Delaying establishment of controlled atmosphere or CO
2exposure reduces ‘Fuji’ apple CO
2injury without excessive
fruit quality loss
Luiz Argenta
a, Xuetong Fan
b, James Mattheis
c,*
aEPAGRI,Estacao Bom Sucesso – C.P.591,CEP: 89500-000,Cacador,SC,Brazil bUSDA,ARS ERRC,600E.Mermaid Lane,Wyndmoor,PA19038,USA cUSDA,ARS Tree Fruit Research Laboratory,1104N. Western A
6enue,Wenatchee,WA98801,USA Received 7 January 2000; accepted 10 June 2000
Abstract
Storage of ‘Fuji’ apple fruit in a high CO2 (3 kPa) and low O2 (1.5 kPa) controlled atmosphere (CA) reduced
firmness and titratable acidity (TA) loss during long term storage. This CA environment also induced development
of internal CO2-injury (brown-heart) and slowed the disappearance of watercore. The symptoms of internal
CO2-injury were first detected 15 days after CA establishment and the severity increased during the first 4 months of
CA-storage. Delaying establishment of CA conditions for 2 – 12 weeks significantly reduced the severity of CO2-injury.
Delaying CO2accumulation to 3 kPa for 1 – 4 months during CA (1.5 kPa O2+0.05 kPa CO2) storage also reduced
development of CO2-injury symptoms. Delaying CA or CO2 accumulation resulted in lower firmness and TA
compared to establishment of CA within 72 h of harvest. However, the delay treatments did result in firmness and TA that were significantly higher compared to values for fruit stored in air. The incidence and severity of senescent injuries (flesh browning and core flush) detected during the late period of storage were greater in air- than CA-stored fruit. The results indicate the susceptibility of ‘Fuji’ apples to CO2-injury is highest during the first weeks of storage
after harvest. Delaying establishment of CA or exposure to elevated CO2after harvest may be a practical strategy to
reduce CO2-injury while maintaining other important quality attributes at acceptable levels. © 2000 Published by
Elsevier Science B.V.
Keywords:Controlled atmosphere storage; Carbon dioxide injury; Brown-heart
www.elsevier.com/locate/postharvbio
1. Introduction
‘Fuji’ apples are susceptible to the physiological disorders brown-heart, flesh browning, and core flush during cold storage in regular atmosphere (RA) and controlled atmosphere (CA) (Fukuda, 1984). Susceptibility of ‘Fuji’ apples to brown-* Corresponding author. Tel.: +1-509-6642280; fax: +
1-509-6642287.
E-mail address:[email protected] (J. Mattheis).
L.Argenta et al./Posthar6est Biology and Technology20 (2000) 221 – 229 222
heart CO2-injury as described by Wilkinson and
Fidler (1973) increases with CO2 concentration
(Argenta et al., 1994; Fan et al., 1997), harvest at an advanced maturity (Volz et al., 1998) and fruit size (Park et al., 1997). The risk of CO2-injury also
increases with fruit nitrogen content (Meheriuk et al., 1994), low storage temperature (Smock and Blanpied, 1963) and production under cool tem-perature growing conditions (Lau, 1998). The an-tioxidant diphenylamine (DPA) prevents the development of CO2-injury in apples (Burmeister
and Dilley, 1995; Watkins et al., 1997), however, DPA is not registered for this use. As the use of postharvest chemicals on fresh fruits has received closer scrutiny in recent years, alternative non-chemical procedures for prevention of physiologi-cal disorders such as CO2-injury would be a useful
development in apple storage technology.
Alternative storage protocols may provide a means to reduce the risk of CO2-injury. While
rapid establishment of CA (Sharples and Munoz, 1974; Anderson and Abbott, 1975; Lau et al., 1983) improve post-storage quality of many apple cultivars, delaying establishment of CA or CO2
accumulation during storage reduces the inci-dence of CO2 injury (Bramlage et al., 1977;
Handwerker, 1979; Elgar et al., 1998). The inci-dence of external CO2-injury in ‘Bramley
Seedling’ apples was also reduced when CA es-tablished by fruit respiration and by flushing was delayed for 5 and 20 days, respectively (Colgan et al., 1999). Considering these previous reports, the objectives of the present study were to determine if delayed establishment of CA or CO2
accumula-tion reduce the incidence of CO2 injury while
maintaining acceptable fruit quality of ‘Fuji’ ap-ples.
