The organic acids that are accumulated in the flesh of fruits: occurrence, metabolism and factors affecting their contents - a review

Ácidos orgánicos acumulados en la pulpa de los frutos: ocurrencia, metabolismo y factores que afectan sus contenidos - una revisión

Franco Famiani^1*; Alberto Battistelli²; Stefano Moscatello²; Juan G. Cruz-Castillo³; Robert P. Walker¹

¹ Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università degli Studi di Perugia, Perugia, ITALY. Correo-e: franco.famiani@unipg.it y rob.walker@talktalk.net (*Autor para correspondencia).

³ Centro Regional Universitario Oriente, Universidad Autónoma Chapingo, Huatusco, Veracruz, MÉXICO.

Received: January 17, 2014.
Accepted: May 27, 2015.

Abstract

Organic acids are abundant constituents of ripe fruits and are responsible for their sourness. In addition, they contribute to their flavour. In many fruits, the most abundant organic acids are malic and citric. The aims of this review are two-fold. The first is to provide a clear overview of malic and citric acids in the flesh of fruits. The abundance of different organic acids in commercially grown fruits is described. How this abundance changes during fruit development is outlined. The metabolic pathways used in the synthesis and dissimilation of malic and citric acids in fruits are described. The functions of malic and citric acids in the flesh of fruits are discussed. Secondly, how environmental and cultural practices can alter the organic acid content of fruits is considered.

Keywords: citrate, cultural practices, malate, malate dehydrogenase (MDH), malic enzyme, phosphoenolpyruvate carboxykinase (PEPCK), phosphoenolpyruvate carboxylase (PEPC), pyruvate orthophosphate dikinase (PPDK), temperature.

Los ácidos orgánicos son componentes abundantes de los frutos maduros y responsables de la acidez, además contribuyen en su sabor. En muchos frutos, los ácidos más abundantes son el málico y el cítrico. Los objetivos de esta revisión son, en primer lugar, proporcionar una reseña clara respecto de los ácidos málico y cítrico en los frutos. Se describe la abundancia de diferentes ácidos en frutos cultivados comercialmente, la manera en que esta abundancia cambia durante el desarrollo de los frutos y las rutas metabólicas usadas en la síntesis y la desasimilación de los ácidos málico y cítrico en los frutos; adicionalmente, se discute sobre las funciones de estos ácidos en la pulpa de los frutos. En segundo lugar, se aborda la manera en que las prácticas ambientales y culturales pueden alterar el contenido de los ácidos orgánicos en frutos.

Palabras clave: citrato, prácticas culturales, malato, Malato deshidrogenasa (MDH), enzima málica, fosfoenolpiruvato carboxiquinasa (PEPCK), fosfoenolpiruvato carboxilasa (PEPC), piruvato ortofosfato diquinasa (PPDK), temperatura.

INTRODUCTION

Organic acids together with sugars are the main soluble components of ripe fruits and have a major effect on taste, being responsible for sourness and contributing to the flavour. Sourness is generally attributed to proton release from acids, whereas their different anions each impart a distinct taste (Johanningsmeiner et al., 2005). Acidity is also one of the main ripening indices that determines the harvest date of fruits used either for direct consumption or industrial processing (Neri, Pratella, & Brigati, 2003). In this article, organic acids are often referred to by the names of their anions, e.g. citrate and malate, and this is because at the pH of the cytoplasm the bulk of their content is in this form. The vast majority of the malate and citrate content of the flesh of fruits is located in the vacuole, and the pH of the vacuole determines the ratio of the undissociated:dissociated acid (Etienne, Génard, Lobit, Mbeguié-A-Mbéguié, & Bugaud, 2013).

Many fruits accumulate organic acids in their flesh at certain stages of their development. Usually either one or two acids account for the bulk of this content (Ulrich, 1971). Theorganic acid(s) that accumulate are dependent on the fruit in question (Ulrich, 1971). However, the most abundant organic acids in many fruits are citric and malic (Ulrich, 1971). A characteristic feature of this accumulation in many fruits is that the concentrations (mg∙g^-1 fresh weight - FW) of these acids increase until the beginning of ripening and then decrease (Walker, Battistelli, Moscatello, Chen, Leegood, & Famiani, 2011a; Famiani, Baldicchi, Battistelli, Moscatello, & Walker, 2009; Famiani et al., 2012a; Famiani, Farinelli, Palliotti, Moscatello, Battistelli, & Walker, 2014a). However, the patterns of their changes during fruit development are often different when the total amount of these compounds per fruit is considered. In this case, in the flesh of several fruits, there is an increase in their content during most of fruit development and ripening (Walker et al., 2011a; Famiani et al., 2012a).

The bulk of the organic acids present in the flesh of fruits is not imported but rather synthesized in the flesh from imported sugars (Ruffner, 1982a, 1982b; Sweetman, Deluc, Cramer, Ford, & Soole, 2009; Etienne et al., 2013). If these acids are metabolized during ripening there are a number of fates. The main ones are: metabolism by the Krebs cycle (respiration), gluconeogenesis, fermentation to ethanol, amino acid synthesis/interconversion, and as a substrate for the synthesis of secondary metabolites such as pigments (Ruffner, 1982a, 1982b; Famiani, Walker, Tecsi, Chen, Proietti, & Leegood, 2000; Famiani et al., 2005; Famiani, Casulli, Proietti, Walker, & Battistelli, 2007; Famiani et al., 2014a; Famiani, Moscatello, Ferradini, Gardi, Battistelli, & Walker, 2014b; Sweetman et al., 2009; Etienne et al., 2013).

