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Retardation of ‘Hayward’ kiwifruit tissue zone softening during storage by 1-methylcyclopropene
Scientia Horticulturae 259 (2020) 108791
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Retardation of ‘Hayward’ kiwifruit tissue zone softening during storage by 1methylcyclopropene
T
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H.J. Gonga,b,c, , C. Fullertonb, D. Billingb, J. Burdonb a
Agricultural College, Guangxi University, Nanning 530005, China The New Zealand Institute for Plant and Food Research Limited, Private Bag 92169, Auckland Mail Centre, 1142, Auckland, New Zealand c Guangxi Institute of Botany, Chinese Academy of Sciences, Guilin 541006, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Actinidia Storage 1-MCP Firmness Pericarp Core Efficacy
The use of the ethylene action inhibitor 1-methylcyclopropene (1-MCP) is becoming more common in the global kiwifruit industry as a tool for firmness management after harvest. The overall fruit firmness measured by penetrometer or compression is dependent on the relative changes in texture of the three main tissue zones: the outer pericarp, inner pericarp and core. This research has investigated the way in which 1-MCP affects the firmness of individual tissue zones during storage, and the changing response of 1-MCP treated fruit to ethylene. 1-MCP retarded fruit softening as measured by whole fruit compression or penetrometer. However, there was a long period in storage where the compression test did not show the same degree of softening as was detected by the penetrometer measurement. In addition, it was shown that 1-MCP retarded the softening of the three tissue zones investigated. The exposure of 1-MCP treated fruit to ethylene at intervals throughout storage demonstrated the long term nature of the anti-ethylene effect of a 1-MCP treatment at the start of storage; an effect that persisted in all three tissue zones. It is concluded that 1-MCP retards the overall softening of ‘Hayward’ kiwifruit, whether measured by compression or penetrometer. More specifically, the treatment affects the softening of the outer pericarp, inner pericarp and core tissues to a similar extent. The protective effect of a 1-MCP treatment at the start of storage against exogenous ethylene persists to some degree throughout storage.
1. Introduction The firmness of kiwifruit (Actinidia spp.) is a critical quality attribute used to determine the limits for handling procedures and the acceptability of fruit in the commercial supply chain (Burdon and Lallu, 2011). Kiwifruit are harvested in a mature, unripe state and during ripening they must change to a soft, melting texture when ripe and ready to eat (MacRae and Redgwell, 1992). Fruit may be cold stored for several months between harvest and consumption (Burdon and Lallu, 2011). Kiwifruit are often referred to as being climacteric fruit, i.e. ripening with an associated increase in ethylene production and respiratory activity (Kader, 2002; Wills et al., 2007). However, they are clearly not typically climacteric in that the majority of the ripening occurs before any increase in ethylene production (Wright and Heatherbell, 1967; Kim et al., 1999). This late increase in ethylene production has been suggested to be more associated with senescence than ripening (Richardson et al., 2011). However, kiwifruit are particularly responsive to even low concentrations of ethylene, which can accelerate
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the fruit softening (McDonald, 1990; Jeffery and Banks, 1996). Commercially, ethylene treatments can be used to accelerate and co-ordinate the ripening of kiwifruit (Lallu et al., 1989; Crisosto et al., 1997) and this is particularly useful for ripening fruit harvested early, at a low physiological maturity. The softening of ripening kiwifruit has been shown to be slowed to some degree by the application of 1-MCP (Regiroli and Vriends, 2007). 1-MCP functions by binding irreversibly to the ethylene binding site in the fruit, thereby blocking ethylene action and preventing a response. The commercial use of 1-MCP is becoming common in some sectors of the global kiwifruit industry. The greatest effect of 1-MCP on kiwifruit softening may occur in environments where there is an exogenous ethylene source, i.e. as protection from the stimulation of softening by exogenous ethylene rather than simply retarding the natural softening (Defilippi et al., 2011). The kiwifruit is made up of three major tissue zones, the outer and inner pericarp and core, also called a columella, with several layers of compressed dead cells making up the skin at the surface of the fruit (Hopping, 1976). The outer pericarp is made up from distinct
Corresponding author at: Guangxi Institute of Botany, Chinese Academy of Sciences, Guilin 541006, China. E-mail address: [email protected] (H.J. Gong).
https://doi.org/10.1016/j.scienta.2019.108791 Received 17 April 2019; Received in revised form 18 August 2019; Accepted 20 August 2019 0304-4238/ © 2019 Elsevier B.V. All rights reserved.
Scientia Horticulturae 259 (2020) 108791
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two lots of five packs, one for treatment with 1-MCP and the other to be left as an untreated control.
populations of small spherical cells and larger elongated cells. The inner pericarp has large thin walled placental cells which develop into a mucilaginous matrix around the seeds. The core is composed of large homogeneous parenchyma cells. The softening of the three major tissue zones has been reported as occurring synchronously at 20 °C for three kiwifruit genotypes (Jackson and Harker, 1997). More recently, it has become apparent that the degree of synchrony between tissue zones may differ among genotypes, and that differences in the softening rates of the major tissue zones of the kiwifruit can affect the overall firmness perception of the fruit (Li et al., 2016). The most commonly reported aspect of a lack of synchrony in the softening of the different tissue zones within the fruit is the occurrence of hard cores within otherwise ripe fruit. This has been associated with genotype (Burdon, 2018a, b), fruit maturity (MacRae et al., 1989; Stec et al., 1989; Burdon, 2018a), controlled atmosphere storage (Testoni, 1991; Zoffoli et al., 2016; Li et al., 2017) and the use of 1-MCP (Zoffoli et al., 2016). The relative softening rates of the different tissue zones within a kiwifruit, and their response to 1-MCP treatment, would seem to be integral to the acceptability of the fruit. It is therefore necessary to understand how the anti-ethylene action of 1-MCP functions within the different tissue zones of kiwifruit. Kiwifruit firmness is usually measured with a penetrometer after removal of the skin and flesh to a depth of about 1 mm (Watkins and Harman, 1981). While for many years hand-held penetrometers were used, it is now more common for a motorised texture analyser to be used. The penetrometer measurement is largely of the outer pericarp, although it also depends on the texture of the rest of the fruit since the whole fruit may deform when the penetrometer is pushed against it. It has been suggested that the destructive measurement of fruit firmness by penetrometer can be replaced by a non-destructive whole fruit compression test (Feng et al., 2009). However, differences in the relative softening of the inner and outer pericarp have been shown to affect the relationship between compression firmness values and the standard penetrometer measurement (McGlone et al., 1997; Li et al., 2017). In this paper, the impact of 1-MCP on the softening of ‘Hayward’ kiwifruit through storage is reported. Fruit firmness has been measured by penetrometer with the standard 7.9-mm probe and by whole fruit compression, and the individual outer pericarp, inner pericarp and core tissue zones measured by penetrometer with a 4-mm diameter probe. In addition, the longevity of the 1-MCP effect on the softening of these tissue zones has been investigated by challenging treated fruit with ethylene at intervals throughout storage.
