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Postharvest handling of “etrog” citron ( Citrus medica , L.) fruit

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Citron (Citrus medica, L.) fruits (“etrog” in Hebrew; plural “etrogim”) are used ritually in the Jewish holiday of Sukkot (Tabernacles), and can command as much as US$100/fruit, depending on quality. The etrog is unique among citrus fruits in that only the external attributes are of commercial importance. Maintaining physical fruit quality mandates the use of protective cushioning on the tree, at harvest, and in packaging. Growers use a wide range of chemical treatments post-harvest to reduce to a minimum the possibility of disfiguring insect or disease infestations. Most etrog varieties are highly susceptible to chilling injury if stored at less than 12°C. Etrogim lose water readily during storage, so fruit are stored and almost always marketed in plastic bags that limit water loss. Skin color is regulated with applications of ethylene or gibberellin, depending on whether specific markets prefer fruit that are greener or more yellow.
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Israel Journal of Plant Sciences
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Postharvest handling of “etrog” citron (Citrus
medica, L.) fruit
Joshua D. Klein, Yonit Raz Shalev, Shlomo Cohen & Elazar Fallik
To cite this article: Joshua D. Klein, Yonit Raz Shalev, Shlomo Cohen & Elazar Fallik (2016)
Postharvest handling of “etrog” citron (Citrus medica, L.) fruit, Israel Journal of Plant Sciences,
63:1, 64-75, DOI: 10.1080/07929978.2016.1159409
To link to this article: http://dx.doi.org/10.1080/07929978.2016.1159409
Published online: 11 Apr 2016.
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Postharvest handling of etrogcitron (Citrus medica, L.) fruit
Joshua D. Klein
a
, Yonit Raz Shalev
a
, Shlomo Cohen
b
and Elazar Fallik
c
a
Institute of Plant Sciences ARO-Volcani Center, Bet Dagan, Israel;
b
Institute for Agriculture according to the Torah, Yad Binyamin, Israel;
c
Institute of Postharvest and Food Sciences ARO-Volcani Center, Bet Dagan, Israel
ARTICLE HISTORY
Received 10 November 2015
Accepted 18 February 2016
ABSTRACT
Citron (Citrus medica, L.) fruits (etrogin Hebrew; plural etrogim) are used ritually in the Jewish
holiday of Sukkot (Tabernacles), and can command as much as US$100/fruit, depending on quality.
The etrog is unique among citrus fruits in that only the external attributes are of commercial
importance. Maintaining physical fruit quality mandates the use of protective cushioning on the
tree, at harvest, and in packaging. Growers use a wide range of chemical treatments post-harvest
to reduce to a minimum the possibility of disguring insect or disease infestations. Most etrog
varieties are highly susceptible to chilling injury if stored at less than 12C. Etrogim lose water
readily during storage, so fruit are stored and almost always marketed in plastic bags that limit
water loss. Skin color is regulated with applications of ethylene or gibberellin, depending on
whether specic markets prefer fruit that are greener or more yellow.
KEYWORDS
Fruit storage; hue angle;
chilling injury; storage
temperature
Introduction
Citron (Citrus medica, L.) fruits, together with myrtle,
willow and palm branches (known collectively as the
Four Species), are held and waved as one of the rituals
of the seven-day Jewish holiday Sukkot (Tabernacles;
Leviticus 23:40), which occurs in the period between
mid-September and mid-October. There are a number
of varieties of citron, with shapes ranging from spheri-
cal to ovate to highly irregular nger citronsand
sizes ranging from 100 g to 35 kg (Klein 2014). The
citrons origin is in southwest Chinanortheast India,
where it is used medicinally, and although citrons are
also grown for the confectionary and baking trade,
the major use of fresh fruit is for Jewish ritual (Klein
2014). The spread of citron from Asia to the Mediterra-
nean Basin and to the Arabian Peninsula more than
2000 years ago has been tied both to Persian inu-
ence on Jewish culture and to Jewish exile from the
Land of Israel (Isaac 1959; Nicolosi et al. 2005; Langgut
et al. 2013). Specic varieties of citron that are grown
for Jewish ritual are called etrogin Hebrew (plural
etrogim) and have their origin in Jewish communi-
ties in Morocco, Italy, Yemen, and Greece, as well as
pre-state Israel. There are approximately 100 ha of
etrogim grown in Israel, with another 100 ha grown in
small plots in Morocco, the USA, Italy, Greece, and
Mexico. The major varieties are Chazon Ish (also called
Halperin or Kivilevitch), which originates from a seed-
ling in pre-state Israel; Calabri, originating in Italy;
Temani, from Yemen; Urdang (also known as Barash)
and Braverman, varieties that are older than Chazon
Ish and which also originate from pre-state Israel; and
Moroccai, from Morocco, and which surprisingly, con-
sidering its geographic origin, is closely related to
Temani (Nicolosi et al. 2005; Shapovalov 2011). Con-
sumer demand for etrogim is approximately 1.8 million
fruit per year (H. Kirschenbaum, personal communica-
tion), and is increasing as more Jews around the world
observe the ritual. Supplying high-quality etrogim to
Jewish communities in northern Europe, North Amer-
ica and the southern hemisphere mandates the devel-
opment of postharvest technology for treatment,
storage, and transport of the fruit.
