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Applications of ionizing radiation for the control of postharvest diseases in

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DOI: 10.1111/ppa.12739

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Plant Pathology (2018) 67, 18–29 Doi: 10.1111/ppa.12739

REVIEW

Applications of ionizing radiation for the control of

postharvest diseases in fresh produce: recent advances

M.-A. Jeonga and R.-D. Jeongb*

a
Department of Dental Hygiene, Kangwon National University, Samcheok, Kangwon-do 25913; and bDepartment of Applied Biology,
Institute of Environmentally Friendly Agriculture, Chonnam National University, Gwangju 61185, Korea

Postharvest diseases cause considerable losses to harvested fruits and vegetables worldwide. In addition to various
treatments to control postharvest losses caused by pathogens, the global trend is shifting toward more ecofriendly
alternatives safer to human health. Thus far, the main approach to postharvest disease control has mostly relied on the
use of chemicals. However, the intense use of chemical fungicides has caused side effects such as environmental issues
and evolution of fungicide-resistant isolates. With increasing demand for the use of non-chemicals, ionizing radiation
has been investigated for application in many aspects of postharvest treatment, especially as an approach with signifi-
cant potential for the control of postharvest disease. Recently, a number of more or less technologically advanced
methodologies, e.g. irradiation combined with other types of treatments and induced disease-resistance, have been
developed to control postharvest diseases as well as to increase the quality and storage life of fresh commodities. Chal-
lenges for future application of irradiation in fresh produce are the cost, lack of irradiation facilities, lack of knowledge
about optimal conditions for different commodities, and lack of acceptance of irradiated fresh produce. This review
aims to document the advances in understanding of the effects of irradiation on postharvest disease, the possible modes
of action, and the perspectives in commercial use.

Keywords: combined treatment, inactivation of pathogens, induced resistance, ionizing radiation, postharvest diseases

1998). Therefore, to prevent fruit or vegetable spoilage

Introduction
Fruits and vegetables play an important role in human
nutrition and health. With increasing consumption of
these commodities, the demand for intensive farming and
ecofriendly postharvest technologies has become urgent
(Usall et al., 2015). Economic losses caused by posthar-
vest diseases are severe because microbial diversity in
fresh produce increases during its transport from the field
at harvest to the consumer. The Food and Agriculture
Organization (FAO) of the United Nations has estimated
that approximately 20–40% of harvested fruits and veg-
etables are lost due to decay, although the damage can
also be the result of physical injury during postharvest
handling, especially in developing countries, as a result
of poor storage conditions and transportation facilities
(Droby, 2006; Braghini et al., 2009a). Diseased produce
also has potential health risks; for example, several fun-
gal pathogens such as Penicillium, Aspergillus and Fusar-
ium produce mycotoxins such as patulin, aflatoxin, and
citrinin in pome and stone fruits (Sweeney & Dobson,
*E-mail: jraed2@jnu.ac.kr
Published online 14 August 2017
and decrease the health risks, proper management of
these crops/produce is required during cultivation, har-
vest, storage, transport and marketing. Most postharvest
losses by pathogens are caused by fungi and bacteria
(Prusky et al., 2013). Currently, several approaches,
including conventional synthetic fungicides, natural
chemicals, chemical elicitors of induced natural host
defences, biological control, and physical means such as
ultraviolet illumination, cold or heat treatment and ioniz-
ing radiation, have been evaluated for the control of
postharvest diseases and maintaining fresh produce qual-
ity (Hallman, 2011). The primary methods for control-
ling postharvest diseases are compared in Table 1
(Hallman, 2011; Wisniewski et al., 2016). Chemical pes-
ticides, i.e. fungicides, are commonly applied to com-
modities to reduce infection. However, the continued use
of chemical pesticides such as methyl bromide, fludiox-
onil and azoxystrobin is not acceptable because of the
development of pathogen resistance and growing public
concern over human health and environmental risks due
to chemical residues. Although physical treatments such
as cold or heat treatments have been proposed as
promising treatments, there are some limitations, such as
their cost, effectiveness at nonphytotoxic temperatures,
lack of preventive activity, and low persistence (Lurie &
Pedreschi, 2014). An effective worldwide trend to

