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Controlling Fruit Ripening: A Review of the Role of Ethylene

Authors:
  • Cultivation Bioengineering LTD
Joseph Chidiac
11/23/2015
Plant Growth and Development Review
Controlling Fruit Ripening: A Review of the Role of Ethylene
Abstract:
Ethylene has long been considered to have a major role in the ripening of fruits, and
studies on tomatoes have generated a lot of information on ethylene synthesis and
sensitivity mechanism as well as the roles of other compounds and hormones in the
ripening process. Tomatoes, however, serve as a poor model for fruit ripening when it
comes to acquiring useful knowledge concerning the control of ripening of a variety of
fruits, as responses to ethylene and other effectors vary widely and are very much
dependent on crop species, treatment dosages, as well as environmental conditions.
Green tomatoes treated with ACC or PCIB had an accelerated color change and an
enhancement in carotenoid content and ABA, while treatment with IAA delayed and
prevented ripening and reduced carotenoids and ABA. In peaches, treatment with AVG
or select polyamines (ethylene synthesis inhibitors) had varying effects on ripening that
depended greatly on dosage, with most low dosage treatments delaying ripening and
maintaining flesh firmness longer than controls. Exogenous ethylene application
resulted in more rapid ripening and softening of papaya fruit compared to controls, and
1-MCP treatment prevented softening as well as endogenous ethylene evolution. Kiwi
fruit softened considerably after one week in cold storage; however 1-MCP treatment
delayed softening as well as ascorbic acid degradation with an effect proportional to the
treatment dosage. Treatment of unripe fig fruits with 1-MCP caused a 2.5 fold increase
in ethylene production compared to controls, and it affected the transcription of several
genes implicated in the ripening process at different stages. Therefore, further studies
into the effects of ethylene and inhibitors of its synthesis and action on the ripening of
each fruit crop will yield the information necessary to apply precise and effective
solutions to control this process in a desirable manner. Treating each fruit crop with a
higher number of different dosages of ethylene, polyamines, AVG, 1-MCP and other
compounds will help to clarify the importance of using the right dosage to obtain desired
results, as the same chemical treatment or storage conditions can have different or
opposite effects from one crop to another.
Introduction:
There is great diversity in the way fruiting plants nourish, disperse, and protect
their newly developed seeds. Some species form a simple, dry seed pod that bursts to
disperse seeds when they mature, while the fruiting plants typically chosen for
cultivation have larger, fleshy fruits, some of which have evolved complex textures,
aromas, and flavors to attract the fauna necessary for seed dispersal. The process of
forming these relatively substantial fruits varies from species to species, as does the
process of fruit maturation, also known as ripening (Barry and Giovannoni 2007).
Regardless of the apparent diversity in fleshy fruits, there are many aspects of fruit
ripening that are evolutionarily conserved between species. Those observed include the
production of aromatic compounds, color alteration, a change in fruit texture, and
increased susceptibility to infection. These similarities support the notion that the
genetic mechanisms for fruit ripening are also conserved between species (Giovannoni
2004). Many major fruit crops suffer from postharvest spoilage and rotting due to
uncontrolled ripening (Saltveit 1999), and the economic impact on farmers can be
severe. A lack of understanding of the underlying molecular mechanisms for fruit
ripening is delaying the widespread application of effective solutions and thereby
allowing large amounts of produce to be wasted.
In order to study these mechanisms, researchers have relied heavily on the study
of ripening tomato fruits. This is due to the tomato plant’s simple diploid genetics, a
short generation time, an easily scored ripening phenotype, as well as the fact that it is
some of the most highly studied and available germplasm with much about its genetics
known and tested through induced mutants (Mueller et al. 2005). In order to get a more
complete picture on fruit ripening, however, one must consider a number of different
species and the differences that make them unique.
While many of the enzymes involved in downstream regulation of ripening have
been well defined, such as cell wall hydrolases which are involved in carotenoid
synthesis and the metabolism of sugars as well as enzymes responsible for flavor and
aromatic compounds (Hirschberg 2001), less is known about the signals and pathways
that initiate fruit ripening or determine a fruit’s ability to ripen. However, due to the
molecular categorization of ripening impaired mutants, various hormones, such as
auxin, jasmonates, and brassinosteroids, have been implicated to promote ripening
(Manning et al. 2006; Symons et al. 2006; Vrebalov et al. 2002). Still, ethylene gas plays
an essential role as a hormone in fruit ripening (Lanahan et al. 1994), and can affect
fruit physiology whether the species is climacteric or non-climacteric (Giovannoni 2001).