Postharvest treatments for storage of citrus crops
have been used commercially for more than 100 years
(Reuther 1989). Thiabendazole (Kellerman et al. 2014)
and intermittent warming (Cohen et al. 1994) to pro-
long storage and avoid chilling injury and maintain
quality in lemons, and oiled or chemically treated
papers were used to individually wrap and protect
CONTACT Joshua D. Klein vcjosh@volcani.agri.gov.il
Contribution no. 5/2016 of the ARO, Volcani Center, Bet Dagan, Israel.
© 2016 Informa UK Limited, trading as Taylor & Francis Group
ISRAEL JOURNAL OF PLANT SCIENCES, 2016
VOL. 63, NO. 1, 6475
http://dx.doi.org/10.1080/07929978.2016.1159409
grapefruit and oranges for nearly a century (Eckert &
Eaks 1989; Reuther 1989). Degreening of oranges and
lemons with ethylene to attract consumers is also a
well-established practice (Grierson & Newhall 1960).
Postharvest treatments to prevent fungal, bacterial,
and insect attack in storage are carried out universally,
usually employing thiabendazole, imazalil, and
sodium ortho-phenyl-phenol (SOPP) in various combi-
nations (Erasmus et al. 2015). Growers who produce
organic produce can use physical methods of pest
and pathogen removal and protection such as a hot-
water brushing machine (Porat et al. 2000; Fallik
2011), biological methods such as applications of pro-
tective yeast cultures (Droby et al. 1998), or combina-
tions of microorganisms and physical treatments such
as salts, UV light or temperature (Talibi et al. 2014).
Some citrus fruit can be stored for up to 68 months
after harvest, depending on variety and storage condi-
tions. Consumer demand for fresh citrus is steady
throughout the year (Gao et al. 2011).
In contrast to oranges, lemons, grapefruit, and other
citrus fruit, consumer demand for etrogim is so limited
to a specic time of year that the standard paradigms
for fruit storage are not relevant. Citrons, like lemons,
have two major ushes of owering, one in early
spring (FebruaryMarch) and one in the summer, with
a lesser intermediary ushinlatespring(Klein2014).
Etrogim from the early ushcanbeharvestedinlate
Juneearly July, although the quality of these bikker
(early, in Arabic) fruit is often considered inferior
because of irregular shape and peel texture. Fruit from
the tenne bettenintermediary ush are harvested in
July. Meah(literally, water) fruit of the later ush
(so called because growers often irrigate the orchards
more heavily to get the fruit to marketable size in time
for the Sukkot holiday) have superior quality and are
harvested from late July up until the holiday itself, as
there is a very minor but seemingly necessary market
for fruit to replace etrogim that become unsuitable for
religious use during the holiday. The market for etro-
gim is exclusively in early fall, with a very minor confec-
tionery market, mostly using fruit that was too small at
the time of Sukkot, but which later reaches sufcient
size to be processed and marketed as sugar-infused sli-
ces for Tu BShvat, the New Year of the trees, in mid-
January (Klein 2014). The storage period required of
the vast majority etrogim is therefore limited to a maxi-
mum of 34 months from late June at the earliest to
early October at the latest.
