disease resistance in strawberry (Li et al., 2013). GT is implicated in the presence or absence of a smoky aroma in tomato fruits. Recently, a NON-SMOKY GLYCOSYLTRANSFERASE1 (NSGT1) gene was identified in tomato (Tikunov et al., 2013). Both BG and GT are members of large gene families, and their roles in the regulation of the ABA level during fruit ripening are still unclear. Further research is needed to identify and isolate the specific substrates for these enzymes in fruits. ABA signal transduction and its transcriptional regulation The ABA-mediated signalling cascade is initiated by perception of ABA through ABA receptors. In recent years, considerable progress has been made in studies of ABA signal transduction, and several different types of ABA receptors have been reported in the literature, including ABAR/CHLH (Mg-chelatase H subunit) (Mochizuki et al., 2001; Shen et al., 2006; Shang et al., 2010) and the GPCR-type G proteins (Liu et al., 2007; Pandy et al., 2009). For these receptors, their exact nature and roles have not been confirmed, and are still the subject of some debate (Muller and Hansson, 2009; Wu et al., 2009). Recently, a major breakthrough in the field of ABA signalling was achieved, which was the identification of the PYR/PYL/RCAR protein family, the type 2C protein phosphatases (PP2Cs), and subfamily 2 of the SNF1-related kinases (SnRK2s) (Ma et al., 2009; Melcher et al., 2009; Nishimura et al., 2009; Park et al., 2009; Santiago et al., 2009; Yin et al., 2009; Gonzalez-Guzman et al., 2012). The current ABA signal transduction model can be described as follows (Fig. 2): in the absence of ABA, PP2Cs inhibit SnRK2s by physical interaction and through their phosphatase activity. Binding of an ABA molecule to the ABA receptor PYR/PYL/RCAR leads to structural changes in the receptor, enabling the interaction of the ABA receptors with PP2Cs, thus disrupting the interaction between PP2Cs and SnRK2s. SnRK2s are released from the PP2C inhibition, and are able to activate their downstream targets, which include transcription factors as well as other targets, such as ABA-responsive element binding proteins (AREBs) and ABA-responsive element binding factors (ABFs) (Klingler et al., 2010). AREB/ABFs are ABA-responsive transcription factors containing a basic leucine zipper family (bZIP)-type DNA-binding domain that binds the ABA-responsive element (T/CACGTGGC) and have a pivotal role in ABA-dependent gene activation (Choi et al., 2000; Hattori et al., 2002; Kang et al., 2002; Gómez-Porras et al., 2007). For example, AREB1, AREB2, ABF3, and ABF4 positively regulate the expression of ABA signalling response genes (Fujita et al., 2009; Yoshida et al., 2010). Potential perception of ABA through different types of receptors or by different members of the PYR/PYL/RCAR family raises several questions that have yet to be addressed, such as: what is the relative contribution of each type of receptor, and how do multiple inputs of perception integrate into ABA signalling? ABA in different subcellular compartments may require different ABA receptors to initiate ABA-mediated signalling. According to this scenario, it is possible that different physiological responses can be induced by ABA receptors which perceive different subcellular pools of ABA (Gonzalez-Guzman et al., 2012). In recent years, considerable progress has been made in the understanding of ABA signal transduction pathways in fruits. There are a few transcription factors which are important for fruit ripening, and these have also been described as being related to the ABA response. For example, VvABF2, a grape bZIP transcription factor belonging to group A of bZIPs, has been reported. Overexpression of VvABF2 in grape cells resulted in up-regulation and/or modification of existing networks related to ABA responses, enhanced responses to ABA treatment, and changes in the synthesis of phenolic compounds and cell wall softening (Nicolas et al., 2014). The Fragaria xananassa MYB10 transcription factor plays a general regulatory role in the flavonoid/phenylpropanoid pathway during ripening in strawberry fruit. The R2R3-MYB10 transcription factor expressed in strawberry fruit is repressed by auxins and activated by ABA, in parallel with the ripening process. This transcription factor regulates the expression of most of the early-regulated biosynthesisgenes (EBGs) and the late-regulated biosynthesisgenes (LBGs) which are involved in anthocyanin