18 ª 2017 British Society for Plant Pathology

 Ionizing radiation & plant diseases
Table 1 Comparison of major treatments against postharvest diseases.
Commodity
Treatment tolerance Cost
Cold Moderate High
Heated air Moderate Moderate
Hot water immersion Moderate Low
Postharvest fungicide Moderate Low
Biological control Moderate Moderate
Natural compounds Moderate Moderate
Salts Moderate Low
Essential oils Moderate Moderate
Irradiation Moderate High
explore alternative technologies for the control of
postharvest diseases and thus reduce the use of chemical
fungicides is emerging. Indeed, the recent exploitation of
ionizing radiation to control postharvest diseases and
extend the storage life of fresh produce has attracted
attention as an ecofriendly approach.
Postharvest ionizing radiation has been studied exten-
sively since 1950 and used successfully in more than 50
countries to prevent decay of over 60 products, despite
the safety issues raised by consumers. Postharvest
ionizing radiation preserves fresh produce by inactivating
the pathogens, as well as by inhibiting sprouting of
potatoes and onions (Piri et al., 2011). Additionally,
ionizing radiation is used worldwide as a promising phy-
tosanitary treatment to disinfect agricultural commodi-
ties of quarantine pests (Hallman, 2011). The ability of
ionizing radiation to penetrate fresh produce renders
irradiation a more effective means for controlling
postharvest diseases. However, the use of high doses of
ionizing radiation is limited because of the susceptibility
of the host tissues, leading to changes in colour, texture,
flavour or aroma. Thus, the employment of ionizing
radiation for decay control should be considered while
keeping in mind the balance between pathogen sensitiv-
ity and host resistance (Li et al., 2010; Liu et al., 2011).
The optimum radiation doses and type of radiation,
such as gamma rays, X-rays and electron-beam, for fresh
produce are usually decided empirically. Currently, the
USA, EU and Asian countries allow irradiation doses of
1 kGy or less for fruits and vegetables (European Union,
2007; US Food and Drug Administration, 2012; Ghosh,
2014). Many studies have investigated physiological
responses of postharvest pathogens to ionizing radiation
alone or combined with other treatments to assess the
optimal doses or conditions for their inactivation (Li
et al., 2010; Hallman, 2011; Liu et al., 2011). Neverthe-
less, postharvest ionizing radiation is not used as much
as other conventional technologies due to the high costs
of irradiation units and the negative perception of con-
sumers about its safety.
This review details recent advances in the use of irradi-
ation to control postharvest diseases in fresh produce,
the possible mechanisms underlying pathogen inactiva-
tion, radiation efficiency, safety, critical issues and future
prospects.
Plant Pathology (2018) 67, 18–29
19
Examples of commonly
Residues Speed Logistics treated commodity
No Very slow Difficult Apple
No Moderate Difficult Mango, papaya
No Fast Moderate Mango
Yes Fast Easy Apple, citrus, pear
Yes Very slow Moderate Apple, grape, peach
Yes Slow Moderate Apple, tomato, strawberry
Yes Slow Moderate Citrus
Yes Slow Moderate Avocado, peach
No Fast Difficult Mango, guava
Postharvest Diseases
Most postharvest diseases develop due to latent infec-
tions initiated before harvest or wound infections initi-
ated before, during or after harvest. The latter, in
general, occur through surface wounds caused by
mechanical injuries, such as cuts, abrasions, insect inju-
ries, pressure damage, and impact injuries, which often
occur during harvesting and storage. Symptoms may
develop more rapidly after harvest, particularly if condi-
tions are favourable for growth of pathogens. Thus, stor-
age is a major stage in the handling system of fruits and
vegetables suitable for inhibition of pathogen growth. To
prevent fungal attack and infection, fresh produce exhi-
bits two different lines of defence: physical defence,
derived from the components of the skin or peel; and
biochemical defence, derived from the presence of anti-
fungal proteins, organic acids, phenols, or phytoalexins
(Romanazzi et al., 2017). However, the first, physical,
line of defence can easily be broken by mechanical dam-
age during the preharvest and/or handling stages, thereby
creating suitable conditions for growth of pathogens.
Fungi are the most prominent pathogens causing
postharvest decay. They include Alternaria, Aspergillus,
Botrytis, Colletotrichum, Dothiorella, Fusarium, Geotri-
chum, Lasiodiplodia, Penicillium and Phomopsis. Like-
wise, bacterial soft rots are caused by Bacillus, Dickeya,
Lactobacillus, Pectobacterium, Pseudomonas and Xan-
thomonas. Bacteria are more common in vegetables than
in fruits because of their lower acidity. Pectobacterium
carotovorum is the most common bacterium causing seri-
ous infections in almost all vegetables. Certain bacteria
cause only internal or external blotches on commodities,
decreasing their grade or quality. Postharvest diseases
caused by plant viruses are rare, although Tobacco rattle
virus and Turnip mosaic virus have been found in potato
and cabbage, respectively (Prusky et al., 2013).
The severity of postharvest diseases is largely influ-
enced by the environment, such as fruit physical condi-
tions, temperature, atmosphere composition and
humidity (Kushalappa & Zulfiqar, 2001). The conditions
of fresh produce at harvest determine how long the crop
can be safely stored; for example, slightly immature
apples can be stored safely for several months whereas
ripened fruits or vegetables are easily decayed by
20 M.-A. Jeong & R.-D. Jeong
pathogens. In addition, spraying of the commodities with
optimum levels of calcium induces disease resistance and
delays decay by reinforcing the tissues in the cell wall
(Talibi et al., 2014). Low temperature is a key factor in
the reduction of postharvest diseases during storage
because it not only directly influences the rate of patho-
gen growth, but also affects the rate of fruit ripening.
Low-temperature storage of commodities is used exten-
sively to delay ripening and development of the diseases.
The storage atmosphere can have a direct effect on
pathogen growth. Short-term exposure to high levels of
CO2 delays anthracnose symptoms in avocado (Lange &
Kadar, 1997), whereas high humidity resulting from the
accumulation of free moisture in storage rooms and con-
tainers often increases the disease levels. Besides the
appearance of blemishes on commodities, the symptoms
originated by pathogens may lead to an increase in respi-
ration, heat production, and increased hormone levels
(i.e. ethylene) in the host tissue, speeding up the final
deterioration of the commodities.
Ionizing Radiation Technology for Control of
Postharvest Disease
Principles of ionizing radiation
Radiation is generally defined as the energy emitted from a
source. Ionizing radiation is radiation with sufficient
energy to break the chemical bonds of an atom via electro-
magnetic radiance or high-energy particles. There are sev-
eral forms of electromagnetic radiation: heat waves, radio
waves, infrared light, visible light, ultraviolet light, X-rays,
electron beams and gamma rays, depending on the fre-
quency and wavelength. Currently, only three sources of
ionizing radiation are commercially used to preserve fresh
produce: gamma rays, electron beam and X-rays. Gamma
rays emitted by the isotopes cobalt-60 (1.17 and
1.33 MeV) and caesium-137 (0.66 MeV) are legally
allowed, and, although both are commercially accepted,
cobalt-60 is mainly used because of its deep penetration
capacity. Electron beams and X-rays are produced by
machine sources of radiation; about 14% of the energy
from an electron beam is converted into X-rays. The unit
of irradiation dose is the gray (Gy), which is the energy
absorbed in J per kg of material. The absorbed dose is nor-
mally referred to as the amount of ionizing radiation
energy treatment for a product. Although gamma rays and
electron beams or X-rays are produced by different
sources, they have the same mode of action. However,
gamma rays are most commonly used in food irradiation
because of their ability to penetrate. They cause atoms and
molecules to become ionized or excited, thereby producing
free radicals, breaking chemical bonds, and damaging
molecules involved in cell processes (Fig. 1).
Biological effects of ionizing radiation
The key factors that affect the resistance of microbial cells
to ionizing radiation are the size of the organism (the
smaller the genome of the organism, the more resistant
to irradiation) and specific biological characteristics (i.e.
pigmentation, cell wall, and, for bacteria, being Gram-
positive or Gram-negative; Slade & Radman, 2011).
Induction of DNA damage by ionizing radiation is a key
event that affects the life of all organisms. The types of
DNA damage by irradiation include a misincorporation
of bases during the replication process, hydrolytic dam-
age, oxidative damage caused by direct interaction of
ionizing radiation with DNA molecules, and alkylating
agents (Rothkamm et al., 2015). Exposure to irradiation
may result in single- as well as double-strand DNA
breaks. Of the two, the double-strand breaks are the most
serious because irradiation breaks both strands of DNA,
resulting in the loss of genetic material. In addition, reac-
tive oxygen species (ROS) can induce damage to cell
structure, lipids, proteins and DNA, because they react
randomly with cellular components. The hydroxyl radi-
cals eliminate hydrogen atoms from the sugar backbone
or the four bases of DNA strands, and other free radicals
break down different organic molecules. Lethal DNA
lesions are scattered throughout the genome during
ionization, thereby killing cells if the DNA repair system
is not sufficient (Fig. 2).
Mechanism of pathogen inactivation by ionizing
radiation
An understanding of the physiological response of patho-
gens to ionizing radiation is critical for their postharvest
control in produce. It helps to explain the biological
meaning of the kinetics of inactivation and predict the
pathogen inactivation under various irradiation condi-
tions. Thus, a better knowledge of the mechanism of
inactivation of pathogens by irradiation gives rise to
effective irradiation processes.
Evidence of the antimicrobial activity of ionizing radia-
tion is the disruption of the pathogen’s cell membrane,
resulting in a loss of cytoplasmic nutrients from the cell.
In addition, ionizing radiation can cause either direct or
indirect damage. The main direct effect of ionizing radia-
tion on a pathogen is damage to the genetic material,
either DNA or RNA, described above. Single-strand
breaks may not be lethal or may lead to a mutation, but
multiple breaks render the pathogen non-viable. The indi-
rect effect of ionizing radiation on pathogens involves the
interaction between the radiation and other atoms or
molecules within the pathogens. Thus, when water
molecules are irradiated, they lose an electron,
H2O ? H2O+ + e . These products combine with each
other or other water molecules to form molecular hydro-
gen and oxygen, hydrogen peroxide (H2O2), hydroxyl
radicals ( OH), hydrogen radicals (H˙), and hydroperoxyl
radicals (HO2˙). Of these compounds, hydroxyl radicals
and hydrogen peroxide are important because they affect
the nucleic acids and break the bonds that maintain their
structure (Shama & Alderson, 2005). Moreover, ionizing
radiation can also affect enzymes, plasmids or proteins
that are essential for the growth of pathogens (Fig. 2).
Plant Pathology (2018) 67, 18–29
 Ionizing radiation & plant diseases 21

Figure 1 Biological effects of ionizing radiation. Radiation may affect DNA directly, causing ionization of the atoms in the DNA molecules. This is an
uncommon occurrence due to the small size of the target. Alternatively, radiation interacts with non-critical target atoms or molecules, usually water.
This results in the production of highly reactive free radicals, which can attack critical targets such as the DNA. Damage from such indirect action is
much more common than from direct action. The sensitivity of an organism is correlated with its complexity and the repair mechanisms by which
many cells can reverse the damage caused by radiation. Viruses are more resistant towards ionizing radiation than bacteria and fungi. [Colour
figure can be viewed at wileyonlinelibrary.com]