Etrog quality is subjective, depending on the
desires of a particular consumer or group of consum-
ers. Because the citron is an ancient fruit (Barkley et al.
2006), it has considerable phenotypic plasticity, which
does not always correspond to the religious or aes-
thetic standards of consumers. It is estimated that as
much as 1000 tons of etrogim are discarded annually
during sorting after harvest, mostly for aesthetic rea-
sons. All consumers desire fruit that is uniformly either
pyriform or ovate in shape, weighing at least 100 g
(and usually 150250 g), and without any blemishes
from thorns, limb or leaf rubs, insects, or disease. The
peel of etrogim varies in texture by variety, from
smooth to slightly bumpy to extremely warty, but a
high-quality fruit will be uniform in peel texture, with-
out irregular protrusions. The axis dened by the stem
and stylar ends of the fruit should be straight. Some
consumers prefer fruit with a prominent residual style
(called a pitamin Hebrew) while others seek fruits
without a style, as long as it is clear that the style
abscised naturally and was not broken. Peel color can
be light green or yellow, depending on consumer
preference, as long as the color is uniform. Aestheti-
cally perfect fruits command a considerable premium;
the retail cost of a standardetrog is US$520, but
there are thousands of fruit that are sold each year at
US$50100 each.
Etrogim are stored either on the growers property,
or more frequently in storage rooms near the main
wholesale markets of Bnei Braq and Jerusalem. Some
fruit are shipped overseas by boat to major markets in
Europe (Paris) or North America (New York, Los Angeles)
and arrive as early as 4 weeks before the holiday, while
in most cases fruit are sent by air closer to the time of
the holiday itself (H. Kirschenbaum, personal communi-
cation). Sending fruit by ship and by horse-drawn cart
was of course the way etrogim were sent from Calabria
(Italy), Greece, and pre-state Israel when Jews were
spread more thinly in the Diaspora and lived in areas
where etrog trees could not grow readily (northern and
central Europe, Russia, North America), but the resultant
quality of fruit would not be accepted in any Jewish
outpost these days. The desired quality of even a low-
cost studentor youthetrog is such that exquisite
care must be taken to protect the fruit from both physi-
calandphysiologicaldamageonitswaytobeingused
for7or8daysatmost.
Because the demands for quality of etrogim are so
stringent, and because the cost of production even
ISRAEL JOURNAL OF PLANT SCIENCES 65
with conventional orchard and postharvest practices
is so high (largely because of the huge amount of
hand labor involved in production, harvesting, and
packing), there is no such thing as a commercial
organic etrog orchard. Such an orchard would have
unimaginably high rates of discarded fruit, because
external blemishes that consumers of organic produce
are willing to overlook would be considered obstacles
to performing the mitzvah (religious commandment)
of the Four Species in the case of etrogim. Etrog
growers therefore employ the same postharvest
chemical treatments that other citrus producers use
(usually SOPP, imazalil, thiabendazole), often at the
highest allowed dosage in order to ensure as much as
possible that postharvest diseases do not affect the
fruit. Growers of other citrus are concerned about
both internal and external postharvest quality of the
fruit. Etrog producers are only concerned with maxi-
mal preservation of external fruit quality, and there-
fore their procedures differ from other citrus growers
in ways of protecting the fruit from physical damage
and in regulating the color of the skin.
Physical treatments and protection
from water loss
Even slight physical pressure can result in unsightly
marks on etrog peel within 12 hours or less, which
means that fruit must be harvested with great deli-
cacy. The marks become more pronounced over time,
and can ultimately become weakened, water-soaked
and a host site for pathogens. Etrogim often grow in
clusters of 37 fruit (Figure 1), although some grow at
the end of long exible stems that wave in the slight-
est breeze (Figure 1). Growers often thin excess fruit
at different stages of development, removing those
that show signs of being less than perfectly shaped. In
order to maintain the remaining fruit in acceptable
condition during the growing season, fruit-bearing
branches are often tied with twine to a frame sur-
rounding the tree. This prevents excessive movement
due to wind, and helps reduce incidence of blemishes
caused by other fruit, limbs, thorns, and leaves.