production in ripened fruit receptacles (Medina-Puche et al., 2013). The R2R3-type transcription factor MYB30 is involved in the regulation of ABA signalling. Coordination of ABI5 and MYB30 sumoylation by SIZ1 may balance gene expression, which is required for regulation of ABA signalling during seed germination (Zhenga et al., 2012). ABA production and PacMYBA expression work closely together to control anthocyanin biosynthesis in red-coloured sweet cherry pigmentation. Moreover, ABA might directly regulate PacMYBA expression at the transcriptional level (Shen et al., 2014). In addition, there are other large groups of genes encoding transcription factors that could be important in fruit development; for instance, the bZIP genes have been shown to be involved in the control of nitrogen/carbon balance, and in the response to ABA (Nijhawan et al., 2008; Lovisetto et al., 2013). Different calcium-dependent protein kinases (CDPKs) could play a role in the control of ripening; an example is the protein kinase FvCDPK1 from wild diploid strawberry, which is expressed in fruits during ripening, and is up-regulated by ABA (Feng et al., 2013). In each ABA signal gene family, there is only one or several genes with expression patterns that correspond to the variation in ABA content and are involved in fruit ripening (Gambetta et al., 2010; Romero et al., 2012). For example, in tomato, 14 SlPYL genes from the same gene family had different sensitivities to endogenous/exogenous ABA and drought (Sun et al., 2011), showing that their individual regulation is complex. Although some PYL, PP2C, and SnRK2 genes may not play roles in ABA signal transduction, they may have important functions in other biological processes (Schweighofer et al., 2004; Gonzalez-Ballester et al., 2008), and whether they are involved in ABA responses still needs to be investigated. Transport of ABA ABA metabolism, perception, and transport together allow plants to use ABA as a signalling molecule. Since ABA accumulation occurs in different tissues and cells, and ABA has systemic effects, a requirement for efficient intercellular transport of ABA has been proposed (Cheng et al., 2002; Koiwai et al., 2004; Endo et al., 2008). Although ABA transport has long been demonstrated in plants, the first breakthroughs in the identification of plasma membrane-localized ABA transporters came in 2010, with the detection of two ATP-binding cassette (ABC) proteins. More recently, two ABA transporters in the nitrate transporter 1/peptide transporter (NRT1/PTR) family, which are involved in the transport of nitrogen compounds, have been described, and further work needs to be done to determine whether there is an interaction between ABA and nitrogen signalling or nutrition (Boursiac et al., 2013). At present, the molecular cloning of ABA transporters and the phenotypes of their respective mutants genetically support the requirement of ABA transport for proper signalling throughout the plant. ABA is transported from the site of synthesis to the site of action, and where ABA receptors decode the message within a fruit is different from that in vegetative organs, because the morphological structure of fruit is unlike that of the root, stem, or leaf (Antoni et al., 2011). Transport of ABA in fruits is mainly via the phloem. In the fruit of sweet cherry (Prunus avium L.), ABA was shown to be transported only in the phloem (Else et al., 2004). The amount of ABA exported from the developing fruit was greatest during stone formation and the beginning of fruit expansion, and declined markedly as the fruit began to mature (Else et al., 2004). Phloem export of ABA from developing fruit also decreased during the later stages of fruit ripening. This may reflect a general decrease in phloem export, but it could also contribute to the accumulation of ABA in the ripening fruit. Ripening of the sweet fruit is coordinated by ABA, and fruit concentrations rise markedly during the final stages of maturity (Ren et al., 2011). Phloem import of ABA into fruit significantly promoted ripening during the onset of ripening. For example, a 2-year-old shoot with fruit was cut when the fruit had become straw yellow. The shoot was then placed in a 1 mmol l–1 ABA solution in the laboratory, with an untreated control consisting of distilled water. Five days after the initiation of treatment, maturity index (SSC/TA), fruit softening, and anthocyanin levels were significantly increased with