17
REVIEW / SYNTHÈSE
Effect of gamma (γ) radiation on morphological,
biochemical, and physiological aspects of plants
and plant products
Sumira Jan, Talat Parween, T.O. Siddiqi, and X. Mahmooduzzafar
Abstract: Research on the basic interaction of radiation with biological systems has contributed to human society through
various applications in medicine, agriculture, pharmaceuticals and in other technological developments. In the agricultural
sciences and food technology sectors, recent research has elucidated the new potential application of radiation for microbial
decontamination due to the inhibitory effect of radiation on microbial infestation. The last few decades have witnessed a
large number of pertinent works regarding the utilization of radiation with special interest in g-rays for evolution of superior
varieties of agricultural crops of economic importance. In this review, general information will be presented about radiation,
such as plant specificity, dose response, beneficial effects, and lethality. A comparison of different studies has clarified how
the effects observed after exposure were deeply influenced by several factors, some related to plant characteristics (e.g., species, cultivar, stage of development, tissue architecture, and genome organization) and some related to radiation features (e.
g., quality, dose, duration of exposure). There are many beneficial uses of radiation that offer few risks when properly employed. In this review, we report the main results from studies on the effect of g-irradiations on plants, focusing on metabolic alterations, modifications of growth and development, and changes in biochemical pathways especially physiological
behaviour.
Key words: growth modulation, metabolic alteration, elicitation.
Résumé : French French French French French French French French French French French French French French French
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Mots‐clés : , , .
[Traduit par la Rédaction]
1. Introduction
With the discovery of X-rays by W.C. Roentgen in 1896,
there was hope for employing this new technology as a tool
Received 5 February . Accepted 12 October 2011. Published at
www.nrcresearchpress.com/er on XX January 2012.
S. Jan, T.O. Siddiqi, and X. Mahmooduzzafar. Department of
Botany, Hamdard University, New Delhi-62, India.
T. Parween. Department of Biosciences, Jamia Millia Islamia,
New Delhi-25, India.
Corresponding author: Mahmooduzzafar (e-mail: sumira.
[email protected]).
Environ. Rev. 20: 17–39 (2012)
in plant improvement programs. Hugo de Varies in 1901 and
1903 presented (in two volumes) Die mutations theorie in
which an integrated concept for the occurrence of mutation
was outlined. The first attempts to stimulate plant growth by
exposing seeds or growing plants to low doses of ionizing radiation or by the use of radioactive fertilizers, dates back to
the 1960s (Sax 1963). Low and high-LET (linear energy
transfer) ionizing radiations have been used widely in breeding programs because they are expected to cause mutations
over a wide spectrum (Yamaguchi et al. 2003; Okamura et
al. 2003; Zhou et al. 2006). Examples of favourable traits induced after exposures are semi-dwarf growth, earlier maturity, higher yields, and resistance to diseases (Mei et al. 1994;
doi:10.1139/A11-021
PROOF/ÉPREUVE
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Pagination not final/Pagination non finale
18
Environ. Rev. Vol. 20, 2012
Li et al. 2007). The different results obtained by various
groups of plants allowed Muller (1927) to first conclude that
the rate of appearance of sudden heritable change in plants
and animals can be greatly increased by ionizing radiation.
Much evidence of modification and injury to plant parts is
found in the extensive literature on the effects of X-ray treatment of plants. Johnson (1939) listed the effects produced on
70 species of flowering plants. Seedlings from soaked dry
wheat (Triticum aestivum L.) and barley seeds (Hordeum vulgare L.) with 1000 and 5000 R reduced all growth respects,
but showed increased tillering. Such exposures mainly stimulated seed germination, plantlet growth, flowering, plant size,
and yield (reviewed by Breslavets 1946). However, it is difficult to compare the current data on plant responses to g-irradiation as the models and parameters of past experiments
varied greatly. Thus, the type of irradiation (e.g., acute or
chronic), the dose rate or the dose applied, the physiological
parameters such as the species/variety/cultivar considered, the
developmental stage at the time of irradiation and, finally,
inter-individual response variations could all different among
studies (Gunckel et al. 1953; Gunckel 1957; Boyer et al.
2009; Kim et al. 2009) and even among genotypes of the
same species (Kwon and Im 1973). Emerging seedlings are
the stage of development most sensitive to radiation. The survival of grain seedlings was determined by using simulated
fallout g exposure. It is well known that the resistance of
plant seeds is stronger than that of animal cells (Casarett
1968; Kumagai et al. 2000; Real et al. 2004). Indeed, the
seed is a peculiar stage of a plant’s life cycle characterized
by higher resistance to environmental factors because of its
structural and metabolic traits, when compared with organs
at different life stages. There are also differences in sensitivity to irradiation between dry and fresh seeds because of their
water content and structures that affect the capacity of ions to
penetrate and reach the embryo (Yu 2000; Wu and Yu 2001;
Qin et al. 2007). Complex tissue organization seems to be
more resistant to the harmful and mutagenic effects of radiation because the multicellular status allows cell and tissue repair (Chadwick and Leenhouts 1981; Friedberg 1985; Kranz
et al. 1994; Huang et al. 1997; Shikazono et al. 2002; Durante and Cucinotta 2008). This lack of uniformity is further
complicated by the co-existence of experimental data, applied
data from the food industry, and data emerging from accidents (e.g., Chernobyl). Further complexity was created by
radiation applied in different dosage measurements. To avoid
confusion we have inculcated historical dosimetery (Table 1).
Therefore, in the field of plant radiation, doses vary from
only a few Grays (Gy) up to several hundred Gy in experimental irradiations, but can reach kGy in agribusiness or for
varietal selections (e.g., Bhat et al. 2007; Maity et al. 2009).
Furthermore, the dose range response is strongly dependent
on the species studied. It is difficult to predict a standard response to g-irradiation in plants; however, some patterns do
emerge.
g-rays are the most energetic form of electromagnetic radiation and they possess an energy level from 10 keV (kilo
electron volts) to several hundred keV. they are considered
the most penetrating radiation source compared with other
sources such as alpha and beta rays (Kovács and Keresztes
2002). g-rays fall into the category of ionizing radiation and
interact with atoms or molecules to produce free radicals in
Table 1. Unit equivalences between systems.
SI units
1 Gray (Gy)
1 Sievert
10 mGy
10 mSv
Historical dosimetry
100 R
100 rem = 100 rad
1 Roentgen
1 rem = 1 rad
cells. These radicals can damage or modify important components of plant cells and have been reported to affect the
morphology, anatomy, biochemistry, and physiology of plants
differentially, depending on the irradiation level. These effects include changes in the plant cellular structure and metabolism e.g., dilation of thylakoid membranes, alteration in
photosynthesis, modulation of the antioxidative system, and
accumulation of phenolic compounds (Kim et al. 2004; Wi
et al. 2005). Several cytogenetic and mutational studies have
been performed with plant systems exposed to ionizing radiation (Table 2). The purposes of these studies was both to try
and determine the harmful effects of radiation and to establish the radiation quality and dose range in which benefits,
in terms of more productive or in general more suitable plant
systems, could be obtained.
2. Seed germination
The resumption of active growth in the embryo of a seed,
as demonstrated by the protrusion of a radicle (embryonic
root axis) is termed germination. Results regarding the effect
of radiation exposure on germination are variable, especially
when pre-irradiation treatments are involved. In various experiments, parameters such as germination rate and per cent
are reported to increase, decrease, or remain unchanged after
irradiation. Higher exposures were usually inhibitory (Bora
1961; Radhadevi and Nayar 1996; Kumari and Singh 1996),
whereas some authors refer to the concept of hormesis, the
stimulation of different biological processes (e.g., faster germination, increased growth of roots and leaves), that occurs
when seeds are subjected to pre-irradiation with low doses
of a radiation source (Luckey 1980; Bayonove, et al. 1984;
Zimmermann et al. 1996; Sparrow 1966; Thapa 1999). The
stimulatory effects of g-rays on germination may be attributed to the activation of RNA synthesis (Kuzin et al. 1975)
on castor bean (Ricinus communis L.) or protein synthesis
(Kuzin et al. 1976), which occurred during the early stage of
germination after seeds irradiated with 4 krad (40 Gy). This
could be due to the enhanced rate of respiration or auxin metabolism in seedlings. The inability of seeds to germinate at
higher doses of g-rays has been attributed to several reasons:
(i) numerous histological and cytological changes; (ii) disruption and disorganisation of the tunica or seed layer that is directly proportional to the intensity of exposure to g-rays; (iii)
impaired mitosis or virtual elimination of cell division in the
meristematic zones during germination (Lokesha et al. 1992).
The inhibition of seed germination and seedling growth exerted by irradiation has often been ascribed to the formation
of free radicals in irradiated seeds (Kumagai et al. 2000; Kovács and Keresztes 2002). Many studies have been carried
out evidencing the effects of variable doses of g-irradiation
levels on germination, survival rate and lethality (Table 3).
Published by NRC Research Press
PROOF/ÉPREUVE
Jan et al.
19
Table 2. Effects of exposure to g radiation on chromosome aberrations of different plant parts.