Growers often also place protective small foam cush-
ions between fruit on a cluster, or put stockings of
expanded polystyrene on the fruit itself (Figure 1), in
addition to tying the stem, especially if two high-qual-
ity fruits would otherwise touch and rub against each
other (Klein 2014). Fruit are clipped from the tree with
Figure 1. Single (top) or multiple (middle) citron fruit clusters
with polystyrene protection against limb-, leaf-, or self-abrasion.
Fruit at the bottom is in need of protection from thorns.
66 J. D. KLEIN ET AL.
a12 cm stem, and are placed directly (and carefully)
in citron-shaped exible foam inserts (10 or 12 etro-
gim in a single layer per box) for transport to the pack-
ing house (Figure 2).
The most important physical aspect of postharvest
treatment and protection of etrogim is the prevention
of water loss from the fruit. Etrog peels are quite rigid,
which allows for maintenance of fruit shape even if
there has been signicant water loss. This is particu-
larly the case with the fruit harvested from the early
(bikker) wave of owering, although such fruit are
not always marketed. On the other hand, fruit har-
vested from the second (meah) major wave of ow-
ering often achieve their size by intensive irrigation
before harvest. The size of the fruit is therefore due to
water-induced swelling of the cells, rather than to the
accumulation of dry matter. Such fruit can lose water
after harvest, and in extreme cases of >10% water
loss can actually appear slightly shriveled. Many types
of citrus fruits are coated before storage with natural
or synthetic waxes such as TAG(which has been
used in Israel for more than 50 years) (Gassner et al.
1969), in order to prevent water loss as well as fungal
attack (Haigenmeir & Baker 1994). However, there is a
religious concept of hatzitza(physically intervening
material), whereby the Four Species must be held
directly in the hand without an intervening layer or
object, be it tellin straps, a cloth, or a silver handle
(Sukka 37a, Shulchan Aruch 451:7, Hishukei Hemed
417419). Therefore, many religious authorities and
kashrut supervisors including the Eida Haredit (per-
sonal communication) recommend not using etrogim
that have been coated with wax.
At the packing house, harvested fruit are divested
of their individual expanded polystyrene protective
sleeves, if they were used in the orchard, before being
sorted and graded. Fruit are then often placed in indi-
vidual plastic bags to protect against water loss
(Figure 3). Bagged fruit can be stored and shipped in
foam-lined trays (Figure 2), or in individual protective
expanded polystyrene socks that are packed in single-
layer cartons or in individual retail boxes that are then
packed in cartons for shipment. In some cases, fruit
are placed bare in protective socks, packed in multiple
layers in a single carton, and the carton itself is placed
in a plastic bag for shipping and storage. There is no
Figure 2. Citrons harvested directly into cartons with foam inserts that can hold 1012 fruit in coddled comfort. Note that insert on the
left has ample room for the pitam(the residual style that for many is the ne plus ultraof etrog beauty).
ISRAEL JOURNAL OF PLANT SCIENCES 67
need to use individual plastic bags when such fruit are
repacked in individual retail boxes with foam inserts,
as the Sukkot holiday is usually imminent.
Although plastic bags can prevent water loss, they
can also cause undesirable effects. At temperatures
greater than 4C, fruit often tend to sweatin
enclosed storage. If fruit are stored in plastic that is
highly impermeable to water vapor (such is the case
with polyethylene, the most common plastic used for
such bags), the humidity will rise in the bag, and water
droplets will form on the fruit, providing an excellent
substrate for any pathogens whose spores are pres-
ent. This is why growers are very careful to treat etro-
gim with postharvest fungicides and pesticides. In
addition to being a barrier to water vapor, plastic bags
can limit gas exchange between the fruit and the
ambient environment. As the fruit consumes oxygen
in the bags atmosphere through respiration, CO
2
accumulates. If enough CO
2
accumulates, the fruit can
switch to anaerobic respiration and begin producing
ethanol and acetaldehyde, which at high levels can
cause physical damage to fruit (Prange & DeLong
2006). If pathogens accumulate, the fruit can sustain
physical damage that results in the generation of
wound ethylene (McManus 2012), which in turn will
trigger fruit yellowing or even abscission of the stem,
the latter of which disqualies the fruit from ritual use.