This review of literature should substantiate claims that postharvest fruit spoilage
can be averted through the strategic control of ethylene in the fruit flesh and the storage
environment.
The objectives of the review will be to determine the role of ethylene in the
ripening of a selection of fruiting species, analyze the differences in their production of
and reactions to ethylene, as well as to summarize the current state of knowledge about
ethylene’s role in fruit ripening for the purpose of advancing preventative solutions.
Review of Literature:
The Effect of Ethylene on Fruit
Ethylene occurs naturally in plants, yet is only released into the surroundings in
sufficient amounts to affect neighboring tissues during wounding, disease, or fruit
ripening. Climacteric fruits are classically distinguished from non-climacteric fruits by
their increased ethylene synthesis and respiration during ripening (Lelievre et al. 1997).
Whether endogenous or exogenous in nature, ethylene has various effects on the
growth, development, and storage life of fruits even at very small concentrations, which
can be desirable or undesirable. It is important to note that ethylene often promotes its
own production in plants (Yang 1987), therefore controlling levels of this important
compound is crucial in maintaining crop quality. Saltveit (1999) summarizes the
observable effects of ethylene on fresh fruit. The beneficial effects include: chemical
thinning of fruit, aiding of harvest by induction of fruit drop, enhancing color and flavor
development, and accelerating ripening. For example, ethylene is used in tomato,
apple, cherry, citrus, cucumber, grape, guava, peach, pepper, and pineapple crops
among many others to induce or accelerate ripening (Abeles et al. 1992). The
detrimental effects of ethylene on fruit are much of the same under a different context.
Unintended ethylene exposure is considered a form of contamination and can lead to
accelerated senescence, excessive softening, increased phenylpropanoid metabolism,
and discoloration. One main reason ethylene is used as a controlled treatment for fruit is
to achieve the aesthetic standards that consumers demand; in apple, banana, and
pepper crops, for example, ethylene would be used to achieve the characteristic ripe
color before the fruit flesh has aged excessively, which can result in a higher quality of
produce. Ethylene applied for an overly extended period of time can lead to unwanted
softening, such as in cucumbers and peppers. In an experiment by Risse and Hatton
(1982), excessive flesh softening in watermelons occurred within three days of
exposure to 5 μL.L-1 of ethylene at 18°C. While ethylene application enhances fruit
flavor and aroma through promoting ripening (Watada 1986), total volatiles may be
reduced when compared to naturally ripened fruit (Stern et al, 1994).
Tomato as a Model
Tomato fruit ripening is directly controlled by ethylene and can be characterized by a
change in color from green to red which represents a degradation of chlorophyll and an
alteration of the carotenoid profile from xanthophylls, such as lutein and neoxanthin, to
carotenes, such as phytoene, lycopene, and β-carotene (Fraser et al. 1994). Apart from
ethylene’s well characterized role, auxins have also been implicated as having a
regulatory role in the ripening of tomato fruits. To investigate the significance of ethylene
and auxin effects on carotenoids in tomatoes, Su et al. (2015) treated mature green
fruits with indole acetic acid (IAA), aminocyclopropane carboxylic acid (ACC), or p-
chlorophenoxy isobutyric acid (PCIB). IAA is an auxin, ACC is the precursor of ethylene,
and PCIB is an auxin antagonist.
Tomatoes were harvested at the mature green stage and injected with a buffer
containing 100 μM of each treatment, after which they were stored at 26°C. Pericarps of
the fruits were taken after 24 and 96 hours and frozen at -80 °C. Surface color was
assessed by a chromameter. ABA and ethylene were assayed by ultra performance
liquid chromatography (UPLC) and mass spectrometry (MS). RNA was isolated and
underwent quantitative polymerase chain reaction (qPCR) using SI-actin as the
housekeeping gene.