2. Materials and methods
‘Fuji’ apples (MalusX domestica Borkh.) were harvested 173 and 177 days after full bloom in 1997 and 1998, respectively, from a commercial orchard in Orondo, WA. The fruit were placed into 0.145 m3 stainless steel chambers and cooled
to 0.5°C within 36 h of harvest. Fruit were stored at 0.5°C in RA, or in CA at 1.5 kPa O2+0.05
kPa CO2or 1.5 kPa O2+3 kPa CO2under static
conditions. Establishment of CA conditions was initiated 36 h after harvest and atmospheres were established within 72 h of harvest (rapid CA). Chamber O2 and CO2 concentrations were
moni-tored and corrected automatically (Techni-Sys-tems) at 90 min intervals. Atmospheres were established and maintained using compressed air and CO2 plus N2 from a membrane generator
system (Permea). Hydrated lime [Ca(OH2)] (0.1
kg per kg fruit) was placed in chambers to help maintain the CO2 concentration at 0.05 kPa. For
the CA delay treatments, fruit were held in RA at 0.5°C for 2 – 12 weeks after harvest, and then CA (1.5 kPa O2+3 kPa CO2) was established and
maintained for the remainder of the 8 month storage period. For the CO2 delay treatments,
fruit were stored in 1.5 kPa O2+0.05 kPa CO2
Fig. 2. Firmness and titratable acidity of ‘Fuji’ apples harvested in 1997 and 1998 and stored at 0.5°C in air or controlled atmosphere with 1.5 kPa O2+3 kPa CO2or 1.5 kPa O2+0.05 kPa CO2. Values are means of 18 fruit. Vertical bar indicates LSD0.05 for significant treatment×days interaction.
for 1, 2, 3 or 4 months after harvest, then CO2
was increased to 3 kPa for the remainder of the 8 month storage period.
Maturity and quality were determined for indi-vidual fruit at harvest and after storage by analy-ses of fruit respiration rate, internal ethylene concentration (IEC), flesh firmness, soluble solids content (SSC) and titratable acidity (TA). There were three replicate 1 kg samples for respiration analysis, all other analyses used 18 individual fruit. For respiration analyses, fruit were placed into 20 l chambers at 20°C supplied with com-pressed, ethylene-free air flowing at 100 ml min−1
. Effluent air was analyzed for CO2using a
gas chromatograph (Hewlett Packard 5890) equipped with a methanizer (John T. Booker), flame ionization detector and a 0.6 m, 2 mm i.d. stainless steel column packed with 80 – 100 mesh Poropak Q (Supelco). Oven, detector, methanizer and injection temperatures were 50, 200, 290 and 150°C, respectively. Gas flows for N2, H2 and air
were 70, 30 and 300 ml min−1, respectively.
Inter-nal ethylene concentrations of individual fruit were measured on gas samples removed from the
fruit core (Williams and Patterson, 1962) using a gas chromatograph (Hewlett Packard 5880A) equipped with a flame ionization detector and a 0.5 m, 3.2 mm i.d., glass column packed with 80 – 100 mesh Poropak Q. Oven, detector, and injection temperatures were 90, 200 and 100°C, respectively. N2, H2, and air flows were 25, 25,
and 300 ml min−1, respectively. Flesh firmness
was measured on two pared surfaces per fruit using a penetrometer with an 11 mm tip (Lake City Technical). Determination of SSC and TA used juice freshly prepared with a Champion juicer (Plastaket Mfg.). A refractometer (Atago) was used to measure SSC and TA was determined by titrating 10 ml of juice with 0.1 M KOH to pH 8.2 using an autotitrator (Radiometer).
Severity of watercore, CO2-injury (wet, well
-L.Argenta et al./Posthar6est Biology and Technology20 (2000) 221 – 229 224
Fig. 3. Watercore (A) and development of CO2-injury (B) in ‘Fuji’ apples. (A) Apples were stored at 0.5°C in air, 1.5 kPa O2+3 kPa CO2 or 1.5 kPa O2+0.05 kPa CO2. (B) Apples stored in 1.5 kPa O2+3 kPa CO2. Pooled data from 1997 and 1998 seasons is presented. Both watercore and brown-heart were scored using a scale from 1 (none) to 4 (severe). Incidence of cavities was rated as 1 (none) or 2 (present). Vertical bar indicates LSD0.05for significant treatment×days interaction.
injury was scored as: (1) none; (2) 1 – 30% of flesh (cortex and pith) dark brown; (3) 31 – 60% of flesh dark brown; and (4) 61 – 100% of flesh dark brown. Incidence of cavities was rated as absent (1) or present (2). Flesh browning and core flush were assessed as: absent (1), slight (2) and severe (3).