A low-level accumulation of CO
2
can also simulate the
effect of ethylene, resulting in fruit yellowing and
stem abscission, although high levels of CO2 can
inhibit ethylene action (Sisler & Wood 1988). The mere
act of handling etrogim after harvest induced ele-
vated amounts of CO
2
and ethylene in both Temani
and Chazon Ish fruit (Figure 4). However, the gases
did not reach concentrations that would induce physi-
ological activity in the fruit, and the rates of produc-
tion decreased considerably within ve days, even at
20C(Figure 4).
Hot-water brushing is a recently developed post-
harvest treatment that is designed to remove posthar-
vest pathogens from the fruit surface, and which
often also results in a reduction in fruit shrinkage due
to postharvest water loss, as well as a decrease in chill-
ing injury in susceptible crops (Fallik 2011). While
most fruits can easily withstand the gentle brushing
and rolling movement that is associated with any fruit
treatment on a conveyor belt, the volatile oil glands
on the peel of etrogim are particularly sensitive to
pressure. Fruit treated with hot-water brushing at
45C, a mild method which has been successfully
used in a range of tropical and subtropical fruit includ-
ing citrus (Fallik 2011), developed skin browning
Figure 3. From left to right: citrons immediately after harvest, after 6 months in 15C storage with no bag, bagged Calabriafter 6
months in 15C storage, bagged Temaniafter 6 months in 15C storage.
68 J. D. KLEIN ET AL.
within a week of storage. The browning was associ-
ated with damaged oil glands on the peel. Brushing
fruit at 38C did not curb water loss over 12 weeks
storage, and even slightly increased chilling injury in
Temani etrogim (Table 1). Placing fruit in plastic bags
reduced water loss considerably and chilling injury to
a certain extent, but enhanced stem rotting. No signif-
icant synergism was found between hot-water brush-
ing and bagging fruit (Table 1). Hot-water brushing
did not induce greater production of CO
2
or ethylene
compared to control fruit (data not shown).
Two ways to regulate the atmosphere inside the
bag are to change the composition or density of the
plastic or to make microperforations in the material
(Rodov et al. 2010). Composition and density affect
the water vapor transmission characteristics of the
plastic material itself, while microperforations physi-
cally alter the barrier, regardless of the plastics prop-
erties. Microperforations ranging from 4 to 16 holes
per cm
2
did not affect weight loss of etrogim over one
month at 20C, nor was there a signicant effect on
peel color. Although CO
2
accumulation was inversely
proportional to microperforation density regardless of
the water vapor transmission rate of the plastic, there
was no consistent effect on peel color after storage
(Table 2). On the other hand, the density of the plastic
itself did affect weight loss, regardless of microperfo-
ration density, but did not affect color change or CO
2
accumulation.
Most growers use inexpensive high-density poly-
ethylene bags to store fruit. It is not unusual for the
humidity inside the bags to promote callus formation
on the cut pedicel. In extreme cases, rootlets may
form (Figure 5). Growers and shippers always clip the
stem to remove the calli rootlets before marketing the
fruit, whose quality is not affected by these growths.
Treating etrogim with 10 ppm copper chloride imme-
diately after harvest signicantly reduced callus for-
mation (Klein et al. 2013).
Many citrus fruits are susceptible to chilling injury if
stored at temperatures lower than 10C for longer
than six weeks (Wang 1990). Chilling injury begins
with the breakdown of cell membranes, and becomes
evident on a larger scale with sunken areas on the
fruit, which become discolored and soften. The soften-
ing is often hastened by opportunistic fungi that colo-
nize the weakened tissue and then spread to other
areas of the fruit. Although etrogim are stored for a
relatively short period of time compared to other
Figure 4. Ethylene and CO
2
production by Temani and Chazon
Ish etrogim in the rst ve days after harvest. Fruit were sealed
in jars for 4 hours each day to accumulate gases for measure-
ment. ND4§SE.
Table 1. Weight loss (%) in etrogim after hot-water brushing at
38C after harvest and subsequent storage at 16Cfor6or12
weeks. Weight loss is averaged over four etrog varieties (ND
4£12 fruit); chilling injury and stem rot are from Temani only,
after 12 weeks at 11C(ND12). Mean separation in columns by
LSD, pD0.05.
