- Email: [email protected]
Pectin role in woolliness development in peaches and nectarines: A review
Scientia Horticulturae 180 (2014) 1–5
Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Review
Pectin role in woolliness development in peaches and nectarines: A review Goran Fruk a,∗ , Zlatko Cmelik a , Tomislav Jemric a , Janez Hribar b , Rajko Vidrih b a b
University of Zagreb Faculty of Agriculture, Department of Pomology, Svetosimunska cesta 25, HR – 10 000 Zagreb, Croatia University of Ljubljana Biotechnical Faculty, Department of Food Science and Technology, Jamnikarjeva 101, SI – 1000 Ljubljana, Slovenia
a r t i c l e
i n f o
Article history: Received 25 July 2014 Received in revised form 20 September 2014 Accepted 24 September 2014 Keywords: Peach and nectarine Ethylene Chilling injury Pectin Cell anatomy Temperature
a b s t r a c t One of the main problems during peach and nectarine cold storage is the associated chilling injuries, which can include woolliness, mealiness, leatheriness, flesh browning, internal reddening, and flesh or pit cavities. Woolliness is one form of chilling injury. It manifests as a lack of juiciness and a dry ‘woolly’ texture of the fruit flesh. Its occurrence is correlated with pectin metabolism and is controlled directly or indirectly by the pectolytic enzymes (i.e., polygalacturonase, pectin esterase, cellulase, lipoxygenase). Chilling injury to these fruit also results in changes in the fruit physiology and cell anatomy. A reduction in woolliness is possible with post-harvest treatments, such as with heat (which must be carried out carefully), calcium, ethylene (blocking or producing), nitrogen monoxide, or a controlled atmosphere. This paper focuses only on woolliness and factors affecting its occurrence. In this paper the role of pectin metabolism, temperature and postharvest treatments on occurrence of woolliness is discussed. The role of some enzymes, such as pectin esterase, and postharvest treatment with 1-MCP still remain unclear and further research is needed to elucidate physiological mechanisms that lead to development of woolliness. © 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6. 7. 8. 9.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The development of woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The role of temperature in the development of woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cell anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pectin metabolism in peaches and nectarines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other metabolic processes and woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Harvest date and maturity stage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Post-harvest treatments to alleviate woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction During cold storage of peaches (Prunus persica Batsch.) and nectarines (P. persica var. nectarina Ait.), one of the main problems is chilling injuries, which are a collective term for the physiological
∗ Corresponding author. Tel.: +385 1 239 3842; fax: +385 1 239 3630. E-mail address: [email protected] (G. Fruk). http://dx.doi.org/10.1016/j.scienta.2014.09.042 0304-4238/© 2014 Elsevier B.V. All rights reserved.
1 2 2 2 2 3 3 3 4 4 4
disorders that can occur during such fruit storage. Chilling injuries develop during ripening on 20 ◦ C (shelf life) after fruit is stored at 2.2–7.6 ◦ C for at least 2 weeks or at 0 ◦ C for 3 weeks or more (Lill et al., 1989; Lurie and Crisosto, 2005). Furthermore, chilling injuries are an internal disorder, and are therefore not generally noticed until the fruit reaches customers. With peaches and nectarines, chilling injuries can include woolliness, mealiness, leatheriness, flesh browning, internal reddening, and flesh or pit cavities (Lurie and Crisosto, 2005). Woolliness manifests as a lack of juiciness and a dry ‘woolly’ texture of the fruit flesh (Zhou et al., 2000a), and it
2
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
is caused by an imbalance in pectin metabolism during cold storage (Ben-Arie and Sonego, 1980). A previous review about such chilling injuries of peaches and nectarines was focused on a description of the symptoms of chilling injuries and the methods of their prevention or reduction (Lurie and Crisosto, 2005). Therefore, the aim of the present review is to provide an overview of studies on woolliness development, reduction and prevention in peaches and nectarines. 2. The development of woolliness Woolliness is a result of gel formation due to high-molecularweight pectin binding and a low degree of esterification in combination with calcium, extracellular water and the solutes that pass through the cell wall (Sonego et al., 1995). The juiciness decreases due to the strong water binding in calcium-pectate gels, and although the amount of water in woolly and healthy fruit is the same (Lill and Mespel, 1988; Zhou et al., 2000a), woolliness can also be measured as a lack of extractable juice (Zhou et al., 2000d). However, water-soluble pectins do not form a gel in vitro, while alkali-soluble pectins and calcium do form a gel in vitro (Levaj et al., 2003), which means that as well as the pectins, calcium is needed for juice gelling and the occurrence of woolliness. A prerequisite for woolliness development is deesterification of the pectins, while the degree of polymerisation and the level of calcium pectates are maintained (Lurie et al., 2003). During chilling, along with a mealy texture, injured fruit can appear dry, and the arabinan loss in the pectins is reduced, with changes to the pectin polymerisation. These changes in the cell wall result in weakening of intercellular adhesion and reduced cell rupture, which are reflected as reduced fruit juiciness (Brummell, 2007). In addition to the degradation of the arabinose and galactose of the pectin chain side branches during the ripening of peaches, the main pectin chains can also be degraded (Kan et al., 2013). In woolly peaches, the content of insoluble pectin is increased (e.g., protopectin, deesterified pectates), which favours the formation of pectin gels (Lurie et al., 2003). During ripening, pectin degradation can also cause only a temporary woolliness, which disappears following further hydrolysis of the cell wall (Mollendorff et al., 1992). 3. The role of temperature in the development of woolliness Peaches and nectarines stored at 0 ◦ C can develop symptoms of woolliness. Due to reduced polygalacturonase (PG) activity, these fruit have less water-soluble pectins and more sodium-carbonatesoluble pectins than the fruit ripened at 20 ◦ C immediately after harvest. Pectin esterase has a reduced activity at low temperatures, so it is more likely that this woolliness is caused by altered PG activity (Choi and Lee, 1997). The storage of peaches for a few days at 8 ◦ C and then at 0 ◦ C can maintain a lower content of water-soluble pectins, and a higher content of protopectins and extractable juice (Li et al., 2009). Similar results in plums reports Taylor et al. (1995). Soluble pectins remain low during storage at low temperature (0 ◦ C), but significantly increases when transferred to higher temperature (8 ◦ C), most likely because higher temperature stimulates ripening. Mao and Zhang (2001) argued that woolliness in peaches develops due to the abnormal degradation of the pectins in the cell wall, which is caused by reduced activities of the pectolytic enzymes and of cellulase (EC 3.2.1.4). Cellulase participates in normal peach ripening (Bonghi et al., 1998). Heat treatment before and during peach storage can alleviate the occurrence of chilling injuries and prevent the irreversible destruction of endopolygalacturonase (endoPG; EC 3.2.1.15) and cellulase that can occur due to low
temperatures. This allows the normal pectin degradation processes (Mao and Zhang, 2001). Also, although Zhou et al. (2000c) reported that there is reduced cellulase activity in woolly nectarines, they also argued that the role of cellulases is probably only in the initial stages of fruit softening during ripening, and therefore cellulases do not directly affect the woolliness of nectarines. With peaches that have been dipped in hot water, there is a greater reduction in the pectin content during storage than for peaches that are treated with hot moist air (Bakshi and Masoodi, 2010). However, heat treatments need be carefully adjusted, as Sasaki et al. (2010) observed increased woolliness in peaches treated at 50 ◦ C for 1 h or 2 h. This might be due to the optimum temperature being reached in the fruit for the activity of the enzyme pectin esterase (40–45 ◦ C). 4. Cell anatomy Peaches that have been ripened immediately after harvest at ambient temperatures have cells of regular shape, with maintained adhesion to other cells and typical intercellular spaces. In contrast, woolly peaches ripened after cold storage have cells with irregular shapes that are separated from each other (Lurie et al., 2003; Luza et al., 1992). However, Ghiani et al. (2011) showed cells with irregular shapes and that were separated in ripened meltingflesh and non-melting-flesh peaches that had not been cold stored. This phenomenon was attributed to the loss of the turgor of the cells, due to the degradation of the cell walls under the influence PG, which leads to fruit softening. Rodriguez and Lizana (2006) did not note the separation of cells and an increase in intercellular space in woolly nectarines, although they noted the accumulation of pectin substances in cell walls and in the intercellular spaces. The juice obtained by squeezing healthy (juicy) peaches contained almost no whole cells, while the juice from mealy peaches contained approximately 30% viable cells (Brummell et al., 2004b). 5. Pectin metabolism in peaches and nectarines Pectins are heterogeneous macromolecules of polysaccharides that can contain up to 17 different monosaccharides, and that are rich in galacturonic acids (Vincken, 2003; Yang et al., 2005, 2009). Pectins are located in the primary cell wall and in the central lamella (Brummell et al., 2004a), and they have very important roles as they are the most common macromolecules in the cell wall. Softening of fruit accompanies solubilisation and depolymerisation of the pectins, which result in the weakening and disintegration of the cell wall (Billy et al., 2008). Indeed, it is this pectin solubilisation and the associated cell-wall swelling that leads to fruit softening (Redgwell et al., 1997). The pectins can be solubilised prior to their depolymerisation, and it has been shown that the depolymerisation of pectins is not the first step in their degradation (Dawson et al., 1992). During the storage of peaches, the water-soluble and chelatesoluble pectins are reduced, with an increasing number of single linear polysaccharide chains seen (Zhang et al., 2012). The most important biochemical indicator of a change in texture is the galacturonic acid content in water-soluble pectin extracts (Billy et al., 2008). In addition to these structure changes to the pectins (Ketsa et al., 1999; Zhang et al., 2010), fruit softening is associated with cleavage of the arabinose and galactose side chains of uronide-acidcontaining polysaccharides (i.e., the polyuronides (Brummell et al., 2004a). These side chains are responsible for the size of the pores in the cell wall, and thus they can prevent pectolytic enzymes from disassembling the pectins, and protect the polysaccharides in the cell wall from excessive deesterification (Ortiz et al., 2010). Peach fruit softening is thus accompanied by the transition of the water-insoluble pectins into the water-soluble pectins that