Moreover, repeated cycles of irradiation give rise to radi-

Susceptibility (or sensitivity) of postharvest pathogens
to ionizing radiation
The control of postharvest diseases by irradiation
depends on the radiation sensitivity of the pathogens.
The sensitivity of an organism is correlated with its com-
plexity and the repair mechanisms by which many cells
can reverse the damage caused by radiation. Thus,
viruses show the highest resistance to inactivation by
irradiation, whereas insects and parasites are the most
sensitive. Spores and cysts are resistant to ionizing radia-
tion because of the small amount of DNA they contain.
The effectiveness of irradiation for control also depends
on the type and growth stages of the pathogen, the num-
ber of viable cells on or within the tissue, treatment dose,
moisture condition, composition of products, and storage
conditions (Aziz et al., 2006). However, the effects of
the inevitable mutations caused by irradiation should be
considered, as they can lead to greater, lower, or similar
levels of pathogenicity (Galhardo et al., 2007).
ation-resistant microorganisms, and therefore, safe irradi-
ation doses should be employed to completely kill the
pathogens (Shea, 2000). The lethal effect of irradiation
on microbes is measured by the D10 value, which is the
dose required to inactivate 90% of a population; for
example, the D10 value for Penicillium expansum is
0.23 kGy, which means that irradiation with 0.23 kGy
will kill 90% of a population of this pathogen (Kim
et al., 2010). The D10 value is calculated in several ways,
all of which compare the surviving population to the ini-
tial population: either (i) mathematically by a variation
of the Karber–Spearman or Stumbo equation or (ii) by
graphic analysis of the slope of the dose–survival curve
(Stumbo, 1973; Shintani et al., 1995). The D10 values
are different for each microbial pathogen due to their
biological characteristics (Table 2). Lower D10 values
indicate greater sensitivity of the organism. One of the
main differences of the three commonly used radiation
techniques is that X-rays and electron beams are emitted

Plant Pathology (2018) 67, 18–29

22 M.-A. Jeong & R.-D. Jeong

Figure 2 Cell responses to damage of DNA

by ionizing radiation. Ionizing radiation
causes single and double strand breaks of
DNA, either directly or indirectly, resulting in
oxidized proteins, DNA, lipids and other
biomolecules. Within minutes, the cell
responds by altering gene expression and
modifying stress-related proteins. High doses
of radiation lead to cell death or genomic
instability. [Colour figure can be viewed at
wileyonlinelibrary.com]

Table 2 Summary of D10 valuesa for gamma-irradiated spores. elimination of pathogens in industrial processes. How-
ever, irradiation of fruits and vegetables is limited to
D10 value doses below 1 kGy, owing to nutritional losses and
Fungus Source (kGy) References chemical changes in irradiated products (Aziz et al.,
Alternaria tenuissima Tomato 2.409 Temur & Tiryaki (2013) 2006; Braghini et al., 2009b). In addition, the use of
Aspergillus flavus Maize 0.060 Prusky et al. (2013) gamma ray, electron beam, and X-ray irradiation as a
Aspergillus niger Mango 0.042 Prusky et al. (2013) phytosanitary treatment against insects has increased dra-
Botrytis cinerea Rose 0.950 Jeong et al. (2015) matically in recent years. This application of irradiation
Botrytis elliptica Lily 0.526 Kim & Yun (2014) technology is critical owing to uncertainties in the future
Monilinia fructicola Peach 0.160 Kim et al. (2010)
and restrictions imposed under the Montreal Protocol on
Penicillium digitatum Lemon 1.100 Lebaijuri et al. (1995)
the use of methyl bromide, which is still widely used for
Penicillium expansum Pear 0.268 Jeong et al. (2015)
Penicillium italicum Orange 1.430 Temur & Tiryaki (2013)
quarantine purposes.
Rhizopus nigricans Peach 2.740 Lebaijuri et al. (1995) Several species of postharvest pathogens have been
Rhizopus stolonifer Sweet 0.541 Jeong et al. (2014) irradiated with various radiations to examine their
potato radiosensitivity and determine their D10 values (Lebaijuri
Stemphylium Pear 0.210 Geweely & Nawar (2006) et al., 1995; Jeong et al., 2015). The D10 values of vari-
botryosum ous postharvest pathogens for gamma rays are listed in
Table 2. Botrytis cinerea and P. expansum are sensitive
a
One D10 value is the dose required to inactivate 90% of a population. to radiation, whereas Alternaria tenuissima and Stem-
The D10 value is calculated in several ways, all of which compare the
phylium botryosum are resistant. In addition, young
surviving population to the initial population either (i) mathematically by
mycelia are more resistant than mature mycelia. Interest-
some variation of the Karber–Spearman or Stumbo equation or (ii) by
graphic analysis of the slope of dose–survival curves.
ingly, fungal pathogens show different radiosensitivity to
various irradiations, indicating that differences in fungal
response to radiation reflect species-specific radiosensitiv-
in one direction only, whereas a gamma ray is emitted in ity, which might be linked to their adaptive strategies
all directions uniformly. In addition, an electron beam or under radiation stress (Jeong et al., 2015). Their
X-ray can penetrate a few centimetres, whereas a gamma responses to ionizing radiation are linked to certain fac-
ray passes through thick walls. Due to the deeper pene- tors such as the presence of mycelial water content as a
tration, a gamma ray is the method most used for natural radioprotector, the ability to repair DNA breaks,

Plant Pathology (2018) 67, 18–29

 Ionizing radiation & plant diseases
the induction of certain enzymes associated with the
recovery from radiation damage, and the presence of
chemical substances suppressing the process of growth
(Geweely & Nawar, 2006).
The inhibition of spore germination and morphology
of fungal spores subsequent to treatment are directly
related to the strength of the radiation dose. Increasing
doses inhibit spore germination and crush the spore sur-
face (Geweely & Nawar, 2006; Tugay et al., 2006;
Jeong et al., 2015). In addition, lower doses of gamma
radiation increase the total protein or total lipid produc-
tion in Fusarium solani and P. notatum, suggesting that
proteins or lipids may play a role in protection against
the harmful effects of radiation (Osman et al., 1987).
Identification of these proteins and lipids would elucidate
their roles as radioprotectors. The radiosensitivity of a
specific fungal species may depend on various factors
including the moisture content of spores or commodities,
the age of spores, and the time of storage before or after
ionizing radiation (Fig. 3). Dried spores show more resis-
tance to radiation. Postharvest pathogens that exist in
products with a high moisture content will easily recover
after irradiation if inactivation is not complete (Shea,
2000; Farkas, 2006). Thus, an empirical study for the
control of postharvest diseases by irradiation should be
performed with care because many unconsidered factors
may affect their susceptibility.
Ionizing radiation is one technology that can contribute
to inactivation of fungal toxins. As discussed, its action
inhibits fungal growth, thereby preventing the biosynthesis
of mycotoxins by fungal pathogens. For example, the toxi-
city of aflatoxin B1 (AFB1), found in peanut meal, was
reduced by 75% and 100% after gamma irradiation doses
of 1 and 10 kGy, respectively (Ghanem et al., 2008).
Figure 3 Factors affecting the effectiveness
of irradiation of fresh produce for postharvest
disease control. [Colour figure can be
viewed at wileyonlinelibrary.com]
Plant Pathology (2018) 67, 18–29
23
Water is a critical factor in the destruction of aflatoxin by
ionizing radiation, because radiolysis of water triggers the
formation of highly reactive free radicals, which destroy
the terminal furan ring of AFB1, thereby lowering its bio-
logical activity (Ghanem et al., 2008).
Instead of irradiating pathogens directly, some studies
have investigated the antimicrobial activity of ionizing
radiation on diseases in their hosts. Gamma irradiation
was applied to citrus fruits to control citrus canker
caused by Xanthomonas citri subsp. citri. The disease
severity was suppressed without physiological changes to
the citrus by a low dose of gamma irradiation, indicating
that X. citri subsp. citri can be controlled by ionizing
radiation (Kim & Yun, 2014). In addition, an electron
beam of 1.5 and 2 kGy was sufficient to eradicate
B. cinerea and Agrobacterium rhizogenes from infected
vegetable seeds without affecting the seed germination
rate (Bae, 2013).
Another key factor in inactivating pathogens is the
time interval between inoculation and irradiation. This
time interval was found to affect the growth response of
Monilinia fructicola in peach fruits (Kuhn et al., 1968).
Gamma irradiation for 36, 48 or 60 h after inoculation
of M. fructicola increased the incidence of the disease to
60%, 70% and 90%, respectively.
Advantages and disadvantages of irradiation
Irradiation is a physical treatment used to control
postharvest diseases and appears to offer one of the most
viable alternatives to the use of chemicals. The penetrat-
ing power and uniformity of irradiation and its derived
effectiveness on the inactivation of pathogens is better
than that of fungicides. Irradiation is essentially a
24 M.-A. Jeong & R.-D. Jeong