2.2.1. 1-MCP Fruit in the MB packs were treated with 650 nL 1-MCP L−1 (ppb) for 24 h by exposure to the gas whilst the fruit were being cooled to 0 °C in a 12 m3 coolstore. The 1-MCP gas was released from SmartFresh™ research powder (0.14% a.i.; AgroFresh Inc.; www.agrofresh.com) by mixing with warm (˜40 °C) water. 2.2.2. Ethylene Samples of 10 fruit per orchard were first warmed overnight to 20 °C before being placed into 360 L chambers. Treatment with ethylene was by injection of known volumes of ethylene into the chambers to give final concentrations of 10 or 100 μL L−1. The treatments lasted for ˜ 16 h at 20 °C. 2.2.3. Storage Fruit were cooled to ˜ 2 °C within 24 h and then stored at 0.0 °C for up to 21 weeks. After 21 weeks of storage, fruit were transferred to 20 °C for 1 week. 2.3. Fruit assessments A 30 fruit sample of fruit from each orchard was measured for soluble solids content (SSC) and firmness on receipt. Throughout storage, 10 fruit samples from each orchard were measured for firmness by flat plate compression and standard 7.9-mm penetrometer, and tissue zones measured with a 4-mm penetrometer. Samples during storage were taken equally from 5 MB packs. Immediately after 1-MCP treatment, and at intervals through storage, the treated and non-treated fruit were exposed to ethylene and the firmness (whole fruit and tissue zones) were measured after 3 d at 20 °C. 2.4. Fruit assessment methodology 2.4.1. Compression firmness measurement The whole fruit was compressed a distance of 2 mm by flat plate applied at 5 mm s−1. The force recorded after 2 mm displacement was taken as the firmness value. 2.4.2. Standard penetrometer firmness measurement Fruit firmness was measured using a Fruit Texture Analyser (Güss, model GS14, South Africa) fitted with a 7.9-mm Effegi™ penetrometer probe after removal of skin and flesh to a depth of approximately 1 mm. The probe was driven into the flesh at 5 mm s−1 to a depth of 7.9 mm, and the maximum force recorded as the firmness value. Firmness was measured twice at the equator of each fruit, with the two measurements taken at 90° to each other.
2. Materials and methods 2.1. Fruit The kiwifruit cultivar used in this study was Actinidia chinensis var. deliciosa ‘Hayward’, the most commonly commercially grown greenfleshed kiwifruit cultivar. Fruit were harvested and packed commercially from three orchards around Te Puke, Bay of Plenty, New Zealand (37°49′S, 176°19′E). Fruit (count size 33 / 36) were supplied direct from the packhouse in commercial modular bulk packs (MB, 10 kg of fruit loose filled in a polythene bag inside the box), with 10 MB packs per orchard. The Bay of Plenty region in New Zealand is characterised as having good winter chilling, warm springs and mild summers and autumns (Snelgar et al., 2010). The soil is deep, free-draining and of volcanic origin. Rainfall is distributed throughout the year and averages 1600 mm per year.
2.4.3. Fruit core, outer pericarp and inner pericarp firmness measurement The fruit core firmness was measured after removal of approximately 15 mm of the fruit at the stem end. The measurement was made with a 4 mm diameter probe driven into the core at 5 mm s−1 to a depth of 6 mm, and the maximum force recorded as the firmness value. After the core measurement had been made, the inner and outer pericarp was each measured twice, at two positions at 90° to each other using the same probe and setting as for the core. 2.4.4. Soluble solids content An average soluble solids content was determined for individual fruit by measuring juice samples from the stylar and stem ends of the fruit separately using a hand-held refractometer (Master Series, 0–30%, Atago) or, in riper fruit, a digital refractometer (0–50 %, ‘pocket’ PAL-1, Atago), and the two values averaged.
2.2. Treatments The 10 MB packs from each orchard were allocated randomly into 2
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slower and ceased after 4–6 weeks of storage. The lack of discrimination of any change in firmness by compression for the period 6–16 weeks of storage (both readings ˜ 37.3 N), contrasts with the continued softening that was recorded by penetrometer (from ˜ 20.6 N to ˜ 13.7 N). There was a marked increase in softening recorded by both methods on transfer of fruit to 20 °C after 21 weeks of storage, although the rate of softening was also dependent on the actual firmness of the fruit when transferred. Softer fruit had less firmness still to be lost and were already in a naturally slower softening state. 1-MCP treatment did not alter the overall pattern of softening as measured by the two firmness methods. 1-MCP slowed the softening of the fruit whether measured by penetrometer or compression test. The degree of difference between treated and untreated fruit increased slowly up to 6 weeks into storage and remained similar for the rest of storage period. After 6 weeks of storage, the 1-MCP treated fruit were ˜ 6.9 N firmer than the untreated fruit by both penetrometer and compression test. The effect of 1-MCP retarding fruit softening was consistent for the fruit from the three orchards, although the fruit from Orchard 3 took a few weeks in storage for the effect to develop (Fig. 2). All tissue zones had a similar exponential decay pattern of softening, although there was a less marked fast to slow softening rate change in the core than in the outer or inner pericarp samples (Fig. 3). Between the inner and outer pericarp, the inner pericarp reached the change to slow softening earlier than the outer pericarp and softening stopped completely whereas in the outer pericarp there was still slow softening at the end of storage. This may reflect the lack of physical structure within the inner pericarp when fully ripe, with cells developing into a mucilaginous matrix around the seeds. There was a marked difference in starting firmness of the three tissue zones: ˜ 58.9 N in the core, ˜ 19.6 N in the outer pericarp and ˜ 9.8 N in the inner pericarp. These values are all directly comparable, as they were measured with the same size of penetrometer probe. The inner pericarp reached a lower plateau of ˜ 3.9 N after ˜ 8 weeks and remained at that firmness for a further 8–12 weeks, whereas the outer pericarp was still softening slowly from ˜ 4.4 N to ˜ 2.9 N over this period. The core softening did not reach a lower plateau, softening from ˜ 19.6 N at week 8 to ˜ 7.8 N by storage week 21. The difference in softening of the tissue zones can be more easily compared in the figures showing the normalised firmness values (Fig. 4). After 6 weeks of storage, without 1-MCP treatment, the firmness of the outer pericarp, inner pericarp and core had reduced to 34%, 35% and 50% of the initial firmness value, respectively. However, the softening of the inner pericarp may also be affected by the nature of the
Table 1 Characterisation of ‘Hayward’ kiwifruit from three orchards (O1, O2 and O3) at the start of the trial. Orchard values are the mean of 30 fruit (s.e.m.). Orchard
SSC (%)
Firmness (N)
O1 O2 O3 Mean
11.1 (0.23) 10.7 (0.20) 9.8 (0.17) 10.5
56.9 (1.1) 53.0 (2.3) 61.8 (1.9) 57.2
2.5. Data analysis Firmness was measured as kg force(kgf) and data converted to N, where 1 kgf = 9.81 N. Data have been presented as the sample means and standard error of means (s.e.m.). Graphics were created using Origin v8.5 (OriginLab Corporation, One Roundhouse Plaza, Northampton, MA01060, USA) with firmness data presented either as the raw data in N or normalised where the start value = 100 to allow easier relative comparisons of softening. 3. Results 3.1. Fruit characterisation At the start of the trial, the fruit were on average 10.5% SSC and 57.2 N firmness (Table 1). Among the orchards, the average SSC values were between 9.8% and 11.1% and the average firmness between 53.0 N and 61.8 N. 3.2. Impact of 1-MCP on whole fruit and tissue zone softening Both penetrometer and compression measurements of whole fruit firmness gave similar patterns for softening in storage; an overall exponential decay with an initial fast softening phase followed by a gradual slowing of softening as storage progressed (Fig. 1). Transfer of the fruit from 0 °C to 20 °C after 21 weeks of storage increased the softening rate as measured by both methods. As the actual data measured by penetrometer and compression were numerically similar, there was little difference between actual data plots and the normalised data (Fig. 1). Within the overall pattern of softening there were differences between the two assessment methods. The initial rapid decrease in firmness was greater (faster and more prolonged) when measured by penetrometer, whereas the measurement by flat plate compression was
Fig. 1. Softening of ‘Hayward’ kiwifruit during storage at 0 °C following treatment with 1-MCP (650 nL L−1, 24 h, •, ), or untreated control fruit (○, ). Fruit firmness measured by a flat plate compression test ( , ) or 7.9-mm penetrometer (•, ○). Fruit were transferred to 20 °C after 21 weeks of storage. Values presented as raw data (A) or normalised where the start value = 100 (B). Values are the mean of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 3
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Fig. 2. Softening of ‘Hayward’ kiwifruit from three orchards (A, B, C) during storage at 0 °C following treatment with 1-methylcyclopropene (650 nL L−1, 24 h, •), or untreated control fruit (○). Fruit firmness measured by 7.9-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are the means of 10 fruit (30 at week 0) ± s.e.m.