The organic acid content of the flesh of fruits is affected by environmental factors and cultivation practices (e.g. temperature, light intensity, cultivar, rootstock, mineral nutrition, water availability, fruit load/ pruning). However, how these factors alter metabolism to bring about changes in organic acid content is in most cases uncertain (Etienne et al., 2013).

This review focuses on malic and citric acids, which are the most abundant organic acids in many fruits. The aims of this review are two-fold. Firstly, to give a clear overview of the occurrence, metabolism and functions of these organic acids in fruits. Secondly, to outline how different environmental conditions and cultivation practices can alter the amount of these compounds in the fruits.

Changes in the organic acid content of fleshy fruits during their development and ripening

Organic acids accumulate in the flesh of many types of fruits at certain stages of their development (Hulme, 1971; Ruffner, 1982a, b; Famiani et al., 2005). The organic acids that are accumulated in fruits can be divided into several metabolic groups, and these are synthesized by different pathways. Firstly, the anions of citric, isocitric and malic acids, namely citrate, isocitrate and malate, are Krebs cycle intermediates (we refer to these in this review as Krebs cycle acids), and one or more of them (usually citric or malic) accounts for a large proportion of the organic acid content of the flesh of all fruits that have been studied (Ulrich, 1971). Nevertheless, other types of organic acids may also be abundant in certain fruits.

A second metabolic group is represented by ascorbic and tartaric acid. Tartaric acid is synthesized from ascorbic acid, and the latter is synthesized from imported sugars (Ruffner, 1982a; Ford, 2012). Grapes usually contain large amounts of tartaric acid in addition to malic acid (Ruffner, 1982a).

A third metabolic group includes quinic acid, which is synthesized by the shikimate pathway (Herrmann, 1995). Several fruits, such as apple, kiwifruit, papaya, pear, quince, stone fruits, and soft fruits, often contain substantial amounts of quinic acid (Arfaioli & Bosetto, 1993; Kalt & McDonald, 1996; Moing, Svanella, Gaudillere, Gaudillere, & Monet, 1999; González- Aguilar, Buta, & Wang, 2003; Wu et al., 2007; García-Mariño, de la Torre, & Matilla, 2008; Nishiyama, Fukuda, Shimohashi, & Oota, 2008; Ayaz, Kadioglu, Bertoft, Acar, & Turna, 2001; Bae, Yun, Jun, Yoon, Nam, & Kwon 2014; Szychowski, Munera-Picazo, Szumny, Carbonell-Barrachina, & Hernández, 2014). For a given type of fruit, which organic acids are accumulated in the flesh, and when this accumulation occurs during development, are often characteristic features. Table 1 summarizes the main organic acid(s) that are accumulated in large amounts during development and/or contained in the flesh of ripe fruits of different shrubby and woody species.

In the flesh of many fruits, such as grape, cherry and several soft fruits, the concentration of malate and/ or citrate (mg∙g^-1 FW) increases until the beginning of ripening and then decreases (Ruffner, 1982a; Famiani et al., 2005, 2014a, 2014b; Walker et al., 2011a). The bulk of the volume of the flesh of most fruits consists of parenchyma cells, and in turn the bulk of the volume of these cells consists of a large vacuole. Most of the stored Krebs cycle acids are contained in these vacuoles (Ruffner, 1982a, 1982b; Etienne et al., 2013).

During the ripening of some fruits, such as grape, tomato and some soft fruits, the amount of malate/ citrate in terms of both concentration (mg∙g^-1 FW) and content per fruit (mg∙fruit^-1) decreases, and this shows that stored organic acids are dissimilated/metabolized (Ruffner, 1982b; Goodenough, Prosser, & Young, 1985; Famiani et al., 2005, 2009, 2014a, 2014b; Famiani & Walker, 2009; Sweetman et al., 2009) (Figure 1). In other fruits, such as mango, strawberry and some cherries, the concentration of citrate/malate (mg∙g^-1 FW) decreases during ripening; however, the amount of these compounds per fruit (mg∙fruit^-1) increases up to commercial harvest (Figure 2). Therefore, in these fruits there is no net dissimilation of malate/citrate, and the decrease in their concentration (mg∙g^-1 FW) is only a dilution effect due to the increase in the size of the fruits, which is brought about largely by vacuolar expansion (Selvaraj & Kumar, 1989; Famiani et al., 2005; Walker et al., 2011a). Also, in kiwifruit no net dissimilation was observed up to harvesting (Walton & de Jong, 1990). In some plums the concentration (mg∙g^-1 FW) of malate decreases during ripening. By contrast, the amount of malate per fruit (mg∙fruit^-1) increases or remains constant for most of ripening, and decreases only at a very advanced stage of ripening (Famiani et al., 2012a) (Figure 3). Finally, in banana, feijoa and lemon both the organic acid concentration (mg∙g^-1 FW) and content per fruit (mg∙fruit^-1) increase throughout ripening (Bartholomew & Sinclair, 1951; Harman, 1987; Agravante, Matsui, & Kitagawa, 1991). Therefore, during ripening there can be either a net dissimilation or synthesis of stored Krebs cycle acids, and which occurs is dependent on which fruit is considered. However, a complicating factor is that superimposed on any net synthesis or dissimilation of malate/citrate that occurs over a period of days, there is a cycle of synthesis and dissimilation (Walker et al., 2011a and references therein). The function of this turnover is uncertain; however, it could be associated with the coordination of the import and utilisation of nitrogenous compounds and associated pH regulation (Walker et al., 2011a; Famiani et al., 2012a).