nonthermal process, with minimal to no heating of fresh
produce, thus eliciting negligible sensory changes in the
produce. Ionizing radiation does not render food
radioactive because it is not strong enough to affect the
neutrons in the nucleus (Smith & Pillai, 2004). There-
fore, ionizing radiation is considered a safe, energy effi-
cient and environmentally safe process.
While irradiated products are still not widely popular
in developed countries, ionizing irradiation of fresh pro-
duce is used to control quarantine pests rather than
postharvest diseases. The maximum US FDA permitted
dose of 1 kGy to treat fruits and vegetables is too low
for effective fungal pathogen control, whereas higher
effective doses are often phytotoxic to treated fresh pro-
duce (Kader, 1999). In addition to safety concerns, irra-
diated products have other issues such as resistant
strains, cost and nutrient content of treated produce.
One common concern about irradiating fresh produce is
that long-term use of irradiation promotes development
of radiation-resistant strains of fungi and bacteria. In
addition, some studies have shown that irradiation
increases mycotoxin levels because of the absence of
competitive inhibition by mould growth, leading to
toxin-producing strains eventually dominating the myco-
flora (Braghini et al., 2009a; Ribeiro et al., 2011).
Another disadvantage is that irradiated fresh produce
can be more expensive owing to the upfront costs of an
irradiation facility. Irradiation can also have a negative
effect on the physical and/or physiological conditions of
the fruit, for example, causing softening, discolouration,
and the development of ‘off-flavours’. Moreover, irradia-
tion can deplete fruits and vegetables of nutrition such as
vitamins, proteins, carbohydrates, lipids and undesirably
changes the taste at high dosages (Mostafavi et al.,
2012).
Application of combined treatments to control
postharvest diseases
The purpose of combined treatments is to increase the
effectiveness of lower doses of irradiation without nega-
tively affecting the skin colour or texture of stored fruits
and vegetables. Studies have been made of irradiation
treatment combined with heat, pulsed light, microwave
drying, UV, ozone, environmental conditions, biocontrol
agents and ecofriendly chemicals (Table 3; Orsat et al.,
2006; Vicente et al., 2005).
Synergistic effects of gamma radiation combined with
heat treatment (38 °C for 4 days) contributed to the 5-
to 10-fold increase in the inactivation of spores of

Table 3 Case studies of irradiation combined treatments.

Commodity Pathogen Irradiation Treatment References

Apple Monilinia fructigena Gamma (2 kGy) Cold (0 °C) Mostafavi et al. (2012)
Penicillium expansum Gamma (0.6 kGy) Cold (1 °C)
Gamma (0.5 kGy) Heat (38 °C) Conway et al. (2004)
Lily Botrytis elliptica Gamma (0.2 kGy) NaDCC (40 mg L 1) Kim & Yun (2014)
NA (50 mg L 1)
NSS (50 mg L 1)
Mandarin P. digitatum X-ray (0.875 kGy) SC Palou et al. (2007)
P. italicum X-ray (0.875 kGy) SC Palou et al. (2007)
Mango Aspergillus flavus Gamma (1 kGy) Hot water (55 °C) El-Samahy et al. (2000)
A. niger
A. oryzae
A. sydowii
A. terreus
A. ustus
Cladosporium cladosporoides
Fusarium oxysporum
P. brevicompactum
P. chrysogenum
P. corylophylium
P. janthinellum
P. oxalicum
Scopulariopsis brevicaulis
Paprika B. cinerea Gamma (0.4 kGy) NaDCC (30 mg L 1) Yoon et al. (2014)
Pear B. cinerea Gamma (3 kGy) Cold (0 °C) Temur & Tiryaki (2013)
P. expansum Gamma (3 kGy) Cold (0 °C) Temur & Tiryaki (2013)
Gamma (0.5 kGy) Hot water (47 °C)
Rhizopus nigricans Gamma (3 kGy) Cold (0 °C) Temur & Tiryaki (2013)
Tomato B. cinerea Gamma (1 kGy) Hot water (55 °C) Barkai-Golan et al. (1993)
R. stolonifer

NaDCC, sodium dichloro-S-triazinetrione; NA, nano-silver particles; NSS, nano-sized silica silver; SC, sodium carbonate.