fruit treated with 10 and 100 μL L−1 ethylene. In contrast, the fruit treated with 1-MCP showed little or no response to ethylene throughout storage. There was a small decrease in firmness in response to ethylene after > 12 weeks of storage when measured by compression, but no consistent effect when measured by penetrometer. For both firmness measurement techniques, the degree of softening induced by ethylene in fruit not treated with 1-MCP depended on the starting firmness value. In both cases, there was a greater decrease in firmness from the firmer fruit early in storage. For compression measurement of firmness, 3 d after ethylene treatment fruit were of a similar firmness at ˜ 20–25 N, irrespective of storage duration. For the penetrometer measurements, the firmness after ethylene treatment decreased slightly with storage, from ˜ 10 N at the start of storage to ˜ 6 N after 21 weeks of storage. The response of individual tissue zone firmness to 1-MCP treatment at the start of storage and subsequent exposure to ethylene were similar to the overall effect on fruit firmness measured by the standard penetrometer (Fig. 6). 1-MCP treatment at the start of storage reduced or eliminated the softening response in the outer pericarp, inner pericarp and core when fruit were exposed to ethylene throughout storage (Fig. 6).
inner pericarp tissue zone structure, in which there was relatively less firmness to be lost after harvest. 1-MCP treatment retarded the softening of all tissue zones, after 6 weeks of storage, the firmness of the outer pericarp, inner pericarp and core had reduced to 45%, 42% and 61% of the initial firmness value, respectively (Fig. 4). These figures suggest that the relative impact of 1MCP on the tissue zones was similar with respect to the proportion of firmness lost. An effect of treatment developed over the first 4–6 weeks of storage and was maintained at about that level for the rest of the storage period. Later in storage, the 1-MCP treated fruit tended to have an outer pericarp that was ˜ 1 N firmer than the non-treated fruit and an inner pericarp that was between 0.5 and 1 N firmer. The core tended to retain firmness better than the pericarp, irrespective of treatment, and the 1-MCP treatment improved core firmness retention by on average ˜ 6.9 N. The overall effect of retarded softening measured for the tissue zones was similar to that seen in the whole fruit compression and penetrometer data (Fig. 2).
3.3. Duration of 1-MCP effect on tissue zone softening The protective effect of 1-MCP against exogenous ethylene was tested at intervals throughout 21 weeks of storage, by exposing fruit to ethylene at 0, 10 or 100 μL L−1 for 16 h at 20 °C and measuring firmness 3 d later. For firmness measured by both compression and penetrometer (Fig. 5), the 1-MCP treatment at the start of storage continued to prevent a softening response to exogenous ethylene throughout storage (Fig. 5). The non-1-MCP treated fruit responded to ethylene by softening significantly over 3 d, but with no consistent difference between the
4. Discussion This trial has demonstrated that 1-MCP is capable of retarding kiwifruit softening as measured by whole fruit compression or penetrometer. In addition, it was shown that 1-MCP retarded the softening of each of the three tissue zones investigated; the outer pericarp, inner pericarp and the core. The exposure of 1-MCP-treated fruit to ethylene at intervals throughout storage demonstrated the long term nature of
Fig. 3. Softening of the outer pericarp (A), inner pericarp (B) and core (C) of ‘Hayward’ kiwifruit during storage at 0 °C following treatment with 1-MCP (650 nL L−1, 24 h, •), or untreated control fruit (○). Firmness was measured by a 4-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 4
Scientia Horticulturae 259 (2020) 108791
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Fig. 4. Softening of the outer pericarp (◼), inner pericarp ( ) and core ( ) of ‘Hayward’ kiwifruit during storage at 0 °C. Untreated control fruit (A) and following treatment with 1-MCP (650 nL L−1, 24 h, B). Fruit firmness measured by a 4-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are mean of 3 orchards, 10 fruit per orchard (30 at week 0), normalised where the week 0 value = 100.
with 1-MCP. The treatment resulted in slightly firmer fruit throughout storage, yet the difference between compression and penetrometer measurements was maintained. Both 1-MCP-treated and non-treated fruit showed a lack of discrimination in softening for a long period between 6 and 16 weeks of storage when measured by compression. This difference between penetrometer and compression measurements was more marked than reported previously (Li et al., 2016). The data suggest that the inference that measurement of firmness by
the anti-ethylene effect of a 1-MCP treatment at the start of storage; an effect that persisted in all three tissue zones. The data also show a difference in sensitivity of the whole fruit compression and penetrometer measurements, with a long period in storage where the compression test did not show the same degree of softening as was detected by the penetrometer measurement. The difference observed in the softening patterns measured by compression and 7.9 mm penetrometer was not affected by treatment
Fig. 5. Impact of exogenous ethylene (0, ◼; 10 ; or 100 μL L−1, ˜ 16 h, 20 °C) on the firmness of ‘Hayward’ kiwifruit after different periods of storage at 0 °C. Fruit were either untreated (A, C) or treated with 1-MCP (650 nL L−1, 24 h, B, D) at the start of storage. Fruit firmness measured by a flat plate compression test (A, B) or 7.9-mm penetrometer (C, D) 3 d after the start of ethylene treatment. Values are the means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 5
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Fig. 6. Firmness of the outer pericarp (A, B), inner pericarp (C, D) and core (E, F) of ‘Hayward’ kiwifruit after treatment with exogenous ethylene (0, ◼; 10 ; or 100 μL L−1, ˜ 16 h, 20 °C) after different periods of storage at 0 °C. Fruit were either untreated (A, C, E) or treated with 1-MCP (650 nL L−1, 24 h; B, D, F) at the start of storage. Fruit firmness measured by 4 mm penetrometer 3 d after the start of ethylene treatment. Values are the means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m.