The studies outlined above have dealt with changes in organic acid content up to commercial ripeness. In many fruits that are over-ripe there is a decline in organic acid content (e.g. sour cherry, plum and grape, unpublished data). If fruits are stored, the storage conditions can affect the organic acid content. In apple after storage under normal air for 3-6 months the malic acid concentration is lower than at harvest (Ackermann, Fischer, & Amad, 1992; Róth et al., 2007). However, this decrease can be reduced if the atmosphere surrounding the apples is modified (Róth et al., 2007). Also, in kiwifruit a slight reduction of citric and malic acid contents was observed after about five months of storage under normal air (temperature = 0° ± 0.5 °C, relative humidity > 90 %) (unpublished data).

Metabolism of Krebs cycle acids in fleshy fruits

Synthesis. The Krebs cycle acids that accumulate within the flesh of fruits do not appear to be imported, but rather they are synthesized within the flesh from imported sugars (Ruffner, 1982b; Law & Plaxton, 1995). Sugars can also derive from photosynthesis within the fruit, however, these sugars account for only a very small proportion of the sugars present in the fruit (Kanellis & Roubelakis-Angelakis, 1993; Palliotti, Silvestroni, & Petoumenou, 2010).

The bulk of Krebs cycle acids present in fruits is synthesized from sugars in the following way. Products from the metabolism of sugars enter the glycolytic pathway and this converts them to phosphoenolpyruvate (PEP). For example, imported sucrose is often hydrolysed to glucose and fructose by one of the invertases. These sugars are then phosphorylated by either glucokinase or fructokinase and enter glycolysis. In plants, the cytosolic enzyme phosphoenolpyruvate carboxylase (PEPC) is necessary for the synthesis of the Krebs cycle acids from sugars. It catalyses the conversion of PEP to oxaloacetate (OAA) (Ruffner, 1982b; Law & Plaxton, 1995). If the fruit is accumulating malate, OAA is converted to malate by cytosolic malate dehydrogenase (NAD-MDH), and malate is transported across the tonoplast into the vacuole in which it is stored (Ruffner, 1982b; Terrier & Romieu, 2001) (Figure 4). If citrate is being accumulated one molecule of PEP is converted to OAA by PEPC (Figure 5). A second PEP is converted to acetyl CoA by the sequential actions of pyruvate kinase and pyruvate dehydrogenase. Aceytl CoA and OAA are then combined by citrate synthase in the mitochondrion to give citrate. Citrate is then transported across the tonoplast into the vacuole in which it is stored. The amount of acids that are stored in the vacuole is the major determinant of the content of Krebs cycle acids in fruits. In the case of malate, it is thought that transport processes at the tonoplast are the key factor in determining the vacuolar content (Ruffner, 1982b; Terrier & Romieu, 2001; Etienne et al., 2013).

Utilization of organic acids. During the ripening of some fruits, such as grape, tomato and some soft fruits, the amount of malate/citrate in terms of both concentration (mg∙g^-1 FW) and content per fruit (mg∙ fruit^-1) decreases and this means that organic acids are metabolized (Ruffner, 1982b; Goodenough et al., 1985; Famiani et al., 2005, 2009, 2014a, 2014b; Famiani & Walker, 2009; Sweetman et al., 2009). There are a number of possible fates for this citrate/malate, and these are oxidation by the Krebs cycle (respiration), gluconeogenesis, amino acid synthesis/ transformations, synthesis of secondary products and/ or the production of ethanol by fermentation (Farineau & Laval-Martin, 1977; Ruffner, 1982b; Famiani et al., 2000, 2005, 2014a).

Respiration. The catabolism of malate and citrate through respiration implies the following reactions. Malate is transformed into pyruvate, by ME or through the combined action of MDH, PEPCK and pyruvate kinase (Figure 6). Pyruvate is then metabolized by pyruvate dehydrogenase before entering the Krebs cycle. In addition, both malate and citrate can enter the Krebs cycle directly (Figure 7). Then the Krebs cycle either partially or completely oxidizes these compounds to CO₂. Cytosolic NADP-ME is important in the dissimilation of Krebs cycle acids in several fruits (Dilley, 1962; Goodenough et al., 1985; Chen et al., 2009; Sweetman et al., 2009). Moreover, citrate can be converted by cytosolic forms of the Krebs cycle enzymes aconitase and isocitrate dehydrogenase to 2-oxoglutarate, which can then enter the Krebs cycle. In addition, citrate can potentially be converted to OAA and acetyl CoA by cytosolic ATP-citrate lyase. However, there is uncertainty as to which of the above reactions is used in many fruits: these could be dependent on the fruit considered and the stage of development.

While all fruits carry out respiration there are marked differences in both the rates and patterns of changes in respiration between fruits of different plant species. All fruits show a high respiration rate per gram of FW at the beginning of their development and this then decreases (largely as a result of the increase in the size of the vacuole which reduces the amount of cytoplasm per gram of FW). However, some fruits show a sharp increase in respiration during ripening, and this is called the climacteric. Fruits can be divided into two types based on this: climacteric and non-climateric fruits. Climateric fruits include apple, apricot, avocado, chinene (Persea schiedeana Nees), kiwifruit, mamey sapote, pear, peach, plum, soursop, and tomato; non- climacteric fruits include cherry, strawberry, citrus, grape, and pineapple (Tucker, 1993; Kader, 2002; del Angel-Coronel, Cruz-Castillo, de la Cruz-Medina, & Famiani, 2010). Organic acids may be utilized by respiration during the climacteric. An increase in the abundance of NADP-ME together with a dissimilation of malate occurs in some fruits, such as tomato and loquat, during the climacteric (Hirai, 1982; Goodenough et al., 1985; Amorós, Zapata, Pretel, Botella, & Serrano, 2003). However, in the flesh of the non-climacteric fruit grape there is a net dissimilation of malate during ripening (Famiani et al., 2007, 2014a, 2014b), and, in at least one variety of the non-climacteric cherry there is no net dissimilation of stored organic acids in its flesh during ripening (Walker et al., 2011a). Therefore, there does not appear to be a correlation between the net dissimilation of Krebs cycle acids in the flesh of fruits during ripening and the occurrence of a respiratory climacteric.