Weight loss (%)
6 weeks 12 weeks Chilling injury (15) Stem rot (15)
Control 7.2 a 12.1 a 2.3 a 1.1 b
Brush 7.2a 12.7 a 2.9 a 1.1 b
XF lm 5.5b 10.1 b 1.7 b 1.7 ab
Brush CXF 5.1b 9.6 b 1.9 b 2.2 a
Table 2. Effect of water vapor transmission and microperfora-
tion density in plastic bags on weight loss, peel color (hue),
color change since harvest and CO
2
production in Urdang citrons
after one month at 20C. ND10 fruit per treatment. Values fol-
lowed by different letters are signicantly different at pD0.05.
Water vapor
transmission
Perforations/
mm
2
Weight
loss (%) HueHuechange
CO
2
(ml/g/h)
High 4 7.2 a 90.2 a 29.4 a 5.6 a
8 7.2 a 96.0 a 26.6 a 3.5 b
16 7.0 a 94.8 a 29.0 a 2.3 c
Low 4 3.2 b 95.0 a 28.7 a 5.3 a
8 3.0 b 93.8 a 30.0 a 3.8 b
16 3.3 b 93.5 a 30.8 a 2.4 c
ISRAEL JOURNAL OF PLANT SCIENCES 69
citrus fruits, they are still susceptible to chilling injury,
which is inuenced both by storage temperature and
by variety of etrog (Figure 6). Temperatures lower
than 11C resulted in chilling injury in Chazon Ish etro-
gim after four months of storage, which would corre-
spond to the maximum commercial storage time of
bikkerfruit (Table 3). Chilling promotes color
change, usually to orange, in most varieties, in addi-
tion to inducing lesions. Delaying storage by holding
fruit at 17C for three days (Chaudhary et al. 2014)
before transfer to the nal storage temperature was
not consistently effective in reducing incidence and
severity of chilling injury in Chazon Ish etrogim held
at 6 or 8C(Table 3), nor did it maintain peel color
(Figure 7). The etrog variety least susceptible to chill-
ing injury is Calabri (Figures 7,8), which is also the
variety that is less genetically related to other types of
citron used for Sukkot (Nicolosi et al. 2005; Shapovalov
2011). Temani etrogim were most susceptible to chill-
ing injury (Figures 6,7,8), along with their genetically
close variety Moroccai (Nicolosi et al. 2005; Shapova-
lov 2011). Many growers use air conditioners in insu-
lated rooms to store fruit at »20C before shipment,
but some now hold them at 1718C, despite the
extra cost of electricity, to maintain superior quality
(especially reduced water loss) for a longer period of
time (Table 3).
Managing the color of etrogim
After fruit shape, the color of etrogim is the most
important quality parameter that inuences custom-
ers. Many customers in Israel prefer fruit that are light
green in color (Hueof »110115). According to the
Talmud (Sukka 31a), an etrog that is as green as a
leek, which seems to be a deeper green color (Hue
>120), is not acceptable for religious use. Many cus-
tomers in the Diaspora prefer fruit that are already yel-
low (Hue»8590). Because etrogim from the last
wave of owering ripen on the tree only towards the
end of autumn, it is imperative that growers be able
to manage color development in the harvested fruit.
For approximately 120 years, ethylene has been
considered the plant hormone most responsible for
ripening, especially for causing a change in citrus peel
color from green to yellow or orange (Grierson & New-
hall 1960). This change occurs naturally, but can take
place much more slowly than marketers would like.
Commercial use of ethylene for active degreening of
citrus began approximately 100 years ago, using kero-
sene lamps as sources of the gas, despite the potential
for explosions (Abeles et al. 1992). Much has been
learned since then about the physiology, biochemis-
try, and molecular biology of ethylene production and
action in plants (McManus 2012). Apples are a natural
source of ethylene, especially rapidly ripening varie-
ties such as Golden Delicious. Until relatively recently,
etrog growers would place Golden Delicious (but not
the slow-ripening Granny Smith) apples in non-air-
tight containers, such as leather suitcases, with green
etrogim, in order to induce yellowing of the peel (M.
Friedmann, zl, personal communication). In airtight
containers, CO
2
can accumulate in the atmosphere, in
turn inhibiting ethylene formation and decreasing the
rate of degreening, although growers were not aware
of the physiological mode of action of ethylene
(Abeles et al. 1992).