Source of radiation
X-rays, 1.7 MeV neutrons
g, 16 MeV neutrons
g, 40Ar,56Fe
Species
H. gracilis (Nutt.)
N. plumbaginfolia (L.)
Rice (Oryza sativa L.)
Plant part
Cell suspensions
Protoplasts
Seeds
g, H+, He and N+
g, H+, He, C5+
g
P. sativum (L.)
N. tabacum L.
A. thaliana (L.)
g, C5+
N. tabacum (L.)
Seedlings
Seeds
Transgenic seed
and seedlings
Seeds
g, C5+
g60Co,137Cs
g
N. tabacum (L.)
N. tabacum (L.)
T. durum (L.)
Protoplasts
Protoplasts
Seeds
Ne, Si,40Ar
A. cepa (L.)
Seedlings
3. Plant growth and development
Growth and development in crop plants do not proceed at
constant or fixed rates through time. Plant development is a
term that includes a broad spectrum of processes by which
plant structures originate and mature as growth occurs. Any
change in growth pattern will ultimately affect maturity and
yield. g-irradiation of seed has been found to exert pronounced effects on plant growth. The exposure to g-irradiations can have stimulatory effects on specific morphological
parameters and can increase the yield of plants in terms of
growth (e.g., taller plants), reproductive success (e.g., formed
seeds) and ability to withstand water shortage (Dishlers and
Rashals 1977; Zaka et al. 2002; Maity et al. 2005; Yu et al.
2007; Melki and Dahmani 2009). A more detailed description of morphological abnormalities were documented by
Gunckel (1957) and Sparrow (1966). These results allowed
several authors (Patskevich 1961; Davies and Mackay 1973;
Auni et al. 1978) to conclude that the irradiation of seeds
prior to sowing held great promise from a viewpoint of its
practical application in agriculture. It was generally observed
that low doses of g-rays stimulated cell division, growth, and
development in various organisms, including animals and
plants. This phenomenon, termed “hormesis”, has been discussed at length for various plant species (Luckey 1980; Sagan 1987; Korystov and Narimanov 1997). However, the way
radiation influences plant growth and development is still unknown and the available data remains controversial. Indeed,
the magnitude of reported hormetic effects of radiation is
usually small; being approximately 10% of control values
and often not providing critical evidence that crop yield is
significantly increased by irradiating seeds (Miller and Miller
1987). The morphological, structural, and functional changes
depend on the strength and duration of the g-irradiation dose
applied. The symptoms frequently observed in plants irradiated with a low or high dose were enhancement or inhibition
of germination, seedling growth, and other biological responses (Kim et al. 2000; Wi et al. 2005). Although no conclusive explanations for the stimulation effects of low dose girradiation have been available until now, papers support a
hypothesis that the low dose irradiation will induce growth
stimulation by changing the hormonal signalling network in
plant cells or by increasing the antioxidative capacity of cells
Parameter studied
Cell survival
Cell survival
Micronuclei and chromosomal
aberrations
Micronuclei
Chromosomal aberrations
Homologus recombination
Chromosomal aberrations in
roots of different length
Cell survival
Unrepaired dsb
Chromosomal aberrations in
the M1 generation
Micronuclei
References
Werry and Stoffelsen (1979)
Magnien et al. (1981)
Mei et al. (1994)
Vasilenko and Sidorenko (1995)
Hase et al. (1999)
Kovalchuk et al. (2000)
Hase et al. (2002)
Yokota et al. (2003)
Yokota et al. (2007)
Cao et al. (2009)
Takatsuji et al. (2010)
to easily overcome daily stress factors such as fluctuation of
light intensity and temperature in growth conditions (Kim et
al. 2004; Wi et al. 2007). In contrast, the growth inhibition
induced by high-dose irradiation has been attributed to the
cell cycle arrest at the G2/M phase during somatic cell division and (or) varying damage to the entire genome (Preuss
and Britt 2003). The relationship between growth of irradiated plants and the dose of g-irradiation has been manifested
by investigating the morphological changes and seedling
growth of irradiated plants. Low doses apparently inhibit
auxin synthesis while larger doses can destroy auxin activity
directly. As with other wound responses, irradiated tissues
often produce endogenous ethylene (Maxie et al. 1966;
Dwelle 1975; Chervin et al. 1992; Liu et al. 2008). Many
studies have been carried out to evidence the effects of variable doses of g-irradiation levels on growth and yield attributes (Table 4).
Growth inhibition by g-irradiation may be related to auxin
and DNA biogenesis in a relationship as shown indicated in
Fig. 1. These relationships postulate exclusive possibilities:
(1) that DNA is required for and is previously synthesized sequentially to auxin formation, the radiation block occurring
in the formation of nucleic acid; (2) that the primary radiation block is in auxin synthesis, the auxin required for the
formation of DNA; and (3) that the effect of radiation is on
an undefined entity in reaction previous to and essential for
both DNA and auxin synthesis (Lage and Esquibel 1995;
Momiyama et al. 1999).
g-irradiation had a stimulatory effect on primary branches
and yield attributes, including number of pods per plant,
number of flowers per plant, seed index, etc. following low
doses of g-rays and inhibition of the same attributes at higher
rates (Charumathi et al. 1992; Khan et al. 2000; Jan et al.
2010). These groups further investigated the effectiveness of
g-irradiation for induction of early flowering in legumes.
Yousaf et al. (1991) and Svetleva and Petkova (1992) reported inhibitory effects of g-irradiation on seed maturity,
flowering, plant height, and seed yield per plant. g-irradiation
prolonged the growth period and retarded plant height in
french beans (Phaseolus vulgaris L.). An increased number
of okra fruit per plant and fruit length as a result of g-irradiation was recorded by many authors (Dubey et al. 2007; MisPublished by NRC Research Press
PROOF/ÉPREUVE
20
Table 3. Effects of exposure to g irradiation on seed germination of different plant.
Dosage applied and duration
of irradiations
2–50 krad
Lentil (Lens culinaris Medik)
Seed
Rice (Oryza sativa L.)
Sweet potato (Ipomoea batatas L.)
Pinus kesiya and P. wallichiana
Seeds
Tuber
Seeds
Maize (Zea mays, Okra
(Abelmoschus esculentus and
Groundnut (Arachis hypogeal L.)
Long bean (Vigna sesquipedalis).
Seeds
Tomato (Lycopersicon esculentum
cv)
Snap bean (Phaseolus vulgaris)
Seeds
Atropa belladonna
Seeds
Chilli (Capsicum annuum)
Seeds
Chick pea (Cicer arietinum L)
Seed
Pumpkin (Cucurbita pepo L.)
Seed, Pollen
20–80 krad g radation at the
rate of 2.8 kR/min.
100–400 Gy; dose rate of
0.864 kGy/h
10, 30, 50 kR
Lepidum sativum L.
Seeds
Wheat (Triticum aestivum L.)
Seeds, Seedlings
Corn (Zea mays L.)
Seeds
300–500 Gy
Okra (Abelmoschus esculentus
Moench
Seeds
0.1–1 kGy, 1.66 kGy h–1 at
the time of irradiation
150–300 Gy
0.085 and 0.15 kGy
1.0–30.0 kR g-radation at
the rate of 2.8 kR/min.
PROOF/ÉPREUVE
150, 300, 500, 700, 900,
1000 Gy; dose rate
10 Gy/28.97 s
300, 400, 500, 600 and
800 Gy
300–800 Gy
300, 400, 500, 600, and
800 Gy
20–110 Gy
300, 400, 500, 600, and
800 Gy
100–1200 Gy, 1.66 kGy h–1
at the time of irradiation
50–300 Gy
Seeds
Seeds
Published by NRC Research Press
Parameter studied seed germination
2 krad resulted 2% stimulation of germination
and 0.7% with 50 krad
Germination percentage was reduced to 40.87%
at 0.2 kGy and no germination at 1.0 kGy dose
Germination decrease from 100% to 97.2%
(8.5 and 15 krad) inhibits sprouting
Seeds exposed to 30 kR germinated whereas in
P. wallichiana 30 kR was lethal and seed
germination was restricted up to 20 kR only
90% germination was achieved at 240 Gy in
maize, 70% at 170 Gy in Okra and 58% at
300 Gy in groundnut.
70.56% increase at 400 Gy. At 800 Gy no
germination.
Germination decrease from 88% to 48.70% with
800 Gy
Germination decrease from 75.56% to 51.11%.
At 800 Gy failed to germinate
Germination rate increased from 21.18% to
93.33% at 110 Gy
Decrease in germination 42.22% to 15.56%, seeds
irradiated with 800 Gy failed to germinate.
Seed germination, 60%–76% increase with 100–
500 Gy, 80%–96% decrease with700–1200 Gy
75.0% increment in germination (at 50 Gy) to
63.0% (at 100 Gy)
92.50%–97.50% increment in germination with
8krad
Germination percentage decrease from 8.8%
(100Gy) to 5.5% (400Gy)
10 kR had 30% germination and the untreated
had 50% germination.