increasing ABA concentrations in the fruit (Luo et al., 2013). This indicates that ABA is readily imported into fruits from the shoot during the onset of fruit ripening. ABA regulation of metabolic pathways related to fruit ripening There is evidence to support a role for ABA in photosynthate unloading from phloem in developing fruits. For example, ABA treatment enhanced the uptake of sugar into vacuoles in apple fruit flesh (Yamaki and Asakura, 1991), and increased the sugar content of developing citrus fruit (Kojima et al., 1995). Sugar and ABA signalling have revealed intimate connections in sugar-insensitive and sugar-hypersensitive mutants of Arabidopsis. For example, many sugar mutants turn out to be allelic to known ABA-sensitive and ABA-insensitive mutants, such as ABI3-5, ABF2-4, and ABA1-3 (Smeekens et al., 2000; Gazzarrini and McCourt, 2001). ABA and sugar often exert similar or antagonistic effects on diverse developmental processes (Finkelstein and Gibson, 2002; Rolland et al., 2006; Gambetta et al., 2010). For example, supplementation with exogenous sugars is able to relieve the inhibition of seed germination caused by added ABA (Price et al., 2003; Dekkers et al., 2004). Recently, it has been found that the manipulation of endogenous sucrose content alters the expression of FaNCED genes and the content of endogenous ABA in strawberry fruit (Jia et al., 2013). Even so, the complexity of fruit ripening and the potential role of ABA in this process indicates the presence of multiple signalling pathways that are influenced by hormone balance and sugar signalling. ABA also regulates the anthocyanin biosynthetic pathway in fruit. ABA induces anthocyanin accumulation to make the fruit colour-up, and also participates in the activation of plant tissue defence against potential damage, apparently by triggering biosynthesis of phenols which filter out harmful radiation and also act as antioxidants (Lacampagne et al., 2009). For example, during fruit development in bilberry (Vaccinium myrtillus L.), ABA levels and expression of VmNCED1 and the neoxanthin synthase gene (VmNSY) increased sharply at the onset of ripening, the stage in which expression of the chalcone synthase (VmCHS) and anthocyanidin synthase genes (VmANS) also increases along with the accumulation of ABA (Karppinen et al., 2013). Recent studies have also shown that the transcriptional regulators of structural genes in the phenylpropanoid and flavonoid pathways, as well as genes considered to be involved in the acylation and transport of anthocyanin into the vacuole, are up-regulated by ABA treatment in grape berries (Koyama et al., 2010; Berli et al., 2011). ABA also participates in fruit texture formation. The cell walls in fruits are generally composed of cellulose microfibrils tethered with xyloglycans embedded in pectin mesh, and glycoproteins (Carpita and Gibeaut, 1993). Changes in the cell wall are associated with fruit softening, which is related to the expression of a number of hydrolase and transglycosylase genes (Huber, 1983), including increases in enzyme activity and mRNA levels of polygalacturonase (PG) (Smith and Gross, 2000), pectin methylesterase (PME) (Tieman et al., 1992; Deytieux-Belleau et al., 2008), endo-β-1,4-glucanases (Cels) (Lashbrook et al., 1994), and expansin (Exp1) (Brummell et al., 1999; Cosgrove et al., 2000). Because ethylene has variable effects on the activities of these hydrolases during ripening (Nishiyama et al., 2007), it is generally accepted that fruit softening is induced by ethylene. However, direct observation and molecular level evidence of the involvement of ABA in fruit softening has recently been provided (Sun et al., 2012a, b). In SlNCED1-RNAi transgenic fruits, the pectin content was shown to be significantly higher, the shelf life was longer, and the pulp was firmer and more flexible than in control fruits during the ripening stage (Sun et al., 2012a). Also the role of ABA in regulating these genes depended on the stage of fruit development. In addition to ethylene, ABA also shows reciprocity with other phytohormones during fruit development. It has been demonstrated that auxin acts upstream of the major regulator of seed dormancy by recruiting the auxin response factors AUXIN RESPONSE FACTOR 10/16 to control the expression of ABI3 during seed germination (Liu et al., 2013). In strawberry fruit, auxin promotes fruit expansion at the start of development; however, the ripening period is