pericarp and core of kiwifruit have been shown to be affected by 1-MCP treatment (Ilina et al., 2010). However, irrespective of treatment, there was a difference in the softening pattern of the core relative to the outer or inner pericarp, with a less marked transition from fast to slow softening in the core relative to the outer and inner pericarp. This is in agreement with previously published data suggesting that the core softening in storage is closer to linear than the marked exponential softening pattern of the pericarp (Burdon et al., 2017). With the rapid initial softening of the outer and inner pericarp relative to the more consistent but slower softening rate of the core, it may be that for some fruit there may be a relatively firm core when the fruit is ripe. The
compression can be used in place of penetrometer (Feng et al., 2009) is only partially true. Coupled with previous reports of abnormal kiwifruit softening (McGlone et al., 1997), later explained by differences in the softening rates of the outer and inner pericarp (Li et al., 2017), the use of compression measurements in place of the penetrometer may at times miss some changes occurring in the fruit. The impact of 1-MCP on overall fruit softening was reflected in each of the three tissue zones, suggesting a similar capacity to respond to 1MCP in each tissue zone. The ethylene biosynthesis enzymes 1-aminocyclopropane-1-carboxylic acid synthase (ACS) and 1-aminocyclopropant-1-carboxylic acid oxidase (ACO) gene expression in both the outer 6
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presence of hard cores in ripe ‘Hayward’ fruit has been commented on previously, usually associated with less mature fruit (MacRae et al., 1989), and in particular when less mature fruit have been ripened without ethylene. While both 1-MCP treatment (Zoffoli et al., 2016) and controlled atmosphere storage (Testoni, 1991; Zoffoli et al., 2016) have been implicated in the occurrence of hard cores, it may simply reflect the combined effect of genotype, maturity at harvest and the time at which the fruit were checked for ripening (Burdon, 2018a, b). It is most unusual to store fruit in controlled atmospheres, or treat with 1-MCP, unless the fruit are being targeted at very long-term storage. Long term storage inevitably results in fruit softening towards ripeness during storage. Also, the problems associated with the ripening of 1-MCP treated kiwifruit after only a short period of storage has been documented (Burdon et al., 2007). While it has been reported that there is no impact of treatment on consumer liking of kiwifruit (Regiroli and Vriends, 2007), the very nature of the treatment in slowing fruit softening makes the sensory comparison of treated and non-treated fruit difficult, since it is almost impossible to have fruit of the same firmness on the same day for a direct taste panel comparison if 1-MCP has had the desired effect of slowing the fruit softening. Yet the firmness of kiwifruit is critical to their sensory quality when evaluated by consumers and fruit from different treatments should be carefully matched for evaluation (Stec et al., 1989). The data showed that treatment of kiwifruit with 1-MCP at the start of storage had a long term effect throughout storage in both maintaining fruit firmness, and also in protecting the fruit against exogenous ethylene. The duration of the 1-MCP effect against exogenous ethylene was similar for the outer and inner pericarp and core tissue zones. This finding possibly explains why one of the major benefits of 1-MCP treatment of kiwifruit is the slight improvement of fruit firmness late in storage when at about 10 N. While the overall mean firmness value of kiwifruit treated with 1-MCP may be only slightly firmer than untreated fruit from the same line, commercial trials have shown that the absence of fruit which are too soft in the 1-MCP treated fruit can significantly improve the perceived quality when checked after shipping (Lallu and Burdon, 2007). It is also worth noting that late in storage, when fruit firmness has decreased to 10 N or less, is the time at which endogenous production of ethylene tends to increase in kiwifruit (Kim et al., 1999). The finding that the duration of the 1-MCP treatment effect may last for a prolonged period of storage, raises questions about the precise nature and timeframe of the long-standing presumption that 1-MCP treated fruit re-develop the capacity to respond to ethylene through receptor turnover and the creation of new receptors replacing those previously blocked irreversibly by the 1-MCP molecule. Elsewhere, research has focussed on the effect of 1-MCP through a quantification of ethylene receptor transcripts during development or ripening of kiwifruit (Yin et al., 2010) and also other fruits including apple (Cin et al., 2005, 2006; Li et al., 2013) and pear (Xie et al., 2014). Inhibition and delayed increase of ethylene receptor gene expression by 1-MCP treatment have been observed in apple(Cin et al., 2005) and pear (Xie et al., 2014). In a comparison of the response to 1-MCP of apple and peach, the long term effect of 1-MCP on apple softening has been contrasted to a lack of effect in peach and associated with a slow or rapid recovery of MdETR1 in apple and PpETR1 in peach, respectively (Cin et al., 2005). In 1-MCPtreated pear fruit, an effect of a small difference in storage temperature (+1.1 °C and -1.1 °C) on expression levels of PcETR1 and PcETR2 has been demonstrated (Xie et al., 2014). While 1-MCP treatment downregulated PcETR1 and PcETR2 for the first 3 months of storage irrespective of storage temperature, the increased expression observed between 4 and 6 months of storage in fruit at +1.1 °C did not occur in fruit stored at -1.1 °C (Xie et al., 2014).It is concluded that 1-MCP retards the overall softening of ‘Hayward’ kiwifruit, whether measured by compression or penetrometer. More specifically, the treatment affects the softening of the outer pericarp, inner pericarp and core tissues to a similar extent. The protective effect of a 1-MCP treatment at the start of storage against exogenous ethylene persists to some degree throughout
storage. Acknowledgment The authors gratefully acknowledge the following: the ‘Study Abroad Program for Excellent PhD Students of Guangxi Zhuang Autonomous Region’ for financial support to H J Gong, Matt Adkins at Zespri for fruit supply and AgroFresh for the SmartFresh™ research powder. This research was undertaken as part of the Plant & Food Research SSIF Premium Kiwifruit programme. References Burdon, J., 2018a. New cultivars: physiological challenges to commercial success. Acta Hortic. 1218, 45–60. Burdon, J., 2018b. Kiwifruit biology: the commercial implications of fruit maturation. Hortic. Reviews. 46, 385–421. Burdon, J., Lallu, N., 2011. Kiwifruit (Actinidia spp.). In: Yahia, E.M. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruit. vol. 3, Cocona to Mango. Woodhead Publishing Limited, UK, pp. 326–360. Burdon, J., Pidakala, P., Martin, P., Billing, D., 2017. Softening of ‘Hayward’ kiwifruit on the vine and in storage: the effects of temperature. Sci. 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Application of compression force in monitoring firmness of ‘Hayward’ kiwifruit (Actinidia deliciosa). Acta Hortic. 880, 283–289. Hopping, M.E., 1976. Structure and development of fruit and seeds in Chinese gooseberry (Actinidia chinensis Planch.). New Zealand Journal of Botany 14 (1), 63–68. Ilina, N., Alem, H.J., Pagano, E.A., Sozzi, G.O., 2010. Suppression of ethylene perception after exposure to cooling conditions delays the progress of softening in ‘Hayward’ kiwifruit. Postharvest Biol. Technol. 55, 160–168. Jackson, P., Harker, F.R., 1997. Changes in firmness of the outer pericarp, inner pericarp, and core of Actinidia species during ripening. N. Z. J. Crop Hortic. Sci. 25, 185–189. Jeffery, P.B., Banks, N.H., 1996. Effects of ethylene on kiwifruit softening in coolstorage. N. Z. Kiwifruit J. 114 (March), 9–10. Kader, A.A., 2002. Postharvest Technology of Horticultural Crops, 3rd edition. University of California, Agriculture and Natural Resources Publication 3311. Kim, H.O., Hewett, E.W., Lallu, N., 1999. The role of ethylene in kiwifruit softening. Acta Hortic. 498, 255–262. Lallu, N., Burdon, J., 2007. Experiences with recent postharvest technologies in kiwifruit. Acta Hortic. 