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
give the characteristic texture of the ripened fruit (Jia et al., 2006). Indeed, the ratio of the water-soluble to water-insoluble fractions of the pectins can provide an indicator of nectarine ripening (Manganaris et al., 2005a). However, although fruit firmness is associated with water-soluble or sodium-carbonate-soluble pectins, the pectin structure is not solely responsible for fruit softening (Zhang et al., 2008, 2010). The activity of endoPG is strongly correlated with the characteristics of melting-flesh peaches. It has been reported that the lack of the melting phase in non-melting-flesh peaches is caused by deletion of the gene for endoPG or by truncation of its mRNA, and thus by a lack of synthesis of the endoPG protein. Therefore, it appears that endoPG is responsible for the increased softening in melting-flesh peaches, as compared to nonmelting-flesh peaches (Manganaris et al., 2006b). The main changes in the cell wall during peach ripening are hemicellulose depolymerisation, reduction in pectin arabinan content, and pectin depolymerisation (Brummell, 2007). Clingstone peaches have an exo-polygalacturonase (exoPG; EC 3.2.1.82) and water insoluble pectins, while freestone peaches have both an endoPG and an exoPG and a high water-soluble pectin content (Pressey and Avants, 1978). During storage, the water-soluble pectins lose their side chains, which are mainly composed of arabinose and/or galactose (Kan et al., 2013; Needs et al., 2001; Yang et al., 2005). Approximately 15–17 weeks after full bloom of peach and nectarine trees, the protopectins, which are insoluble in water, are hydrolysed to pectic acids, which are soluble in water (Selli and Sansavini, 1995). Lower storage temperatures can reduce this degradation of the pectins, probably due to inhibition of the enzymatic activity (Zhang et al., 2012; Zhou et al., 2000b). Choi and Lee (1997) reported that pectin esterase (PE; EC 3.1.1.11; also known as pectin methyl esterase) does not affect the occurrence of woolliness in peaches, but Zhou et al. (2000b) showed that at the relatively high PE and low PG activities in injured peaches, the pectic matrix can be deesterified without subsequent depolymerisation. This leads to the formation of high-molecularweight pectins that have a low degree of esterification. This type of pectin forms a gel, possibly in combination with calcium from the cell wall, which then binds the free water in the flesh, thereby causing woolliness. Zhou et al. (2000b) reports that imbalance of PG and PE activity is responsible for development of woolliness. Thus, Girardi et al. (2005) in their study concludes that wooliness development in peach (cv. ‘Chiripa’) could be alleviated in two ways: (1) by increasing PG (endo- and exo-) activity, or (2) decreasing PE activity. Flesh browning is accompanied by an increased content of neutral sugars, reduced content of pectins and cellulose, reduced content of pectic enzymes (PG and PE), and the binding of cations (e.g., calcium) within the cell wall (Manganaris et al., 2006a). The juice viscosity and the molecular weight of the watersoluble pectins are reduced during peach ripening (Davidyuk, 1972). The differences in juice viscosity in healthy and woolly peaches are caused by the type of polymers in the juice, rather than by their quantity. Thus, high-molecular-weight pectins in the juice of woolly peaches results in higher juice viscosity than seen for the juice of healthy peaches that contains low-molecular-weight pectins (Zhou et al., 1999).
6. Other metabolic processes and woolliness Some studies have reported that as well as the roles in woolliness development in peaches of the already mentioned enzymes (PG, PE, cellulase), lipoxygenase (EC 1.13.11.12) might also participate (Li et al., 2012; Zhang et al., 2011). The linoleic and linolenic fatty acids are an integral part of the cell wall and are the precursors for volatile aroma compounds (e.g., hexanal and hexenal).
3
Lipoxygenase is involved in their conversion to these volatile aroma compounds (Schwab et al., 2008). Indeed, Zhang et al. (2011) reported that with chilling injuries to peaches, the fatty acids in the cell wall showed changed profiles, which the lipoxygenase activity affected, and which led to a reduced content of volatile aroma compounds. Li et al. (2012) suggested that ethylene treatment and low-temperature acclimatisation can increase the PG and lipoxygenase activities, which leads to reduced woolliness of peaches. The role of lipoxygenase in the development of chilling injuries in peaches and nectarines has not, however, been studied in detail. 7. Harvest date and maturity stage During storage, early harvested peaches show more leatheriness than mealiness, while those that are late harvested show more mealiness than leatheriness, as compared to the peaches harvested at commercial maturity (Ju et al., 2000). Girardi et al. (2005) also found that early harvest of peaches can promote chilling injury development during cold storage. Leathery (dry) peaches synthesise less ethylene, have lower PG activity and higher firmness, and contain more insoluble pectins than mealy peaches, although such differences have not been seen between mealy and juicy peaches (Ju et al., 2001). 8. Post-harvest treatments to alleviate woolliness Choi and Lee (1997) observed that woolliness reduction is based on an increase in water-soluble pectin content and a reduction in sodium-carbonate-soluble pectins, under the influence of increased PG activity. Peaches that were stored at low temperatures with intermittent warming had similar PG activities to those that were not stored at low temperatures, while the PE activities were lower than in cold-stored peaches (Ben-Arie and Sonego, 1980). However, peaches that were stored at low temperatures immediately after harvest had lower PG activities than peaches that underwent delayed storage (Mollendorff and Villiers, 1988). Obenland and Carroll (2000) reports that intermittent warming cannot alleviate chilling injuries to satisfactory level if pre-storage heat treatment (high temperature forced air) was used. They also reports that long heat treatment (3 or 4 h) can inhibit or drastically decrease PG activity and by this alteration promote chilling injury development. If intermittent warming is used alone it could be useful in alleviating chilling injuries in peaches (Ben-Arie and Sonego, 1980; Girardi et al., 2005). Periodical warming of peaches during their storage at low temperatures can maintain the PG activity, which promotes solubilisation of the water-soluble pectins and normal peach ripening (Ben-Arie and Sonego, 1980). During woolliness development, liquids and solutes pass through the cell membranes (as a result of long-term storage at low temperatures) and bind to the high-molecular-weight pectins, thus forming pectic gels in the intercellular spaces, and resulting in the typical dry texture observed for woolly nectarines (Mollendorff et al., 1993). Bassi et al. (1998) reported that non-melting-flesh peaches have 35% more calcium bound to the insoluble pectins than for meltingflesh peaches. Therefore, the logical question that has been raised is what would happen if peaches were immersed in a solution of calcium after harvest, as can be done with apples. The dipping of the fruit into a solution of calcium chloride increases the concentration of calcium in the insoluble fraction of the pectins, which maintains the firmness and physico-chemical properties of the fruit (Manganaris et al., 2005b). Exogenous calcium can stabilise and protect the cell wall from the cell-wall-degrading enzymes (i.e., PG, PE) (Nunez et al., 2005; White and Broadley, 2003). In peaches treated with calcium, their content of covalent and ionic bonded pectins decreased during their shelf life. Reduced PG activity was
4
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
also noted, while PE activity increased (Cao et al., 2008). However, calcium propionate and calcium lactate are not recommended as calcium treatments for nectarines, because their too high concentrations can damage the fruit skin (Manganaris et al., 2005b). Nitrogen monoxide treatment can alleviate symptoms of chilling injuries, and especially woolliness. Nitric monoxide changes the relationship between PE and PG, which stops the increase in the content of soluble pectins and the reduction in the ionic pectins. The consequence here is reduced woolliness (Zhu et al., 2006). Post-harvest peach treatments with 1-methylcyclopropene (1MCP; an inhibitor of ethylene action) can significantly reduce the loss of the pectins (Oliveira et al., 2005; Wang et al., 2005). This appears to be due to the low PG activity for pectin degradation. Ethylene is known to act as a trigger for the indirect synthesis of PG in tomato (Grierson and Tucker, 1983); therefore, ethylene should have an important role in the solubility of the polyuronides and in the development of mealiness in peaches (Murayama et al., 2009). Post-harvest application of 1-MCP to peaches also reduces the activity of PE (Oliveira et al., 2005). Although this 1-MCP treatment of peaches can significantly affect fruit ripening, it does not completely prevent ripening, and therefore Liu et al. (2005) considered that the ethylene receptors in the fruit are constantly being synthesised during storage. Ortiz et al. (2011) reported different results, as they found that application of 1-MCP resulted in increased PE activity and inhibited the other pectolytic enzymes. A controlled atmosphere during storage of peaches can be used to inhibit degradation of the water-soluble pectins, the sodiumcarbonate-soluble pectins, and the chelate-soluble pectins (Yang et al., 2006a,b, 2005). High CO2 and low O2 contents in the storage atmosphere can inhibit PG transcription during such controlled atmosphere conditions (Zhou et al., 2000b). In contrast, Ortiz et al. (2011) reported that a controlled atmosphere can only partially inhibit the pectolytic enzymes in peaches, and increases the content of the pectin polysaccharides. This leads to an increase in the content of chelate-soluble pectins within the cell walls. The combined application of 1-MCP and a controlled atmosphere was seen not to be sufficient to maintain peach firmness, probably due to increased degradation of the pectins (Ortiz et al., 2011). These results are probably related to the peach ripening stage at harvest. Ethylene treatment can also delay and reduce woolliness in peaches stored at a temperature of 0 ◦ C. This ethylene treatment also stimulates PG activity during storage, while ethylene has no influence on the PE activity of these peaches (Sonego et al., 1999).