accompanied by a decrease in auxin levels, although endogenous ABA in both achenes and receptacles increased as the fruit ripened (Archbold and Dennis, 1984). Application of the synthetic auxin NAA (1- naphthaleneacetic acid) down-regulated the expression of FaNCED genes and reduced ABA accumulation during development and ripening of strawberry fruit (Ji et al., 2012). ABA also regulates the development of abscission in the fruit/flower pedicel. In the apple (Malus domestica) fruitlet, a strong correlation between abscission and ABA levels in the fruit cortex was observed (Eccher et al., 2014). During the early phases of the shedding process, major transcriptomic changes and metabolic rearrangements occur within the fruit. A metabolomic study identified isoprene as an early marker of abscission induction. According to the hypothetical model, ABA may transiently cooperate with other hormones and secondary messengers in the generation of an intra-fruit signal, which then leads to the downstream activation of the abscission zone (Eccher et al., 2014). Endogenous ABA variation also alters the production of carotenoids, which are precusor substrates for ABA biosynthesis (Kachanovsky et al., 2012). In the tomato mutants high-pigment 3 (hp3) and high-pigment 2 (hp2), the fruits are redder in colour than are the control fruits (Bino et al., 2005; Kolotilin et al., 2007; Galpaz et al., 2008). The tomato hp3 mutant contains an altered gene for zeaxanthin epoxidase (Zep), which catalyses the conversion of zeaxanthin to violaxanthin and neoxathin. The levels of lycopene and β-carotene were increased due to the up-regulation of phytoene synthase (SlPSY1), a rate-limiting enzyme (Fraser et al., 2002), and down-regulation of lycopene β-cyclase (SlBcyc) expression in the SlNCED1-RNAi lines compared with the control fruit (Sun et al., 2012a, b). An alternative explanation of why the transgenic fruit contained more carotenoids could be that the carbon flux, which normally channels carbon to free ABA and ABA metabolite accumulation during ripening, is partially blocked by a significant reduction in NCED activity. The ‘backlogged’ carbon is then shunted to the carotenoid pathway in the RNAi lines, resulting in the increased biosynthesis and accumulation of upstream compounds in the pathway, mainly lycopene and β-carotene. Regulating the effect of ABA during abiotic stress in fruits Fruits possess an adversity monitoring system. When fruits experience environmental stresses, they can launch a variety of reactions through signal transduction, thereby avoiding the impact or harm caused by abiotic stress. On a broader scale, ABA is a stress-related signalling molecule, and the main function of ABA in plants is to regulate water balance and osmotic stress tolerance (Cakir et al., 2003). The accumulation of ABA in fruits has been shown to correlate with abiotic stresses (Deluc et al., 2007, 2009). For example, the persimmon fruit has a large calyx which adheres to the fruit throughout ripening, and the response of the calyx lobes to the stress of water loss was more rapid than that observed in the fruit (Leng et al., 2009; Zhao et al., 2012). We propose a persimmon softening model in which the DKNCED1 gene initiates ABA biosynthesis in the dehydrating calyxes of fruits: (i) ABA may induce ethylene biosynthesis via the regulation of ACS and ACO gene expression; and (ii) the ethylene produced diffuses into the pulp of the fruit, where autocatalytic ethylene biosynthesis is induced and results in an abrupt increase in ethylene production and fruit softening. In cherry, fruits have a long pedicel that contains large numbers of stomates, which are the site for gas exchange nearest the developing fruit. The evaporation of water from cherry fruit occurs mainly through the stomata on the pedicels (Luo et al., 2013). The ABA peak occurred sooner than did the ethylene peak in the pedicels post-harvest. The peak values for ABA, ethylene release, and the expression of related genes all started to increase earlier in pedicles than in pulp tissues (Luo et al., 2013), indicating that softening in cherry fruit begins with pedicle dehydration, and that ABA plays a role in its regulation. Therefore, it can be assumed that the characteristics of stress resistance in fruit are related to its special morphological structure. Recent studies have shown that many genes respond to ABA in fruits under stress. For example, expression of Fxaltp, a strawberry