Plant Pathology (2018) 67, 18–29

 Ionizing radiation & plant diseases
postharvest pathogens (Temur & Tiryaki, 2013). Heat
treatment may also affect the susceptibility of the host to
pathogens by triggering the synthesis of an inhibitory
substance in the peel. The combination of hot water and
gamma irradiation synergistically reduced fungal devel-
opment in tomato fruits, resulting in 1.7% and 10.0%
infection rates by B. cinerea and Rhizopus stolonifer,
respectively (Barkai-Golan et al., 1993). Moreover, a hot
water dip followed by irradiation at 0.5 kGy totally
eliminated the decay caused by Alternaria alternata for
8 days at 23 °C in mango fruits (Spalding & Reeder,
1986). However, the combination of hot water with irra-
diation is not commonly used on citrus due to the detri-
mental effect it has on the quality of treated clementines
and the contradictory results presented in different stud-
ies (Palou et al., 2007; Mahmoud et al., 2011). Another
study suggested that a combined treatment of 0.5 kGy of
gamma irradiation with hot water (47 °C for 7 min)
inactivates P. expansum but does not prevent the growth
of B. cinerea and Alternaria tenuis. In addition, the fun-
gal population on mangoes was reduced by treatment
with hot water (55 °C for 5 min) and 1 kGy of gamma
irradiation (El-Samahy et al., 2000). A similar study on
tomato found that the B. cinerea, R. stolonifer and
A. alternata decay is reduced with a combined treatment
of 1 kGy of gamma irradiation and a hot water dip at
50 °C for 2 min (Barkai-Golan et al., 1993).
The potential of biological control to reduce the decay
varies compared to that of chemical fungicides as biocon-
trol is easily affected by environmental conditions. A
combined treatment of irradiation with biocontrol is not
easy to regulate due to variable environmental conditions
and fastidious nature of the biocontrol agent. A study
was carried out by Mostafavi et al. (2011) on the effect
of gamma irradiation and biocontrol agent Pseudomonas
fluorescens on germination and mycelial growth of P. ex-
pansum. When spores of P. expansum were treated with
gamma irradiation alone, a dose of 0.6 kGy was
required for complete inhibition of spore germination.
However, if spores of P. expansum were exposed to
gamma irradiation, then incubated in a 3:5 ratio with a
suspension of P. fluorescens for 48 h, spore germination
was almost completely inhibited by a dose of only
0.3 kGy. Thus, the combination of gamma irradiation
and P. fluorescens was more effective than irradiation
treatment alone. It seems, therefore, that the integration
of irradiation and antagonist may lead to more effective
control of pathogens.
Another combined treatment includes ionizing radia-
tion and chlorination. At present, chlorine is one of the
few effective and relatively inexpensive chemical agents
used for postharvest disinfection of produce. Sodium
dichloro-S-triazinetrione (NaDCC), a chlorine donor and
an ecofriendly chemical, has been approved by the Uni-
ted States Environmental Protection Agency and the
World Health Organization for use with drinking water
(Clasen & Edmondson, 2006). Treatment with NaDCC
reduced the initial microbial load in various vegetables
by up to log10 1.69 to log10 2.42 compared to a water-
Plant Pathology (2018) 67, 18–29
25
treated control. Although NaDCC has antibiotic activity,
its efficiency is not maintained during storage. A combi-
nation of gamma irradiation with NaDCC treatment
showed a synergistic effect on the control of B. cinerea
on paprika. The sensitivity of B. cinerea was dramati-
cally increased with the combined treatment compared
with gamma irradiation alone (Yoon et al., 2014). Based
on artificial inoculation, a combined treatment of gamma
irradiation with 30 lg L 1 of NaDCC completely inhib-
ited the growth of B. cinerea on paprika, reducing the
minimum required dose of gamma radiation from 2 to
0.4 kGy. This reduced dosage contributed to the preser-
vation of the physical properties of irradiated paprika.
The use of carbonic acid salts, such as sodium carbon-
ate (SC) and sodium bicarbonate, provides another eco-
friendly and nontoxic treatment. SC has been used as a
potential alternative to synthetic fungicides to control
citrus postharvest disease because it is inexpensive and
can be used with a minimal risk of damage to the fruits.
SC treatment in combination with an X-ray irradiation
dose of 0.875 kGy is more effective in controlling Peni-
cillium digitatum and P. italicum compared to a single
treatment (Palou et al., 2007).
Some studies have used nano-silver particles (NA) and
nano-sized silica silver (NSS) in combination with
gamma irradiation for disinfection of paprika and lily
from B. cinerea, and B. elliptica (Kim & Yun, 2014;
Yoon et al., 2014). Several investigations have shown the
inhibitory nature of NA associated with sterilization
(Kim et al., 2011; Jung et al., 2014). Gamma irradiation
showed no antifungal activity at a dose of 1 kGy, but in
combined treatments with NA or NSS at concentrations
above 1 lg L 1, the same dose of gamma rays showed
the strongest antifungal activity.
In addition, a study has suggested that combination of
irradiation with cold storage is also promising for the
control of postharvest diseases. The growth of Col-
letotrichum acutatum on apples was dramatically inhib-
ited when gamma irradiation was combined with storage
at 0 °C for 4 months compared to those stored at 20 °C
(Kim et al., 2011). Recently, a study demonstrated that
the germination of P. expansum spores was completely
inhibited with a 0.6 kGy dose of gamma rays when com-
bined with storage at 1 °C, without causing significant
physical changes in apples (Mostafavi et al., 2012).
Resistance in postharvest fruits induced by irradiation
Increasing the natural defence response of fruits through
induction of resistance is a straightforward strategy to
control pathogens during postharvest handling. Com-
pared with intact plants, relatively little is known about
host defence responses in fresh produce. Irradiation-
induced resistance to plant pathogens in fruits may
involve DNA damage mediated by the dimerization of
thymine and other pyrimidines. Ionizing radiation trig-
gers secondary intermediary processes eventually result-
ing in induced resistance (Fig. 4). Intricate biochemical
host defence responses contribute to induction of
26 M.-A. Jeong & R.-D. Jeong
Figure 4 Resistance induced in fruits by ionizing radiation. The
application of ionizing radiation results in a significant increase in
reactive oxygen species (ROS), thereby increasing the expression of
defence-related genes through unknown pathways in the nucleus,
leading to an increase in phenylalanine ammonia-lyase (PAL),
peroxidase (POD), polyphenol oxidase (PPO), phenolic compounds,
chitinase and b-1,3-glucanase within the cells. Thus, pathogen growth
is effectively inhibited. [Colour figure can be viewed at
wileyonlinelibrary.com]
resistance in harvested fruits. Treatment with low dose
irradiation results in the synthesis of several antifungal
compounds. Low dose gamma irradiation increases
phenylalanine ammonia-lyase (PAL) and biosynthesis of
constitutive and/or induction of phenolic compounds in
citrus fruits and seeds (Oufedjikh et al., 2000; Sumira
et al., 2012). In addition, irradiation-induced glucanases
and chitinases inhibit fungi, while lysozymes and some
chitinases inhibit bacteria (Charles et al., 2003). Irradi-
ated tomato and grapes accumulate high levels of phy-
toalexin, PAL and peroxidase (POD) as antimicrobial
compounds to counteract B. cinerea (Nigro et al., 1998).
PAL is the first enzyme in the phenylpropanoid pathway,
whereas POD plays a key role at a later stage of the
pathway during the synthesis of lignin, which acts as a
cell wall reinforcement, enhancing resistance against sev-
eral pathogens and thus altering the antioxidant ability
of citrus to suppress Penicillium infection (Macarisin
et al., 2007). The efficacy of irradiation in eliciting
induced resistance varies and depends on the maturity of
the fruit. It is noteworthy that antifungal compounds