Seed germination 87%–91% increase with
500 Gy
References
Zeid et al. (2001)
Chaudhuri (2002)
Cheema and Atta (2003)
Tabares and Perez (2003)
Thapa (2004)
Pagination not final/Pagination non finale
Plant part or age /stage of
plant growth for g-irradiation
Seeds
Mokobia and Anomohanran
(2005)
Kon et al. (2007)
Norfadzrin et al. (2007)
Ellyfa et al. (2007)
Abdelhady et al. (2008)
Omar et al. (2008)
Shah et al. (2008)
Kurtar (2009)
Majeed et al. (2009)
Borzouei et al. (2010)
Itol et al. (unpublished)
Hegazi and Hemeldeldin
(2010)
Environ. Rev. Vol. 20, 2012
Species
Fennel (Foeniculum vulgare Mill.)
Jan et al.
Table 4. Effects of exposure to g irradiation on morphological and yield attributes of different plant species.
Dosage applied and duration
of irradiation
1–20 Gy
0.5–60 Gy, dose rate 2.94
Gy /min
150–300 Gy
Species
Chineses Cabbage (Brassica
campestris L.Cv.)
Pea (Pisum sativum)
Plant part or age /stage of
plant growth for g-irradiation
Seeds
Seeds
PROOF/ÉPREUVE
Seeds
1, 1.5, 2.5, 5, and 10 krad
Corn (Zea mays L.)
Seeds
2, 4, 8, and 16 Gy Dose rate
150 TBq of capacity
Red pepper (Capsicum annuum)
Seeds
1.0–30.0 kR g radation at
the rate of 2.8 kR/min.
Pinus kesiya and P. wallichiana
Seeds
2, 4, 8, and 16 Gy, dose rate
150 TBq of capacity
Red pepper (Capsicum annuum)
Seeds
50–350 Gy; dose rate 120 G/
h
Rice (oryza sativa), Mung
(Phaseolus vulgaris)
Seeds
150, 250, 350, and 450 Gy
Wheat (Triticum aestivum L.)
Seeds
10–100 Kr; dose rate 5000
ci Co60
20–80 krad g radation at the
rate of 2.8 kR/min.
10–100 Gy, dose rate 1.858
Gy/s
100–400 Gy; dose rate of
0.864 kGy/h
200, 700, 1200 Gy
Crotalaria saltiana L.
Seeds
Lepidum sativum L
Seeds
Thai Tulip (Curcuma
alismatifolia Gagnep)
Wheat (Triticum aestivum L.).
Seeds
Barley (Hordeum vulgare spp.)
Seeds
Seeds
Mean survival rate 50% with 20 Gy and 2% survival
at 40 Gy.
80.61%, 62.5%, 31.42% decrease in root length, root
fresh weight and shoot length, respectively.
50% reduction in shoot length with 1200 Gy, 29.67%
decrease in root number with 1200 Gy.
References
Kim et al. (1998)
Zaka et al. (2002)
Cheema and Atta (2003)
Al Salhi et al. (2004)
Kim et al. (2004)
Thapa (2004)
Kim et al. (2004)
Maity et al. (2005)
Abdelhady and Ali (2006)
Shah et al. (2008)
Majeed et al. (2009)
Abdullah et al. (2009)
Borzouei et al. (2010)
Nasab et al. (2010)
21
Published by NRC Research Press
Rice (Oryza sativa L.)
Morphological and yield attributes response
45.67% increment in plant height and 14% increase in
fresh weight with 20Gy.
20% Decrease in plant height with 6 Gy. Doses between 10 and 40 Gy were lethal.
300 Gy causing 50% seedling height reduction and
induction of >71% sterility with the was same in all
the three rice varieties.
Grains exposed to 1.5 and 2.5 krad resulted in 84%
and 76% decrease in shoot length.
Except for 16 Gy dose seedlings showed 13% to
25%, 5% to 20%, or 26% to 44% increase in stem
length, diameter and leaf area, respectively.
In Pinus .kesiya, root length showed more than 50%
inhibtion by g dose 10 kR. While asin P. wallichaina 10kR proved lethal
Except for 16 Gy dose seedlings showed 13% to
25%, 5% to 20%, or 26% to 44% increase in stem
length, diameter and leaf area, respectively.
50 Gy resulted in 60% increase in seed yield, plant
height in Oryza sativa L., for Phseolus mungo 200
Gy resulted in 56% increase in plant height.
88.99% callus induction with 150 Gy, 45.98% and
28.65% reduction with 350 and 450 Gy. 15.94% increment in grain yield and 37.85% decrease ingrain
yield with 450 Gy.
64.1% and 51.85% increment in plant height with 30
Kr and 50 Kr.
Shoot length decreased 76.42% to 28.20%,
Pagination not final/Pagination non finale
22
Environ. Rev. Vol. 20, 2012
Fig. 1. Effect of g radiation plant growth, development, and metabolism.
WHOLE PLANT LEVEL
BIOCHEMICAL LEVEL
Survival of
Resultant
Individuals
CELLULAR LEVEL
CHRONIC EXPOSURE
γ
R
A
Y
S
Enzyme effects
(in vivo)
Metabolic Pathways
Disruption
Cellular organelles
Membrane
Impairment
Cell Death
Plant Death
Necrosis
Break down of metabolic
Pathways
Cell Changes
Imbalances
Chlorosis
Senescence
Biochemical Reactions
Changes in cellular
Constituents
Enzyme effects
(in vitro)
In vitro changes
In cellular organelles
Genetic code
Transcription &
translation
Growth, yield,
quality reduction
hra et al. 2007; Sharma and Mishra 2007). Soehendi et al.
(2007) stated that modification obtained by g-irradiation of
mung bean (Vigna radiata L.) leaflet type could affect leaf
canopy and alter seed yield. A higher dose of g-irradiation
(500 Gy) in this study was less effective than the two other
lower doses. This observation was also stated by (Artık and
Pekşen 2006), who found a reduction in faba bean (Vicia
faba L.) seed yield and harvest index in some varieties when
seeds were treated with relatively low doses (25 and 50 Gy)
of g-irradiation. Plant biomass in plants was significantly affected by g-irradiation. The biomass was reduced by approximately 50% at a dose of 20–60 Gy. This is consistent with
the radiation responses of cereals, in which doses of 20–60
Gy reduced yield by 50% depending on the stage of development at exposure (Fillipas et al. 1992). Carbon partitioning is
altered by increasing the radiation dose because of damage to
radiosensitive cells responsible for the transport of carbohydrates in the phloem (Thiede et al. 1995).
4. Biochemical and physiological effects
g-irradiation can be useful for the alteration of one or a
few physiological characters (Lapins 1983). Photons of g-irradiation are powerful enough to be completely democratic
with regard to the molecular species with which they interact
(Fig. 1). Based on previous research reports, the total protein
and carbohydrate contents decreased with increasingly higher
dosage of g-irradiation caused by higher metabolic activities
and hydrolyzing enzyme activity in germinating seed (Barros
et al. 2002; Maity et al. 2004). Radiation resulted in the increased absorption of glucose, pyruvate, and the decreased
Growth, yield
Quality reduction
Reduce vigor, moresusceptibility
absorption of acetate and succinate in carrot (Dacus carrota
L.). Radiation reduced the anabolic utilization of all substrates (Bourke et al. 1967). Bourke et al. reported a decrease
in all amino acids upon irradiation except for serine and valine, which were increased at 100 krad (1 Gy). Irradiation
with doses of 15–30 kGy could reduce viscosity of pectin
and alginate (Irawati and Pilnik 2001). Subtle differences in
the degradation of oligosaccharides in processed legumes
were reported by (Machaiah and Pednekar 2002) between
control and irradiated dry seeds of Bengal gram (Cicer arietinum L.), Horse gram (Macrotyloma uniflorum (Lam.)
Verdc.) and cow pea (Vigna unguiculata (L.) Walp.). g-irradiation breaks the seed protein and produces more amino
acids (Barros et al. 2002; Maity et al. 2004; Kiong et al.
2008). This process may also inhibit protein synthesis. Total
proteins and carbohydrates decreased with increasing high gray dosage in wheat and rice plants (Hagberg and Persson
1968; Inoue et al. 1975). Lester and Whitaker (1996) observed the retention of proteins in the plasma membrane of
muskmelon (Cucumis melo L.) fruit 10 days after treatment
with 1 kGy irradiation. The effect of g-irradiation on the concentration of total free amino acid nitrogen of five varieties
of Iraqi dates (Phoenix dactylifera L.) was studied. The most
sensitive amino acids appear to be proline, glutamic acid, aspartic acid, serine, histidine, lysine, and tyrosine, while methionine, isoleucine and leucine showed a slight increase in
two varieties (Auda and Al-Wandawi 1980). Extensive research has shown that proteins, essential amino acids, minerals, trace elements and most vitamins do not represent
significant losses during irradiation, even at doses over 10
kGy. Pradeep et al. (1993) reported that amino acids like lyPublished by NRC Research Press
PROOF/ÉPREUVE
Jan et al.
23
sine and histidine were resistant to g-irradiation (5 kGy) in
Ginseng panax leaf tea (herb). Al-Jassir (1992) found that
the contents of arginine, methionine, lysine, phenylalanine,
and leucine of garlic bulbs (Allium sativum L.) increased
slightly. However, reduction in other amino acids in irradiated samples also occurred, especially at higher doses.
Many studies by (Marchenko et al. 1996; Ussuf et al.