Figure 5. Desiccation and callus-root formation in pedicels of Urdang citrons held at 18C for two months without (left) or with (right)
polyethylene bags.
70 J. D. KLEIN ET AL.
Most modern etrog growers have small, purpose-
built insulated degreening rooms near their packing
house, into which they stream ethylene gas from a cyl-
inder outside the room. The temperature, exact con-
centration used and the period of exposure depend
on initial peel color and on variety, as some varieties
such as Temani turn yellow very quickly. Great care
must be taken that the fruit are not overdosedwith
ethylene, because the hormone also induces forma-
tion of abscission zones (McManus 2012), and both
the stem and the pedicel (pitam) can fall off, rendering
the fruit not kosher for ritual use. Most growers jeal-
ously keep secret the precise combination of ethylene
concentration and exposure time used in degreening,
but it is generally known that exposure to 5 ppm eth-
ylene for 1224 hours at »20C will initiate yellowing
of citron peel. Copper is a cofactor in the response of
plants to ethylene (Rodr
ıguez et al. 1999). Dipping
etrogim in solutions of copper chloride can also initi-
ate degreening (Klein et al. 2013).
While there is a denite market for yellow etrogim,
especially in the Diaspora, most Israelis prefer etrogim
that are light to medium green in color. Rather than
induce degreening, the goal of growers for the Israeli
market is to limit ripening. This is done by dipping
fruit in solutions of gibberellin (usually GA
3
), which
counteracts induction of chlorophyllase activity by
endogenous or exogenous ethylene (Fuji et al. 2008),
thus reducing the rate at which peel color changes
from green to yellow. With proper timing and dosage,
fruit will arrive at the market at the desired commer-
cial light green color. Fruit are also treated with GA to
prevent senescence-related abscission of the stem
after harvest, thus maintaining the kosher status of
the fruit. The bell-curvephenomenon is observed
with GA treatments in many crops (Aharoni 1989).
Figure 6. Etrogim with chilling injury lesions. Top: Yemenite after
12 weeks at 3C (left) or 8C; middle: Chazon Ish after 12 weeks
at 3C, 6 C, or 12C (left to right); bottom: Urdang.
Table 3. Effect of storage temperature, delayed storage (3 days at
17C) and presence or absence of a polyethylene bag on weight
loss, peel color and chilling injury in Chazon Ish citrons stored for
four months. ND15 fruit per temperature/bag combination.
Weight
loss (%)
Color
(hue)
Chilling
injury (15)
Temperature
regime (C) Bag CBag Bag CBag Bag CBag
6 6.5 0.7 92 96 2.5 2.9
17!6 10.5 1.1 91 96 2.8 2.3
8 5.2 1.4 86 87 2.9 2.2
17!8 5.9 0.9 85 86 2.0 2.2
11 12.1 1.4 85 83 1.0 1.0
17!11 14.6 1.5 84 83 1.0 1.0
17 47.1 9.7 85 89 1.0 1.0
20 57.0 11.3 89 88 1.0 1.0
ISRAEL JOURNAL OF PLANT SCIENCES 71
That is, neither a low nor a high dose of GA is effective
in preventing natural degreening; only an intermedi-
ate dose of 50 ppm GA maintained peel color of the
desired hue(Klein et al. 2013)(Figure 9).
Placing fruit in plastic bags can also delay color
change during extended storage (Figure 10), probably
by allowing for sufcient accumulation of CO
2
to
inhibit the activity of endogenous ethylene (Sisler &
Wood 1989) in inducing chlorophyllase activity
Figure 7. Effect of 3 days preconditioning at 16C after harvest on citron peel color after 3 months at 3C, 8C, or 12C. Preconditioned
Calabrietrogim of Italian origin developed appropriate color at 8C, and at 12C even without preconditioning. Temanietrogim of
Yemenite origin did not survive 3C even with preconditioning, and had chilling-related bronzing at 8C and 12C without
preconditioning.
Figure 8. Chilling injury in etrogim. Fruit were held at 20C (top)
or 11C (bottom) for four months. Note that all except Calabri
(Italy) turn orange as a symptom of chilling injury, and that most
have blotches or sunken areas. Yemenite turns orange even at
non-chilling temperatures.