may be involved in the induction of resistance to patho-
gens triggered by ionizing radiation.
Quality of irradiated fresh produce
Irradiation treatment has not been found to affect human
health under international standards. However, there is a
concern that radiation treatment affects not only plant
pathogens, but also the physical properties and nutrition
of the fresh produce. Mostly, irradiation is applied at
doses below 1 kGy because higher doses severely affect
the physical properties of the produce (Smith & Pillai,
2004; Hallman, 2011). Most studies have suggested that
nutrient losses after postharvest irradiation do not occur
in fruits at the optimal dose for phytosanitary security.
Thus, irradiation at optimal levels (0.3 kGy) did not affect
the ascorbic acid content of apples (Fan et al., 2005).
Similarly, irradiation doses up to 0.25 kGy did not show
any negative impact on the vitamin C content in bananas,
and doses up to 0.6–0.8 kGy did not affect their sugar
content, vitamin C or protein content (Akhter, 2003).
Furthermore, gamma irradiation treatment of guava fruit
with a 0.25 kGy dose increased their postharvest life by
3–4 days, maintained fruit quality, and reduced the decay
incidence (Singh & Pal, 2009). In general, the quality of
proteins, lipids and carbohydrates is not affected by irra-
diation at less than 10 kGy. Studies have also indicated
that irradiated fresh produce shows higher antioxidant
content than non-irradiated controls because irradiation
induces phenolic compounds (Conway et al., 2004; Fan
et al., 2005; Akhter et al., 2008). The effects of ionizing
radiation on nutrients depend on the radiation dose and
modifying factors such as temperature, humidity and the
presence of oxygen. Irradiation of fresh produce leads to a
reduction in firmness (Palekar et al., 2004; Wall & Khan,
2008). In addition, the effect of irradiation on grapefruit
depends on the time of harvest. Lower doses (at or below
0.2 kGy) of gamma irradiation increased health promot-
ing compounds but higher doses (0.4 and 0.7 kGy) of
irradiation showed detrimental effects on the quality of
early season grapefruit (Patil et al., 2004). The maximum
doses applied to fruits or vegetables range between 1 and
2 kGy, and their values depend on the type of product.
Combined treatment can prevent softening of fresh pro-
duce with the use of reduced irradiation doses. The firm-
ness of paprika irradiated with 1 kGy was decreased, but
a combined treatment with NaDCC and a lower irradia-
tion dose (0.4 kGy) alleviated the physical changes of the
produce (Yoon et al., 2014). In a study of dragon fruits,
their quality was evaluated after X-ray irradiation for con-
trol of quarantine pests (Wall & Khan, 2008). Irradiation
doses of up to 0.8 kGy did not affect soluble solids con-
tent, titratable acidity or fructose concentration. How-
ever, glucose, sucrose and total sugar concentrations were
decreased in a dose-dependent manner. In addition, a
study by Alonso et al. (2007) found that treatment of
clementine mandarin cv. Clemenules with X-ray doses of
0.195 and 0.395 kGy, optimal for control of clementine
and mandarin pests, did not have a detrimental effect on
the fruit quality such as the rind colour, firmness, juice
yield, maturity index, internal volatiles, deterioration
index or sensory evaluation.
Safety Issues of Irradiated Fresh Produce
Food irradiation remains unpopular compared to con-
ventional technologies. Nuclear disasters and their
derived radioactive contamination have given consumers
a negative perception of irradiated fresh produce. For
this reason, more than 50 years of extensive research has
been devoted to the safety and effectiveness of irradiation
Plant Pathology (2018) 67, 18–29
 Ionizing radiation & plant diseases
as a food sterilization technique to kill pathogens in food
and extend its shelf life. There are three primary cate-
gories of safety that need to be considered: radiological
safety (existence of radioactivity in the irradiated food),
microbiological safety (occurrence of radiation-resistant
microbial populations), and toxicological safety (effect of
irradiated food on humans). The safety and efficacy of
irradiation has been proved and accepted by the World
Health Organization (WHO), the FAO, the International
Atomic Energy Agency (IAEA), Codex Alimentarius, and
the governments of different countries commending the
process (Smith & Pillai, 2004). It was concluded that
there are no microbiological risks for consumers, and
that chemical substances generated during irradiation in
fresh produce are not significantly higher than those
induced by heat treatment. These documents have been
widely adopted internationally, and specific applications
are being applied in over 55 countries worldwide (US
Food and Drug Administration, 2012; European Union,
2007).
Issues for Future Applications of Irradiation
Against Postharvest Disease
In recent years, there has been considerable development
of the commercial use of irradiation of fresh produce.
Many countries have taken advantage of this technology
as a replacement for methyl bromide for plant quarantine
purposes. Irradiation not only eliminates postharvest dis-
eases, but also kills quarantine pests in produce aimed for
export (Smith & Pillai, 2004). Although the use of irradia-
tion is a well-organized and promising technology, several
obstacles should be considered before commercial use.
Irradiation of fresh produce generally costs more than
any other conventional technology due to the initial costs
of the treatment facility. However, its increased use will
lower the per-unit cost of the treatment. In addition, dif-
ferent ionizing radiations are used for different commodi-
ties. For example, X-ray irradiation controls B. cinerea
in cut roses more effectively than gamma irradiation,
whereas gamma irradiation is the optimal radiation to
control P. expansum and P. italicum in pears and man-
darins (Jeong et al., 2015). A study suggested that rela-
tively low doses (0.15–0.4 kGy) of X-ray irradiation cost
about 55% of the expense of cobalt-60 irradiation,
whereas at higher doses required for spices (over
10 kGy), cobalt-60 is a much cheaper option for com-
mercial use (Hallman, 2011). In addition, a lack of radi-
ation facilities is closely related to the increase in cost. It
is worth noting that it is possible to design irradiation
facilities that could be incorporated into packing lines or
located near ports or airports for the export of commodi-
ties to decrease handling costs (Hallman, 2011). More
importantly, more research should be carried out to
establish optimal doses to control key postharvest dis-
eases in a broad variety of fresh commodities because a
single dose cannot cover all commodities.
Despite the fact that irradiated fresh produce has been
carefully evaluated, there is a lack of acceptance of food
Plant Pathology (2018) 67, 18–29
27
irradiation by the public, although health organizations
worldwide have concluded that irradiated fruits or veg-
etables pose no health hazard. In addition, people fail to
differentiate between irradiated fresh produce and
radioactive fresh produce. Education and outreach to
consumers may be an initial requirement for commercial
application of irradiation for commodities.
Conclusion
A wide variety of fungal and bacterial pathogens cause
postharvest disease in fresh produce. Losses caused by
postharvest diseases are a very important issue because
the value of fresh fruits and vegetables increases several
times on its way from the field to the consumer. Posthar-
vest diseases in a wide variety of fresh produce are a par-
ticular problem in developing countries due to a lack of
well-equipped storage facilities. Therefore treatments that
are effective against postharvest diseases of fruits and
vegetables are essential (Temur & Tiryaki, 2013).
Although there are several alternatives for the control of
postharvest diseases, they are limited by concerns for
human health and environmental issues associated with
fungicide residues. Despite the conflicting issues regard-
ing the effects of irradiation on postharvest pathogens in