753, 733–740. Lallu, N., Searle, A.N., MacRae, E.A., 1989. An investigation of ripening and handling strategies for early season kiwifruit (Actinidia deliciosa cv. Hayward). J. Sci. Food Agric. 47, 387–400. Li, H., Pidakala, P., Billing, D., Burdon, J., 2016. Kiwifruit firmness: measurement by penetrometer and non-destructive devices. Postharvest Biol. Technol. 120, 127–137. Li, H., Billing, D., Pidakala, P., Burdon, J., 2017. Textural changes in ‘Hayward’ kiwifruit during and after storage in controlled atmospheres. Sci. Hortic. 222, 40–45. Li, M., Zhang, Y.M., Zhang, Z.Y., Ji, X.H., Zhang, R., Liu, D.L., Gao, L.P., Zhang, J., Wang, B., Wu, Y.S., Wu, S.J., Chen, X.L., Feng, S.Q., Chen, X.S., 2013. Hypersensitive ethylene signaling and ZMdPG1 expression lead to fruit softening and dehiscence. PLoS One 8 (3), 1–10. MacRae, E., Redgwell, R., 1992. Softening in kiwifruit. Postharvest News and Inform. 3, 49N–52N. MacRae, E.A., Bowen, J.H., Stec, M.G.H., 1989. Maturation of kiwifruit (Actinidia deliciosa cv. Hayward) from two orchards: differences in composition of the tissue zones. J. Sci. Food Agric. 47, 401–416. McDonald, B., 1990. Precooling, storage, and transport of kiwifruit. In: Warrington, I.J., Weston, G.C. (Eds.), Science and Management. Ray Richards Publisher in association with the N. Z. Soc. Hortic. Sci., Kiwifruit, pp. 429–459. McGlone, V.A., Jordan, R.B., Schaare, P.N., 1997. Anomalous firmness changes in coolstored kiwifruit. Postharvest Biol. Technol. 12, 147–156. Regiroli, G., Vriends, P., 2007. SmartFreshSM (1-methylcyclopropene) benefits for kiwifruit. Acta Hortic. 753, 745–753. Richardson, A.C., Boldingh, H.L., McAtee, P.A., Gunaseelan, K., Luo, Z., Atkinson, R.G., David, K.M., Burdon, J.N., Schaffer, R.J., 2011. Fruit development of the diploid kiwifruit, Actinidia chinensis’ Hort16A’. BMC Plant Biol. 11, 182. Snelgar, B., Thorp, G., Spinelli, R., Brun, S., 2010. We don’t know how lucky we are? N. Z. Kiwifruit J. (July/August), 14–18. Stec, M.G.H., Hodgson, J.A., MacRae, E.A., Triggs, C.M., 1989. Role of fruit firmness in
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physio-chemical changes of Chinese gooseberry fruit Actinidia chinensis (yang-tao) during the later stages of development. N. Z. J. Agric. Res. 10, 405–414. Xie, X.B., Song, J.K., Wang, Y., Sugar, D., 2014. Ethylene synthesis, ripening capacity, and superficial scald inhibition in 1-MCP treated ‘d’Anjou’ pears are affected by storage temperature. Postharvest Biol. Technol. 97, 1–10. Yin, X.R., Allan, A.C., Chen, K.S., Ferguson, I.B., 2010. Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiol. 153, 1280–1292. Zoffoli, J.P., Flores, K., D’Hainaut, D., 2016. Effect of ethylene on ripening of kiwifruit stored under controlled or modified atmosphere packaging and treated with 1-methylcyclopropene. J. Berry Res. 6, 381–393.
sensory evaluation of kiwifruit (Actinidia deliciosa cv. Hayward). J. Sci. Food Agric. 47, 417–433. Testoni, A., 1991. Influence of storage conditions on softening of the columella. Acta Hortic. 297, 587–593. Watkins, C., Harman, J., 1981. Use of penetrometer to measure flesh firmness of fruit. Orchardist N. Z. 54, 14–16. Wills, R., McGlasson, B., Graham, D., Joyce, D., 2007. Postharvest: an Introduction to the Physiology and Handling of Fruit, Vegetables and Ornamentals, 5th edition. University of New South Wales Press, Australia/CABI, UK. Wright, H.B., Heatherbell, D.A., 1967. A study of respiratory trends and some associated
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Retardation of ‘Hayward’ kiwifruit tissue zone softening during storage by 1methylcyclopropene
T
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H.J. Gonga,b,c, , C. Fullertonb, D. Billingb, J. Burdonb a
Agricultural College, Guangxi University, Nanning 530005, China The New Zealand Institute for Plant and Food Research Limited, Private Bag 92169, Auckland Mail Centre, 1142, Auckland, New Zealand c Guangxi Institute of Botany, Chinese Academy of Sciences, Guilin 541006, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Actinidia Storage 1-MCP Firmness Pericarp Core Efficacy
The use of the ethylene action inhibitor 1-methylcyclopropene (1-MCP) is becoming more common in the global kiwifruit industry as a tool for firmness management after harvest. The overall fruit firmness measured by penetrometer or compression is dependent on the relative changes in texture of the three main tissue zones: the outer pericarp, inner pericarp and core. This research has investigated the way in which 1-MCP affects the firmness of individual tissue zones during storage, and the changing response of 1-MCP treated fruit to ethylene. 1-MCP retarded fruit softening as measured by whole fruit compression or penetrometer. However, there was a long period in storage where the compression test did not show the same degree of softening as was detected by the penetrometer measurement. In addition, it was shown that 1-MCP retarded the softening of the three tissue zones investigated. The exposure of 1-MCP treated fruit to ethylene at intervals throughout storage demonstrated the long term nature of the anti-ethylene effect of a 1-MCP treatment at the start of storage; an effect that persisted in all three tissue zones. It is concluded that 1-MCP retards the overall softening of ‘Hayward’ kiwifruit, whether measured by compression or penetrometer. More specifically, the treatment affects the softening of the outer pericarp, inner pericarp and core tissues to a similar extent. The protective effect of a 1-MCP treatment at the start of storage against exogenous ethylene persists to some degree throughout storage.
1. Introduction The firmness of kiwifruit (Actinidia spp.) is a critical quality attribute used to determine the limits for handling procedures and the acceptability of fruit in the commercial supply chain (Burdon and Lallu, 2011). Kiwifruit are harvested in a mature, unripe state and during ripening they must change to a soft, melting texture when ripe and ready to eat (MacRae and Redgwell, 1992). Fruit may be cold stored for several months between harvest and consumption (Burdon and Lallu, 2011). Kiwifruit are often referred to as being climacteric fruit, i.e. ripening with an associated increase in ethylene production and respiratory activity (Kader, 2002; Wills et al., 2007). However, they are clearly not typically climacteric in that the majority of the ripening occurs before any increase in ethylene production (Wright and Heatherbell, 1967; Kim et al., 1999). This late increase in ethylene production has been suggested to be more associated with senescence than ripening (Richardson et al., 2011). However, kiwifruit are particularly responsive to even low concentrations of ethylene, which can accelerate
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the fruit softening (McDonald, 1990; Jeffery and Banks, 1996). Commercially, ethylene treatments can be used to accelerate and co-ordinate the ripening of kiwifruit (Lallu et al., 1989; Crisosto et al., 1997) and this is particularly useful for ripening fruit harvested early, at a low physiological maturity. The softening of ripening kiwifruit has been shown to be slowed to some degree by the application of 1-MCP (Regiroli and Vriends, 2007). 1-MCP functions by binding irreversibly to the ethylene binding site in the fruit, thereby blocking ethylene action and preventing a response. The commercial use of 1-MCP is becoming common in some sectors of the global kiwifruit industry. The greatest effect of 1-MCP on kiwifruit softening may occur in environments where there is an exogenous ethylene source, i.e. as protection from the stimulation of softening by exogenous ethylene rather than simply retarding the natural softening (Defilippi et al., 2011). The kiwifruit is made up of three major tissue zones, the outer and inner pericarp and core, also called a columella, with several layers of compressed dead cells making up the skin at the surface of the fruit (Hopping, 1976). The outer pericarp is made up from distinct
Corresponding author at: Guangxi Institute of Botany, Chinese Academy of Sciences, Guilin 541006, China. E-mail address: [email protected] (H.J. Gong).
https://doi.org/10.1016/j.scienta.2019.108791 Received 17 April 2019; Received in revised form 18 August 2019; Accepted 20 August 2019 0304-4238/ © 2019 Elsevier B.V. All rights reserved.