1996) have also shown that irradiated plant cells have a selfprotection mechanism. This mechanism works by enhancing
the synthesis of substance groups or enzymes containing sulfur such as amino acids (cysteine, cystine), glycation, and
superoxide dismutase, which can protect, remove free radicals, and participate in the simultaneous release of protective
substances in an organism (Qui et al. 2000). The maximum
increase in sucrose content in both potato tubers and sweet
potato roots was achieved by an irradiation dose of 3 to 4
kGy for potatoes (Solanum tuberosum L.) and 0.8 to 2 kGy
for sweet potatoes (Ipomoea batatas L.) Hayashi and Kawashima (1982). Low doses of g-rays enhance chlorophyll synthesis by increasing the activating enzyme system. These
results were almost in agreement with those of other groups
(Zeerak et al. 1994; Al-Kobaissi et al. 1997; Gautam et al.
1998; Rascio et al. 2001; Osama 2002), who reported that
the improvement of yield components and chlorophyll parameters in various plants such as tomato (Lycopersicon esculentum L.), maize (Zea mays L.), rice (Oryza sativa L.),
and wheat (Triticum aestivum L.) was induced after variable
doses of g-rays. Soehendi et al. (2007) stated that the modification obtained by g-irradiation of mung bean leaflet type
could affect leaf canopy and alter seed yield. Thus, modified
mung bean lines that exhibited greater leaf area per plant
would have enhanced photosynthetic rate and hence gave
greater yield. g-rays were also found to cause modulation in
protein patterns by inducing appearance and (or) disappearance of some protein bands (Rashed et al. 1994). Yoko et al.
(1996) studied the effect of g-irradiation on the genomic
DNA of corn, soybean, and wheat. They concluded that large
DNA strands were broken into small strands at low irradiation dose but small and large DNA strands were broken at
higher irradiation doses. This observation was also stated by
Artık and Pekşen (2006) who found a reduction in faba bean
seed yield and harvest index in some varieties when seeds are
treated with relatively low doses 25 and 50 Gy of g-irradiation.
Higher g-irradiation inhibits chlorophyll synthesis in wheat
(Kovács and Keresztes 2002) and changes in pigmentation
(reddening) were observed in the older leaves of Holcus lanatus L. treated with 40, 80, and 160 Gy (Jones et al. 2004).
This was demonstrated in etiolated barley and wheat leaves,
in potato tubers. In fruits with chloroplast in hypodermis at
the time of harvest (Hardenpont pear) it was found that g-irradiation (1 kGy) altered chloroplast structure characteristically (Kovács and Keresztes 1991). Byun et al. (2002)
utilized irradiation technology to reduce or eliminate the residual chlorophyll in oil processing without developing lipid
peroxidation during irradiation.
g-irradiation can be useful for the alteration of physiological characteristics (Kiong et al. 2008). The biological effect
of g-rays is based on the interaction with atoms or molecules
in the cell, particularly water, to produce free radicals (Kovács and Keresztes 2002). These radicals can damage or
modify important components of plant cells and have been
reported to affect differentially the morphology, anatomy, biochemistry, and physiology of plants depending on the radiation dose (Ashraf et al. 2003). These effects include changes
in the plant cellular structure and metabolism e.g., dilation of
thylakoid membranes, alteration in photosynthesis, modulation of the anti-oxidative system, and accumulation of phenolic compounds (Kovács and Keresztes 2002; Kim et al.
2004; Wi et al. 2007; Ashraf 2009). From the ultra-structural
observations of the irradiated plant cells, the prominent structural changes of chloroplasts after radiation with 50 Gy revealed that chloroplasts were more sensitive to a high dose
of g-rays than the other cell organelles. Plastids were affected
by irradiation in two ways: (i) inhibition of senescence and
(ii) dedifferentiation into agranal stage (Kim et al. 2004) (Table 5). The developmental regression of chloroplasts can be
assumed primarily from destruction of grana (Kovács and
Keresztes 1989). Similar results have been reported to be induced by other environmental stress factors such as UV,
heavy metals, acidic rain, and high light (Molas 2002; Gabara et al. 2003; Quaggiotti et al. 2004). However, the lowdose irradiation did not cause these changes in the ultrastructure of chloroplasts. The irradiation of seeds with high
doses of g-rays disturbs the synthesis of protein, hormone
balance, leaf gas exchange, water exchange, and enzyme activity (Hameed et al. 2008). The chlorophyll content of g-irradiated wheat displayed a gradual decrease at 200 Gy dose
(Borzouei et al. 2010). Kiong et al. (2008) reported that the
reduction in chlorophyll b is due to a more selective destruction of chlorophyll b biosynthesis or degradation of chlorophyll b precursors. Furthermore, Kim et al. (2004) have
evaluated the chlorophyll content on irradiated red pepper
plants; their results showed that plants exposed at 16 Gy
may have ~23% increase in their chlorophyll content that can
be correlated with stimulated growth. Modulation in photosynthesis in irradiated plants might partly contribute to increased growth (Kim et al. 2004; Wi et al. 2007).
The effect of presowing g-irradiation treatments on the
growth and respiration of germinating corn was investigated.
Exposures of 40 and 80 krads caused marked inhibition in
seedling growth and inhibited the rate of respiration, measured as oxygen uptake per seedling (Woodstock and Combs
1965). In contrast to radiation chemistry of food proteins
and carbohydrates, where indirect radiation effects mediated
through water play a major role, reactions of lipids with reactive species of water radiolysis play only minor role in most
situations, quantitatively at least. The primary effect of an
electron upon fats leads to cation radicals and excised molecules. Regardless of localization, the main reactions of the
cation radical are deprotonation, followed by dimerization or
disproportionation. Another primary effect is electron attachment, which may be followed by dissociation and decarbonylation or dimerization (Diehl 1990). Additional reactions
can be initiated from the excited triglyceride molecules. This
leads to formation of particular free radicals as principal intermediates, and ultimately to a particular end product. The
low dose used could have produced its long term effects in
part by means of stimulation of lipid degradation, possibly
mediated through the action of free radicals that are known
to be generated after irradiation (Katsaras et al. 1986; Voisine
et al. 1991). Increases in irradiation doses to 10 and 15 kGy
Published by NRC Research Press
PROOF/ÉPREUVE
Dosage applied and duration
of irradiation
2,4 and 8 kGy; dose rate
38.1 kGy/h
3.35, 6.70, 10.05, and 13.40
Gy; dose rate of 0.8 mGy/s
Dose range 5–160 Gy; dose
rate 7.0 Gy/min
0.15 and 0.30 kGy; exposure
time 30 and 55 min, respectively
2, 4, 6, 8, and 10 k rad; dose
rate 10 min/k-dose rate
Plant part or age /stage of
plant growth for g-irradiation
Dry kidney beans
Phyiological and biochemical response
8 kGy increased deamidation by 65.89%, sulfahydryl content
was reduced to 23.1%
Relative chlorophyll concentration increased from 6.3% at
3.35 Gy to 16.8% at 13.40%
Shoot nitrogen concentration increased to 3.7% at 20 Gy
References
Dogbevi et al. (1999)
Bulbs
Glucose, fructose, sucrose were decreased to 21.34, 45.65%
and 34.8%, respectively
Benkeblia et al. (2004)
Chamomile (Chamomilla
recutita L.)
Seeds
Nassar et al. (2004)
Sunatoarea (Hypericum
perforatum L.)
Rocket (Eruca vesicaria
ssp. .sativa)
Leaves
1, 2, 4, 6, 8, and 10 kGy;
dose rate 228Gy/min
5, 10, 25, and 50 Gy; dose
rate /min 10 Gy
Soybean seeds (Glycine
max (L.) Merr.)
Paulowinia tomentosa
Seeds
2.5, 5, 7.5, 10, 15, and 30
kGy. Dose rate 6.5 kGy/h
Velvet beans (Macuna
pruriens)
Seeds
0, 10, 20, 30, 40, 50, 60,
and 70 Gy; dose rate 4.64
kGy/h
2, 4, 8, 10, 12, and 16 kGy;
done rate . 0.96 kGy/h
Orthosiphon stamineus
Shoot tips
47.2% increment in essential oil, 33.69% increment in carbohydrate content with 10k rad and 21.17% increase in sugar
content
Mono saccharide content reduced to12.59% at 5 Kr. At 3 Kr
polysaccharide content increased to 23%
At 20 Gy, total sugar increased by 70.3%, total free aminoacid by 92.6%, total soluble phenol by 109%. At 200 Gy total sugar decreased by 70.7%, total free aminoacid by 69.5%
and soluble phenol by 67.5%
10% increase in total phenols, 21.6% for tannins at 1kGy. At
10 kGy increase in phenol 7.6% and tannins 11%
Chlorophyll a, chlorophyll b and total chlorophyll was reduced to 34.69%, 33.33% and 35.21% at 25 Gy, respectively
Protein content increased to 31.06% at 30 kGy, carbohydrate
content increased 2.2% at 15kGy, linoleic acid increased at
30 kGy
Plantlets irradiated at 10 and 20 Gy exhibited total soluble
protein content of 39.61 and 34.00 mg/g, respectively
Kalungi (Nigella sativa)
Seeds
0, 5, 10, 15, and 20 kGy;
dose rate of 2.38 kGy/h
Tea (Camellia sinensis L.)