fruits and vegetables, ionizing radiation is a promising
non-chemical treatment for inactivating harmful patho-
gens in fruits and vegetables. Compared to other foods,
very little research has been done to determine the effects
of irradiation on postharvest pathogens found in fruits
and vegetables. There are some factors that might affect
the efficacy of irradiation, including oxygen concentra-
tion, host, temperature, radiation dose and type of
pathogens. Thus, it is necessary to understand which fac-
tors are directly associated with the postharvest health of
produce. In addition, irradiation can improve the safety
of fresh produce and increase its shelf life. In general,
ionizing radiation is considered safe for both the environ-
ment and human health, and the need for irradiation of
commodities has increased over the last few years. Many
studies have been conducted that have confirmed the
benefits of irradiation in controlling many postharvest
diseases. A disadvantage of postharvest irradiation is that
it is not accepted by the organic industry. A single irradi-
ation dose required to kill postharvest pathogens can
negatively affect the physical properties, such as skin col-
our, texture and firmness, of the stored fruits and vegeta-
bles. A combined treatment with other agents can
decrease the required dose of radiation and thereby
decrease its effect on physical properties of the commod-
ity. In addition, irradiation causes a temporary response
that significantly modifies the metabolism of fresh pro-
duce, increasing the enzyme activities and gene expres-
sion. A defence response to pathogens induced by
irradiation in fruits triggers disease resistance through
modification of enzyme activities, secondary metabolites
and pathogenesis-related proteins (PR). The determina-
tion of appropriate irradiation conditions (irradiation
dose, other agents) will enable the application of
28 M.-A. Jeong & R.-D. Jeong
effective treatments against postharvest diseases at the
commercial scale. However, there are some barriers to
the commercial application of irradiation. It is necessary
to prepare strategies that will help the consumers to
overcome their fear of irradiated products. Another chal-
lenge of postharvest irradiation is to reduce the cost so
that it is economic for commercial use. Finally, it is
worth emphasizing that the knowledge about postharvest
irradiation compared to other treatments used against
postharvest diseases is still limited, but its progress and
the increase in its effectiveness over the last several dec-
ades have been remarkable. Better understanding of the
mode of action of irradiation on fresh produce will help
the application of more effective treatments. There is no
doubt that if the challenges such as the ineffectiveness of
permitted doses for treatment of fruits and vegetables
and the phytotoxicity associated with effective doses to
irradiation treatment are handled well, irradiation will
be an ideal technology for the control of postharvest dis-
eases in fruits, and vegetables, and will lead to its use for
export markets in the future.
Acknowledgements
This work was supported by a 2016 Research Grant
from Kangwon National University (no. D2000128-01-
01).
References
Akhter ABM, 2003. Irradiation Quarantine Treatment Against Fruit Fly,
Bactrocera dorsalis (Diptera: Tephritidae) and Some Quality Aspects
of the Irradiated Host Fruit, Banana (Sagar Kala, Musa sp.). Dhaka,
Bangladesh: Dhaka University, MS thesis.
Akhter ABM, Kahn SA, Akter H, Islam MA, Howlader MA, 2008.
Evaluation of gamma irradiation as a quarantine treatment against the
oriental fruit fly, Bactrocera dorsalis (Hendel). Journal of the Asiatic
Society of Bangladesh Science 34, 157–68.
Alonso M, Palou L, Rıo MAD, Jacas J, 2007. Effect of X-ray irradiation
on fruit quality of clementine mandarin cv. ‘Clemenules’. Radiation
Physics and Chemistry 76, 1631–5.
Aziz NH, Souzan RM, Azza AS, 2006. Effect of gamma irradiation on
the occurrence of pathogenic microorganism and nutritive value of our
principal cereal grains. Applied Radiation and Isotopes 64, 1555–62.
Bae YM, 2013. Effect of electron beam irradiation on selected vegetable
seeds and plant-pathogenic microorganisms. Journal of Life Science
23, 1415–9.
Barkai-Golan R, Padova R, Ross I, Lapidot M, Davidson H, Copel A,
1993. Combined hot water and radiation treatments to control decay
of tomato fruits. Scientia Horticulturae 56, 101–5.
Braghini R, Pozzi CR, Aquino S, Rocha LO, Correa B, 2009a. Effects
of gamma radiation on the fungus Alternaria alternata in artificially
inoculated cereal samples. Applied Radiation and Isotopes 67,
1622–8.
Braghini R, Sucupira M, Rocha LO, Reis TA, Aquino S, Correa B,
2009b. Effects of gamma radiation on the growth of A. alternata and
on the production of alternariol and alternariolmonomethyl ether in
sunflower seeds. Food Microbiology 26, 927–31.
Charles MT, Corcuff R, Roussel D, Arul J, 2003. Effect of maturity and
storage on rishitin accumulation disease resistance to Botrytis cinerea
in UV-C treated tomato fruit. Acta Horticulturae 599, 573–6.
Clasen T, Edmondson P, 2006. Sodium dichloroisocyanurate (NaDCC)
tablets as an alternative to sodium hypochlorite for the routine
treatment of drinking water at the household level. International
Journal of Hygiene & Environmental Health 209, 173–81.
Conway WS, Leverentz B, Janisiewicz WF, Blodgett AB, Safter RA,
Camp MJ, 2004. Integrating heat treatment, biocontrol and sodium
bicarbonate to reduce postharvest decay of apple caused by
Colletotrichum acutatum and P. expansum. Postharvest Biology and
Technology 34, 11–20.
Droby S, 2006. Improving quality and safety of fresh and vegetables
after harvest by the use of biocontrol agents and natural materials.
Acta Horticulturae 709, 45–51.
El-Samahy SK, Youssef BM, Askar AA, Swailam HMM, 2000.
Microbiological and chemical properties of irradiated mango. Journal
of Food Safety 20, 139–56.
European Union, 2007. Food irradiation-Community legislation. [http://
ec.europa.eu/food/food/biosafety/irradiation/comm_legsl_en.htm].
Accessed 31 May 2017.
Fan X, Niemira BA, Matheis JP, Zhuang H, Olson DW, 2005. Quality
of fresh-cut apples slices as affected by low dose ionizing radiation and
calcium ascorbate treatment. Journal of Food Science 70, 143–8.
Farkas J, 2006. Irradiation for better foods. Trends in Food Science &
Technology 17, 148–52.
Galhardo RS, Hastings PJ, Rosenberg SM, 2007. Mutations as a stress
response and the regulation of evolvability. Critical Reviews in
Biochemistry and Molecular Biology 42, 399–435.
Geweely NSI, Nawar LS, 2006. Sensitivity to gamma irradiation of post-
harvest pathogens of pear. International Journal of Agriculture and
Biology 8, 710–6.
Ghanem I, Orfi M, Shamma M, 2008. Effect of gamma radiation on the
inactivation of aflatoxin B1 in food and feed crops. Brazilian Journal
of Microbiology 39, 787–91.
Ghosh D, 2014. Food safety regulations in Australia and New Zealand
Food Standards. Journal of the Science of Food and Agriculture 94,
1970–3.
Hallman GJ, 2011. Phytosanitary applications of irradiation.
Comprehensive Reviews in Food Science and Food Safety 10, 143–51.
Jeong J, Yoon M, Lee K et al., 2014. Effect of the combined treatment
with gamma irradiation and sodium dichloroisocyanurate on
postharvest Rhizopus soft rot of sweet potato. Journal of Plant
Diseases and Protection 121, 243–9.
Jeong RD, Shin EJ, Chu EH et al., 2015. Effects of ionizing radiation
on postharvest fungal pathogens. The Plant Pathology Journal 31,
1–5.
Jung K, Yoon M, Park HJ et al., 2014. Application of combined
treatment for control of Botrytis cinerea in phytosanitary irradiation
processing. Radiation Physics and Chemistry 99, 12–7.
Kader AA, 1999. Current and potential applications of ionizing radiation
in postharvest handling of fresh horticultural perishables. International
Produce Journal 8, 38–9.
Kim JH, Yun SC, 2014. Effect of gamma irradiation and its convergent
treatments on lily blight pathogen, Botrytis elliptica, and the disease
development. Research in Plant Disease 20, 71–8.
Kim KH, Kim MS, Kim HG, Yook HS, 2010. Inactivation of