Data were analyzed using SAS ver 6.12 (SAS Institute, 1992). Treatment effects were analyzed by the ANOVA procedure and treatment mean separation was determined using Fisher’s pro-tected LSD or Duncan’s multiple range tests (PB
0.05).
3. Results and discussion
3.1. Physiological and quality changes during storage
Increased internal ethylene concentration (IEC) in RA-stored fruit was initially detected after 1 month storage (Fig. 1). IEC and respiration rates remained low in CA-stored fruit similar to previ-ous reports (Fan, 1992; Jobling and McGlasson, 1995). Fruit stored in CA with 1.5 kPa O2 and 3
kPa CO2 for 8 months had lower IEC but similar
respiration rate compared with fruit stored in CA with 1.5 kPa O2+0.05 kPa CO2.
Firmness and TA of CA and RA fruit were similar after 2 months (1997) and 4 months (1998) storage (Fig. 2). After 6 and 8 months storage, firmness and TA were higher in CA- compared to RA-stored fruit. High (3 kPa) CO2 was more
effective than low (0.05 kPa) CO2 in maintaining
firmness and TA during long-term storage. Short-term CA storage may have minor beneficial ef-fects on maintenance of firmness and acidity of ‘Fuji’ apples (Drake, 1993), but high CO2 is
re-quired to maintain quality during long-term stor-age. Relatively high CO2 concentrations retard
softening and acidity loss during low O2 CA
storage of most apple cultivars (Fidler, 1973). In both seasons, dissipation of watercore was slower in CA- than in RA-stored fruit while symptoms of internal CO2-injury (brown-heart)
were first observed after 15 days of CA storage (Fig. 3). The severity of CO2-injury increased
Fig. 5. Severity of CO2-injury in ‘Fuji’ apples harvested in 1997 and 1998. Apples were stored for 8 months at 0.5°C in air or in controlled atmosphere (CA). Rapid CA: Fruit cooled within 36 h of harvest and CA established within 72 h of harvest. CA delay: Fruit held at 0.5°C in air for 2 – 12 weeks then moved to CA with 1.5 kPa O2+3 kPa CO2. CO2delay: Fruit cooled to 0.5°C within 36 h of harvest and CA established within 72 h of harvest. Fruits held in CA with 1.5 kPa O2+0.05 CO2kPa for 1 – 4 months then moved to CA with 1.5 kPa O2+3 kPa CO2. Severity of CO2-injury was rated as 1 (none) to 4 (severe). Values are means of 18 fruit per treatment. Bars with the same letter are not significantly different (Duncan’s Multiple Range Test,PB0.05).
during the first 4 months of storage then remained constant for the remainder of the storage period. Cavities in cortical tissue were detected after 6 months storage. The symptoms of CO2-injury
(wet, dark browning in fruit mesocarp) may give rise to typical cork-like cavities as desiccation of damaged tissue occurs during storage (Wilkinson and Fidler, 1973).
Core flush and flesh browning were detected after 4 (1997) and 6 (1998) months storage (Fig. 4). Core flush did not occur in CA-stored fruit
while flesh browning occurred in RA- and CA-(1.5 kPa O2+0.05 kPa CO2) stored fruit in both
L.Argenta et al./Posthar6est Biology and Technology20 (2000) 221 – 229 226
tissue and was often associated with browning of vascular tissue. In CA- (1.5 kPa O2+0.05 kPa
CO2) stored fruit, the symptoms of flesh browning
(diffuse, light browning in the fruit flesh) were similar to that described for ‘Delicious’ apples (Meheriuk et al., 1994). Flesh browning resembles senescent breakdown in appearance and is more predominant in fruits with severe watercore, fruit harvested over-mature, large fruit, fruit grown in
locations with cool temperatures and in some cases in CA-stored fruit (Meheriuk et al., 1994).
3.2. Effects of delayed CA or CO2
Delaying CA establishment (1.5 kPa O2+3
kPa CO2) for 2 – 12 weeks resulted in a significant
reduction in the severity of CO2-injury (Fig. 5).