9. Conclusions Although the metabolism of pectins participates in a number of physiological disorders during peach and nectarine storage (e.g., mealiness, leatheriness, woolliness), its biggest role is in the woolliness of these fruit, as the pectins in intercellular spaces bind the free juice into pectate gels. Disorders of pectin metabolism are caused by changes in the pectolytic enzyme activities (i.e., mainly endoPG and exoPG, PE, cellulose, lipoxygenase). Such disorders lead to an imbalance in the degradation of the pectins, which has the effect of binding the juice into pectate gels. Post-harvest heat treatments can reduce the woolliness, but they must be precise because they can also increase woolliness, and so they need to achieve the optimum temperature for the fruit pectolytic enzyme activity. Post-harvest application of 1-MCP and ethylene has different effects on PE activity. This leads to the conclusion that 1-MCP and ethylene have no direct impacts on PE, and that instead the changes in PE activity are triggered by some other processes in the fruit. In peaches, 1-MCP cannot be used for the classical intention of maintaining the fruit firmness or stopping ripening, although it can slow down these
processes and alleviate chilling injuries. The application of nitric oxide or calcium to reduce the woolliness of cold-stored fruit can be a successful treatment. Detailed studies of cellulase and lipoxygenase in pectin metabolism should be carried out to determine their roles in chilling injuries. Acknowledgements This review was written as part of the scientific specialisation of Goran Fruk, with the support of a bilateral scholarship provided by the Centre of the Republic of Slovenia for Mobility, and the European Educational and Training Programmes (CMEPIUS). This article was also supported by the Ministry of Science, Technology and Sports of Republic of Croatia (Projects 1780000000-3583). References Bakshi, P., Masoodi, F.A., 2010. Effect of pre-storage heat treatment on enzymological changes in peach. J. Food Sci. Technol. 47, 461–464. Bassi, D., Mignani, I., Rizzo, M., 1998. Calcium and pectin influence peach flesh texture. Acta Hortic. 465, 433–438. Ben-Arie, R., Sonego, L., 1980. Pectolytic enzyme activity involved in woolly breakdown of peach. Phytochemistry 19, 2553–2555. Billy, L., Mehinagic, E., Royer, G., Renard, C.M.G.C., Arvisenet, G., Prost, C., Jourjon, F., 2008. Relationship between texture and pectin composition of two apple cultivars during storage. Postharvest Biol. Technol. 47, 315–324. Bonghi, C., Ferrarese, L., Ruperti, B., Tonutti, P., Ramina, A., 1998. Endo--1,4glucanases are involved in peach fruit growth and ripening, and regulated by ethylene. Physiol. Plant. 102, 346–352. Brummell, D.A., 2007. How dynamic primary cell wall properties affect fruit tissue firmness; intercellular adhesion and the characteristics of processed fruit products. Mitteilungen der Bundesforschungsanstalt fur Forst- und Holzwirtschaft 223, 53–60. Brummell, D.A., Dal Cin, V., Crisosto, C.H., Labavitch, J.M., 2004a. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J. Exp. Bot. 55, 2029–2039. Brummell, D.A., Dal Cin, V., Lurie, S., Crisosto, C.H., Labavitch, J.M., 2004b. Cell wall metabolism during the development of chilling injury in cold-stored peach fruit: association of mealiness with arrested disassembly of cell wall pectins. J. Exp. Bot. 55, 2041–2052. Cao, Y., Cao, Y., Li, Z., Ren, J., Leng, P., 2008. Effect of pre-harvest calcium sprays on fruit quality and softening during storage of melting flesh peach. J. China Agric. Univ. 13, 31–36. Choi, J.H., Lee, S.K., 1997. Effect of MA storage on woolliness of ‘Yumyeong’ peaches. Postharvest Horticulture Series – Department of Pomology, University of California 17., pp. 132–138. Davidyuk, L.P., 1972. Studies on the quality of soluble pectin in relation to peach fruit ripening. Byulleten’ Gosudarstvennogo Nikitskogo Botanicheskogo Sada 3, 53–56. Dawson, D.M., Melton, L.D., Watkins, C.B., 1992. Cell wall changes in nectarines (Prunus persica): solubilization and depolymerization of pectic and neutral polymers during ripening and in mealy fruit. Plant Physiol. 100, 1203–1210. Ghiani, A., Onelli, E., Aina, R., Cocucci, M., Citterio, S., 2011. A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endo-polygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. J. Exp. Bot. 62, 4043–4054. Girardi, C.L., Corrent, A.R., Lucchetta, L., Zanuzo, M.R., Costa, T.S.D., Brackmann, A., Twyman, R.M., Nora, F.R., Nora, L., Silva, J.A., Rombaldi, C.V., 2005. Effect of ethylene, intermittent warming and controlled atmosphere on postharvest quality and the occurrence of woolliness in peach (Prunus persica cv. Chiripá) during cold storage. Postharvest Biol. Technol. 38, 25–33. Grierson, D., Tucker, G.A., 1983. Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato fruit ripening. Planta 157, 174–179. Jia, H.J., Mizuguchi, K., Hirano, K., Okamoto, G., 2006. Effect of fertilizer application level on pectin composition of Hakuho peach (Prunus persica Batsch) during maturation. HortScience 41, 1571–1575. Ju, Z.G., Duan, J.S., Ju, Z.Q., 2000. Leatheriness and mealiness of peaches in relation to fruit maturity and storage temperature. J. Hortic. Sci. Biotechnol. 75, 86–91. Ju, Z.G., Duan, Y.S., Ju, Z.Q., Guo, A.X., 2001. Different responses of ‘Snow Giant’ and ‘Elegant Lady’ peaches to fruit maturity and storage temperature. J. Hortic. Sci. Biotechnol. 76, 575–580. Kan, J., Liu, J., Jin, C.H., 2013. Changes in cell walls during fruit ripening in Chinese ‘Honey’ peach. J. Hortic. Sci. Biotechnol. 88, 37–46. Ketsa, S., Chidtragool, S., Klein, J.D., Lurie, S., 1999. Firmness, pectin components and cell wall hydrolases of mango fruit following low-temperature stress. J. Hortic. Sci. Biotechnol. 74, 685–689. Levaj, B., Dragovic-Uzelac, V., Dancevic, A., Frlan, J., 2003. The effect of ripening and storage on peach pectin and gel strength of related jams. Acta Aliment. Hung. 32, 329–340.