gene encoding a non-specific lipid transfer protein, responds to ABA, wounding, and cold stress (Yubero-Serrano et al., 2003). Using a Bulked Segregant Gene Expression Analysis (BSGA) approach, many new cold-regulated genes have been identified in peach, which provides the foundation for further experiments to explore the network of gene regulation in the cold and to determine the function of cold-responsive genes in peach fruits (Pons et al., 2014). Recently, it has been reported that spraying the entire plant with ABA increases xylem sap flow and Ca2+ movement into the fruit, resulting in higher water-soluble apoplastic Ca2+ concentrations, reduced membrane leakage, and reduced fruit susceptibility to blossom-end rot development (Tonetto de Freitas et al., 2014). In addition, the ABA–glucose conjugation pathway also participates in the regulation of cellular ABA levels under conditions of stress (Iuchi et al., 2001; Seo and Koshiba, 2002). In strawberry, FaBG3 expression increases more rapidly than FaNCED2 expression following dehydration treatment, which suggests that ABA produced by BGs occurs faster than through the lengthy and complex de novo biosynthesis pathways involving FaNCED2. It is possible that under conditions of abiotic stress, it is difficult for plants to increase endogenous ABA levels that result from de novo synthesis of proteins. This is supported by the observation that FaBG3-RNAi fruits exhibit down-regulated expression of dehydration-responsive proteins (FaRDs), calcineurin B-like protein (FaCBL), and dehydration responsive-element binding protein (FaDREB1B). The gene-silenced fruits also show a variety of ABA-deficient phenotypes, including failure to close the stomates fully on the sepals, and more rapid water loss in both sepals and fruits compared with the controls (Li et al., 2013). Therefore, the ABA–glucose ester hydrolysis pathway is important, as these conjugates provide fruits with a means to increase ABA levels rapidly which enable them to respond to dehydration stress, despite the presence of intact de novo biosynthetic pathways. Fruits, like whole plants, are subjected to ever-changing environmental conditions, and, accordingly, they require constant fine-tuning of the active ABA pools to respond to the severity and duration of the stress. In future studies, it will be important to identify the site of action of the BGs, the specific reaction substrates, and the transporter of the BG enzymes in fruits under stress conditions. Conclusions and future prospects During fruit ripening, ABA accumulation appears to be critical, because it participates in the regulation of ripening of both climacteric and non-climacteric fruits, although the exact role of ABA remains obscure. Many basic scientific issues remain unclear, such as the mechanisms behind early expression of NCED genes that encode the key enzyme of ABA synthesis. In other words, how is the transcription of NCED induced at the onset of fruit ripening? The existence of different ABA sources, together with ABA transporters and multiple ABA receptors in different subcellular compartments, may allow fruits to have multiple ABA signalling circuits. This aspect raises an important question about how ABA production is coordinated in fruits as a whole. Plants must have a mechanism to coordinate these multiple ABA sources and signalling pathways as well as to regulate transport in order to achieve the desired cellular ABA levels under variable developmental stages and environmental conditions. A new strategy is needed to address these questions. In previous research into fruit ripening, most of the studies focus on a single point (such as the role of ABA) or process (such as ABA metabolism and regulation); therefore, these research results are unable to explain the relationships between the biological processes in a highly complex three-dimensional network. We propose that future investigations need to take a systems biology approach when investigating the fruit-specific-ABA-deficient transcriptome, proteome, and metabolome. 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TI - The role of abscisic acid in fruit ripening and responses to abiotic stress
JF - Journal of Experimental Botany
DO - 10.1093/jxb/eru204
DA - 2014-05-12
UR - https://www.deepdyve.com/lp/oxford-university-press/the-role-of-abscisic-acid-in-fruit-ripening-and-responses-to-abiotic-3lLtrB05Ra
SP - 4577
EP - 4588
VL - 65
IS - 16
DP - DeepDyve
ER -