Treatment with ACC significantly accelerated the change from green to red compared to
controls as did PCIB treatment, while IAA treatment caused a delay and fruits under this
treatment never became fully red. Fruits treated with both ACC and IAA experienced a
slower transition in color. The ACC and PCIB treatments also induced significant
changes in the profile of carotenoids after 96 hrs; lycopine, β-, α- and δ-carotene,
phytofluene, and Ϛ-carotene were enhanced, lutein was unaffected, and neoxanthin and
violaxanthin were reduced. Neoxanthin and violaxanthin are the precursors of abscisic
acid (ABA) which stimulates ethylene production and ripening. ABA content was
increased by the ACC and PCIB treatments and decreased by treatment with IAA. ACC
treatment was found to induce the transcription of Psy1 and inhibit that of β-Lcy1 and
Crtr-β2. IAA inhibits the transcription of numerous upstream carotenoid transcripts.
Peach Fruit Ripening: Ethylene and Polyamines
Aminoethoxyvinylglycine (AVG) is known to inhibit activity of ACC synthase (ACC),
which is responsible for converting S-adenosylmethionine (SAM). Ethylene and
polyamines have opposite effects on fruit ripening and senescence, though they both
share SAM as a mutual precursor (Li et al. 1992). Ethylene production has been
previously shown to be inhibited by exogenous polyamine application in fruits such as
orange and tomato. Bregoli et al. (2002) chose peach fruit as model to study how
applications of AVG and ployamines interfere with ethylene production and affect fruit
size, weight, and quality.
15 year old peach trees were sprayed with a product containing 15% AVG, or with the
polyamines putrescine, spermidine, or spermine (Sigma-Aldrich, Milano, Italy), and each
compound was sprayed at three different doses. To establish a growth curve, fruit
diameter was measured weekly on 50 untreated fruits. Treated fruits were sampled
weekly then every three days. Ten fruits were sampled per treatment during the
experiment, and fifty from each at harvest. Dry and fresh weights were measured for all
fruits sampled. Ethylene evolution was measured by placing individual fruits in sealed
jars and removing a small air sample for analysis by gas chromatography (GC). Fruit
flesh firmness was measured using a pressure tester, and soluble solid content (SSC)
was measured by placing juice from each fruit on a digital refractometer. Polyamines
were extracted and then separated by high performance liquid chromatography (HPLC);
peaks were detected by a spectrofluorometer. The activity SAMDC, the enzyme
producing SAM, was measured by the rate of CO2 evolution in an optimized buffer
solution.
The diameters of fruits never differed significantly between treatments, and the growth
curve of the control fruits was the normal double sigmoidal demonstrating four distinct
growth phases. The growth curve of each treatment differed, however only those treated
with spermidine and AVG weighed significantly less than the control fruits, as those
treated with putrescine and spermine had no significant weight differences from the
control. Ethylene emission from control fruits was detectable from day 5 and increased
an increasing trend, while fruits treated with AVG began to emit ethylene later and at
lower levels than controls. All polyamines reduced or eliminated ethylene production in
the final days of fruit growth. The highest concentration of spermidine actually induced
ethylene emission earlier than control fruits. Flesh firmness in control fruits began to
decline at day 90 and continued until harvest, while SSC gradually increased, especially
after day 106. AVG treatments delayed softening and nearly doubled flesh firmness
compared to control, while also resulting in significantly higher SSC as AVG dose
increased. Polyamines each decreased the rate of late stage softening, while only
spermidine treatments yielded a lower SSC than controls and both putrescine and
spermine resulted in no differences. Low doses of AVG resulted in no change in
endogenous polyamines, yet high dosages of AVG resulted in modest decreases in free
spermidine while enhancing soluble polyamines. Exogenous polyamines all resulted in
a notable decrease in endogenous polyamines when tested at days 11, 17 and 103,
while insoluble conjugates were unaffected. AVG significantly increased SAMDC activity
at low dosages and decreased it at high dosages. Spermidine was the only polyamine
to temporarily decrease SAMDC activity.
Papaya Fruit Ripening: Ethylene and 1-Methylcyclopropene
Cyclopropenes have recently been employed to inhibit the action of ethylene and
increase the shelf life of some climacteric fruits (Blankenship and Dole 2003). 1-
methylcyclopropene (1-MCP) is one of the most efficient ethylene inhibitors in this class.