For many years it was thought that the increase in the respiratory quotient (RQ = CO2 evolution/O2 consumption) during the ripening of grapes was a result of the use of organic acids as a respiratory substrate (Peynaud & Ribéreau-Gayon, 1971; Ruffner, 1982b; Kanellis & Roubelakis-Angelakis, 1993). However, recent studies have shown that this increase in RQ is largely brought about by other processes such as fermentation and the use of NADH in biosynthesis rather than oxidative phosphorylation (Famiani et al., 2014a; Famiani, Farinelli, Palliotti, Battistelli, Moscatello, & Walker, 2015).

For many years it was thought that glycolysis was inhibited in ripening grape and that malate provided the bulk of the substrate used by metabolism. Gluconeogenesis was thought to occur because there was an excess of malate (Ruffner, 1982b; Sweetman et al., 2009). However, recent work has shown that this is untrue and that sugars provide the bulk of the substrate used by metabolism (Famiani et al., 2014a, 2015). One explanation for the occurrence of gluconeogenesis is that malate flux from the vacuole is not constant during ripening, and there are times when there is an enhanced efflux of malate which results in an excess of malate in the cytosol (Famiani et al., 2015).

Amino acid and secondary product synthesis. Protein synthesis occurs in the flesh of fruits during ripening, as does the conversion of either stored or newly imported amino acids into those amino acids that accumulate within the ripe fruit (Kanellis & Roubelakis-Angelakis, 1993). Moreover, secondary products, such as pigments that give the fruit its color, are synthesized during ripening. Stored Krebs cycle acids may provide precursors for such amino acids and secondary product synthesis in the flesh of fruits in which Krebs cycle acids are dissimilated during ripening (Famiani et al., 2005, 2009, 2014a, 2014b; Pereira et al., 2006; Famiani & Walker, 2009). Amino acids can be divided into families on the basis of their biosynthetic pathway, with each family having a different precursor. Aspartate, glutamate, PEP and pyruvate are the precursors for the synthesis of many amino acids (Lea, 1993). The carbon skeletons of glutamate and aspartate are the organic acids 2-oxoglutarate and OAA respectively, which are intermediates of the Krebs cycle. OAA can also be obtained from malate through the action of cytosolic MDH. PEP can be synthesized from malate through the action of MDH and PEPCK or ME and PPDK. Pyruvate can be obtained through the combined action of MDH, PEPCK and pyruvate kinase or through the action of ME. Hence, the metabolism of many organic and amino acids is closely linked. PEP is also a substrate for the synthesis of secondary products (e.g. phenolic compounds and pigments). Acetyl CoA is used as a precursor for the synthesis of flavonoids and isoprenoids, and acetyl CoA can derive from either pyruvate by the action of pyruvate dehydrogenase, or citrate by the action of ATP isocitrate lyase (Etienne et al., 2013).

Fermentation. Krebs cycle acids can also be converted to ethanol. There is evidence for the occurrence of aerobic fermentation to ethanol in the grape pericarp, and this may be of common occurrence in the vineyard (Romieu, Tesniere, Thanham, Flanzy, & Robin, 1992; Tesnière, Romieu, Dugelay, Nicol, Flanzy, & Robin, 1994; Terrier & Romieu, 2001). Similarly, in the juice sacs of citrus during ripening there can be an accumulation of ethanol and decreased aerobic respiration, and this also occurs during the storage of harvested fruits (Roe, Davis, & Bruemmer, 1984; Baldwin, 1993). Krebs cycle acids are converted into ethanol as follows (Figure 9). Citrate is converted to malate by reactions catalysed by Krebs cycle enzymes (or in some cases their cytosolic form). Malate is converted into pyruvate by either ME or the combined actions of MDH, PEPCK and pyruvate kinase. This pyruvate is then converted to ethanol by the sequential actions of pyruvate decarboxylase and alcohol dehydrogenase.

Glyoxylate cycle. This effectively enables acetyl- CoA to be converted into malate. This cycle has been suggested to function in malate synthesis in young grape and banana fruits and also to provide substrates for gluconeogenesis during post-harvest ripening of banana (Surendranathan & Nair, 1976; Pua, Chandramouli, Han, & Liu, 2003; Liu, Yang, Murayama, Taira, & Fukushima, 2004; Terrier et al., 2005). However, the enzyme isocitrate lyase (ICL), which is necessary for the cycle to work, was not detected in either the pericarp of several soft fruits or grape berries at several stages of development (Famiani et al., 2005; 2014b). Hence, our view is that the occurrence of ICL (potentially as a component of the glyoxylate cycle) in many fruit at certain stages of development or under certain conditions remains uncertain and further investigations are required. However, these studies should determine the abundance of the enzyme and not just its transcript.