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two lots of five packs, one for treatment with 1-MCP and the other to be left as an untreated control.
populations of small spherical cells and larger elongated cells. The inner pericarp has large thin walled placental cells which develop into a mucilaginous matrix around the seeds. The core is composed of large homogeneous parenchyma cells. The softening of the three major tissue zones has been reported as occurring synchronously at 20 °C for three kiwifruit genotypes (Jackson and Harker, 1997). More recently, it has become apparent that the degree of synchrony between tissue zones may differ among genotypes, and that differences in the softening rates of the major tissue zones of the kiwifruit can affect the overall firmness perception of the fruit (Li et al., 2016). The most commonly reported aspect of a lack of synchrony in the softening of the different tissue zones within the fruit is the occurrence of hard cores within otherwise ripe fruit. This has been associated with genotype (Burdon, 2018a, b), fruit maturity (MacRae et al., 1989; Stec et al., 1989; Burdon, 2018a), controlled atmosphere storage (Testoni, 1991; Zoffoli et al., 2016; Li et al., 2017) and the use of 1-MCP (Zoffoli et al., 2016). The relative softening rates of the different tissue zones within a kiwifruit, and their response to 1-MCP treatment, would seem to be integral to the acceptability of the fruit. It is therefore necessary to understand how the anti-ethylene action of 1-MCP functions within the different tissue zones of kiwifruit. Kiwifruit firmness is usually measured with a penetrometer after removal of the skin and flesh to a depth of about 1 mm (Watkins and Harman, 1981). While for many years hand-held penetrometers were used, it is now more common for a motorised texture analyser to be used. The penetrometer measurement is largely of the outer pericarp, although it also depends on the texture of the rest of the fruit since the whole fruit may deform when the penetrometer is pushed against it. It has been suggested that the destructive measurement of fruit firmness by penetrometer can be replaced by a non-destructive whole fruit compression test (Feng et al., 2009). However, differences in the relative softening of the inner and outer pericarp have been shown to affect the relationship between compression firmness values and the standard penetrometer measurement (McGlone et al., 1997; Li et al., 2017). In this paper, the impact of 1-MCP on the softening of ‘Hayward’ kiwifruit through storage is reported. Fruit firmness has been measured by penetrometer with the standard 7.9-mm probe and by whole fruit compression, and the individual outer pericarp, inner pericarp and core tissue zones measured by penetrometer with a 4-mm diameter probe. In addition, the longevity of the 1-MCP effect on the softening of these tissue zones has been investigated by challenging treated fruit with ethylene at intervals throughout storage.
2.2.1. 1-MCP Fruit in the MB packs were treated with 650 nL 1-MCP L−1 (ppb) for 24 h by exposure to the gas whilst the fruit were being cooled to 0 °C in a 12 m3 coolstore. The 1-MCP gas was released from SmartFresh™ research powder (0.14% a.i.; AgroFresh Inc.; www.agrofresh.com) by mixing with warm (˜40 °C) water. 2.2.2. Ethylene Samples of 10 fruit per orchard were first warmed overnight to 20 °C before being placed into 360 L chambers. Treatment with ethylene was by injection of known volumes of ethylene into the chambers to give final concentrations of 10 or 100 μL L−1. The treatments lasted for ˜ 16 h at 20 °C. 2.2.3. Storage Fruit were cooled to ˜ 2 °C within 24 h and then stored at 0.0 °C for up to 21 weeks. After 21 weeks of storage, fruit were transferred to 20 °C for 1 week. 2.3. Fruit assessments A 30 fruit sample of fruit from each orchard was measured for soluble solids content (SSC) and firmness on receipt. Throughout storage, 10 fruit samples from each orchard were measured for firmness by flat plate compression and standard 7.9-mm penetrometer, and tissue zones measured with a 4-mm penetrometer. Samples during storage were taken equally from 5 MB packs. Immediately after 1-MCP treatment, and at intervals through storage, the treated and non-treated fruit were exposed to ethylene and the firmness (whole fruit and tissue zones) were measured after 3 d at 20 °C. 2.4. Fruit assessment methodology 2.4.1. Compression firmness measurement The whole fruit was compressed a distance of 2 mm by flat plate applied at 5 mm s−1. The force recorded after 2 mm displacement was taken as the firmness value. 2.4.2. Standard penetrometer firmness measurement Fruit firmness was measured using a Fruit Texture Analyser (Güss, model GS14, South Africa) fitted with a 7.9-mm Effegi™ penetrometer probe after removal of skin and flesh to a depth of approximately 1 mm. The probe was driven into the flesh at 5 mm s−1 to a depth of 7.9 mm, and the maximum force recorded as the firmness value. Firmness was measured twice at the equator of each fruit, with the two measurements taken at 90° to each other.
2. Materials and methods 2.1. Fruit The kiwifruit cultivar used in this study was Actinidia chinensis var. deliciosa ‘Hayward’, the most commonly commercially grown greenfleshed kiwifruit cultivar. Fruit were harvested and packed commercially from three orchards around Te Puke, Bay of Plenty, New Zealand (37°49′S, 176°19′E). Fruit (count size 33 / 36) were supplied direct from the packhouse in commercial modular bulk packs (MB, 10 kg of fruit loose filled in a polythene bag inside the box), with 10 MB packs per orchard. The Bay of Plenty region in New Zealand is characterised as having good winter chilling, warm springs and mild summers and autumns (Snelgar et al., 2010). The soil is deep, free-draining and of volcanic origin. Rainfall is distributed throughout the year and averages 1600 mm per year.
2.4.3. Fruit core, outer pericarp and inner pericarp firmness measurement The fruit core firmness was measured after removal of approximately 15 mm of the fruit at the stem end. The measurement was made with a 4 mm diameter probe driven into the core at 5 mm s−1 to a depth of 6 mm, and the maximum force recorded as the firmness value. After the core measurement had been made, the inner and outer pericarp was each measured twice, at two positions at 90° to each other using the same probe and setting as for the core. 2.4.4. Soluble solids content An average soluble solids content was determined for individual fruit by measuring juice samples from the stylar and stem ends of the fruit separately using a hand-held refractometer (Master Series, 0–30%, Atago) or, in riper fruit, a digital refractometer (0–50 %, ‘pocket’ PAL-1, Atago), and the two values averaged.
