Lipid and Fatty Acid Compositions of Chilling Tolerant Sweet potato (Ipomoea batatas L.) Genotypes
James O. Garner
Chilling injury is when morphological and physiological damage is sustained by plant tissue that is exposed to freezing temperatures. An experiment was conducted using four chilling tolerant sweet potato genotypes such as 105MS1, 108MS2, 180MS3 and 183MS4, which were selected from seventy nine lines from three major variety crosses for tolerant to chilling injury. The effects of chilling exposure on fatty acids compositions and peroxidase enzyme activity were studied. Chilling exposure increased the Peroxidase Enzyme Activity (PEA). Genotypes differences were also found in PEA following chilling exposure. All four genotypes that were tested had a high level (over 50%) of unsaturated fatty acid on their glycolipids. There were no differences found for the fatty acid percentage composition of the total glycolipid and phospholipid fractions from the four chilling tolerant genotypes except for C18:0 of the glycolipid fraction. However, C18:0 was found in low percentage and was not considered a major fatty acid. Sixty percent of total fatty acid in glycolipid fraction was C18:2 and C18:3. It was concluded that if lipids fatty acid composition was indeed a factor in chilling tolerance, it did not vary among the chilling tolerant genotypes. The result suggests that the genotypes were considered chilling tolerant to chilling environment, but that differences existed in their mechanism for tolerance. Thus, by breeding and selecting for chilling tolerance, it could enhance chilling tolerance in sweet potatoes.
Received: July 27, 2012;
Accepted: December 11, 2012;
Published: January 23, 2013
Sweet potato (Ipomoea batatas L. Lam.) is an important food crop which
is enriched in health beneficial components (Ibaraki and
Murakami, 2007; Islam et al., 2009a). In
general, sweet potato is growing well under the warm climate, low temperature
caused chilling damaged. Chilling injury is the physiological damage sustained
by plant tissues exposed to nonfreezing temperature of approximately 0-15°C.
A number of mechanisms have already been proposed based on the physiological
and biochemical functions associated with chilling injury (Al-Shoaibi,
2008; Saleh, 2007; Khorshidi
and Nojavan, 2006; Anjum and Khatoon, 2003; Ali
et al., 2000). The severity and length of time required to cause
an irreversible dysfunction are generally determined by the temperature extreme,
duration of exposure to cold conditions, plant species and morphological and
physiological conditions of the plant material at time of exposure (Islam
et al., 2009b). Chilling injury disrupts metabolic and physiological
processes of higher plants, so it is unlikely that a single basic cause could
explain injury. These include an increased concentration of cytosolic calcium;
a marked decreased in protoplasmic streaming, an alteration in the cytoskeleton,
a conformational change in some enzymes and temperature induced change in the
molecular ordering of membrane lipids (Kim et al.,
2007). The plasma membrane is regarded as the sensitive site of injury during
low temperature stress in herbaceous plants (Zhang and Tian,
2009). Limited component begins to freeze at chilling temperature, the opposite
occurred in chilling-resistance species (Sthapit and Witcombe,
Alterations in Membrane lipids composition during cold-acclimation and low
temperature stress has been the focus of investigations for the last 20 years
yet conclusive results have not been established (De la
Roche et al., 1972). Research findings have shown significant elevated
levels of unsaturated fatty acids especially fatty acids associated with phospholipids
in response to chilling and freezing temperature stress (Levitt,
1980). Gerloff et al. (1966) found that the
fatty acids composition of alfalfa roots changed during hardening due to differential
accumulation of polyunsaturated fatty acids. Kuiper (1970)
reported difference in lipids composition of alfalfa leaves relatively cold
hardiness. On the hand, investigations failed to observe any increased in membrane
lipid fatty acids unsaturation during and after acclimation and no recorded
information linked membrane fatty acid unsaturation with increased chilling
resistance (Vigh et al., 1985; De
la Roche et al., 1972). Kenrick and Bishop (1986)
showed that the content of high melting point fatty acids of phosphotidylglycerol
was negatively correlated to chilling sensitively of plants rather it may be
related to genetic origin of the plants. Wang (1982)
stated that the primary response of plants to chilling temperature stress is
the physical change of the membrane fatty acids composition. There was no correlation
between chilling tolerance and the presence of unsaturated fatty acid, when
the fatty acid composition of 13 chilling tolerant and sensitive plants were
compared (Wilson and Crawford, 1974). According to Moon
et al. (1995), study following cold-acclimation, lipids components
in thylakoid membrane of tolerant wild-type and transgenic tobacco plants did
not significantly differ in photosystem II and photo inhibition response to
high or low temperature stress. The results suggest that unsaturation of fatty
acids of phosphatidylglycerol in thylakoid membrane of the wild-type tobacco
stabilized and enhanced the photosynthetic capacity and the recovery of photo
system II protein complex during low temperature stress.