Tea leaves
300, 400, and 500 Gy
Okra (Abelmoschus esculentus L.)
Seeds
100, 200, 300, 400, and 500
Gy; dose 10 Gy/min
Soybean (Glycine max L.
Merrill)
Seeds
PROOF/ÉPREUVE
50–300 Gy; dose rate
0.54 Gy/min
Seedlings
Five-leaf growth stage
Seeds
Node explants
Ichim et al. (2005)
Moussa (2006)
Štajner et al. (2007)
Alikamanoglu et al.
(2007)
Bhat et al. (2007)
Kiong et al. (2008)
Khattak et al. (2008)
Fanaroi et al. (2009)
Hegazi and Hamideldin
(2010)
Alikamanoglu et al.
(2010)
Environ. Rev. Vol. 20, 2012
Published by NRC Research Press
Extraction yields increases were 3.7%, 4.2%, 5.6%, and 9.0%
for hexane, acetone, water and methanol extracts. Phenol
content increase from 3.7 for control to 3.8 mg/g for 16
kGy
37.86% of the compounds were stable at all radiation doses
and 47.53% of new compounds were identified after irradiation
Chlorophyll a, chlorophyll b and total chlorophyll was increased to 17.19%, 18.29%, and 14.44% at 500 Gy, respectively.
Total chlorophyll decrease was 81.36% at 400 Gy and 80.91%
at 500 Gy. Increase varied between 4.75% and 87.39% for
Fe, 24.08% and 163.09% for Cu, and 9.86% and 45.14% for
Zn with respect to the control plants. Soluble protein increased 43.48% at 400 Gy and 69.57% at 500 Gy g-ray exposures
Jovanić and Dramicanin
(2003)
Jones et al. (2004)
Pagination not final/Pagination non finale
1, 3, 5, 8, 10, 12, and 15 Kr.
Species
Kidney beans (Phaseolus
vulgaris L.)
Pumpkin (Cucurbita
pepo)
Yorkshire fog grass
(Holcus lanatus)
Onion (Allium cepa L.)
24
Table 5. Effects of the exposure to g radiation on eco-physiology and biochemistry in different vegetal systems.
Nasab et al. (2010)
25
Seeds
Dosage applied and duration
of irradiation
100–400 Gy; dose rate of
0.864 kGy/h
200, 700, 1200 Gy
Table 5 (concluded).
Species
Wheat (Triticum aestivum
L.)
Barley (Hordeum vulgare
spp.)
Plant part or age /stage of
plant growth for g-irradiation
Seeds
Phyiological and biochemical response
Total chlorophyll increased 64.5% at 100 Gy. Proline content
decreased to 30%
50% reduction in shoot length with 1200 Gy, 29.67% decrease in root number with 1200 Gy.
References
Borzouei et al. (2010)
Jan et al.
resulted in an increase in free fatty acids (FFA) levels. A
dose-dependent decrease in the triacylglycerol content and
concomitant increase in free fatty acids was observed after
g-irradiation of nutmeg (Niyas et al. 2003). Similarly a prolonged irradiation of seeds with UV light led to an increase
in level of lipid peroxidation in wheat sprouts (Rogozhin et
al. 2000). This suggested a breakdown of acylglycerol during
radiation processing, resulting in the release of free fatty
acids (Niyas et al. 2003). Phospholipids, glycolipids, and
neutral lipids were considerably reduced after g-irradiation,
with concomitant reduction in the process of sprout growth
in garlic sprouts (Pérez et al. 2007).
5. Oxidative stress and anti-oxidant defense
system
Plants often face the challenge of several environmental
conditions that include such stressors as drought, salinity, pesticide, low temperature, and irradiation, all of which exert adverse effects on plant growth and development (Foyer et al.
1994). g-irradiation is reported to induce oxidative stress with
overproduction of reactive oxygen species (ROS) such as
superoxide radicals (O2–), hydroxyl radicals (OH–) and H2O2
(Apel and Hirt 2004), which react rapidly with almost all
structural and functional organic molecules including proteins,
lipids, nucleic acids causing disturbance of cellular metabolism (Salter and Hewitt 1992). Hydroxyl radicals are generated by ionizing radiation either directly by oxidation of
water, or indirectly by the formation of secondary, partially
generated ROS. The generation of ROS is widespread in biological materials and oxygen derived radicals include species
such as peroxyl (ROO·) and alkoxyl (RO·) radicals. One result
of oxidative stress is cellular damage by hydroxyl radical attack. The amount and rate of hydroxyl radicals generation
from ROS is controlled partly by the cellular antioxidant status and partly by the availability of systems capable of reducing (or ‘activating’) superoxide or hydrogen peroxide. It has
been shown that the effects of H2O2 resemble those of ionizing radiation (Riley 1994). A major, direct target of g-irradiation that is probably the most important one is the water
molecule, which is omnipresent in organisms. The primary reactions are excitation and ionization, which produce ionized
water molecules (H2O˙+) and the radicals H˙ and ˙OH. However, in biological tissue these ionizations are induced all
along the path of the radiation and lead to chain reactions,
which produce secondary reactive oxygen species (ROS) as a
result of H˙ and eaq– becoming trapped. The most important
ROS is H2O2; O2˙– is produced to very low extent, depending
of the O2 concentration (Tubiana 2008; Lee et al. 2009). The
˙OH radical can react rapidly with various types of macromolecules, including lipids, proteins and, in particular, DNA.
However, some of the resulting injuries can be readily repaired and recovered, depending on the dose range. Different
workers have described effect of g-irradiation on expression
of anti-oxidant enzymes as represented in (Table 6).
5.1 Superoxide dismutase (SOD; EC 1.15.1.1)
Superoxide dismutase (SOD) isozymes are compartmentalized in higher plants and play a major role in combating oxygen radical mediated toxicity. In this review, we evaluate the
mode of action and effects of the SOD isoforms with respect
Published by NRC Research Press
PROOF/ÉPREUVE
26
Table 6. Effects of the exposure to g radiation on antioxidant enzymatic and non-enzymatic components in different vegetal systems.
Dosage applied and duration
of irradiation
30 or 50 Gy
2, 4, 8, or 16 Gy; dose rate
150 TBq
Species
(Nicotiana tabacum cv.
Xanthi)
Red pepper (Capsicum
annuum L. cv.
Taeyang)
Plant part or age/stage of
plant growth for g-irradiation
Young tobacco plants 6- to
8-leaf stage
Seeds
Seeds
2, 4, 8, 10, 12, and 16 kGy;
dose rate 0.96 kGy/h
Kalungi (Nigella sativa
L)
Seeds
0, 40, 60, 80, 100 Krad;
dose rate of 233.5 rad/ min
Trigonella stellata, Trigonella hamosa and
Trigonella anguina
Seeds
2, 5, 10, 15, 20, 30, 50, 80,
and 100 Gy; dose rate of
0.54 Gy/min
Broad beans (Vicia
faba L.)
Seeds
0.5, 2.0, and 5.0 kGy; dose
rate 0.09072kGy/min
2.5, 5.0, 10.0, and 20.0 kGy;
dose rate, 6.5 kGy/h
Soybean seeds (Glycine
max (L.) Merr.)
Broad beans (Vicia
faba L.)
Seeds
Seeds
Kim et al. (2005)
Štajner et al. (2007)
Khattak et al. (2008)
Al-Rumaih and Al Rumaih
(2008)
Moussa (2009)
Dixit et al. (2010)
Aly and El-Beltagi (2010)
Environ. Rev. Vol. 20, 2012
Published by NRC Research Press
Soybean seeds (Glycine
max (L.) Merr.)
References
Cho et al. (2000)
Pagination not final/Pagination non finale
PROOF/ÉPREUVE
1, 2, 4, 6, 8, and 10 kGy;
dose rate 228Gy/min
Antioxidant defense response
GST, sodCp (CuZnSOD), POD, Ngcat1 (CAT) expression induced at 30Gy.
SOD activity was 2% to 25% and APX activity increased
dose-dependently from 27% to51%higher in the irradiation
groups than in the control, while that of GR was 56% to
61% lower in the former, ascorbate content also increased in
a similar manner, by 4% to 22%
Decrease of CAT activity significant only at 100 and 120 Gy
and the maximum decrease was detected at 120 Gy
(62.4%), 140 Gy which caused a decrease in GSH-Px activity by 33.7%, The GSH quantity increased as to 140 Gy
(27.0% greater than the control) and then decreased at the
highest irradiation dose (36.0% less than the control), LP
increased by 21.6% and HO˙ quantity by 79.3% at 140 Gy.
g irradiation enhanced the scavenging activity in acetone and
methanol extracts by 10.6% and 5.4%, respectively, at 16
kGy.
CAT activity in shoots of T. hamosa decreased by 7%, 14%,
34%, and 48% at 40, 60, 80 and 100 Krad, respectively as
compared with control. Induction of APOX and GR activities in T. stellata roots was significant (P < 0.05) at 40
Krad and high significant (P < 0.01) at 60, 80 and 100
Krads
g-rays of 20 Gy increased the activities of GR by 87.5%,
SOD by 12.6%, APOX by 22.9%, and G6PDH by 38.9%
and decreased H2O2 content by 17.8% as compared with the
nonirradiated plants
Maximum relative enhancement of 80% in FRSA and 33% in
FRAP at 2.0 kGy
H2O2 content and concentration of MDA significantly increased reached its maximum (36.3 and 38.2 mmol/g dw)
compared to the control (2.3 and3.9 mmol/g dw) at dose level 20.0 kGy
Jan et al.