2.2. Treatments The 10 MB packs from each orchard were allocated randomly into 2
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slower and ceased after 4–6 weeks of storage. The lack of discrimination of any change in firmness by compression for the period 6–16 weeks of storage (both readings ˜ 37.3 N), contrasts with the continued softening that was recorded by penetrometer (from ˜ 20.6 N to ˜ 13.7 N). There was a marked increase in softening recorded by both methods on transfer of fruit to 20 °C after 21 weeks of storage, although the rate of softening was also dependent on the actual firmness of the fruit when transferred. Softer fruit had less firmness still to be lost and were already in a naturally slower softening state. 1-MCP treatment did not alter the overall pattern of softening as measured by the two firmness methods. 1-MCP slowed the softening of the fruit whether measured by penetrometer or compression test. The degree of difference between treated and untreated fruit increased slowly up to 6 weeks into storage and remained similar for the rest of storage period. After 6 weeks of storage, the 1-MCP treated fruit were ˜ 6.9 N firmer than the untreated fruit by both penetrometer and compression test. The effect of 1-MCP retarding fruit softening was consistent for the fruit from the three orchards, although the fruit from Orchard 3 took a few weeks in storage for the effect to develop (Fig. 2). All tissue zones had a similar exponential decay pattern of softening, although there was a less marked fast to slow softening rate change in the core than in the outer or inner pericarp samples (Fig. 3). Between the inner and outer pericarp, the inner pericarp reached the change to slow softening earlier than the outer pericarp and softening stopped completely whereas in the outer pericarp there was still slow softening at the end of storage. This may reflect the lack of physical structure within the inner pericarp when fully ripe, with cells developing into a mucilaginous matrix around the seeds. There was a marked difference in starting firmness of the three tissue zones: ˜ 58.9 N in the core, ˜ 19.6 N in the outer pericarp and ˜ 9.8 N in the inner pericarp. These values are all directly comparable, as they were measured with the same size of penetrometer probe. The inner pericarp reached a lower plateau of ˜ 3.9 N after ˜ 8 weeks and remained at that firmness for a further 8–12 weeks, whereas the outer pericarp was still softening slowly from ˜ 4.4 N to ˜ 2.9 N over this period. The core softening did not reach a lower plateau, softening from ˜ 19.6 N at week 8 to ˜ 7.8 N by storage week 21. The difference in softening of the tissue zones can be more easily compared in the figures showing the normalised firmness values (Fig. 4). After 6 weeks of storage, without 1-MCP treatment, the firmness of the outer pericarp, inner pericarp and core had reduced to 34%, 35% and 50% of the initial firmness value, respectively. However, the softening of the inner pericarp may also be affected by the nature of the
Table 1 Characterisation of ‘Hayward’ kiwifruit from three orchards (O1, O2 and O3) at the start of the trial. Orchard values are the mean of 30 fruit (s.e.m.). Orchard
SSC (%)
Firmness (N)
O1 O2 O3 Mean
11.1 (0.23) 10.7 (0.20) 9.8 (0.17) 10.5
56.9 (1.1) 53.0 (2.3) 61.8 (1.9) 57.2
2.5. Data analysis Firmness was measured as kg force(kgf) and data converted to N, where 1 kgf = 9.81 N. Data have been presented as the sample means and standard error of means (s.e.m.). Graphics were created using Origin v8.5 (OriginLab Corporation, One Roundhouse Plaza, Northampton, MA01060, USA) with firmness data presented either as the raw data in N or normalised where the start value = 100 to allow easier relative comparisons of softening. 3. Results 3.1. Fruit characterisation At the start of the trial, the fruit were on average 10.5% SSC and 57.2 N firmness (Table 1). Among the orchards, the average SSC values were between 9.8% and 11.1% and the average firmness between 53.0 N and 61.8 N. 3.2. Impact of 1-MCP on whole fruit and tissue zone softening Both penetrometer and compression measurements of whole fruit firmness gave similar patterns for softening in storage; an overall exponential decay with an initial fast softening phase followed by a gradual slowing of softening as storage progressed (Fig. 1). Transfer of the fruit from 0 °C to 20 °C after 21 weeks of storage increased the softening rate as measured by both methods. As the actual data measured by penetrometer and compression were numerically similar, there was little difference between actual data plots and the normalised data (Fig. 1). Within the overall pattern of softening there were differences between the two assessment methods. The initial rapid decrease in firmness was greater (faster and more prolonged) when measured by penetrometer, whereas the measurement by flat plate compression was
Fig. 1. Softening of ‘Hayward’ kiwifruit during storage at 0 °C following treatment with 1-MCP (650 nL L−1, 24 h, •, ), or untreated control fruit (○, ). Fruit firmness measured by a flat plate compression test ( , ) or 7.9-mm penetrometer (•, ○). Fruit were transferred to 20 °C after 21 weeks of storage. Values presented as raw data (A) or normalised where the start value = 100 (B). Values are the mean of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 3
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Fig. 2. Softening of ‘Hayward’ kiwifruit from three orchards (A, B, C) during storage at 0 °C following treatment with 1-methylcyclopropene (650 nL L−1, 24 h, •), or untreated control fruit (○). Fruit firmness measured by 7.9-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are the means of 10 fruit (30 at week 0) ± s.e.m.
fruit treated with 10 and 100 μL L−1 ethylene. In contrast, the fruit treated with 1-MCP showed little or no response to ethylene throughout storage. There was a small decrease in firmness in response to ethylene after > 12 weeks of storage when measured by compression, but no consistent effect when measured by penetrometer. For both firmness measurement techniques, the degree of softening induced by ethylene in fruit not treated with 1-MCP depended on the starting firmness value. In both cases, there was a greater decrease in firmness from the firmer fruit early in storage. For compression measurement of firmness, 3 d after ethylene treatment fruit were of a similar firmness at ˜ 20–25 N, irrespective of storage duration. For the penetrometer measurements, the firmness after ethylene treatment decreased slightly with storage, from ˜ 10 N at the start of storage to ˜ 6 N after 21 weeks of storage. The response of individual tissue zone firmness to 1-MCP treatment at the start of storage and subsequent exposure to ethylene were similar to the overall effect on fruit firmness measured by the standard penetrometer (Fig. 6). 1-MCP treatment at the start of storage reduced or eliminated the softening response in the outer pericarp, inner pericarp and core when fruit were exposed to ethylene throughout storage (Fig. 6).
inner pericarp tissue zone structure, in which there was relatively less firmness to be lost after harvest. 1-MCP treatment retarded the softening of all tissue zones, after 6 weeks of storage, the firmness of the outer pericarp, inner pericarp and core had reduced to 45%, 42% and 61% of the initial firmness value, respectively (Fig. 4). These figures suggest that the relative impact of 1MCP on the tissue zones was similar with respect to the proportion of firmness lost. An effect of treatment developed over the first 4–6 weeks of storage and was maintained at about that level for the rest of the storage period. Later in storage, the 1-MCP treated fruit tended to have an outer pericarp that was ˜ 1 N firmer than the non-treated fruit and an inner pericarp that was between 0.5 and 1 N firmer. The core tended to retain firmness better than the pericarp, irrespective of treatment, and the 1-MCP treatment improved core firmness retention by on average ˜ 6.9 N. The overall effect of retarded softening measured for the tissue zones was similar to that seen in the whole fruit compression and penetrometer data (Fig. 2).
3.3. Duration of 1-MCP effect on tissue zone softening The protective effect of 1-MCP against exogenous ethylene was tested at intervals throughout 21 weeks of storage, by exposing fruit to ethylene at 0, 10 or 100 μL L−1 for 16 h at 20 °C and measuring firmness 3 d later. For firmness measured by both compression and penetrometer (Fig. 5), the 1-MCP treatment at the start of storage continued to prevent a softening response to exogenous ethylene throughout storage (Fig. 5). The non-1-MCP treated fruit responded to ethylene by softening significantly over 3 d, but with no consistent difference between the
4. Discussion This trial has demonstrated that 1-MCP is capable of retarding kiwifruit softening as measured by whole fruit compression or penetrometer. In addition, it was shown that 1-MCP retarded the softening of each of the three tissue zones investigated; the outer pericarp, inner pericarp and the core. The exposure of 1-MCP-treated fruit to ethylene at intervals throughout storage demonstrated the long term nature of
Fig. 3. Softening of the outer pericarp (A), inner pericarp (B) and core (C) of ‘Hayward’ kiwifruit during storage at 0 °C following treatment with 1-MCP (650 nL L−1, 24 h, •), or untreated control fruit (○). Firmness was measured by a 4-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 4
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Fig. 4. Softening of the outer pericarp (◼), inner pericarp ( ) and core ( ) of ‘Hayward’ kiwifruit during storage at 0 °C. Untreated control fruit (A) and following treatment with 1-MCP (650 nL L−1, 24 h, B). Fruit firmness measured by a 4-mm penetrometer. Fruit were transferred to 20 °C after 21 weeks of storage. Values are mean of 3 orchards, 10 fruit per orchard (30 at week 0), normalised where the week 0 value = 100.