contaminated fungi and antioxidant effects of peach (Prunus persica L.
Batsch cv. Dangeumdo) by 0.5–2 kGy gamma irradiation. Radiation
Physics and Chemistry 79, 495–501.
Kim HJ, Park HJ, Choi SH, 2011. Antimicrobial action effect and
stability of nanosized silica hybrid Ag complex. Journal of
Nanoscience and Nanotechnology 11, 5781–7.
Kuhn GD, Merkley MS, Dennison RA, 1968. Irradiation inactivation of
brown rot infections on peaches. Food Technology 22, 91–2.
Kushalappa AC, Zulfiqar M, 2001. Effect of wet incubation time and
temperature on infection, and of storage time, and temperature on soft
rot lesion expansion in potatoes inoculated with Erwinia carotovora
ssp. carotovora. Potato Research 3, 233–42.
Lange D, Kadar AA, 1997. Effects of elevated carbon dioxide on key
mitochondrial respiratory enzymes in ‘Hass’ avocado fruit and fruit
disks. Journal of the American Society for Horticultural Science 122,
238–44.
Plant Pathology (2018) 67, 18–29
 Ionizing radiation & plant diseases
Lebaijuri M, Omar M, Yusof N, 1995. Sensitivity of the conidia of plant
pathogenic fungi to gamma-rays, electron particles and X-ray
irradiation. World Journal of Microbiology and Biotechnology 11,
610–4.
Li J, Zhang Q, Cui Y et al., 2010. Use of UV-C treatment to inhibit the
microbial growth and maintain the quality of Yali pear. Journal of
Food Science 75, 503–7.
Liu C, Cai L, Han X, Ying T, 2011. Temporary effect of postharvest
UV-C irradiation on gene expression profile in tomato fruit. Gene 15,
56–84.
Lurie S, Pedreschi R, 2014. Fundamental aspects of postharvest heat
treatments. Horticulture Research 1, 14030.
Macarisin D, Cohen L, Eick A et al., 2007. Penicillium digitatum
suppresses production of hydrogen peroxide in host tissue during
infection of citrus fruit. Phytopathology 97, 1491–500.
Mahmoud GA, Mohamed G, Botros HW, Sabri MA, 2011. Combined
effect of gamma irradiation, hot water and sodium bicarbonate on
quality and chemical constituents of stored mandarin fruits. Archives
of Phytopathology and Plant Protection 44, 1115–27.
Mostafavi HA, Mirmajlessi SM, Fathollahi H, Minassyan V, Mirjalili
SM, 2011. Evaluation of gamma irradiation effect and Pseudomonas
florescens against Penicillium expansum. African Journal of
Biotechnology 10, 11290–3.
Mostafavi HA, Mirmajlessi SM, Mirjalili SM, Fathollahi H, Askari H,
2012. Gamma radiation effects on physico-chemical parameters of
apple fruit during commercial post-harvest preservation. Radiation
Physics and Chemistry 81, 666–71.
Nigro F, Ippolito A, Lima G, 1998. Use of UV-C to reduce storage rot of
tablegrape. Postharvest Biology and Technology 13, 171–81.
Orsat V, Changrue V, Raghavan GSV, 2006. Microwave drying of fruits
and vegetables. Stewart Postharvest Review 6, 4–9.
Osman M, Mohamed YA, Abo-Zeid A, 1987. Effect of UV-irradiation
on total protein and nucleic acids in Alternaria alternata and Fusarium
solani. Annals of Botany 60, 677–80.
Oufedjikh H, Mahrouz M, Amiot MJ, Lacroix M, 2000. Effect of
gamma-irradiation on phenolic compounds and phenylalanine
ammonia-lyase activity during storage in relation to peel injury peel of
Citrus clementina hort. Ex. Tanaka. Journal of Agricultural and Food
Chemistry 48, 559–65.
Palekar MP, Cabrera-Diaz E, Kalbasi-Ashtari A et al., 2004. Effect of
electron beam irradiation on the bacterial load and sensorial quality of
sliced cantaloupe. Journal of Food Science 69, 267–73.
Palou L, Marcilla A, Jojas-Argudo C, Alonso M, Jacas J, Angel del Rio
M, 2007. Effects of X-ray irradiation and sodium carbonate
treatments on postharvest Penicillium decay and quality attributes of
clementine mandarins. Postharvest Biology and Technology 46, 252–
61.
Patil BS, Vanamala J, Hallman G, 2004. Irradiation and storage influence
on bioactive components and quality of early and late season ‘Rio
Red’ grapefruit (Citrus paradisi Macf.). Postharvest Biology and
Technology 34, 53–64.
Piri I, Babayan M, Tavassoli A, Javaheri M, 2011. The use of gamma
irradiation in agriculture. African Journal of Microbiology Research 5,
5806–11.
Prusky D, Alkan N, Mengiste T, Fluhr R, 2013. Quiescent and
necrotrophic lifestyle choice during postharvest disease development.
Annual Review of Phytopathology 51, 155–76.
Ribeiro J, Cavaglieri L, Vital H et al., 2011. Effect of gamma radiation
on Aspergillus flavus and Aspergillus ochraceus ultrastructure and
mycotoxin production. Radiation Physics and Chemistry 80, 658–63.
Romanazzi G, Feliziani Z, Banos SB, Sivakumar D, 2017. Shelf life
extension of fresh fruit and vegetables by chitosan treatment. Critical
Reviews in Food Sciences and Nutrition 11, 579–601.
Plant Pathology (2018) 67, 18–29
View publication stats
29
Rothkamm K, Barnard S, Moquet J, Ellender M, 2015. DNA damage
foci: meaning and significance. Environmental and Molecular
Mutagenesis 56, 491–504.
Shama G, Alderson P, 2005. UV hormesis in fruits: a concept ripe for
commercialization. Trends in Food Science & Technology 16, 128–36.
Shea KM, 2000. Technical report: irradiation of food. Committee on
Environmental Health. Pediatrics 106, 1505–10.
Shintani H, Tahata T, Hatakeyama K, Takahashi M, Ishii K, Hayashi H,
1995. Comparison of D10-value accuracy by the limited Spearman-
Karber procedure (LSKP), the Stumbo-Murphy-Cochran procedure
(SMCP), and the survival-curve method (EN). Biomedical
Instrumentation & Technology 29, 113–24.
Singh SP, Pal RK, 2009. Ionizing radiation treatment to improve
postharvest life and maintain quality of fresh guava fruit. Radiation
Physics and Chemistry 78, 135–40.
Slade D, Radman M, 2011. Oxidative stress resistance in Deinococcus
radiodurans. Microbiology and Molecular Biology Reviews 75, 133–91.
Smith SJ, Pillai S, 2004. Irradiation and food safety. Food Technology
58, 48–55.
Spalding DH, Reeder WF, 1986. Decay and acceptability of mangoes
treated with combinations of hot water, imazalil and gamma
irradiation. Plant Disease 70, 1149–51.
Stumbo CR, 1973. Thermobacteriology in Food Processing. New York,
NY, USA: Academic Press.
Sumira J, Parween T, Siddiqi TO, Mahmooduzzafar, 2012. Enhancement
in furanocoumarin content and phenylalanine ammonia lyase activity
in developing seedlings of Psoralea corylifolia L. in response to gamma
irradiation of seeds. Radiation and Environmental Biophysics 51,
341–7.
Sweeney MJ, Dobson ADW, 1998. Mycotoxin production by
Aspergillus, Fusarium and Penicillium species. International Journal of
Food Microbiology 43, 141–58.
Talibi I, Boubaker H, Boudyach EH, Ait Ben Aoumar A, 2014.
Alternative methods for the control of postharvest citrus diseases.
Journal of Applied Microbiology 117, 1–17.
Temur C, Tiryaki O, 2013. Irradiation alone or combined with other
alternative treatments to control postharvest diseases. African Journal
of Agriculture Research 8, 421–34.
Tugay T, Zhdanova NN, Zheltonozhsky V, Sadovnikov L, Dighton J,
2006. The influence of ionizing radiation on spore germination and
emergent hyphal growth response reactions of microfungi. Mycologia
98, 521–7.
US Food and Drug Administration, 2012. Irradiation in the production,
processing and handling of food. Final rule. Federal Register 77,
71316–20.
Usall J, Casals C, Sisquella M, Palou L, De Cal A, 2015. Alternative
technologies to control postharvest disease of stone fruits. Stewart
Postharvest Review 4, 2.
Vicente AR, Pineda C, Lemoine L, Civello P, Martinez GA, Chaves AR,
2005. UV-C treatments reduce decay, retain quality, and alleviate
chilling injury in pepper. Postharvest Biology and Technology 35,
69–78.
Wall M, Khan S, 2008. Postharvest quality of dragon fruit (Hylocereus
spp.) after X-ray irradiation quarantine treatment. HortScience 43,
2115–9.
Wisniewski M, Droby S, Norelli J, Liu J, Schena L, 2016. Alternative
management technologies for postharvest disease control: the journey
from simplicity to complexity. Postharvest Biology and Technology
122, 3–10.
Yoon M, Jung K, Lee KY, Jeong J, Lee J, Park H, 2014. Synergistic
effect of the combined treatment with gamma irradiation and sodium
dichloroisocyanurate to control gray mold (Botrytis cinerea) on
paprika. Radiation Physics and Chemistry 98, 103–8.