27
to radiation induced oxidative stress resistance, correlating
age, species, and specificity of plants during development.
Cells exhibiting high levels of SOD, catalase, and peroxidase
activity are relatively less vulnerable to secondary effects of
radiation. Since superoxide is sufficiently stable to permit diffusion within the cell it is possible that it acts as an electron
donor to transition metals in irradiated tissue and may account
for sensitization of cells to the effects of H2O2 by radiation
exposure and the protection afforded by SOD to irradiation
cells (Petkau 1987). Slooten et al. (1995) reported that the
stimulation in SOD activity in response to stresses is possibly
attributed to the de-novo synthesis of the enzymatic protein.
Changes in Peroxidase (POD) and superoxide dismutase isozyme compositions were seen in Vigna radiata (L.) R. Wilczek, as well as in calli of two tobacco species (Nicotiana
tabaccum and Nicotiana debneyi) after the irradiation (20–
200 Gy) established from leaf discs (Roy et al. 2006; Wada
et al. 1998). Pramanik (1997) correlated morphological damage caused by g-rays with the changes in SOD isozyme patterns in callus tissue obtained from irradiated seeds. SOD
activity PAGE gels showed an extra band (Rf value – 0.59)
in all of the irradiated samples of calli, which were absent in
the control. This over expression of SOD is an indication of
radioprotection in vitro. Alteration in levels of SOD isoforms
have also been correlated with effects of UV-B radiation,
ozone, paraquat, methyl viologen (Krupa and Kickert 1989;
Runeckles and Krupa 1994). Over expression of pea chloroplast Cu/Zn SOD in tobacco leaves can improve their photosynthetic performance under moderate stress and maintain
photosynthetic capacity even after severe oxidative stress
(Gupta et al. 1993). The stress induced by g-irradiation might
have imparted a shift in gene expression, which resulted in
formation of new bands. A similar observation has been reported by El-Farash et al. (1993) who showed that induction
of such protein bands depends upon intensity of the stress
and is genetically controlled. The stimulation of SOD activity
is possibly due to a positive regulation of SOD genes or of
one particular encoding allele, in response to g-irradiation
stress as shown in different biological models (Inzé and Van
Montagu 2002). However, the disappearance of some bands
in irradiated samples immediately after exposure to g-rays
could be due to either degradation (Sen Raychaudhuri and
Deng 2000) or to the switching off of the transcription–translation machinery during radiation exposure and it getting
turned on again in the irradiation recovery phase. It has been
propounded by (Zaka et al. 2002) that change in antioxidant
enzymes must be directly linked to protein synthesis. Ascorbate peroxidase (APX) and SOD activities in peppers also increased at low doses (from 2 to 8 Gy), whereas glutathione
reductase (GR) activity decreased (Kim et al. 2004, 2005).
Catalases (CAT) were stimulated at 5.16 C kg–1 Singh (1974)
in safflowers. SOD, POD, CAT, and G6PDH (glucose-6P dehydrogenase) activities are strongly stimulated in the case of
new chronic external irradiation. Thus, it has been suggested
that these enzymes protect plants more efficiently than the ascorbate glutathione ROS detoxification cycle.
5.2 Peroxidase (APX;EC 1.11.1.11) and Catalases (CAT;
EC 1.11.1.6)
Plant exposure to g-irradiation brings about changes in biochemical activity through various metabolites produced as
function of g-irradiation. The most important of these metabolites are peroxyl radicals. The accumulation of organic peroxides and oxidation of membrane lipids place a stress on
cellular activity (Mead 1976). In plants, physiological effects
of g-irradiation were recognised by Ikeya et al. (1989); Voisine et al. (1991) to have caused the production of free peroxyl radicals through the peroxidation of unsaturated fatty
acids. The general equation for peroxidases activity is:
H2O2 + DH2→ 2H2O + D
Hydrogen peroxide deposits were clearly increased in
pumpkin leaves and petioles at the high acute dose of 1 kGy
(Wi et al. 2006a, 2006b). These deposits were present in the
vessels, in the plasma membrane, in the cell corners of the
middle lamella and especially in the parenchyma cells. This
accumulation is concomitant with an increase in POD activity in the corners of the middle lamella, where H2O2 is eliminated (Wi et al. 2007). This stimulation of POD activity was
also observed in garlic bulbs at low doses (10 Gy) (Croci et
al. 1991, 1994), in Saintpaulia petioles at high-doses (0.85
and 1.98 C kg–1;Warfield et al. 1975) and in sweet potato
root disks (900 Gy;Ogawa and Uritani 1970). The radiation
protective effect of peroxidase is due to removal of H2O2,
peroxides, and especially lipid hydrogen peroxides. This accounts for the greater effectiveness of peroxidases than catalase (Croute et al. 1982). Khanna and Maherchandani (1981)
observed stimulated growth and increase in peroxidase activity at low doses of g-irradiation in chickpea. g-irradiation can
influence the isozymatic composition of peroxidases, as demonstrated by various authors in other species (Endo 1967;
Ogawa and Uritani 1970; Shen et al. 2010). The study of peroxidase activity will contribute to an understanding of mechanism involved in radiation induced inhibition of plant
growth. The peroxidase isozyme pattern was related to damage caused by irradiation (Shen et al. 1991). g-irradiation of
callus culture of Datura innoxia Mill. resulted in stimulation
of peroxidase activity and particularly increased the peroxidase enzymes with high electrophoretic mobilities (Jain et al.
1990). The activity and isozyme of POD in Nicotiana debneyi Domin. and Nicotiana tabacum L., SOD in Nicotiana
debneyi Domin., and CAT in Nicotiana tabacum L. increased
in response to g-irradiation treatment (Wada et al. 1998). Laser irradiation of Vicia faba L. seeds could raise SOD, POD,
and CAT activities and could eliminate the accumulation of
poisonous free radicals and prevent lipid peroxidation (Aly
and El-Beltagi 2010). In N. tabacum L., the genes GST, Cu/
Zn SOD, POD, and CAT are up-regulated and the gene for
cytosolic and stromal APX is down-regulated (Cho et al.
2000). Indeed APX, GR, and MDHAR (monodehydroascorbate reductase) activities were found to be either poorly
stimulated or not stimulated at all (Calucci et al. 2003).
ROOH catalase → H2O + ROH + A
2H2O → 2H2O + O2
Chaomei and Yanlin (1993) reported an increase in the activity of POD and CAT with a corresponding decline in
growth of Triticum aestivum L. plants under higher irradiation doses (20, 40, 60, 80 Kr). Singh et al. (1993) reported
induction of APX activity in two sugarcane varieties grown
under g-irradiation. The activities of POD, CAT, and SOD
in radish (Raphanus sativus L.) leaves were enhanced by girradiation (10 Gy) treatment. Inhibition of CAT activity was
also reported under irradiation stress (Ye et al. 2000; Štajner
Published by NRC Research Press
PROOF/ÉPREUVE
Pagination not final/Pagination non finale
28
Environ. Rev. Vol. 20, 2012
et al. 2009; Vandenhove et al. 2009). The present increase in
APX activity was reported to compensate for the progressive
drop in catalase activity. Peroxidase was considered to be the
key enzyme for the decomposition of H2O2, especially under
CAT inactivation. Pasternak (1987) attributed peroxidase activation to membrane injury and the resulting shift in cellular
Ca2+ levels. According to Karpinski et al. (1997) APX activation in Arabidopsis thaliana (L.) Heyn subjected to oxidative stress occurred through induction of APX1 and APX2
gene transcription. Zaka et al. (2002) further reported enhanced expression of APX gene in cells undergoing low
chronic g-irradiation stress. Several studies attributed enzyme
induction either to up-regulation of encoding genes or to activation of existing enzyme pools (Foyer et al. 1997) by a
modulatory effect of enzyme structure.
5.3 Glutathione Reductase activity (GR; EC 1.6.4.2)
GR activity in shoots and roots of the three Trigonella L.
genus significantly increased above the control values when
exposed to different doses of g-rays. Increased activity of
this enzyme has been reported earlier in cotton when subjected to elevated atmospheric O2 (Foster and Hess 1980), in
Mg2+ deficient bean leaves, and in peas fumigated with
ozone (Hurkman and Tanaka 1987). Higher GR activity of
salt-stressed cotton was reported to be due to an increase in
glutathione turnover rate (Gossett et al. 1991). Foyer et al.
(1995) reported an increase in GR activity in higher plants
as a result of enhancement of the transcription rate of encoding genes. GR would also be involved in the recycling of the
electron donor (glutathione, GSH) later in the pathway. There
was slight increase in GR activity in Stipa capillata L. when
exposed to g-irradiation, probably due to enhancement of the
transcription rate of encoding genes (Foyer et al. 1991). The
hypothesis of GR radio-induction in Stipa is supported by the
fact that a similar response was reported by other workers
(Zaka et al. 2002; Kim et al. 2004; Moussa 2006). The role
of GR in H2O2 scavenging mechanism in plant cells was well
established in Halliwell–Asada enzyme pathways (Yamane et
al. 2009).