Fruit harvested during 1998 required a longer
Fig. 7. Firmness and titratable acidity in ‘Fuji’ apples harvested in 1998. Apples were stored for 8 months at 0.5°C in air or in controlled atmosphere (CA). Rapid CA: Fruit cooled within 36 h of harvest and CA established within 72 h of harvest. CA delay: Fruit held at 0.5°C in air for 2 – 12 weeks then moved to CA with 1.5 kPa O2+3 kPa CO2. CO2delay: Fruit cooled within 36 h of harvest and CA established within 72 h of harvest. Fruits were stored in CA with 1.5 kPa O2+0.05 kPa for 1 – 4 months then moved to CA with 1.5 kPa O2+3 kPa CO2. Values are means of 18 fruit per treatment. Bars with the same letter are not significantly different (Duncan’s Multiple Range Test,PB0.05).
delay to reduce injury severity than fruit harvested during 1997. Delaying CO2 (3 kPa) accumulation
for 1 – 4 months during CA (1.5 kPa O2+0.05
kPa CO2) storage also reduced the development
of CO2-injury symptoms in both seasons. Delayed
CA or CO2 accumulation allowed greater
disap-pearance of watercore during storage compared to rapid CA (Fig. 6). There was development of mild flesh browning (average rating 1.5) during the 1997 season, but there were no treatment
differ-ences (data not presented). The severity of flesh browning during the 1998 season was highest in RA-stored fruit and in fruit subjected to the longest CO2delay (Fig. 6). Fruit stored in CA (1.5
kPa O2+3 kPa CO2) delayed for 2 – 8 weeks did
not develop flesh browning. Firmness and acidity loss during eight months of storage increased with delayed establishment of CA or CO2
accumula-tion (Fig. 7). Delayed CA or CO2 accumulation
L.Argenta et al./Posthar6est Biology and Technology20 (2000) 221 – 229 228
2.3 – 6 N, during 1997 and 1998, respectively) and TA (8 – 13% and 6 – 20%, during 1997 and 1998, respectively) compared to fruit stored in CA with 3 kPa CO2 established immediately after harvest.
However, delaying CA or CO2 resulted in higher
firmness and TA compared to fruit stored in CA with 0.05 kPa CO2 established immediately. After
8 months of storage, the firmness and TA of fruit stored after CA or CO2delay were approximately
the same of those fruit stored in CA with 1 kPa CO2
established immediately (data not presented). Rapid cooling (Smock and Blanpied, 1963) and rapid establishment of CA conditions (Sharples and Munoz, 1974; Anderson and Abbott, 1975; Olsen, 1980; Little and Peggie, 1987) are important for maintenance of fruit quality for many apple cultivars. However, delaying CO2 accumulation
can reduce the incidence of CO2injury in
suscepti-ble cultivars (Bramlage et al., 1977; Handwerker, 1979; Watkins et al., 1997; Elgar et al., 1998; Colgan et al., 1999). Most of the CO2-injury in
‘Fuji’ apples developed during the first month of storage (Fig. 3) and 2 – 6 weeks of CA delay or 4 weeks of CO2delay significantly reduce the severity
of CO2-injury (Fig. 5). These results confirm
previ-ous studies with ‘Bramley Seedling’ (Colgan et al., 1999) and ‘Braeburn’ apples (Elgar et al., 1998) where incidence and severity of CO2disorders were
decreased by storing fruit in air at 0°C for 2 – 3 weeks prior to establishment of CA conditions. While delaying CA or CO2 accumulation reduces
development of CO2induced disorders, the delays
may increase the chance that development of senes-cent diffuse flesh browning in ‘Fuji’ (Fig. 6) and coreflush in ‘Braeburn’ apples (Elgar et al., 1998) will occur.
The results of the present study indicate that susceptibility of ‘Fuji’ apples to CO2-injury is
highest during the first weeks of storage after harvest, and that delaying CA or CO2
accumula-tion in the storage environment reduces the inci-dence of CO2-injury. The delay can result in
increased loss of firmness and TA, however, the additional quality loss is not sufficient to negate the benefits of CA compared to fruit stored in RA. Delaying establishment of CA or CO2after harvest
may be a practical strategy to reduce CO2-injury,
but the delay should be as short as possible to
preserve the beneficial effects of CA on fruit quality and control of other physiological disorders such as flesh browning. The period of CA or CO2-delay
required may vary between seasons (Fig. 5). As the susceptibility of apples to CO2 injury varies
be-tween seasons and orchards (Elgar et al., 1998; Lau, 1998) a reliable method to segregate fruit by susceptibility to CO2injury would allow
determina-tion of the period of CA or CO2 delay necessary
for each lot of fruits. ‘Fuji’ apples are more tolerant to high CO2 during the later storage period
(Ar-genta, unpublished data), therefore new strategies for ‘Fuji’ CA storage may reduce CO2-injury
dur-ing early period of storage and also reduce energy costs of CO2 removal during the later storage
period.
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