Chemical analyses of proxidase isoenzymes in acclimated chilled plants suggest
possible association with cell wall lignification. Several authors (Bassal
and El-Hamahmy, 2011; Cao et al., 2011; Lee
and Lee, 2000) asserted that location of peroxidase enzymes in cell wall
of acclimated seedling is an indicative that antioxidants likely improved and
maintained the mechanical strength of chilling sensitive mesocotyl. Hodgson
and Raison (1991) reported that carbohydrates were less utilized in comparison
with photosynthetic rate by chilling sensitive plants compared with tolerant
plant. Enzymes activity increased in sensitive plant partly attributable to
the productions of more chilling tolerant isoenzymes. Hetherington
et al. (1989) showed that high intensity light hastens the symptoms
of chilling injury. Under chilling temperature of 4°C and high light intensity
(800 μM m-2 sec-1), approximately 10-15% of the leaf
area of mug bean (Vigna radiata) were necrotic, whereas under low light
intensity (155 μM m-2 sec-1) no symptoms of chilling
damages were apparent. The objectives of this study were: to evaluate lipids
compositions and peroxidase enzyme activity among the selected genotypes of
sweet potatoes to possibly explain tolerance to chilling injury.
MATERIALS AND METHODS
Plant materials and cultural methods: Plant selection to determine genotypes
tolerant to chilling injury from lines of a genetically diverse population was
commenced in the greenhouse. Four genotypes namely 105MS1, 108 MS2, 180MS3,
183MS4 were selected from seventy nine lines from three major variety crosses
for tolerant to chilling injury (Islam et al., 2009c).
The experiment was conducted during 1998 to 2002 at the Mississippi State University,
USA. Stem cuttings from each line, approximately 12 cm, were placed in 3.8 L
plastic pots containing peat-perlite vermiculite medium (2:1:1 by volume). The
medium was amended with 4.56 kg dolomitic lime, 1.82 kg ON-9P-0K, 1.40 kg calcium
nitrate and 0.17 kg fritted trace element per cubic meter. Following planting,
the plants were kept in a glasshouse under intermittent mist to initiation roots.
After five days, plants were moved to another bench in the same glasshouse where
they were manually watered once a day for five days. Ten days old plants of
each genotype were moved from the glasshouse to walk-in temperature controlled
growth chamber maintained at 5°C and a control room 25°C with 85% relative
humidity, 10 h photoperiod for duration of 72 h chilling treatment and a fluorescence
light intensity of (12 μE M-2 sec-1) suspended over
Extraction and analysis of fatty acids: Total lipids analysis was performed
on 10 days old sweet potato leaves to determine fatty acids composition of glycolipid
and phospholipids. The experimental design was a split-plot with genotypes as
the main plot and temperature as the subplot. The data was analyzed as Completely
Randomized Design (CRD) with three replications. Isolation and identification
of fatty acids in the leaf were performed as outlined by Whitaker
(1986) and modified by Phromtong (1993) and Islam
et al. (2009b). Table 1 gives the general and chemical
characteristics of the fatty acids compositions in sweet potatoes.