5.4 Malondialdehyde (MDA) content and llipid
peroxidation
Lipid peroxidation refers to the process whereby free radicals “steal” electrons from the lipids in cell membranes, resulting in cell damage. This process proceeds by a free
radical chain-reaction mechanism. Thiobarbituric acid reactive substances (TBARS), the cytotoxic product of lipid peroxidation, is normally considered as the major TBA-reacting
compounds that indicate the magnitude of the oxidative stress
(Qadir et al. 2004; Qureshi et al. 2007). The basic effect of
radiation on cellular membranes is believed to induce lipid
peroxidation by the production of free radicals (Leyko and
Bartosz 1986). Lipid peroxidation products in leaves of Arabidopsis thaliana L. present highest at full flowering and decreased with higher g-exposure at this growth stage. At the
other two growth stages, lipid peroxidation products were unaffected by g-treatment (Vandenhove et al. 2009). The Malondialdehyde (MDA) content and HO˙quantities were
observed only under the highest irradiation dose, in soybean
(Glycine max Merill.) seeds. The MDA quantity increase of
21.6%, and HO˙ radical quantity increase of 79.3% compared
with the non-irradiated control (Štajner et al. 2009).
5.5 Ascorbate
Antioxidants are regarded as compounds that are able to
delay, retard, or prevent oxidation processes. They can interfere with oxidation by reacting with free radicals, chelating
metals, and also by acting as oxygen scavengers, triplet as
well as singlet form, and transferring hydrogen atoms to the
free radical structure (Kitazuru et al. 2004). Ascorbate has
been shown to have an essential role in several physiological
processes in plants, including growth, differentiation, and metabolism (Foyer 1993). The effect of ionizing radiation on vitamin C content has produced contrasting results for both
strawberries and potatoes. In the case of strawberries, either
no effect (Beyers et al. 1979) or a decrease in ascorbic acid
content (Graham and Stevenson 1997) has been reported.
Although some loss of vitamin C has been observed in potatoes soon after irradiation (Maltseva et al. 1967), there were
no significant differences between irradiated and non-irradiated samples after a period of prolonged storage (Salkova
1957). On the other hand, several studies have reported a reduction in ascorbic acid content of potatoes following irradiation and storage (Joshi et al. 1990). However, it has been
noted that when reporting vitamin C levels, a number of
workers have not taken into consideration the fact that ionizing radiation can cause partial conversion of ascorbic acid or
ascorbate to dehydroascorbic acid (DHAA) (Diehl 1990; Kilcast 1994). Biosynthesis of ascorbic acid and riboflavin in
radiated corn, chickpea and soybean was found to more than
in control samples during germination. Low doses of g-irradiation in addition to growth catalyzing enzymes or hormones would have accelerated the metabolic activity of
ascorbate during germination just like X-rays (Sattar et al.
1992).
5.6 Glutathione (GSH)
Upon the imposition of oxidative stress, the existing pool
of reduced glutathione is converted to oxidized glutathione
(GSSG) and glutathione biosynthesis is stimulated (May and
Leaver 1993; Madamanchi et al. 1994). Together with ascorbate, the most abundant antioxidant in plants, glutathione
contributes to protect plant tissues by direct scavenging of activated oxygen species (Halliwell and Gutteridge 1989).
DHAR
Dehydro-ascorbate + 2GS → Ascorbate + GSSG
GSSG + NADPH → 2GSH + NADP
Recently, there has been considerable interest in mechanisms for diminishing the GSH levels in cells as a radio sensitization strategy (Riley 1994). Corn seedlings responded to
g-irradiation by increasing the level of the glutathione peroxidase activity and showing no dependence on the genome
complexity (Marchenko et al. 1996). The decrease in ferric
reducing ability of plasma (FRAP) value in soybean seeds indicated a decrease of non-enzymatic antioxidants Vitamin C
and E and polyphenol constituents (Benzie and Strain 1996).
The GSH quantity increased in soybean seeds as irradiation
dose increased to 140 Gy and then decreased at the highest
irradiation dose, which is a hermetic type of response under
applied doses of irradiation (Štajner et al. 2009). The amount
of reduced glutathione, which is one of the most important
Published by NRC Research Press
PROOF/ÉPREUVE
Jan et al.
29
non-enzymatic antioxidants, was positively affected by g-irradiation. It has been reported that low level doses of g-irradiation enhance glutathione reductase activity (Chakravarty and
Sen 2001). However, no effect of irradiation was observed on
concentration or reduction state of the nonenzymatic antioxidants, ascorbate and glutathione in Arabidopsis thaliana L.
(Vandenhove et al. 2009).
6. Effect of γ-radiation on bioactive agents
and oil components
Many of the plant-derived phenolic compounds (flavonoids, isoflavonoids, coumarins, and lignans) are secondary
products of phenylpropaniods metabolism (Dixon and Paiva
1995; Douglas 1996). In higher plants, phenylpropaniods
mainly hydroxycinnamic acid, cinnamoyl esters, flavones,
flavonols, and anthocyanins provide a UV-A and UV-B
screen. Both soluble and insoluble phenylpropaniods absorb
efficiently in the range of 304–350 and 352–385 nm, respectively. Concerning the effect of g-irradiation on contents and
components of volatile oils, different results were reported.
The differences were mainly due to the species of the plant
and the dose applied. Koseki et al. (2002) studied the effect
of radiation doses (0, 10, 20, and 30 kGy) on the flavonoids,
essential oils, and phenolic compounds of Brazil medicinal
herbs. From the described pharmacological tests of Brazilian
medicinal herbs carried out during this study, it was concluded that phytotherapy showed identical therapeutic action
as non-irradiated preparations after exposure to a dose of 10,
20, and 30 kGy of ionizing radiation. The irradiation of traditional medicines and herbal products does not result in any
negative chemical changes or important losses of active components. After irradiation up to 17.8 kGy, the content of the
main biologically active substances of two medicinal herbs
(ginkgo and guarana) were not modified (Soriani et al.
2005). Mishra et al. (2004) reported that the dose of 5 kGy
led to a decrease in 6-gingerol, the compound responsible
for the pungency of ginger. Lee et al. (2005) showed that the
pungency and red colour caused by capsanoids and capsanthin, were not altered when irradiated (3, 7 and 10 kGy) in
red pepper powder. Effect of g-irradiation at 10 kGy on the
free radical and antioxidant contents in nine aromatic herbs
and spices (basil, bird pepper, black pepper, cinnamon, nutmeg, oregano, parsley, rosemary, and sage) were studied by
(Calucci et al. 2003). Irradiation resulted in a general increase of quinone radical content in all of the investigated
samples, as revealed by Electron paramagnetic resonance
(EPR) spectroscopy, and in a significant decrease of total ascorbate and carotenoids content of some herbs. Polovka et al.
(2006) reported that irradiation (5 to 30 KGy) of ground
black pepper shows some significant influences on the antioxidant activities with respect to the non-irradiated samples.
The most significant changes of antioxidant activity were observed in creation of thiobarbituric acid reactive substances.
Irradiation with 15 kGy caused slight increase in phenol content in Brassica nigra L. Koch (0.1%) followed by Cassia
senna L. (pods) (1.3%). However, the maximum increase
was about 70% and was observed in Cassia senna L. (leaves)
followed by Lepidium sativum L. (25.6%) and Cymbopogon
schoenanthus L. (24.9%). On the other hand irradiation with
15 kGy reduced the phenol content of Trigonella foenum-
graecum L. by 4.1% followed by Hibiscus sabdariffa L.
(5.1%) and Acacia nilotica L. (14%). The maximum reduction was 33% and was observed in Cymbopogon citrates L.
The effect of g-irradiation on the phenolic content of the
plants under study has not been investigated previously, but
similar observations on other biological materials were reported. Adamo et al. (2004) reported an increase in phenol
content for irradiated samples of truffles at the dose level in
the 1.0–1.5 kGy and proposed that the destructive process of
oxidation and g-irradiation were capable of breaking the
chemical bonds of polyphenols, thereby releasing soluble
phenols of low molecular weight. In a study on nutmeg, Variyar et al. (1998) found that the essential oil constituents
showed clear quantitative differences upon g-irradiation.
Thus, the content of á-terpeniol, 1-terpinene-4-ol, and myristicin was increased in irradiated nutmeg, while that of sabinene, a-pinene, and elimicin decreased in comparison to the
control sample. Less significant changes in the content of
some of the essential oil constituents between the control
and the irradiated samples were noted in clove and cardamom. Seo et al. (2007) showed that among the essential oils
constituents of Angelica gigas Nakai, oxygenated terpenes
such as a-udesmol, a-eudesmol, and verbenone were increased after irradiation, but their proportions were variable
in a dose dependent manner.