In grape and other fruits, a widespread view is that malate content is largely determined by its compartmentation in the vacuole. That is, most of the malate is located in the vacuole where it is inaccessible to the enzymes that metabolize it. The main factor that is thought to determine this compartmentation is transport of malate across the membrane that separates the vacuole from the cytosol (i.e. the tonoplast) (Ruffner, 1982b; Etienne et al., 2013). Embedded in the tonoplast there are a number of proteins involved in malate/ citrate transport. Those involved in malate transport likely include several different malate transporters, and in addition there are malate channels. One transporter is AttDT, which appears to be regulated by cytosolic pH. That is, if the pH of the cytosol falls, an increase in malate transport to the cytosol occurs (Hu et al., 2005). Less is known about citrate transport processes (Hurth et al., 2005; Etienne et al., 2013). However, for both malate and citrate, the contributions of the different proteins involved in their transport across the tonoplast are poorly understood. In the case of citrate it is thought that a combination of metabolism and transport processes at the tonoplast may control its vacuolar content (Etienne et al., 2013); however, this is not certain. Neither is it certain that in all fruits transport processes at the tonoplast are the predominant factor in determining vacuolar malate content.

Functions of Krebs cycle acids in fleshy fruits

In all fruits, as in all plant tissues, Krebs cycle acid anions are intermediates of many metabolic pathways. However, in many fruits large amounts of Krebs cycle acids accumulate in the vacuole, and these stored acids have other functions. First, in many fruits they are likely to contribute to making the fruit unpalatable until its seed(s) have developed. When the seed(s) are approaching maturity the fruit starts to ripen and its concentration of Krebs cycle acids (mg∙g^-1 FW) decreases. If there is a net dissimilation of these acids during ripening they can be used as substrates for metabolism (see above). Second, recent studies have suggested that a key function of the Krebs cycle acids in fruits may be in the coordination of the import and utilisation of nitrogenous compounds and associated pH regulation (Walker et al., 2011a; Famiani et al., 2012a).

Effects of both environmental conditions and agronomical practices on the content of Krebs cycle acids in fruits

Temperature. The temperature at which fruits are grown affects both their titratable acidity and content of stored organic acids. For both grape and kiwifruit higher temperatures before ripening increase their malate content (Klenert, Rapp, & Alleweldt, 1978; Richardson et al., 2004), whereas higher temperatures during ripening decrease their content (Kliewer, 1970; Buttrose, Hale, & Kliewer, 1971; Hale & Buttrose, 1974; Ruffner, Hawker, & Hale, 1976; Lakso & Kliewer, 1978; Alleweldt, During, & Jung, 1984; Richardson et al., 2004; Lobit, Génard, Soing, & Habib, 2006). Similarly, elevated temperatures during ripening decrease titratable acidity (Kliewer, 1973; Wang & Camp, 2000; Gautier, Rocci, Buret, Grassely, & Causse, 2005; Trad et al., 2013). Furthermore, at least in grape before ripening, the temperature difference between the day and the night has an effect: cool nights and warm days increase organic acid content (especially malic) more than warm days and warm nights (Kliewer, 1973). Recently it was shown that in grape an increase in maximum temperature (4 - 10 °C above controls) before ripening resulted in a higher malate content (this effect was enhanced by warmer nights); during veraison and ripening the effect was to reduce malate content. This was unless the minimum temperatures (during the night) were also raised by 4 - 6 °C, because in this case malate content was not reduced, suggesting that the regulation of malate metabolism differs during day and night (Sweetman, Sadras, Hancock, Soole, & Ford, 2014). Increased temperature of fruits during ripening almost certainly decreases their content of Krebs cycle acids by increasing the rate of many metabolic processes. In fruits, as in all plant tissues, an increase in temperature increases the rate of their metabolism, and hence the consumption of compounds such as sugars and stored Krebs cycle acids that serve as metabolic substrates.

Temperature affects the flux through diverse pathways, for example, respiration and secondary metabolite synthesis (Ruffner, 1982b; Pereira et al., 2006). Moreover, it has been proposed that an increase in temperature could alter transport of malate/citrate at the tonoplast resulting in a decrease in their vacuolar content, and as a result more malate/citrate would be available in the cytosol for use in metabolism (Etienne et al., 2013).

An increase in the rate of respiration of fruits as temperature increases has been shown in many studies (Hansen, 1942; Ruffner et al., 1976; Ruffner, 1982b). The results of Taureilles-Saurel, Romieu, Robin, and Flanzy (1995a, 1995b) support an increase in flux through the Krebs cycle in response to higher temperatures. Transcript levels of several mitochondrial dicarboxylate/ tricarboxylate transporters increased with warming (Rienth et al., 2014), suggesting/supporting an increased import of malate into the mitochondria for respiration (Sweetman et al., 2014).

Light. Several environmental (latitude and orientation of the field if it is on a hill) and cultural factors (training system and pruning) affect light availability for both fruits and leaves. However, the effect of light on fruit composition is difficult to interpret. One reason is that solar irradiance also increases fruit temperature (Smart & Sinclair, 1976), and hence there is an interaction between light and temperature. A second reason is that shade can delay ripening, and this can cause a higher content of organic acids at harvest (Jackson & Lombard, 1993; Tombesi, Antognozzi, & Palliotti, 1993).