Figure 9. Change in hue angle in Chazon Ish etrogim dipped in
0200 ppm gibberellin and held at 20C for 4 weeks. ND10 §SE.
Figure 10. Urdang citrons after four months at 12C in bags (left)
or at 17C without bags.
72 J. D. KLEIN ET AL.
(Azoulay-Shemer et al. 2008). However, the tempera-
ture of storage seems to have more effect on color
change than does the presence or absence of a plastic
bag (Table 3). The use of plastic bags can have a dra-
matic effect on fruit weight loss during storage, espe-
cially at temperatures greater than 11C(Table 3;
Figure 3), but were inconsistent in reducing pitting
associated with chilling injury (Table 3).
During the Shmita (sabbatical) year (Leviticus
25:36) in Israel, agricultural activities that improve the
yield of fruit trees are forbidden, as is charging market
prices, rather than just the cost of production, for fruit
that set and grew during the sabbatical year. Many reli-
gious consumers are wary of acquiring etrogim that
grew in Israel during Shmita, and prefer to use either
fruits that grew outside of Israel or fruits that grew
under special religious supervision in Israel (Jaffee
2015). In an effort to increase the supply of etrogim that
are not subject to the rules of Shmita, we demonstrated
that a certain percentage of bagged fruit could be
Figure 11. Citrons photographed after 12 months at 1718C in individual polyethylene bags (left) or immediately after harvest
(right).
Figure 12. Mr Eliezer Gorelick, an etrog grower from Kfar Habad, Israel, photographed in October 2014 with Calabrietrogim that were
just harvested (green, from September 2014) or that had been held in a polyethylene bag at ambient temperature in his ofce for one
year (yellow, from September 2013).
ISRAEL JOURNAL OF PLANT SCIENCES 73
stored for as long as 12 months at 1718C(Figure 11),
although previously this has been noted ad hoc with
commercially packed fruit (Figure 12). Such a storage
method was suggested as a means for growers to pro-
vide non-Shmita fruit for the Sukkot holiday immedi-
ately after the end of Shmita, and would allow farmers
to charge market prices. Because storing the fruit at
controlled temperatures in plastic bags maintains mois-
ture in the interior of the fruit, there is no concern that
the year-old fruit would dry out and be unsuitable for
religious use (Sukka 31a, Shulchan Aruch 648:1). How-
ever, growers feared that the yellow peel color was not
the usual shade found in the market in other years (it
was impossible to maintain green peel color for 12
months), and rejected the concept. Consumers are con-
ditioned to such a high level of quality in etrogim that
even the concurrent observance of another Biblical
commandment such as Shmita is not allowed to affect
punctilious observance of the commandment of the
Four Species.
The etrog is one of the three ancestors of all citrus
fruits (Barkley et al. 2006), and as such is an ancient
fruit with a rich botanical history. It is not known how
or if the Jews stored citrons for use during Sukkot in
ancient times, but it is known from the Talmud that
the fruits could get very large (Sukka 36b) and sturdy
(Sukka 48b) by the time of the holiday, and that they
had attained a certain degree of ripeness sufcient to
allow them to be eaten (Sukka 36a). In the centuries
since the time of the Temple, Jews have spread across
the globe and the citron has accompanied them in
appropriate climates (Isaac 1959; Nicolosi et al. 2005).
As the standard of living of Jews has increased, so has
their desire for etrogim of superior quality. The mod-
ern methods of postharvest technology have been
put to the service of this ancient fruit, so that Jews
everywhere can be certain of obtaining a quality etrog
for the observance of the mitzvah of the Four Species.
Acknowledgments
We are grateful to the growers who generously provided etro-
gim and packaging materials for our experiments: Hagai Kir-
schenbaum, Naif Abu-Muammar, Moshe Nyman, and Eliezer
Gorelik, to StePac Corporation for supplying specialty plastic
lms and to Dr Ron Porat for suggesting the temperature-delay
experiments.
Disclosure statement
No potential conict of interest was reported by the authors.
Funding
This research was partially funded by grant no. 277-0149 from
the Chief Scientist of the Ministry of Agriculture and Rural
Development.
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