Fabi et al. (2007) compared untreated papaya fruit with those treated with ethylene or 1-
MCP in terms of several parameters such as ethylene synthesis rates, respiration, pulp
firmness, as well as SCC and three major carotenoids.
Papayas were harvested at color break and randomly divided into three groups, one
treated with 100 ppm ethylene in a closed flow system, the second treated with 100 ppb
1-MCP, and the third left to ripen spontaneously as a control. In order to measure
ethylene production and respiration, individual fruits were placed in airtight containers
from which air samples were taken to determine their composition by GC. The pulp
firmness was measured using a texturometer, and the SSC were extracted in ethanol
then water and then analyzed by HPLC. Carotenoids were extracted into acetone and
then analyzed by HPLC and photodiode array (PDA).
In control fruits, endogenous ethylene peaked around day 4 after harvest and preceded
the respiration burst by one day. In papaya fruits treated with exogenous ethylene,
endogenous ethylene was slightly lower, but respiration was significantly higher than in
control fruits. 1-MCP treatment, however, resulted in the inhibition of endogenous
ethylene emission as well a great reduction in respiration. Fruit softening in control fruits
was simultaneous with the ethylene emission and evolution, while ethylene treated fruit
exhibited softening one day after treatment and 1-MCP treated fruit did not soften during
the experiment. All treatments resulted in similar SSC to the control fruits. Interestingly,
ethylene and 1-MCP treatment resulted in higher levels of sucrose than controls, but
similar fructose and glucose levels.
Kiwi Fruit Ripening: 1-MCP
Previously, the storage life of kiwi fruits has been extended by using an edible coating
consisting of numerous chemicals (Fisk et al. 2008), and it has been reported that kiwi
lost physiochemical quality over four weeks in cold storage due to the decrease in
ascorbic acid and phenolics (Krupa et al. 2011). Lim et al. (2016) sought to examine the
effects of 1-MCP on the postharvest quality of hardy kiwifruit.
Kiwifruit were harvested 85 days after flowering and stored at 1 +/- 0.5°C after one half
of fruits were treated with 1-MCP at 10°C. Fruits from each group were sampled at 0, 3,
and 5 weeks of storage. Sampled fruit were individually stored temporarily in individual
airtight containers, and a 1mL sample was drawn from each and analyzed by GC. Ten
fruits were randomly selected from each replication, macerated, and homogenized so
that the level of ascorbic acid could be isolated by HPLC and quantified by a diode array
detector at 255nm. Total phenolic content was measured by use of the Folin-Ciocalteu
reagent using gallic acid as a standard and absorption was measured at 765 nm.
1-MCP inhibited the ripening of hardy kiwifruits during cold storage and maintained
overall quality for up to five weeks, after which weight loss increased to 30% in the
control and 20% in the treated fruits. Control fruits showed a sharp decrease in firmness
after one week of cold storage. 1-MCP treatment extended the period to fruit softening
proportional to the applied dose. While ascorbic acid content decreased gradually for
both control and treated fruit, 1-MCP treatment slowed the degradation of ascorbic acid.
Transcripts of the ripening related genes AcACS, AcACO, and AcLOX were expressed
twice as much in controls, suggesting that 1-MCP is an inhibitor of the accumulation of
RNA for these genes.
Fig Fruit Ripening: ethylene and 1-MCP
Some recent research has even challenged the traditional definitions of climacteric and
non-climacteric fruit (Paul et al. 2012). Fig, for example, is classified as climacteric,
however, ethylene production in the fruit increases after pre- or postharvest treatment
with 1-MCP while no other effects are evident. Treatment of fruit on the tree will improve
the storage capabilities and combat deterioration of fruit quality. The fig is the only fruit
in the human diet with a unique inflorescence structure called the syconium, therefore it
is not unreasonable to think that some mechanisms for the ripening of this species may
differ from other common species. Freiman et al. (2015) characterize ethylene
production and the expression of potential ripening regulator, ethylene synthesis, and
signal transduction genes in on-tree ripened figs and those treated pre-harvest with 1-
MCP. They also sought to pinpoint the genes assumed to be responsible for the positive
effect of pre-harvest 1-MCP treatment.