Breitfellner et al. (2002) studied the effect of g-irradiation
on flavonoids in strawberries and reported that in hydrolyzed
samples four phenolic acids (gallic acid, 4-hydroxybenzoic
acid, p-coumaric acid, and caffeic acid) were identified and
five flavonoids were detected in hydrolyzed samples ((+)-catechin,(-)-epicatechin, kaempferol-3-glucoside, quercetin-3glucoside, and quercetin-3-galactoside). The concentration of
4-hydroxybenzoic acid increased and that of catechins and
kaempferol-3-glucoside decreased as irradiation dose increased, whereas those of quercetin-3-glucoside remained unchanged up to a dose of 6 kGy. Accumulation of phenolic
compounds in cells is demonstrated and may be explained
by the enhancement of phenylalanine ammonia lyase (PAL)
activity. Bhat et al. (2007) reported that some compounds
such as phytic acid in velvet bean seeds (Mucuna pruriens
L.) was completely eliminated on exposure to a dose of 15
kGy. Decrease or elimination of phytic acid is likely due to
the degradation of phytate to lower inositol phosphates and
inositol by the action of free radicals generated during irradiation. Another possible mode of phytate loss could have been
through cleavage of the phytate ring itself (Duodu et al.
1999). Similarly, treatment of broad bean (Vicia faba L.)
seeds with g-irradiation reduced the level of phytic acid compared to controls (Al-Kaisey et al. 2003). Significant quantitative changes were noted by Variyar et al. (1998) in some of
the phenolic acids in clove (Syzygium aromaticum L.) and
nutmeg upon irradiation with 10 kGy dose. They reported
that the content of gallic and syringic acids in irradiated
clove was increased, whereas that of p-coumaric, ferulic, and
synapic acids decreased to approximately half in the control
spice, and that of caffeic and gentisic acids remained unchanged. In the case of irradiated nutmeg (Myristica fragrans
L.), except for protocatechuic acid and p-coumaric acid,
which remained unchanged, the content of other phenolic
acids showed wide variations compared with that of control
samples. Elevation of some compounds by g-irradiation may
Published by NRC Research Press
PROOF/ÉPREUVE
Plant part or age /stage of
plant growth for g-irradiation
Bran
1, 2, and 5kGy
Mushroom (Agaricus bisporus)
Fruiting body
0.3 kGy; dose rate 6kGy/h
Citrus fruit (Citrus clementia
Hort.ex. Tanaka)
Orange (Citrus limonia)
Seed
0.5, 1, 2, and 5 kGy; dose rate
14Gy/min
Soybean (Glycine max Merrill)
Seeds
2, 16, and 32 Gy
Lithospermum erythrorhizon
Seed, seedlings
10, 20, 40, 60, 80, and 100
kGy
1, 3, 5, 10, and 20 kGy
Maytenus aquifolium Martius
Leaves
Welsh onion (Allium fistulosum
L.)
Bulbs
5 and 10 kGy
Dry shiitake (Lentinus edodes
Sing)
Seeds
1, 3, 5, 10, and 20 kGy
Angelica gigas Nakai
Leaves
2, 4, 8, 10, 12, and 16 kGy,
dose rate 0.96 kGy/h
Kalungi (Nigella sativa)
Seeds
1, 3, 5, 10, and 20 kGy
Licorice (Glycyrrhiza uralensis
Fischer)
Root
0.89, 2.24, 4.23, and 8.71gGy;
dose rate 0.1 kGy/min
Orange juice
PROOF/ÉPREUVE
Metabolites and oil content/yield
The loss of total E vitamers and oryzanol occurred in
two stages: 50%–82% and 12%–33% immediately
following 15kGy irradiation.
Eight-carbon compounds decreased as the doses of girradiation increased, from 41.73 for the control (0
kGy) to 20.06 (1 kGy), 8.77 (2 kGy), and 4.04 mg/
g (5 kGy irradiated mushrooms)
Increment and accumulation of scoparone and PAL
activity increased to 250 pKat/gdw
Myrcene, linalool, geranial and neral decreased at
rate of 5.86%, 5.66%, 5.83%, and 6.54% per kGy
dose applied. At 5-D dose myrcene, linalool, neral
and geranial would be reduced by 20.9%, 20.1%,
20.7%, and 23.2%.
Decrease in diazdin (33.95), glycitin (37.14) and genistin (28.34)%, total glycone reduced to 26.97% at 5
kGy.
The g-irradiation significantly stimulated the shikonin
biosynthesis of the cells and increased the total shikonin yields (intracellular+extracellular shikonin
yields) by 400% at 16 Gy and by only 240% and
180% at 2 and 32 Gy, respectively
5.2% decrease in tannic acid at 100 Gy.
Published by NRC Research Press
Enhancement in total concentration of volatile compounds by 31.60% and 24.85% at 10 and 20 kGy,
respectively.
The ratio of the eight carbon compounds, such as 3octanone, 3-octanol and 1-octen-3-ol, to total volatiles decreased from 72% in the control to 21% in
the 10 kGy irradiated samples.
The major volatile compounds were identified 2,4,6trimethyl heptane, a-pinene, camphene, a-limonene, beudesmol, a-murrolene and sphatulenol.
The irradiated samples at doses of 1, 3, 5, 10 and
20 kGy were 84.98%, 83.70%, 83.94%, 82.84%,
and 82.58%, respectively
Extraction yields increases were 3.7%, 4.2%, 5.6%
and 9.0% for hexane, acetone, water and methanol
extracts. Phenol content increase from 3.7 for control to 3.8 mg/g for 16 kGy.
10 kGy dose irradiation induced the maximum level
of total yield of volatile compounds by 12% but
decresed slightly at 20 kGy
References
Shin and Godber (1996)
Mau and Hwang (1997)
Oufedjikh et al. (2000)
Fan and Gates (2001)
Pagination not final/Pagination non finale
Species
Rice (Oryza sativa L.)
Variyar et al. (2004)
Chung et al. (2006)
Campos et al. (2005)
Gyawali et al. (2006)
Lai et al. (1994)
Seo et al. (2007)
Khattak et al. (2008)
Gyawali et al. (2008)
Environ. Rev. Vol. 20, 2012
Dosage applied and duration of
irradiation
5, 10, and 15 kGy; dose rate of
0.98 kGy/h
30
Table 7. Effects on g irradiation on the oil and metabolite content of different species.
Musa et al. (2010)
Kiong et al. (2008)
Khattak et al. (2008)
31
Plant part or age /stage of
plant growth for g-irradiation
Seeds
Seeds
Shoot tips
Leaves
Species
Atropa belladonna L.
Kalungi (Nigella sativa)
Orthosiphon stamineus
Camel hay(Cymbopogon schoenanthus)
2, 4, 8, 10, 12, and 16 kGy;
dose rate 0.96 kGy/h
0, 10, 20, 30,40, 50, 60, and 70
Gy; dose rate 4.64 kGy/h
5, 10, and 15 kGy, The activity
of the source was 6.345Kci
and the energy 1.25 MeV
Dosage applied and duration of
irradiation
50, 80, 110, and 150 Gy; dose
rate 0.54 Gy/min
Table 7 (concluded).
Metabolites and oil content/yield
Seeds irradiated at 110 Gy possessed 4.01 mg/g and
109.67 mg/plant twice alkaloid value than control
(2.03 mg/g and 53.41 mg/plant).
Extraction yields increases were 3.7%, 4.2%, 5.6%,
and 9.0% for hexane, acetone, water and methanol
extracts. Phenol content increase from 3.7 for control to 3.8 mg/g for 16 kGy.
Rosamarinic acid content was lowest 5.27 mg/g fw in
plantlets irradiated at 10kGy and highest 8.40 mg/g
fw at 30 Gy.
21% reduction in tannins as a result of g irradiation
and phenol content by more than 25% at 15 kGy
References
Abdel-Hady et al. (2008)
Jan et al.
be attributed to their higher extractability. Some reports indicate that irradiation decreases tannins in bean seeds (Villavicencio et al. 2000). Such differences may be attributed to the
differential response and variability in the genetic constituents (strains and varieties). Doses of 7.0 and 10 kGy significantly reduced the tannin content of Shahalla sorghum
variety but not that of Hemaira variety (Siddhuraju et al.
2002). Various studies on effects of g-irradiation on active
principles in plants is summarized in Table 7.
7. Perspectives
(g) radiations can be used to enhance the rate of genetic
variability because the spontaneous mutation rate is very
slow,which previously has prevented breeders from using
them in plant breeding programs. Advanced molecular tools
used along with traditional plant breeding can improve crop
production. Efforts in the future should be directed at metabolically engineering plants for the production of secondary
metabolites that confer resistance thereby providing an opportunity for stable genetic character to confer radio resistance.
Elicitation of secondary metabolites has applications in over
production of desired compounds, which is an area of commercial importance especially for high-value low-volume
products. In this category belongs the production of antitumor and anticancer compounds that are of great medicinal
value. As the plant is exposed to a number of external stimuli, studies on signal transduction in plants for various physiological responses would require focused attention to
understand its adaptation. g-rays can be used for inducing
new mutants using local germplasm enhancement for developing new mutant varieties as well as for basic research in
gene discovery and functional genomics. It is difficult to predict the impact of climate changes on global, regional, or national agriculture and therefore new varieties must be
developed and distributed regularly at the national and regional levels for sustainable crop production. g-rays can be
employed to develop new varieties that can be readily
adapted in a short period in different locations with varying
agro-climatic and growing conditions, and where available
resources are limited.
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