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5 Li, Y.X., Guan, J., Feng, Y., Ji, H., Sun, Y., 2009. Effects of cold-storage mode on post-harvest pectin contents and beta-galactosidase activity of peach. Acta Bot. Boreali-Occidential Sin. 29, 1637–1642. Li, Y.X., Wang, G.X., Liang, L.S., 2012. Effect of cold acclimation treatment and exogenous ethylene treatment on woolliness related enzymes on ‘Okubo’ peach fruits during low temperature storage. Acta Hortic. 934, 1103–1109. Lill, R.E., Mespel, G.J.V.D., 1988. A method for measuring the juice content of mealy nectarines. Sci. Hortic. 36, 267–271. Lill, R.E., O’Donoghue, E.M., King, G.A., 1989. Postharvest Physiology of Peaches and Nectarines. Horticultural Reviews. John Wiley & Sons, Inc., pp. 413–452. Liu, H., Jiang, W., Zhou, L., Wang, B., Luo, Y., 2005. The effects of 1methylcyclopropene on peach fruit (Prunus persica L. cv. Jiubao) ripening and disease resistance. Int. J. Food Sci. Technol. 40, 1–7. Lurie, S., Crisosto, C.H., 2005. Chilling injury in peach and nectarine. Postharvest Biol. Technol. 37, 195–208. Lurie, S., Zhou, H.W., Lers, A., Sonego, L., Alexandrov, S., Shomer, I., 2003. Study of pectin esterase and changes in pectin methylation during normal and abnormal peach ripening. Physiol. Plant. 119, 287–294. Luza, J.G., Gorsel, R.V., Polito, V.S., Kader, A.A., 1992. Chilling injury in peaches – a cytochemical and ultrastructural cell-wall study. J. Am. Soc. Hortic. Sci. 117, 114–118. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2005a. Cell wall cation composition and distribution in chilling-injured nectarine fruit. Postharvest Biol. Technol. 37, 72–80. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2005b. Effect of postharvest calcium treatments on the physicochemical properties of cell wall pectin in nectarine fruit during ripening after harvest or cold storage. J. Hortic. Sci. Biotechnol. 80, 611–617. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2006a. Cell wall physicochemical aspects of peach fruit related to internal breakdown symptoms. Postharvest Biol. Technol. 39, 69–74. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2006b. Diverse metabolism of cell wall components of melting and non-melting peach genotypes during ripening after harvest or cold storage. J. Sci. Food Agric. 86, 243–250. Mao, L., Zhang, S., 2001. Role of pectolytic enzymes and cellulase during ripening and woolly breakdown in peaches. Acta Hortic. Sin. 28, 107–111. Mollendorff, L.J.V., Villiers, O.T.D., 1988. Role of pectolytic enzymes in the development of woolliness in peaches. J. Hortic. Sci. 63, 53–58. Mollendorff, V.L.J., Jacobs, G., Villiers, O.T.D., 1992. Effect of temperature manipulation during storage and ripening on firmness, extractable juice and woolliness in nectarines. J. Hortic. Sci. 67, 655–662. Mollendorff, V.L.J., Villiers, O.T.D., Jacobs, G., Westraad, I., 1993. Molecular characteristics of pectic constituents in relation to firmness, extractable juice, and woolliness in nectarines. J. Am. Soc. Hortic. Sci. 118, 77–80. Murayama, H., Arikawa, M., Sasaki, Y., Dal Cin, V., Mitsuhashi, W., Toyomasu, T., 2009. Effect of ethylene treatment on expression of polyuronide-modifying genes and solubilization of polyuronides during ripening in two peach cultivars having different softening characteristics. Postharvest Biol. Technol. 52, 196– 201. Needs, P.W., Rigby, N.M., Ring, S.G., MacDougall, A.J., 2001. Specific degradation of pectins via a carbodiimide-mediated lossen rearrangement of methyl esterified galacturonic acid residues. Carbohydr. Res. 333, 47–58. Nunez, E.E., Boas, B.M.V., Abreu, C.M.P.D., 2005. Storage of ‘Premier’ peaches following postharvest treatment with calcium chloride. Rev. Bras. Armazenamento 30, 25–30. Obenland, D.M., Carroll, T.R., 2000. Mealiness and pectolytic activity in peaches and nectarines in response to heat treatment and cold storage. J. Am. Soc. Hortic. Sci. 125, 723–728. Oliveira, F.E.D.R., Abreu, C.M.P.D., Asmar, S.A., Correa, A.D., Santos, C.D.D., 2005. Firmness of peach ‘Diamante’ treated with 1-MCP. Rev. Bras. Frutic. 27, 366–368. Ortiz, A., Seymour, G.B., Tucker, G.A., Lara, I., 2010. Cell wall disassembly during the melting phase of softening in ‘Snow Queen’ nectarines. Postharvest Biol. Technol. 58, 88–92. Ortiz, A., Vendrell, M., Lara, I., 2011. Softening and cell wall metabolism in late-season peach in response to controlled atmosphere and 1-MCP treatment. J. Hortic. Sci. Biotechnol. 86, 175–181. Pressey, R., Avants, J.K., 1978. Difference in polygalacturonase composition of clingstone and freestone peaches. J. Food Sci. 43, 1415–1417.
5
Redgwell, R.J., MacRae, E., Hallett, I., Fischer, M., Perry, J., Harker, R., 1997. In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203, 162–173. Rodriguez, M.E., Lizana, L.A., 2006. Cytochemical analysis of woolly and normal nectarine mesocarp. Acta Hortic. 713, 505–510. Sasaki, F.F., Cerqueira, T.S., Sestari, I., Kluge, J.S.D.A.R.A., 2010. Woolliness control and pectin solubilization of ‘Douradao’ peach after heat shock treatment. Acta Hortic. 877, 539–542. Schwab, W., Davidovich-Rikanati, R., Lewinsohn, E., 2008. Biosynthesis of plantderived flavor compounds. Plant J. 54, 712–732. Selli, R., Sansavini, S., 1995. Sugar, acid and pectin content in relation to ripening and quality of peach and nectarine fruits. Acta Hortic. 379, 345–358. Sonego, L., Ben-Arie, R., Raynal, J., Pech, J.C., 1995. Biochemical and physical evaluation of textural characteristics of nectarines exhibiting woolly breakdown – NMR imaging, X-ray computed tomography and pectin composition. Postharvest Biol. Technol. 5, 187–198. Sonego, L., Lers, A., Khalchitski, A., Zutkhi, Y., Zhou, H., Lurie, S., Ben-Arie, R., 1999. Ethylene delays onset of woolly breakdown in cold-stored peaches. Biology and biotechnology of the plant hormone ethylene II. In: Proceedings of the EU-TMREuroconference Symposium, Thira (Santorini), Greece, 5–8 September, 1998, pp. 405–410. Taylor, M.A., Rabe, E., Jacobs, G., Dodd, M.C., 1995. Effect of harvest maturity on pectic substances, internal conductivity, soluble solids and gel breakdown in cold stored ‘Songold’ plums. Postharvest Biol. Technol. 5, 285–294. Vincken, J.P., 2003. If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol. 132, 1781–1789. Wang, J., Rao, J., Ren, X., 2005. Effect of 1-methylcyclopropene on softening of nectarine [Prunus persica var. nectarina Maxim] cv. Qinguang. Plant Physiol. Commun. 41, 153–156. White, P.J., Broadley, M.R., 2003. Calcium in plants. Ann. Bot. 92, 487–511. Yang, H.-S., Feng, G.-P., An, H.-J., Li, Y.-F., 2006a. Microstructure changes of sodium carbonate-soluble pectin of peach by AFM during controlled atmosphere storage. Food Chem. 94, 179–192. Yang, H., An, H., Feng, G., Li, Y., Lai, S., 2005. Atomic force microscopy of the watersoluble pectin of peaches during storage. Eur. Food Res. Technol. 220, 587–591. Yang, H., Chen, F., An, H., Lai, S., 2009. Comparative studies on nanostructures of three kinds of pectins in two peach cultivars using atomic force microscopy. Postharvest Biol. Technol. 51, 391–398. Yang, H., Lai, S., An, H., Li, Y., 2006b. Atomic force microscopy study of the ultrastructural changes of chelate-soluble pectin in peaches under controlled atmosphere storage. Postharvest Biol. Technol. 39, 75–83. Zhang, B., Xi, W.-P., Wei, W.-W., Shen, J.-Y., Ferguson, I., Chen, K.-S., 2011. Changes in aroma-related volatiles and gene expression during low temperature storage and subsequent shelf-life of peach fruit. Postharvest Biol. Technol. 60, 7–16. Zhang, L., Chen, F., An, H., Yang, H., Sun, X., Guo, X., Li, L., 2008. Physicochemical properties, firmness, and nanostructures of sodium carbonate-soluble pectin of 2 Chinese cherry cultivars at 2 ripening stages. J. Food Sci. 73, N17–N22. Zhang, L., Chen, F., Yang, H., Sun, X., Liu, H., Gong, X., Jiang, C., Ding, C., 2010. Changes in firmness, pectin content and nanostructure of two crisp peach cultivars after storage. LWT – Food Sci. Technol. 43, 26–32. Zhang, L., Chen, F., Yang, H., Ye, X., Sun, X., Liu, D., Yang, B., An, H., Deng, Y., 2012. Effects of temperature and cultivar on nanostructural changes of water-soluble pectin and chelate-soluble pectin in peaches. Carbohydr. Polym. 87, 816–821. Zhou, H.-W., Ben-Arie, R., Lurie, S., 2000a. Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochemistry 55, 191–195. Zhou, H.-W., Lurie, S., Lers, A., Khalchitski, A., Sonego, L., Ben-Arie, R., 2000b. Delayed storage and controlled atmosphere storage of nectarines: two strategies to prevent woolliness. Postharvest Biol. Technol. 18, 133–141. Zhou, H.-W., Sonego, L., Ben-Arie, R., Lurie, S., 1999. Analysis of cell wall components in juice of ‘Flavortop’ nectarines during normal ripening and woolliness development. J. Am. Soc. Hortic. Sci. 124, 424–429. Zhou, H.-W., Sonego, L., Khalchitski, A., Ben-Arie, R., Lers, A., Lurie, S., 2000c. Cell wall enzymes and cell wall changes in ‘Flavortop’ nectarines – mRNA abundance, enzyme activity, and changes in pectic and neutral polymers during ripening and in wooly fruit. J. Am. Soc. Hortic. Sci. 125, 630–637. Zhou, H.W., Ben-Arie, R., Lurie, S., 2000d. Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochemistry 55, 191–195. Zhu, S., Liu, M., Zhou, J., 2006. Effects of fumigation with nitric oxide on cell wall metabolisms of postharvest Feicheng peaches. Sci. Agric. Sin. 39, 1878–1884.
Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Review
Pectin role in woolliness development in peaches and nectarines: A review Goran Fruk a,∗ , Zlatko Cmelik a , Tomislav Jemric a , Janez Hribar b , Rajko Vidrih b a b
University of Zagreb Faculty of Agriculture, Department of Pomology, Svetosimunska cesta 25, HR – 10 000 Zagreb, Croatia University of Ljubljana Biotechnical Faculty, Department of Food Science and Technology, Jamnikarjeva 101, SI – 1000 Ljubljana, Slovenia
a r t i c l e
i n f o
Article history: Received 25 July 2014 Received in revised form 20 September 2014 Accepted 24 September 2014 Keywords: Peach and nectarine Ethylene Chilling injury Pectin Cell anatomy Temperature
a b s t r a c t One of the main problems during peach and nectarine cold storage is the associated chilling injuries, which can include woolliness, mealiness, leatheriness, flesh browning, internal reddening, and flesh or pit cavities. Woolliness is one form of chilling injury. It manifests as a lack of juiciness and a dry ‘woolly’ texture of the fruit flesh. Its occurrence is correlated with pectin metabolism and is controlled directly or indirectly by the pectolytic enzymes (i.e., polygalacturonase, pectin esterase, cellulase, lipoxygenase). Chilling injury to these fruit also results in changes in the fruit physiology and cell anatomy. A reduction in woolliness is possible with post-harvest treatments, such as with heat (which must be carried out carefully), calcium, ethylene (blocking or producing), nitrogen monoxide, or a controlled atmosphere. This paper focuses only on woolliness and factors affecting its occurrence. In this paper the role of pectin metabolism, temperature and postharvest treatments on occurrence of woolliness is discussed. The role of some enzymes, such as pectin esterase, and postharvest treatment with 1-MCP still remain unclear and further research is needed to elucidate physiological mechanisms that lead to development of woolliness. © 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6. 7. 8. 9.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The development of woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The role of temperature in the development of woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cell anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pectin metabolism in peaches and nectarines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other metabolic processes and woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Harvest date and maturity stage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Post-harvest treatments to alleviate woolliness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction During cold storage of peaches (Prunus persica Batsch.) and nectarines (P. persica var. nectarina Ait.), one of the main problems is chilling injuries, which are a collective term for the physiological
∗ Corresponding author. Tel.: +385 1 239 3842; fax: +385 1 239 3630. E-mail address: [email protected] (G. Fruk). http://dx.doi.org/10.1016/j.scienta.2014.09.042 0304-4238/© 2014 Elsevier B.V. All rights reserved.
1 2 2 2 2 3 3 3 4 4 4
disorders that can occur during such fruit storage. Chilling injuries develop during ripening on 20 ◦ C (shelf life) after fruit is stored at 2.2–7.6 ◦ C for at least 2 weeks or at 0 ◦ C for 3 weeks or more (Lill et al., 1989; Lurie and Crisosto, 2005). Furthermore, chilling injuries are an internal disorder, and are therefore not generally noticed until the fruit reaches customers. With peaches and nectarines, chilling injuries can include woolliness, mealiness, leatheriness, flesh browning, internal reddening, and flesh or pit cavities (Lurie and Crisosto, 2005). Woolliness manifests as a lack of juiciness and a dry ‘woolly’ texture of the fruit flesh (Zhou et al., 2000a), and it
2
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
is caused by an imbalance in pectin metabolism during cold storage (Ben-Arie and Sonego, 1980). A previous review about such chilling injuries of peaches and nectarines was focused on a description of the symptoms of chilling injuries and the methods of their prevention or reduction (Lurie and Crisosto, 2005). Therefore, the aim of the present review is to provide an overview of studies on woolliness development, reduction and prevention in peaches and nectarines. 2. The development of woolliness Woolliness is a result of gel formation due to high-molecularweight pectin binding and a low degree of esterification in combination with calcium, extracellular water and the solutes that pass through the cell wall (Sonego et al., 1995). The juiciness decreases due to the strong water binding in calcium-pectate gels, and although the amount of water in woolly and healthy fruit is the same (Lill and Mespel, 1988; Zhou et al., 2000a), woolliness can also be measured as a lack of extractable juice (Zhou et al., 2000d). However, water-soluble pectins do not form a gel in vitro, while alkali-soluble pectins and calcium do form a gel in vitro (Levaj et al., 2003), which means that as well as the pectins, calcium is needed for juice gelling and the occurrence of woolliness. A prerequisite for woolliness development is deesterification of the pectins, while the degree of polymerisation and the level of calcium pectates are maintained (Lurie et al., 2003). During chilling, along with a mealy texture, injured fruit can appear dry, and the arabinan loss in the pectins is reduced, with changes to the pectin polymerisation. These changes in the cell wall result in weakening of intercellular adhesion and reduced cell rupture, which are reflected as reduced fruit juiciness (Brummell, 2007). In addition to the degradation of the arabinose and galactose of the pectin chain side branches during the ripening of peaches, the main pectin chains can also be degraded (Kan et al., 2013). In woolly peaches, the content of insoluble pectin is increased (e.g., protopectin, deesterified pectates), which favours the formation of pectin gels (Lurie et al., 2003). During ripening, pectin degradation can also cause only a temporary woolliness, which disappears following further hydrolysis of the cell wall (Mollendorff et al., 1992). 3. The role of temperature in the development of woolliness Peaches and nectarines stored at 0 ◦ C can develop symptoms of woolliness. Due to reduced polygalacturonase (PG) activity, these fruit have less water-soluble pectins and more sodium-carbonatesoluble pectins than the fruit ripened at 20 ◦ C immediately after harvest. Pectin esterase has a reduced activity at low temperatures, so it is more likely that this woolliness is caused by altered PG activity (Choi and Lee, 1997). The storage of peaches for a few days at 8 ◦ C and then at 0 ◦ C can maintain a lower content of water-soluble pectins, and a higher content of protopectins and extractable juice (Li et al., 2009). Similar results in plums reports Taylor et al. (1995). Soluble pectins remain low during storage at low temperature (0 ◦ C), but significantly increases when transferred to higher temperature (8 ◦ C), most likely because higher temperature stimulates ripening. Mao and Zhang (2001) argued that woolliness in peaches develops due to the abnormal degradation of the pectins in the cell wall, which is caused by reduced activities of the pectolytic enzymes and of cellulase (EC 3.2.1.4). Cellulase participates in normal peach ripening (Bonghi et al., 1998). Heat treatment before and during peach storage can alleviate the occurrence of chilling injuries and prevent the irreversible destruction of endopolygalacturonase (endoPG; EC 3.2.1.15) and cellulase that can occur due to low
temperatures. This allows the normal pectin degradation processes (Mao and Zhang, 2001). Also, although Zhou et al. (2000c) reported that there is reduced cellulase activity in woolly nectarines, they also argued that the role of cellulases is probably only in the initial stages of fruit softening during ripening, and therefore cellulases do not directly affect the woolliness of nectarines. With peaches that have been dipped in hot water, there is a greater reduction in the pectin content during storage than for peaches that are treated with hot moist air (Bakshi and Masoodi, 2010). However, heat treatments need be carefully adjusted, as Sasaki et al. (2010) observed increased woolliness in peaches treated at 50 ◦ C for 1 h or 2 h. This might be due to the optimum temperature being reached in the fruit for the activity of the enzyme pectin esterase (40–45 ◦ C). 4. Cell anatomy Peaches that have been ripened immediately after harvest at ambient temperatures have cells of regular shape, with maintained adhesion to other cells and typical intercellular spaces. In contrast, woolly peaches ripened after cold storage have cells with irregular shapes that are separated from each other (Lurie et al., 2003; Luza et al., 1992). However, Ghiani et al. (2011) showed cells with irregular shapes and that were separated in ripened meltingflesh and non-melting-flesh peaches that had not been cold stored. This phenomenon was attributed to the loss of the turgor of the cells, due to the degradation of the cell walls under the influence PG, which leads to fruit softening. Rodriguez and Lizana (2006) did not note the separation of cells and an increase in intercellular space in woolly nectarines, although they noted the accumulation of pectin substances in cell walls and in the intercellular spaces. The juice obtained by squeezing healthy (juicy) peaches contained almost no whole cells, while the juice from mealy peaches contained approximately 30% viable cells (Brummell et al., 2004b). 5. Pectin metabolism in peaches and nectarines Pectins are heterogeneous macromolecules of polysaccharides that can contain up to 17 different monosaccharides, and that are rich in galacturonic acids (Vincken, 2003; Yang et al., 2005, 2009). Pectins are located in the primary cell wall and in the central lamella (Brummell et al., 2004a), and they have very important roles as they are the most common macromolecules in the cell wall. Softening of fruit accompanies solubilisation and depolymerisation of the pectins, which result in the weakening and disintegration of the cell wall (Billy et al., 2008). Indeed, it is this pectin solubilisation and the associated cell-wall swelling that leads to fruit softening (Redgwell et al., 1997). The pectins can be solubilised prior to their depolymerisation, and it has been shown that the depolymerisation of pectins is not the first step in their degradation (Dawson et al., 1992). During the storage of peaches, the water-soluble and chelatesoluble pectins are reduced, with an increasing number of single linear polysaccharide chains seen (Zhang et al., 2012). The most important biochemical indicator of a change in texture is the galacturonic acid content in water-soluble pectin extracts (Billy et al., 2008). In addition to these structure changes to the pectins (Ketsa et al., 1999; Zhang et al., 2010), fruit softening is associated with cleavage of the arabinose and galactose side chains of uronide-acidcontaining polysaccharides (i.e., the polyuronides (Brummell et al., 2004a). These side chains are responsible for the size of the pores in the cell wall, and thus they can prevent pectolytic enzymes from disassembling the pectins, and protect the polysaccharides in the cell wall from excessive deesterification (Ortiz et al., 2010). Peach fruit softening is thus accompanied by the transition of the water-insoluble pectins into the water-soluble pectins that