In grape, de Bolt, Ristic, Iland, and Ford (2008) varied light intensity at constant fruit temperature. A much lower amount of malate accumulated during stage I of berry development and a lower decrease in malate content occurred during stage III (ripening) in bunches enclosed in boxes compared to those fully exposed to light. The final content of malate was higher in the berries enclosed by boxes. The final soluble solids content (which is an important parameter in defining the ripening stage) was similar in the two treatments. In addition, Hummel and Ferree (1998) showed that in grape increased illumination (compared to a control) decreased total titratable acidity (TTA) and malate content, and this was observed when grapes were harvested at a similar soluble solids concentration or at the same date. Yang, Zhu, Bu, Hu, Wang, and Huang (2009) studied the effects of bagging on development and quality of longan, and they found that the amount of light transmittance affected malic acid content. Photoperiod can also affect fruit composition (including organic acid content) in some fruits such as raspberry (Mazur et al., 2014). Overall these studies suggest that light can alter the organic acid content of fruits directly, that is by a means that is not dependent on increasing fruit temperature.

Cultivar. The different cultivars of one species can have very different organic acids contents (in terms of either the type of acid present or its content) (Kliewer, Howarth, & Omori, 1967; Arfaioli & Bosetto, 1993; Moing et al., 1998; Gurrieri et al., 2001; Albertini, Carcouet, Pailly, Gambotti, Luro, & Berti, 2006; Saradhuldhat & Paull, 2007; Wu et al., 2007; Muñoz-Robredo, Robledo, Manríquez, Molina, & Defilippi, 2011). For example, for some fruits, such as grape, citrus and pineapple, there are either high or low acidity cultivars (Diakou et al., 1997; Sadka, Dahan, Cohen, & Marsh, 2000; Sadka, Dahan, Or, Roose, Marsh, & Cohen, 2001; Saradhuldhat & Paull, 2007). Hence, cultivar can be one of the main factors affecting organic acid content. However, the differences in metabolism between these cultivars that are responsible for these different organic acid contents are not known with any certainty. It should be noted that cultivars differ in their vegetative characteristics (i.e. vigor and foliage density), and that this too could indirectly affect the organic acid content of the fruit.

There have been many studies that have tried to link organic acid contents to metabolism in the cytoplasm. In peach the activities of PEPC, NAD-MDH and NADP- ME could not explain the difference in malate and citrate content between low- and high-acid cultivars (Moing et al., 1998, 2000). Similarly, PEPC cannot account for differences in malate content of low- and high-acid cultivars in apple and loquat (Chen et al., 2009; Yao et al., 2009). In both plum and cherry, there was no correlation between the abundance of PEPCK and malate/citrate dissimilation (Walker et al., 2011a; Famiani et al., 2012a). The abundance of the enzyme citrate synthase does not appear to be responsible for the differences in the citrate content of fruits of low- and high-acid varieties of several fruits (e.g. citrus, melon, peach and pineapple) (Canel, Bailey-Serres, & Roose, 1996; Sadka et al., 2001; Etienne, Moing, Dirlewanger, Raymond, Monet, & Rothan, 2002; Saradhuldhat & Paull, 2007; Tang, Bie, Wu, Yi, & Feng, 2010). On the other hand, it has been suggested that NADP-ME may play a role in determining the low malate content of low acid cultivars of apple and loquat (Chen et al., 2009; Yao et al., 2009). A comparison of low- and high-acid peach varieties showed that there was a difference in the expression of vacuolar proton pumps and it is possible that this could be related to the ability of the vacuole to store malate and citrate (Etienne et al., 2002).In tomato, altered organic acids levels were found in lines which contained sequences for i) PEPCK, ii) PEPC, numerous membrane transporters and a fructokinase-like protein, or iii) an alcohol dehydrogenase and an NADP-linked malic enzyme (Eshed & Zamir, 1994; Causse et al., 2004), indicating that it is likely that some of these proteins are involved in altering the Krebs cycle acid content of fruits. In citrus and pineapple, studies in which low- and high-acid genotypes were compared led to the suggestion that a reduction of aconitase activity in high acidity genotypes played a role in determining citric acid content (Bogin & Wallace, 1966; Sadka et al., 2000; Saradhuldhat & Paull, 2007).

Taken together the above studies suggest that there is not just one mechanism, but different ones that may use a range of metabolic pathways that determine cultivar- dependent differences in fruit organic acid content.

Rootstock. Fruit of 'Rangpur' (Citrus limonia Osb.) and sweet lemon (Citrus limettioides Tan.), high-acid and low- acid species, respectively, were reciprocally grafted. The fruit content of organic acids was unchanged, and in this situation the rootstock had very little effect (Castle, 1995). However, there are studies which show that rootstock can affect the organic acid contents of fruits, such as cherry, citrus, grape, kiwifruit, peach, etc. (Caruso, Giovannini, & Liverani, 1996; Boyes, Strübi, & Marsh, 1997; Cantín, Pinochet, Gogorcena, & Moreno, 2010; Gong, Blackmore, & Walker, 2010; Usenik, Fajt, Mikulic-Petkovsek, Slatnar, Stampar, & Veberic, 2010; Orazem, Stampar, & Hudina, 2011a, 2011b; Legua et al., 2014). In addition to a possible direct influence on the organic acid content of the fruit, the rootstocks may have indirect effects, that is by altering, for example, vegetative vigor, density of the canopy (hence amount of light reaching the fruit), source/sink ratio, water and mineral salt uptake, and these are known to affect the organic acid content of fruits.

Mineral nutrition. In the leaves of many plants nitrogen metabolism is the major factor affecting the content of Krebs cycle acids and large amounts of these can accumulate (Smith & Raven, 1979). This is because the assimilation of nitrate or ammonium into amino acids is not a proton neutral process. Malate metabolism is associated with the pH regulation necessary for this nitrogen assimilation. For example, the assimilation of nitrate into amino acids in leaves consumes protons. Malic acid is synthesized in the leaf and malate is transported to the root. This leaves protons in the leaf to restore the pH (Raven and Smith, 1976). In contrast to leaves, fruits import amides such as glutamine and asparagine as their main source of nitrogen, and the assimilation of these into compounds such as amino acids is proton neutral. Hence, there is no requirement for the synthesis of large amounts of malate in response to their assimilation (Walker & Chen, 2002).