Deveined leaf tissue, 3 g fresh weight was grounded in a mortar with liquid
nitrogen. The grounded tissues were transferred to 16x100 mm pyrex culture tubes
and extracted with hot isopropanol. Isopropanol was added to approximately half
the volume of tissue in the tubes and the tubes were incubated in boiling water
for five minutes and then cooled at room temperature. Isopropanol was removed
from tissue with a Pasteur pipette and refluxed under nitrogen (N2)
until dry. Tissue was re-extracted with chloroform-methanol (2:1, v/v). Both
extracts were dried under nitrogen and resuspended in chloroform-methanol (2:1,
v/v) and combined. Removal of non-lipids contaminant was performed as
outlined by Folch et al. (1957). Tubes were flushed
with nitrogen and sealed at each stage. The combined washed lipids extract
was reflushed under nitrogen until dry. The extracts were then redissolved with
2 mL chloroform. Total lipids were separated by column chromatography using
silicic acid (hydrated silicon dioxide) 100-200 mesh Bio-sil a (Bio-Rad Laboratories,
Richmond, CA). The lipids were separated into neutral glycolipids, (fraction
3) and phospholipids (fraction 4 and 5). Fractionated eluted lipids were collected
and reflushed under nitrogen, until dry.
|| Features of the fatty acid compositions in sweet potatoes
Samples were redissolved in 2 mL of chloroform in 7 mL borosilicate glass vials
sealed under nitrogen and stored at-10°C until further use. Transesterification
of individual fractions of polar lipids was performed by reflushing samples
in 7 mL borosilicate glass vials under nitrogen until dry. Samples were redissolved
in 0.5 mL chloroform, followed by addition of 0.5 mL of a 0.6 N potassium hydroxide
in dry methanol. Tubes were then flushed with nitrogen, tightly sealed, wrapped
with aluminum foil and placed on a roto-torque rotator at room temperature for
two hours. Following the addition of 0.5 mL distilled water and 50 μL of
6 N HCl, Fatty Acids Methyl Esters (FAME) were reconverted by extraction with
2 mL of hexane.
Quantitative analysis of FAME was performed by Gas Liquid Chromatography (GLC)
on a Varian 3300 Gas Chromatograph (GC, Varian Associates, Sugar Land TX), equipped
with a flame ionization detector and utilizing a supelcowax 10 fused silica
wide bore capillary column, 30 m in lengthx0.53 mm i.d. and 10 μL films
thickens (Supelco, Inc.,Bellenfonte). Injector and detector temperature were
250 and 300°C, respectively.
Helium and nitrogen gas were used as carrier and makeup gas at a flow rate
of 6 and 24 mL min-1, respectively. Initial column temperature was
190°C and after three minutes initial holding time, the column oven temperature
was raised 6°C min-1, to a final temperature of 220°C and
maintained for 20 min. The instrument (GC) was connected to a Varian 4290 Integrator,
for data collection. Standards of FAME mixture GLC Reference #6 (Alltech associates.
Inc. Deer Field, III) were injected for qualitative and qualitative analysis.
Peroxidase enzyme activity: The activity of peroxidase as crude soluble
enzyme and cell wall bound enzymes was determined from 10 days old sweet potato
leaves. The experimental design was a split-plot with genotypes as the main
plots and temperature as the subplots. Data was analyzed in a Completely Randomized
Design (CRD) with three replications. The extracts for enzyme analysis were
prepared by grinding 3 g fresh weight of deveined leaf tissue in 9 mL cold citric
phosphate buffer (pH 4.5), using a pre-chilled mortar and pestle. The homogenate
was transferred to plastic centrifuge tubes and centrifuged in a Sorvall RC-5B
automatic super speed refrigerated centrifuge (Sorvall Instrument, Du point
Co., Wilmington, DL) at 10,000 xg for 10 min. The supernatant was saved as the
soluble enzymes fraction. The remaining pellets were washed with 9 mL deionized
water and centrifuged at 10,000 xg, for 10 min. The supernatant was discarded
and the pellets resuspended in 9 mL of 0.2 M calcium chloride (CaCl2)
solution and centrifuged at 10,000 xg, for 10 min. The supernatant was saved
in 7 mL borosilicate glass vial and analyzed as crude cell wall bound enzymes.