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
give the characteristic texture of the ripened fruit (Jia et al., 2006). Indeed, the ratio of the water-soluble to water-insoluble fractions of the pectins can provide an indicator of nectarine ripening (Manganaris et al., 2005a). However, although fruit firmness is associated with water-soluble or sodium-carbonate-soluble pectins, the pectin structure is not solely responsible for fruit softening (Zhang et al., 2008, 2010). The activity of endoPG is strongly correlated with the characteristics of melting-flesh peaches. It has been reported that the lack of the melting phase in non-melting-flesh peaches is caused by deletion of the gene for endoPG or by truncation of its mRNA, and thus by a lack of synthesis of the endoPG protein. Therefore, it appears that endoPG is responsible for the increased softening in melting-flesh peaches, as compared to nonmelting-flesh peaches (Manganaris et al., 2006b). The main changes in the cell wall during peach ripening are hemicellulose depolymerisation, reduction in pectin arabinan content, and pectin depolymerisation (Brummell, 2007). Clingstone peaches have an exo-polygalacturonase (exoPG; EC 3.2.1.82) and water insoluble pectins, while freestone peaches have both an endoPG and an exoPG and a high water-soluble pectin content (Pressey and Avants, 1978). During storage, the water-soluble pectins lose their side chains, which are mainly composed of arabinose and/or galactose (Kan et al., 2013; Needs et al., 2001; Yang et al., 2005). Approximately 15–17 weeks after full bloom of peach and nectarine trees, the protopectins, which are insoluble in water, are hydrolysed to pectic acids, which are soluble in water (Selli and Sansavini, 1995). Lower storage temperatures can reduce this degradation of the pectins, probably due to inhibition of the enzymatic activity (Zhang et al., 2012; Zhou et al., 2000b). Choi and Lee (1997) reported that pectin esterase (PE; EC 3.1.1.11; also known as pectin methyl esterase) does not affect the occurrence of woolliness in peaches, but Zhou et al. (2000b) showed that at the relatively high PE and low PG activities in injured peaches, the pectic matrix can be deesterified without subsequent depolymerisation. This leads to the formation of high-molecularweight pectins that have a low degree of esterification. This type of pectin forms a gel, possibly in combination with calcium from the cell wall, which then binds the free water in the flesh, thereby causing woolliness. Zhou et al. (2000b) reports that imbalance of PG and PE activity is responsible for development of woolliness. Thus, Girardi et al. (2005) in their study concludes that wooliness development in peach (cv. ‘Chiripa’) could be alleviated in two ways: (1) by increasing PG (endo- and exo-) activity, or (2) decreasing PE activity. Flesh browning is accompanied by an increased content of neutral sugars, reduced content of pectins and cellulose, reduced content of pectic enzymes (PG and PE), and the binding of cations (e.g., calcium) within the cell wall (Manganaris et al., 2006a). The juice viscosity and the molecular weight of the watersoluble pectins are reduced during peach ripening (Davidyuk, 1972). The differences in juice viscosity in healthy and woolly peaches are caused by the type of polymers in the juice, rather than by their quantity. Thus, high-molecular-weight pectins in the juice of woolly peaches results in higher juice viscosity than seen for the juice of healthy peaches that contains low-molecular-weight pectins (Zhou et al., 1999).
6. Other metabolic processes and woolliness Some studies have reported that as well as the roles in woolliness development in peaches of the already mentioned enzymes (PG, PE, cellulase), lipoxygenase (EC 1.13.11.12) might also participate (Li et al., 2012; Zhang et al., 2011). The linoleic and linolenic fatty acids are an integral part of the cell wall and are the precursors for volatile aroma compounds (e.g., hexanal and hexenal).
3
Lipoxygenase is involved in their conversion to these volatile aroma compounds (Schwab et al., 2008). Indeed, Zhang et al. (2011) reported that with chilling injuries to peaches, the fatty acids in the cell wall showed changed profiles, which the lipoxygenase activity affected, and which led to a reduced content of volatile aroma compounds. Li et al. (2012) suggested that ethylene treatment and low-temperature acclimatisation can increase the PG and lipoxygenase activities, which leads to reduced woolliness of peaches. The role of lipoxygenase in the development of chilling injuries in peaches and nectarines has not, however, been studied in detail. 7. Harvest date and maturity stage During storage, early harvested peaches show more leatheriness than mealiness, while those that are late harvested show more mealiness than leatheriness, as compared to the peaches harvested at commercial maturity (Ju et al., 2000). Girardi et al. (2005) also found that early harvest of peaches can promote chilling injury development during cold storage. Leathery (dry) peaches synthesise less ethylene, have lower PG activity and higher firmness, and contain more insoluble pectins than mealy peaches, although such differences have not been seen between mealy and juicy peaches (Ju et al., 2001). 8. Post-harvest treatments to alleviate woolliness Choi and Lee (1997) observed that woolliness reduction is based on an increase in water-soluble pectin content and a reduction in sodium-carbonate-soluble pectins, under the influence of increased PG activity. Peaches that were stored at low temperatures with intermittent warming had similar PG activities to those that were not stored at low temperatures, while the PE activities were lower than in cold-stored peaches (Ben-Arie and Sonego, 1980). However, peaches that were stored at low temperatures immediately after harvest had lower PG activities than peaches that underwent delayed storage (Mollendorff and Villiers, 1988). Obenland and Carroll (2000) reports that intermittent warming cannot alleviate chilling injuries to satisfactory level if pre-storage heat treatment (high temperature forced air) was used. They also reports that long heat treatment (3 or 4 h) can inhibit or drastically decrease PG activity and by this alteration promote chilling injury development. If intermittent warming is used alone it could be useful in alleviating chilling injuries in peaches (Ben-Arie and Sonego, 1980; Girardi et al., 2005). Periodical warming of peaches during their storage at low temperatures can maintain the PG activity, which promotes solubilisation of the water-soluble pectins and normal peach ripening (Ben-Arie and Sonego, 1980). During woolliness development, liquids and solutes pass through the cell membranes (as a result of long-term storage at low temperatures) and bind to the high-molecular-weight pectins, thus forming pectic gels in the intercellular spaces, and resulting in the typical dry texture observed for woolly nectarines (Mollendorff et al., 1993). Bassi et al. (1998) reported that non-melting-flesh peaches have 35% more calcium bound to the insoluble pectins than for meltingflesh peaches. Therefore, the logical question that has been raised is what would happen if peaches were immersed in a solution of calcium after harvest, as can be done with apples. The dipping of the fruit into a solution of calcium chloride increases the concentration of calcium in the insoluble fraction of the pectins, which maintains the firmness and physico-chemical properties of the fruit (Manganaris et al., 2005b). Exogenous calcium can stabilise and protect the cell wall from the cell-wall-degrading enzymes (i.e., PG, PE) (Nunez et al., 2005; White and Broadley, 2003). In peaches treated with calcium, their content of covalent and ionic bonded pectins decreased during their shelf life. Reduced PG activity was
4
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5
also noted, while PE activity increased (Cao et al., 2008). However, calcium propionate and calcium lactate are not recommended as calcium treatments for nectarines, because their too high concentrations can damage the fruit skin (Manganaris et al., 2005b). Nitrogen monoxide treatment can alleviate symptoms of chilling injuries, and especially woolliness. Nitric monoxide changes the relationship between PE and PG, which stops the increase in the content of soluble pectins and the reduction in the ionic pectins. The consequence here is reduced woolliness (Zhu et al., 2006). Post-harvest peach treatments with 1-methylcyclopropene (1MCP; an inhibitor of ethylene action) can significantly reduce the loss of the pectins (Oliveira et al., 2005; Wang et al., 2005). This appears to be due to the low PG activity for pectin degradation. Ethylene is known to act as a trigger for the indirect synthesis of PG in tomato (Grierson and Tucker, 1983); therefore, ethylene should have an important role in the solubility of the polyuronides and in the development of mealiness in peaches (Murayama et al., 2009). Post-harvest application of 1-MCP to peaches also reduces the activity of PE (Oliveira et al., 2005). Although this 1-MCP treatment of peaches can significantly affect fruit ripening, it does not completely prevent ripening, and therefore Liu et al. (2005) considered that the ethylene receptors in the fruit are constantly being synthesised during storage. Ortiz et al. (2011) reported different results, as they found that application of 1-MCP resulted in increased PE activity and inhibited the other pectolytic enzymes. A controlled atmosphere during storage of peaches can be used to inhibit degradation of the water-soluble pectins, the sodiumcarbonate-soluble pectins, and the chelate-soluble pectins (Yang et al., 2006a,b, 2005). High CO2 and low O2 contents in the storage atmosphere can inhibit PG transcription during such controlled atmosphere conditions (Zhou et al., 2000b). In contrast, Ortiz et al. (2011) reported that a controlled atmosphere can only partially inhibit the pectolytic enzymes in peaches, and increases the content of the pectin polysaccharides. This leads to an increase in the content of chelate-soluble pectins within the cell walls. The combined application of 1-MCP and a controlled atmosphere was seen not to be sufficient to maintain peach firmness, probably due to increased degradation of the pectins (Ortiz et al., 2011). These results are probably related to the peach ripening stage at harvest. Ethylene treatment can also delay and reduce woolliness in peaches stored at a temperature of 0 ◦ C. This ethylene treatment also stimulates PG activity during storage, while ethylene has no influence on the PE activity of these peaches (Sonego et al., 1999).