Most studies of the effect of mineral nutrition on fruit quality have dealt with nitrogen and potassium, and for both their effects vary in different studies. Nitrogen supply affects plant vigor and the leaf/fruit ratio, which can then affect both fruit ripening and humidity and sunlight penetration inside the canopy. Therefore, it is often difficult to determine whether the effect of nitrogen is direct or indirect.

In grape, a low nitrogen status of the plant reduces vine vigor, and berries from such plants have both a high soluble solids content and pH together with a low malic acid content (Reynard, Zufferey, Nicol, & Murisier, 2011). In apricot a relatively low N supply (80 kg·ha^-1, as opposed to a higher N supply of 150 kg·ha^-1) resulted in fruits with a slightly higher sugar concentration and lower acid concentration (Radi, Mahrouz, Jaouad, & Amiot, 2003). In peach and tomato a higher nitrogen supply resulted in higher values of titratable acidity and an increase in organic acid contents (Davies & Winsor, 1967; Davies, 1964; Jia et al., 1999). In orange a higher nitrogen supply resulted in a higher titratable acidity (Reitz & Koo, 1960). On the other hand, nitrogen supply caused a reduction in titratable acidity in pineapple (Spironello, Quaggio, Teixeira, Furlani, & Sigrist, 2004), and had no significant effect in peach and kiwifruit (Cummings & Reeves, 1971; Pacheco et al., 2008). In addition, the form in which nitrogen is supplied affects the organic acid content of fruits. Hydroponically-cultivated tomato plants fed with NH₄⁺ had lower citrate and malate contents in ripe fruits than plants fed with NO^-₃ or NO^-₃ + NH₄⁺ (Xin-Juan, Qing-Yu, Xiao-Hui, Shen, & Dong, 2012). Nevertheless, the differences in malate/citrate content observed in these fruits were much less than the differences in content in leaves found in comparable studies (Walker & Chen, 2002). However, in this study (Xin-Juan et al., 2012) no significant correlations were found between the different organic acid contents in the fruits of plants grown using different forms of nitrogen and the content of the enzymes studied (PEPC, NAD- MDH and CS), suggesting that other factors, such as compartmentation, might be involved in determining differences in organic acid content (Gutierréz-Granda & Morrison, 1992).

Water availability. Excess water supply, resulting from either excessive rainfall or irrigation, can affect fruit composition. In over-watered grapevines it appears that a higher organic acid content of the fruit is brought about by both a delay in the ripening of the fruit and excessive growth of the leaves that shade the berries (Smart & Coombe, 1983; Jackson & Lombard, 1993). In grape, especially if grown in dry climatic regions, irrigation can increase titratable acidity and organic acid content (Esteban, Villanueva, & Lissargue, 1999; des Gachons, Leeuwen, Tominaga, Soyer, Gaudillere, & Dubourdieu, 2004; de la Hera-Orts, Martinez-Cutillas, Lopez-Roca, & Gomez-Plaza, 2005).

When fruits of two cultivars of nectarines from well- watered and under-watered trees were compared, it was found that fruits from under-watered plants had a lower amount of both malic and total acids per fruit (Thakur & Singh, 2011). However, in most other studies an increased supply of water decreased the titratable acidity and organic acid content of ripe fruits. In different citrus species (orange, clementine, satsuma mandarin) cultivated using different amounts of water supply, it was found that a lower availability of water resulted in fruits with a higher titratable acidity (Yakushiji, Morinaga, & Nonami, 1998; González-Altozano & Castel, 1999; Brandon, Hockema, & Etxeberria, 2001; Kallsen, Sanden, & Arpaia, 2011). Apple and tomato fruits from well-watered plants had a lower titratable acidity (Mills, Behboudian, & Clothier, 1996; Veit-Köhler, Krumbein, & Kosegarten 1999). In strawberry, fruits from well-watered plants and under-watered plants showed differences in organic acid content, both when expressed on a fresh and dry weight basis; however, these effects were not uniform but cultivar dependent (Bordonaba & Terry, 2010). In peach, irrigation did not result in significant differences in the contents of malic and citric acids, and did not affect the seasonal pattern of changes in the content of these acids (Wu, Genard, Lescourret, Gomez, & Li, 2002).

Hence, the effect of water availability on the organic acid content of fruits is complex, and this is because of the interactions with other factors, such as climatic conditions, cultivar and the time during fruit development when water stress occurs. In addition, water supply can increase vegetative growth, which can have an effect, and increase yield (as result of larger berries) and slows/delays ripening (Jackson & Lombard, 1993). The situation is further complicated because water availability can affect the volume of the fruits and this causes complications when expressing data from experiments. For example, a fruit whose volume has increased as a result of additional water import will have a lower organic acid content per FW but its content per DW will be unaltered.

The use of saline water for the irrigation of tomato resulted in a reduction in fruit growth and yield; however, the fruit had increased contents of organic acids, sugars and soluble solids. In addition, there was an increase in the transcription of a PEPCK gene (Incerti, Navari-Izzo, Pardossi, Mensual, & Izzo, 2007; Saito et al., 2008).