with 1-MCP. The treatment resulted in slightly firmer fruit throughout storage, yet the difference between compression and penetrometer measurements was maintained. Both 1-MCP-treated and non-treated fruit showed a lack of discrimination in softening for a long period between 6 and 16 weeks of storage when measured by compression. This difference between penetrometer and compression measurements was more marked than reported previously (Li et al., 2016). The data suggest that the inference that measurement of firmness by
the anti-ethylene effect of a 1-MCP treatment at the start of storage; an effect that persisted in all three tissue zones. The data also show a difference in sensitivity of the whole fruit compression and penetrometer measurements, with a long period in storage where the compression test did not show the same degree of softening as was detected by the penetrometer measurement. The difference observed in the softening patterns measured by compression and 7.9 mm penetrometer was not affected by treatment
Fig. 5. Impact of exogenous ethylene (0, ◼; 10 ; or 100 μL L−1, ˜ 16 h, 20 °C) on the firmness of ‘Hayward’ kiwifruit after different periods of storage at 0 °C. Fruit were either untreated (A, C) or treated with 1-MCP (650 nL L−1, 24 h, B, D) at the start of storage. Fruit firmness measured by a flat plate compression test (A, B) or 7.9-mm penetrometer (C, D) 3 d after the start of ethylene treatment. Values are the means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m. 5
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Fig. 6. Firmness of the outer pericarp (A, B), inner pericarp (C, D) and core (E, F) of ‘Hayward’ kiwifruit after treatment with exogenous ethylene (0, ◼; 10 ; or 100 μL L−1, ˜ 16 h, 20 °C) after different periods of storage at 0 °C. Fruit were either untreated (A, C, E) or treated with 1-MCP (650 nL L−1, 24 h; B, D, F) at the start of storage. Fruit firmness measured by 4 mm penetrometer 3 d after the start of ethylene treatment. Values are the means of 3 orchards, 10 fruit per orchard (30 at week 0) ± s.e.m.
pericarp and core of kiwifruit have been shown to be affected by 1-MCP treatment (Ilina et al., 2010). However, irrespective of treatment, there was a difference in the softening pattern of the core relative to the outer or inner pericarp, with a less marked transition from fast to slow softening in the core relative to the outer and inner pericarp. This is in agreement with previously published data suggesting that the core softening in storage is closer to linear than the marked exponential softening pattern of the pericarp (Burdon et al., 2017). With the rapid initial softening of the outer and inner pericarp relative to the more consistent but slower softening rate of the core, it may be that for some fruit there may be a relatively firm core when the fruit is ripe. The
compression can be used in place of penetrometer (Feng et al., 2009) is only partially true. Coupled with previous reports of abnormal kiwifruit softening (McGlone et al., 1997), later explained by differences in the softening rates of the outer and inner pericarp (Li et al., 2017), the use of compression measurements in place of the penetrometer may at times miss some changes occurring in the fruit. The impact of 1-MCP on overall fruit softening was reflected in each of the three tissue zones, suggesting a similar capacity to respond to 1MCP in each tissue zone. The ethylene biosynthesis enzymes 1-aminocyclopropane-1-carboxylic acid synthase (ACS) and 1-aminocyclopropant-1-carboxylic acid oxidase (ACO) gene expression in both the outer 6
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presence of hard cores in ripe ‘Hayward’ fruit has been commented on previously, usually associated with less mature fruit (MacRae et al., 1989), and in particular when less mature fruit have been ripened without ethylene. While both 1-MCP treatment (Zoffoli et al., 2016) and controlled atmosphere storage (Testoni, 1991; Zoffoli et al., 2016) have been implicated in the occurrence of hard cores, it may simply reflect the combined effect of genotype, maturity at harvest and the time at which the fruit were checked for ripening (Burdon, 2018a, b). It is most unusual to store fruit in controlled atmospheres, or treat with 1-MCP, unless the fruit are being targeted at very long-term storage. Long term storage inevitably results in fruit softening towards ripeness during storage. Also, the problems associated with the ripening of 1-MCP treated kiwifruit after only a short period of storage has been documented (Burdon et al., 2007). While it has been reported that there is no impact of treatment on consumer liking of kiwifruit (Regiroli and Vriends, 2007), the very nature of the treatment in slowing fruit softening makes the sensory comparison of treated and non-treated fruit difficult, since it is almost impossible to have fruit of the same firmness on the same day for a direct taste panel comparison if 1-MCP has had the desired effect of slowing the fruit softening. Yet the firmness of kiwifruit is critical to their sensory quality when evaluated by consumers and fruit from different treatments should be carefully matched for evaluation (Stec et al., 1989). The data showed that treatment of kiwifruit with 1-MCP at the start of storage had a long term effect throughout storage in both maintaining fruit firmness, and also in protecting the fruit against exogenous ethylene. The duration of the 1-MCP effect against exogenous ethylene was similar for the outer and inner pericarp and core tissue zones. This finding possibly explains why one of the major benefits of 1-MCP treatment of kiwifruit is the slight improvement of fruit firmness late in storage when at about 10 N. While the overall mean firmness value of kiwifruit treated with 1-MCP may be only slightly firmer than untreated fruit from the same line, commercial trials have shown that the absence of fruit which are too soft in the 1-MCP treated fruit can significantly improve the perceived quality when checked after shipping (Lallu and Burdon, 2007). It is also worth noting that late in storage, when fruit firmness has decreased to 10 N or less, is the time at which endogenous production of ethylene tends to increase in kiwifruit (Kim et al., 1999). The finding that the duration of the 1-MCP treatment effect may last for a prolonged period of storage, raises questions about the precise nature and timeframe of the long-standing presumption that 1-MCP treated fruit re-develop the capacity to respond to ethylene through receptor turnover and the creation of new receptors replacing those previously blocked irreversibly by the 1-MCP molecule. Elsewhere, research has focussed on the effect of 1-MCP through a quantification of ethylene receptor transcripts during development or ripening of kiwifruit (Yin et al., 2010) and also other fruits including apple (Cin et al., 2005, 2006; Li et al., 2013) and pear (Xie et al., 2014). Inhibition and delayed increase of ethylene receptor gene expression by 1-MCP treatment have been observed in apple(Cin et al., 2005) and pear (Xie et al., 2014). In a comparison of the response to 1-MCP of apple and peach, the long term effect of 1-MCP on apple softening has been contrasted to a lack of effect in peach and associated with a slow or rapid recovery of MdETR1 in apple and PpETR1 in peach, respectively (Cin et al., 2005). In 1-MCPtreated pear fruit, an effect of a small difference in storage temperature (+1.1 °C and -1.1 °C) on expression levels of PcETR1 and PcETR2 has been demonstrated (Xie et al., 2014). While 1-MCP treatment downregulated PcETR1 and PcETR2 for the first 3 months of storage irrespective of storage temperature, the increased expression observed between 4 and 6 months of storage in fruit at +1.1 °C did not occur in fruit stored at -1.1 °C (Xie et al., 2014).It is concluded that 1-MCP retards the overall softening of ‘Hayward’ kiwifruit, whether measured by compression or penetrometer. More specifically, the treatment affects the softening of the outer pericarp, inner pericarp and core tissues to a similar extent. The protective effect of a 1-MCP treatment at the start of storage against exogenous ethylene persists to some degree throughout
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