9. Conclusions Although the metabolism of pectins participates in a number of physiological disorders during peach and nectarine storage (e.g., mealiness, leatheriness, woolliness), its biggest role is in the woolliness of these fruit, as the pectins in intercellular spaces bind the free juice into pectate gels. Disorders of pectin metabolism are caused by changes in the pectolytic enzyme activities (i.e., mainly endoPG and exoPG, PE, cellulose, lipoxygenase). Such disorders lead to an imbalance in the degradation of the pectins, which has the effect of binding the juice into pectate gels. Post-harvest heat treatments can reduce the woolliness, but they must be precise because they can also increase woolliness, and so they need to achieve the optimum temperature for the fruit pectolytic enzyme activity. Post-harvest application of 1-MCP and ethylene has different effects on PE activity. This leads to the conclusion that 1-MCP and ethylene have no direct impacts on PE, and that instead the changes in PE activity are triggered by some other processes in the fruit. In peaches, 1-MCP cannot be used for the classical intention of maintaining the fruit firmness or stopping ripening, although it can slow down these
processes and alleviate chilling injuries. The application of nitric oxide or calcium to reduce the woolliness of cold-stored fruit can be a successful treatment. Detailed studies of cellulase and lipoxygenase in pectin metabolism should be carried out to determine their roles in chilling injuries. Acknowledgements This review was written as part of the scientific specialisation of Goran Fruk, with the support of a bilateral scholarship provided by the Centre of the Republic of Slovenia for Mobility, and the European Educational and Training Programmes (CMEPIUS). This article was also supported by the Ministry of Science, Technology and Sports of Republic of Croatia (Projects 1780000000-3583). References Bakshi, P., Masoodi, F.A., 2010. Effect of pre-storage heat treatment on enzymological changes in peach. J. Food Sci. Technol. 47, 461–464. Bassi, D., Mignani, I., Rizzo, M., 1998. Calcium and pectin influence peach flesh texture. Acta Hortic. 465, 433–438. Ben-Arie, R., Sonego, L., 1980. Pectolytic enzyme activity involved in woolly breakdown of peach. Phytochemistry 19, 2553–2555. Billy, L., Mehinagic, E., Royer, G., Renard, C.M.G.C., Arvisenet, G., Prost, C., Jourjon, F., 2008. Relationship between texture and pectin composition of two apple cultivars during storage. Postharvest Biol. Technol. 47, 315–324. Bonghi, C., Ferrarese, L., Ruperti, B., Tonutti, P., Ramina, A., 1998. Endo--1,4glucanases are involved in peach fruit growth and ripening, and regulated by ethylene. Physiol. Plant. 102, 346–352. Brummell, D.A., 2007. How dynamic primary cell wall properties affect fruit tissue firmness; intercellular adhesion and the characteristics of processed fruit products. Mitteilungen der Bundesforschungsanstalt fur Forst- und Holzwirtschaft 223, 53–60. Brummell, D.A., Dal Cin, V., Crisosto, C.H., Labavitch, J.M., 2004a. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J. Exp. Bot. 55, 2029–2039. Brummell, D.A., Dal Cin, V., Lurie, S., Crisosto, C.H., Labavitch, J.M., 2004b. Cell wall metabolism during the development of chilling injury in cold-stored peach fruit: association of mealiness with arrested disassembly of cell wall pectins. J. Exp. Bot. 55, 2041–2052. Cao, Y., Cao, Y., Li, Z., Ren, J., Leng, P., 2008. Effect of pre-harvest calcium sprays on fruit quality and softening during storage of melting flesh peach. J. China Agric. Univ. 13, 31–36. Choi, J.H., Lee, S.K., 1997. Effect of MA storage on woolliness of ‘Yumyeong’ peaches. Postharvest Horticulture Series – Department of Pomology, University of California 17., pp. 132–138. Davidyuk, L.P., 1972. Studies on the quality of soluble pectin in relation to peach fruit ripening. Byulleten’ Gosudarstvennogo Nikitskogo Botanicheskogo Sada 3, 53–56. Dawson, D.M., Melton, L.D., Watkins, C.B., 1992. Cell wall changes in nectarines (Prunus persica): solubilization and depolymerization of pectic and neutral polymers during ripening and in mealy fruit. Plant Physiol. 100, 1203–1210. Ghiani, A., Onelli, E., Aina, R., Cocucci, M., Citterio, S., 2011. A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endo-polygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. J. Exp. Bot. 62, 4043–4054. Girardi, C.L., Corrent, A.R., Lucchetta, L., Zanuzo, M.R., Costa, T.S.D., Brackmann, A., Twyman, R.M., Nora, F.R., Nora, L., Silva, J.A., Rombaldi, C.V., 2005. Effect of ethylene, intermittent warming and controlled atmosphere on postharvest quality and the occurrence of woolliness in peach (Prunus persica cv. Chiripá) during cold storage. Postharvest Biol. Technol. 38, 25–33. Grierson, D., Tucker, G.A., 1983. Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato fruit ripening. Planta 157, 174–179. Jia, H.J., Mizuguchi, K., Hirano, K., Okamoto, G., 2006. Effect of fertilizer application level on pectin composition of Hakuho peach (Prunus persica Batsch) during maturation. HortScience 41, 1571–1575. Ju, Z.G., Duan, J.S., Ju, Z.Q., 2000. Leatheriness and mealiness of peaches in relation to fruit maturity and storage temperature. J. Hortic. Sci. Biotechnol. 75, 86–91. Ju, Z.G., Duan, Y.S., Ju, Z.Q., Guo, A.X., 2001. Different responses of ‘Snow Giant’ and ‘Elegant Lady’ peaches to fruit maturity and storage temperature. J. Hortic. Sci. Biotechnol. 76, 575–580. Kan, J., Liu, J., Jin, C.H., 2013. Changes in cell walls during fruit ripening in Chinese ‘Honey’ peach. J. Hortic. Sci. Biotechnol. 88, 37–46. Ketsa, S., Chidtragool, S., Klein, J.D., Lurie, S., 1999. Firmness, pectin components and cell wall hydrolases of mango fruit following low-temperature stress. J. Hortic. Sci. Biotechnol. 74, 685–689. Levaj, B., Dragovic-Uzelac, V., Dancevic, A., Frlan, J., 2003. The effect of ripening and storage on peach pectin and gel strength of related jams. Acta Aliment. Hung. 32, 329–340.