Fruit of female fig trees were harvested from a commercial orchard and five
developmental stages were sampled. Formalin fixed longitudinal cross sections of the
fruit were used to demonstrate parthenocarpic drupelets. Seven fruits per stage and
treatment were sampled for ethylene production analysis. Total RNA was extracted and
concentration was determined by a spectrophotometer and newly isolated transcripts
were sequenced. High-throughput real-time quantitative PCR was performed to amplify
select genes from three biological replicated per stage and treatment.
In the tree-ripened figs, a rise in ethylene production was observed when fruit color
changed from green to yellow and it continued to increase until it peaked at the full
purple stage. Following 1-MCP treatment, ethylene production increased to 2.5 times
that of untreated fruit. Three MADS-box genes (FcMADS2, FcMADS3, and FcMADS8)
were upregulated from the yellow stage to the purple, and three genes (FcMADS4,
FcMADS5, and FcMADS6) were downregulated from the green stage to the yellow
stage. Post translational regulators of type 2 ACS proteins (FcEOL1 and FcEOL2)
showed peaks in their transcription at 10% and 50% purple stage. In the fig receptacles,
FcMADS2, FcMADS3, and FcMADS4 were downregulated from the yellow to purple
stages. FcMADS8 rose at the yellow stage and remained high. Both FcACS1L and
FcACS2 exhibited enhanced expression at 50% purple stage. There were marked
differences in expression patterns of ethylene-signal-transduction genes between the
receptacle and inflorescence. With the exception of FcETR1, there was no detectable
increase in ethylene receptor expression during ripening.
Discussion and Interpretation of Results
Ethylene is thought to have a general role in the ripening of fruit, and the conventional
differentiation is between climacteric and non-climacteric fruit. While ethylene often
does have a significant effect on fruit crops upon exposure, differences in the reactions
of different fruit species, and likely cultivars, elucidate that more investigation into the
different ways in which ethylene and other components play a role in the maturation,
ripening, and storage of different fruits is necessary. Our understanding of climacteric
and non-climacteric fruit changes when we analyze certain exceptions to accepted
rules, such as the fig; hence, a new categorization will inevitably follow further study into
ethylene’s role in the ripening of each fruit variety.
Tomato has commonly been used as a model for studying the process of ripening as
well as the roles of ethylene, auxin, and ABA due to our knowledge about its relatively
simple genetics and the availability of ethylene synthesis or sensitivity negative mutants.
However, tomato does not do well to represent the majority of fruit cultivated for human
consumption, in that it presents different reactions to ripening-affecting compounds, and
it makes use of different signal transduction pathways to cause specific changes in fruit
composition. While tomato is a good model for understanding basic ethylene synthesis
and sensitivity mechanisms, it does not accurately represent the unique interactions of
other fruit species with ethylene. Hence, studies into the respective processes of each
type of fruit will be necessary to achieve the level of knowledge needed for effective
control of plant physiology.
Dosage played a very important role in all treatments of ethylene, cyclopropenes,
polyamines, and AVG with different concentrations of each chemical treatment often
having opposite effects, indicating that further study into proper dosages for each
chemical treatment on each crop type would enhance producers’ ability to control
ripening and storage. While controlling the rate of ethylene evolution and softening is
favorable, many types of fruit treated with exogenous ethylene, cyclopropenes,
polyamines, or AVG were reported to have a lower consumer appeal than naturally
ripened fruit, suggesting that it will be necessary to understand more about the
molecular mechanisms of ripening and to develop newer and more effective chemicals
for controlling different aspects of the process. Alternatively, the control of fruit ripening
and storage ability can be achieved through a reduction of respiration by the alteration
of the growing or storage environment. With this in mind, we must note that some fruit
species have, in effect, opposite reactions to identical environmental conditions. A good
example is that cold storage accelerates the softening of kiwi while it extends the
softening period for apples and peaches.
What has been substantiated by all reviewed studies is that, when concerned with the
ripening process of a certain fruit crop, it is crucial to understand the role of ethylene on
said crop’s ripening process. However, constructing detailed expression profiles for all
candidate genes involved in ripening at multiple developmental stages is imperative to
discover to roles of all components involved in the synthesis of and sensitivity to
ethylene and other relevant plant hormones.
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