Peroxidase, activity was measured according to Venkatarayappa
et al. (1984) and Islam et al. (2009b).
Peroxidase activity determinations were made by adding 50 μL of the enzyme
extract to 3.0 mL of 0.05 M phosphate buffer (pH 4.5) and 50 μL guaiacol
solutions (20 mM). The reaction was initiated by adding 0.5 mL of 8 mM H2O2
(0.03%) to the mixture. The change in absorbance at 420 nm was followed against
a blank containing phosphate buffer. Activity was expressed as the inverse of
the change in absorbance over time every 10 seconds up to 60 seconds.
Statistical analysis: Data for the different parameters were analyzed
by analysis of variance (ANOVA) using the General Linear Models procedures of
SAS version 8.1. Mean separations were done using Fishers
protected Least Significant Difference (LSD) tests.
RESULTS AND DISCUSSION
Lipid and fatty acid composition of chilling tolerant sweet potato genotypes:
There was no effect of chilling temperature on the fatty acid composition of
leaves from the four sweet potatoes studied (data not shown). The fatty acid
composition of the glycolipid fraction of the leaves from the genotypes is given
in Table 2. Linolenic (18:3) and palmitic (16:0) were the
major fatty acids, at approximately 50% (47 to 58%) and 25% (23 to 29%) of the
total fatty acids in the glycolipids. No genotypes differences in percent composition
were found for palmitic (16:0), oleic (18:1), linoleic (18:2) or linolenic (18:3).
Statistical differences among the genotypes were found in oleic (18:0) acid
only. Fatty acid composition of genotypes 180MS3 was higher (5.60) than the
remaining genotypes tested. However, oleic (18:0) acid ranged from 1.75 to 5.6%
in composition of the total fatty acids of the glycolipid fraction.
There were no differences in the fatty acid composition of the total phospholipids
from the leaves of the four sweet potato genotypes (Table 3).
The major lipids of the phospholipids fraction included C16:0, C18:0, C18:2.
C16:0 ranged in compositions from 40.6 to 44.8%. C18:2 and C18:3 were approximately
22 and 25%, respectively. The minimum response obtained for fatty acids compositions,
indicated that the four genotypes were not influenced differently by the fatty
acids makeup of their lipids. However, individual lipids are not examined. Woods
et al. (1991) reported that only minor changes in fatty acids compositions
of sweet potato chloroplast membrane occurred following chilling. Bartkowski
et al. (1978) studied the effects of chilling on long staple cotton
membrane with respect to a change in unsaturated fatty acids composition. Their
results showed that chilling effects were localized in the microsomal membrane
with a significant decrease in unsaturated fatty acid level in the mitochondrial
membrane. The nuclear membrane exhibited no change following chilling treatment.
||Effect of genotype on major fatty acids composition of the
glycolipid fraction of chilling tolerant genotype following exposure average
of 25 and 5°C
|zLSD (0.05); comparison of means between genotypes,
Means followed by the same letter not differ at p<0.05 level
||Effect of genotype on fatty acids composition of the phospholipid
fraction of chilling tolerant genotype following exposure average of 25
and 5°C, respectively for 24 h
|No statistical difference at p<0.05 was found
Additionally, their data showed that greatest change in unsaturated fatty acid
level during cotton chilling occurs with linoleic acids and linolenic acids
of the microsomal membrane. They found that the limiting factor in chilling
resistance of higher plant is the ability of the microsomes to desaturated fatty
acids and efficiently distribute these unsaturated fatty acids to other membranes.