G. Fruk et al. / Scientia Horticulturae 180 (2014) 1–5 Li, Y.X., Guan, J., Feng, Y., Ji, H., Sun, Y., 2009. Effects of cold-storage mode on post-harvest pectin contents and beta-galactosidase activity of peach. Acta Bot. Boreali-Occidential Sin. 29, 1637–1642. Li, Y.X., Wang, G.X., Liang, L.S., 2012. Effect of cold acclimation treatment and exogenous ethylene treatment on woolliness related enzymes on ‘Okubo’ peach fruits during low temperature storage. Acta Hortic. 934, 1103–1109. Lill, R.E., Mespel, G.J.V.D., 1988. A method for measuring the juice content of mealy nectarines. Sci. Hortic. 36, 267–271. Lill, R.E., O’Donoghue, E.M., King, G.A., 1989. Postharvest Physiology of Peaches and Nectarines. Horticultural Reviews. John Wiley & Sons, Inc., pp. 413–452. Liu, H., Jiang, W., Zhou, L., Wang, B., Luo, Y., 2005. The effects of 1methylcyclopropene on peach fruit (Prunus persica L. cv. Jiubao) ripening and disease resistance. Int. J. Food Sci. Technol. 40, 1–7. Lurie, S., Crisosto, C.H., 2005. Chilling injury in peach and nectarine. Postharvest Biol. Technol. 37, 195–208. Lurie, S., Zhou, H.W., Lers, A., Sonego, L., Alexandrov, S., Shomer, I., 2003. Study of pectin esterase and changes in pectin methylation during normal and abnormal peach ripening. Physiol. Plant. 119, 287–294. Luza, J.G., Gorsel, R.V., Polito, V.S., Kader, A.A., 1992. Chilling injury in peaches – a cytochemical and ultrastructural cell-wall study. J. Am. Soc. Hortic. Sci. 117, 114–118. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2005a. Cell wall cation composition and distribution in chilling-injured nectarine fruit. Postharvest Biol. Technol. 37, 72–80. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2005b. Effect of postharvest calcium treatments on the physicochemical properties of cell wall pectin in nectarine fruit during ripening after harvest or cold storage. J. Hortic. Sci. Biotechnol. 80, 611–617. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2006a. Cell wall physicochemical aspects of peach fruit related to internal breakdown symptoms. Postharvest Biol. Technol. 39, 69–74. Manganaris, G.A., Vasilakakis, M., Diamantidis, G., Mignani, I., 2006b. Diverse metabolism of cell wall components of melting and non-melting peach genotypes during ripening after harvest or cold storage. J. Sci. Food Agric. 86, 243–250. Mao, L., Zhang, S., 2001. Role of pectolytic enzymes and cellulase during ripening and woolly breakdown in peaches. Acta Hortic. Sin. 28, 107–111. Mollendorff, L.J.V., Villiers, O.T.D., 1988. Role of pectolytic enzymes in the development of woolliness in peaches. J. Hortic. Sci. 63, 53–58. Mollendorff, V.L.J., Jacobs, G., Villiers, O.T.D., 1992. Effect of temperature manipulation during storage and ripening on firmness, extractable juice and woolliness in nectarines. J. Hortic. Sci. 67, 655–662. Mollendorff, V.L.J., Villiers, O.T.D., Jacobs, G., Westraad, I., 1993. Molecular characteristics of pectic constituents in relation to firmness, extractable juice, and woolliness in nectarines. J. Am. Soc. Hortic. Sci. 118, 77–80. Murayama, H., Arikawa, M., Sasaki, Y., Dal Cin, V., Mitsuhashi, W., Toyomasu, T., 2009. Effect of ethylene treatment on expression of polyuronide-modifying genes and solubilization of polyuronides during ripening in two peach cultivars having different softening characteristics. Postharvest Biol. Technol. 52, 196– 201. Needs, P.W., Rigby, N.M., Ring, S.G., MacDougall, A.J., 2001. Specific degradation of pectins via a carbodiimide-mediated lossen rearrangement of methyl esterified galacturonic acid residues. Carbohydr. Res. 333, 47–58. Nunez, E.E., Boas, B.M.V., Abreu, C.M.P.D., 2005. Storage of ‘Premier’ peaches following postharvest treatment with calcium chloride. Rev. Bras. Armazenamento 30, 25–30. Obenland, D.M., Carroll, T.R., 2000. Mealiness and pectolytic activity in peaches and nectarines in response to heat treatment and cold storage. J. Am. Soc. Hortic. Sci. 125, 723–728. Oliveira, F.E.D.R., Abreu, C.M.P.D., Asmar, S.A., Correa, A.D., Santos, C.D.D., 2005. Firmness of peach ‘Diamante’ treated with 1-MCP. Rev. Bras. Frutic. 27, 366–368. Ortiz, A., Seymour, G.B., Tucker, G.A., Lara, I., 2010. Cell wall disassembly during the melting phase of softening in ‘Snow Queen’ nectarines. Postharvest Biol. Technol. 58, 88–92. Ortiz, A., Vendrell, M., Lara, I., 2011. Softening and cell wall metabolism in late-season peach in response to controlled atmosphere and 1-MCP treatment. J. Hortic. Sci. Biotechnol. 86, 175–181. Pressey, R., Avants, J.K., 1978. Difference in polygalacturonase composition of clingstone and freestone peaches. J. Food Sci. 43, 1415–1417.
5
Redgwell, R.J., MacRae, E., Hallett, I., Fischer, M., Perry, J., Harker, R., 1997. In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203, 162–173. Rodriguez, M.E., Lizana, L.A., 2006. Cytochemical analysis of woolly and normal nectarine mesocarp. Acta Hortic. 713, 505–510. Sasaki, F.F., Cerqueira, T.S., Sestari, I., Kluge, J.S.D.A.R.A., 2010. Woolliness control and pectin solubilization of ‘Douradao’ peach after heat shock treatment. Acta Hortic. 877, 539–542. Schwab, W., Davidovich-Rikanati, R., Lewinsohn, E., 2008. Biosynthesis of plantderived flavor compounds. Plant J. 54, 712–732. Selli, R., Sansavini, S., 1995. Sugar, acid and pectin content in relation to ripening and quality of peach and nectarine fruits. Acta Hortic. 379, 345–358. Sonego, L., Ben-Arie, R., Raynal, J., Pech, J.C., 1995. Biochemical and physical evaluation of textural characteristics of nectarines exhibiting woolly breakdown – NMR imaging, X-ray computed tomography and pectin composition. Postharvest Biol. Technol. 5, 187–198. Sonego, L., Lers, A., Khalchitski, A., Zutkhi, Y., Zhou, H., Lurie, S., Ben-Arie, R., 1999. Ethylene delays onset of woolly breakdown in cold-stored peaches. Biology and biotechnology of the plant hormone ethylene II. In: Proceedings of the EU-TMREuroconference Symposium, Thira (Santorini), Greece, 5–8 September, 1998, pp. 405–410. Taylor, M.A., Rabe, E., Jacobs, G., Dodd, M.C., 1995. Effect of harvest maturity on pectic substances, internal conductivity, soluble solids and gel breakdown in cold stored ‘Songold’ plums. Postharvest Biol. Technol. 5, 285–294. Vincken, J.P., 2003. If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol. 132, 1781–1789. Wang, J., Rao, J., Ren, X., 2005. Effect of 1-methylcyclopropene on softening of nectarine [Prunus persica var. nectarina Maxim] cv. Qinguang. Plant Physiol. Commun. 41, 153–156. White, P.J., Broadley, M.R., 2003. Calcium in plants. Ann. Bot. 92, 487–511. Yang, H.-S., Feng, G.-P., An, H.-J., Li, Y.-F., 2006a. Microstructure changes of sodium carbonate-soluble pectin of peach by AFM during controlled atmosphere storage. Food Chem. 94, 179–192. Yang, H., An, H., Feng, G., Li, Y., Lai, S., 2005. Atomic force microscopy of the watersoluble pectin of peaches during storage. Eur. Food Res. Technol. 220, 587–591. Yang, H., Chen, F., An, H., Lai, S., 2009. Comparative studies on nanostructures of three kinds of pectins in two peach cultivars using atomic force microscopy. Postharvest Biol. Technol. 51, 391–398. Yang, H., Lai, S., An, H., Li, Y., 2006b. Atomic force microscopy study of the ultrastructural changes of chelate-soluble pectin in peaches under controlled atmosphere storage. Postharvest Biol. Technol. 39, 75–83. Zhang, B., Xi, W.-P., Wei, W.-W., Shen, J.-Y., Ferguson, I., Chen, K.-S., 2011. Changes in aroma-related volatiles and gene expression during low temperature storage and subsequent shelf-life of peach fruit. Postharvest Biol. Technol. 60, 7–16. Zhang, L., Chen, F., An, H., Yang, H., Sun, X., Guo, X., Li, L., 2008. Physicochemical properties, firmness, and nanostructures of sodium carbonate-soluble pectin of 2 Chinese cherry cultivars at 2 ripening stages. J. Food Sci. 73, N17–N22. Zhang, L., Chen, F., Yang, H., Sun, X., Liu, H., Gong, X., Jiang, C., Ding, C., 2010. Changes in firmness, pectin content and nanostructure of two crisp peach cultivars after storage. LWT – Food Sci. Technol. 43, 26–32. Zhang, L., Chen, F., Yang, H., Ye, X., Sun, X., Liu, D., Yang, B., An, H., Deng, Y., 2012. Effects of temperature and cultivar on nanostructural changes of water-soluble pectin and chelate-soluble pectin in peaches. Carbohydr. Polym. 87, 816–821. Zhou, H.-W., Ben-Arie, R., Lurie, S., 2000a. Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochemistry 55, 191–195. Zhou, H.-W., Lurie, S., Lers, A., Khalchitski, A., Sonego, L., Ben-Arie, R., 2000b. Delayed storage and controlled atmosphere storage of nectarines: two strategies to prevent woolliness. Postharvest Biol. Technol. 18, 133–141. Zhou, H.-W., Sonego, L., Ben-Arie, R., Lurie, S., 1999. Analysis of cell wall components in juice of ‘Flavortop’ nectarines during normal ripening and woolliness development. J. Am. Soc. Hortic. Sci. 124, 424–429. Zhou, H.-W., Sonego, L., Khalchitski, A., Ben-Arie, R., Lers, A., Lurie, S., 2000c. Cell wall enzymes and cell wall changes in ‘Flavortop’ nectarines – mRNA abundance, enzyme activity, and changes in pectic and neutral polymers during ripening and in wooly fruit. J. Am. Soc. Hortic. Sci. 125, 630–637. Zhou, H.W., Ben-Arie, R., Lurie, S., 2000d. Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochemistry 55, 191–195. Zhu, S., Liu, M., Zhou, J., 2006. Effects of fumigation with nitric oxide on cell wall metabolisms of postharvest Feicheng peaches. Sci. Agric. Sin. 39, 1878–1884.