Fruit load (source/sink ratio). A different fruit load is the result of fruit-set, which can be affected by both environmental and cultivation practices. Fruit thinning and pruning (including defoliation) are important tools to regulate fruit load and the source/sink ratio. An increase in fruit load modifies fruit composition directly by reducing the amount of sugars and other nutrients imported into a fruit in a given period of time. It also changes fruit composition indirectly by slowing fruit development and ripening (Jackson & Lombard, 1993; Poiroux-Gonord, Fanciullino, Bert, & Urban, 2012). In grape, both a higher juice pH and soluble solids content together with a lower content of organic acids are often found in grape berries from plants with a low fruit load (Jackson & Lombard, 1993; Palliotti & Poni, 2011). However, the results of such studies are dependent on when the fruit is sampled. That is whether they are harvested at the same date or when they have a similar soluble solids content (similar ripening stage). When berries were harvested at a similar soluble solids concentration, it was found that an increase in fruit load delayed the time at which berries were suitable for harvesting, and in these berries titratable acidity was reduced, as were tartaric and malic acid contents (Hummel & Ferree, 1998). These results suggest that an increase in crop load decreases the amount of nutrients imported into a given berry, and this then reduces the amount of organic acids synthesized in each berry. Similarly, in kiwifruit yield is negatively correlated with total titratable acidity at harvest (Famiani, Casulli, Baldicchi, Battistelli, Moscatello, & Walker, 2012b). In peach and mango a different behaviour of citric and malic acids was observed.

At the beginning of growth, fruits with high leaf/ fruit ratio had lower malate and higher citrate concentrations, whereas near maturity, greater assimilate supply was related to high malate and low citrate concentrations Souty, Génard, Reich, & Albagnac, 1999; Wu et al., 2002; Léchaudel, Joas, Caro, Génard, & Jannoyer, 2005). In these studies the comparisons were done on samples collected on the same date and not at similar stages of development and ripening; the pattern of changes in organic acid contents indicate a slower development and late ripening of fruits growing on shoots with a low leaf/ fruit ratios. However, it appears that fruits from plants with a higher leaf/fruit ratio often have a higher organic acid content, and this may be a result of an increased import of photoassimilates. In banana, fruit load had no effects on the accumulation of organic acids in the fruits (Etienne et al., 2014).

Source-sink relationships can also be altered by applying compounds that increase the sink strength of the fruit. For example, the application of growth regulators which promote fruit growth (such as the cytokinin-like compounds CPPU and Thidiazuron) alter the acidity of kiwifruits at harvest (Famiani, Battistelli, Moscatello, Boco, & Antognozzi, 1999). However, this change in acidity appears to be a result of earlier ripening, and the effects of these plant growth regulators are dependent on both the time of their application and the concentration that is used (Cruz-Castillo et al., 2014).

CONCLUSIONS

The observation that organic acid concentration (mg∙g^-1 FW) decreases during ripening can be misleading. This is because in many fruits this decrease is not brought about by the metabolism of the organic acid but by an increase in the weight of the fruit caused by its expansion. If there is an actual dissimilation of malate/ citrate during ripening, their metabolic fate can be respiration, gluconeogenesis, amino acid synthesis/ transformations, synthesis of secondary products and/or the production of ethanol by fermentation. If gluconeogenesis occurs, then it appears that in most fruits the PEPCK and not the PPDK pathway is utilized.

Although much progress has been made in understanding the metabolism of malate and citrate metabolism in fruits, many questions remain to be answered. The reason why gluconeogenesis occurs in fruits is one such question. To further understand this requires a combination of biochemical and molecular approaches. For example, metabolic studies in tomato plants with reduced amounts of PEPCK in their fruits have provided useful information on the pathways of gluconeogenesis in tomato fruit (Osorio et al., 2013). In fruits both PEPCK and PEPC are present in the cytosol of the same cells (Famiani et al., 2005). PEPC functions in the conversion of PEP to malate and PEPCK functions in the reverse reaction. To understand how the activity of these enzymes are coordinated will require biochemical approaches as was used to study the regulation of these enzymes in CAM plants (Walker & Chen, 2002). Another example of an important gap in our knowledge of malate metabolism in fruits is how malate transport across the tonoplast is regulated. Molecular approaches have identified homologues of malate transporters in fruits (Etienne et al., 2013). However, to understand how the activity of these transporters is regulated will require biochemical studies using, for example, assays of their activity in systems in which the transporters are reconstituted into lipid vesicles. Such studies could investigate the effects of metabolite effectors and phosphorylation of the transporter. There have been no such studies in fruits.

In several cases how environmental and agronomical factors bring about changes in the organic acid content of fruits is not simple. This may be due in part to the fact that these factors can often change conditions other than the one which is being studied (e.g. an increase in light exposure also increases temperature; a high fruit load can delay ripening). However, the effects of temperature are understood in a number of situations. The light likely has a direct effect on organic acids. For a given type of fruit the cultivar has a large and reproducible effect on organic acid content. However, in different fruits it appears that different mechanisms (e.g. metabolic pathways or transport processes at the tonoplast) are responsible for these differences. Further studies, using a combination of physiological, biochemical and molecular approaches, are necessary to further understand the mechanisms responsible for these differences. An understanding of these mechanisms would be of assistance in both genetic improvement programs and in the optimization of cultural practices. For many species/genotypes, an increased fruit load decreases the organic acid content of the fruits. The direct effects of cultural practices such as irrigation and the application of fertilizers are complex. Often their effects are variable, and this is because there are interactions with other environmental and cultural factors. Therefore, detailed studies are required to define the effects of a given cultural practice under different environmental and cultural conditions.

ACKNOWLEDGEMENTS

The work was partially funded by the "Fondazione Cassa di Risparmio di Perugia e Codice Progetto 2010.011.0470".

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