This limiting factor may possibly be related to the diminishing effects of lower
temperature on Phospholipids Exchange Proteins (PEP) which transfers phospholipids
from the microsomes to the mitochondrial (Bartkowski et
al., 1978). Murata et al. (1982) worked
with blue green algae cell (Anacystis nidulans) and found that when temperature
was reduced from 38 to 28°C, higher desaturation and reduction in hydrocarbons
chain of the glycerol moiety of lipids occurred. Consequently, reduction in
chain length and unsaturation of the fatty acids was suggested to have enhanced
the fluidity and lowered the transition temperature of lipids phase of the thylakoid
membrane. Palta et al. (1993), comparing cold-acclimated
wild types and non-acclimated genotypes Solanum species, found that cold-acclimation
wild types had increased unsaturated fatty acids, free sterol, sitosterol and
slight decrease in cerebroside compared with non-acclimated genotypes. Cold-acclimated
wild types had increased total lipids and phospholipids of 17 and 25%, respectively
compared with non-acclimated genotypes which had a lower ration of sterol phospholipids
ratio. Yamaki and Uritani (1972), found that more than
90 molar percent of the total lipids in the mitochondrial membrane of sweet
potato are phospholipids and composed of the following components: phosphatidylethanolamine,
phosphatidylcholine and lysophosphatidylcholine collectively rich in (18:2)
linoleic. These components were reported to have decreased 40, 20 and 10%, respectively
following chilling treatment compared with the control, according to Yamaki
and Uritani (1974). These studies also found that 65-molar percent of the
total mitochondria membrane fatty acids of white potato phospholipids, including
components reported above were not altered following treatment. The chilling
tolerance difference between two genotypes to fatty acid composition could not
be related. Phromtong (1993), showed the C18:3 increased
with cold treatment in a chilling tolerant sweet potato genotypes on the phospholipids
fraction of the total lipids. Therefore, it is concluded that the mode of tolerance
among genotypes tested in this study was not different with respect to fatty
Peroxidase enzyme activity: The genotypes 180 MS3 and 183 MS4 had higher
peroxidase enzyme activity compared to the genotypes 105 MS1 and 108MS2 (Fig.
1, 2). The chilling temperature showed significantly higher
peroxidases activity as compared to higher temperature (25°C) studied. Similar
results obtained by El-hilali et al. (2003).
They reported that the peroxidase activity increases continuously at 4°C
over the period of storage in fortune mandarin fruits.
|| Peroxidase enzyme activity of chilling tolerant sweet potato
genotypes of studied
||Peroxidase enzyme activity of chilling tolerant genotypes
of sweet potatoes following 24 h of 5°C chilling, 25 and 40°C not
chilled exposure chilling exposure
If the peroxidase enzyme activity is a factor in chilling tolerance as suggested
by Woods et al. (1991), a difference in the tolerance
mechanism is indicated. Chilling sensitive and chilling tolerant plants
responses to low temperature stress by producing differential level of toxic
oxygen compounds were suggested to be the products metabolisms (Li
et al., 2011; Zahra et al., 2009;
Lin et al., 2006; Hodgson
and Raison, 1991). Superoxide dismutase (SOD), catalyzes (CAT) and various
peroxidases and ascorbate peroxidases, glutathione reductases constitute the
cellular defense mechanism against oxidative stress (Bowler
and Chua, 1994). The results revealed that genotypes 180MS3 and 183MS4 may
have a better protective mechanism with respect to peroxidase enzyme activities.
Usually peroxidases are ubiquitous enzymes that have diverse biochemical functions
in higher plants and are involved in the response of plants to chilling stress
(Li et al., 2011; Safizadeh
et al., 2007). Thus, the tolerance of 105MS1 and 108MS2 could be
from other physiological mechanisms (Badea and Basu, 2009;
Falcone et al., 2004).
From the aforementioned results and discussion, it was clinched that selecting
for chilling tolerance could enhance the chilling tolerance in sweet potatoes.
The basis or biochemical mechanism for chilling tolerance was not the same for
the four sweet potato genotypes tested; therefore combining traits for tolerance
could lead to higher tolerance levels.
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