Effect of Seaweed Extract, Humic Acid and Chemical Fertilizers on Morphological, Physiological and Biochemical Characteristics of Trigonella ...
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J. Agr. Sci. Tech. (2018) Vol. 20: 1505-1516
Effect of Seaweed Extract, Humic Acid and Chemical
Fertilizers on Morphological, Physiological and Biochemical
Characteristics of Trigonella foenum-graecum L.
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S. Mafakheri1*, and B. Asghari1
ABSTRACT
Modern agriculture is searching for new biotechnologies that would allow for a
reduction in the use of chemical inputs without negatively affecting crop yield or farmers'
income. Seaweed extract and humic acid are used as nutrient supplements , biostimulants,
or biofertilizers in agriculture and horticulture to increase plant growth and yield. To
investigate the effects of SeaWeed Extract (SWE), humic acid, and chemical fertilizers on
the growth, physiological and biochemical characteristics of Trigonella foenum-graecum
L., a greenhouse experiment was conducted in 2016. Results showed that foliar
applications of seaweed extract enhanced growth parameters. Among the different
treatments, the plants that received SWE showed maximum shoot lengths, fresh and dry
weights, number of pods per plant, chlorophyll “a”, chlorophyll “b”, total chlorophyll,
and carotenoids. Also, application of SWE increased the amount of total phenolic and
flavonoid contents in fenugreek. All fertilizer treatments increased significantly 2,2-
DiPhenyl-1-PicrylHhydrazyl (DPPH) radical scavenging activity of the plants in
comparison to the control. Plants treated with SWE showed stronger activity against α-
glucosidase with IC50 value of 171.37 μg mL-1 in comparison with acarbose (IC50= 19.7 μg
mL-1) as the reference α-glucosidase inhibitor. The data generated by this study revealed
that SWE could be used as foliar spray to maximize the quality and quantity of
fenugreek.
Keywords: Antioxidant activity, Biofertilizers, Fenugreek, Phenolic compound
INTRODUCTION also widely used in traditional medicine as
tonics, as a remedy against stomach
Fenugreek (Trigonella foenum-graecum disorders, diabetes, fever, anaemia,
L.) is an annual crop belonging to the constipation and as a galactogogue as well
Fabaceae family. This crop is native to an as for stimulation of appetite. It also has
area extending from Iran to Northern India, been used in alleviating high cholesterol
but is now widely cultivated in China, North plasma levels, diabetes and oxidative
and East Africa, Ukraine and Greece damage (Acharya et al., 2007).
(Petroponlas, 2002). Its seeds are a good Any improvement in agricultural system
source of protein, vitamins, alkaloid that results in higher production should
trigonellin, and essential oil, with immense reduce the negative environmental impact of
medicinal value, particularly against agriculture and enhance the sustainability of
digestive disorders (Rizvi et al., 2013). The the system. One such approach is the use of
leaves of fenugreek plant are edible and bio stimulants, which can enhance the
often used as a vegetable dish in Iran. It is effectiveness of conventional mineral
fertilizers. Some substances affect plant
_____________________________________________________________________________
1
Department of Horticultural Sciences Engineering, Faculty of Agriculture and Plant Resources, Imam
Khomeini International University, Qazvin, Islamic Republic of Iran.
* Corresponding author; email: smafakheri@gmail.com
1505______________________________________________________________ Mafakheri and Asghari
growth and its physiological activities, properties of plants. Eris et al. (2008)
including Humic Acid (HA) and SeaWeed showed that spraying of Ascophyllum
Extract (SWE). HA and its derivatives are nodosum extract on pepper plants leads to
complex compounds that exist in soils with increase in growth, yield, and concentration
high levels of organic matters and quinine of some nutrient elements, significantly.
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functional groups, which are formed by Zhang et al. (2003), in a study to test the
microbial decay of plant tissues (Zhang et combined effect of humic acid and SWE on
al., 2004; Thygesen et al., 2009). These growth and physiology of some creeping
fertilizers promote plant growth and induce herbaceous plants (Bentgrass), found
soil microorganisms like bacteria and fungi significant positive effects on growth and
and provide carbon as a source for the nutrient content of plants
organisms (Leonard, 2008). El-Bassiony et The present study was undertaken to
al. (2010) stated that growth of green bean investigate the effect of seaweed liquid
organs such as leaf, branch plant wet and fertilizers, humic acid, and chemical
dry weight, height, pods’ green yield and fertilizer (NPK), on the morphological,
their quality such as length and weight, and physiological, and biochemical
chlorophyll content of green leaf was characteristics and antioxidant activity of
increased due to the application of humic Trigonella foenum-graecum.
acid. Results of a research conducted by
Rasaei et al. (2012) with regard to the MATERIALS AND METHODS
physiological effects of application of humic
acid on green peas indicated that use of
humic acid exhibited significant effect on A pot experiment was carried out in 2016
value of chlorophyll “a” and “b”, compared at the Agricultural Research Greenhouse at
to those plants that did not receive this Imam Khomeini International University,
substance. Seaweeds are a renewable, Qazvin, Iran. The experimental design was
competitive local resource along the coastal Complete Randomized Design (CRD) with
agricultural area (Hernandez-Herrera et al., four treatments and seven replications.
2014) The Southern coast of Iran has Treatments included SWE fertilizer
(containing Ascophyllum nodosum extract),
abundant seaweed resources with more than
humic acid (containing 15% humic acid and
160 species being found in Persian Gulf and
2% fulvic acid), chemical fertilizers
Amman Sea. Marine algae are an important
(recommended rates of NPK for fenugreek)
source of diverse components, which have
and control (without the use of fertilizers).
beneficial effects in terms of enhancement
Twenty eight plastic pots (32×30 cm) were
of plant growth and development (Craigie,
prepared and filled with 5 kg of garden soil.
2011; Briceño-Domínguez et al., 2014;
The physical and chemical properties of the
Hernández Herrera et al., 2014), improved
experimental soil and SWE are shown in
tolerance to environment stress (Zhang and Tables 1 and 2, respectively. Seeds were
Schmidt, 2000; Zhang et al., 2003), and purchased from Isfahan Pakan Bazr Seed
increasing antioxidant properties of plants Production Company in Iran and sown at a
(Zhang and Schmidt, 2000). SWE contains depth of 1.5 cm in each pot. Seedlings were
growth promoting hormones (IAA and IBA, thinned to five plants per pot 10 days after
Cytokinins), trace elements (Fe,Cu, Zn, Co, emergence. Irrigation was regularly
Mo, Mn, and Ni), vitamins and amino acids provided during the vegetative period and all
and also enhances leaf total phenolic, agronomic management practices were
flavonols, and tannin contents and, performed as needed. In 4 leaves appearance
consequently, increases the antioxidant stage; SWE was applied as a foliar spray in
activity of plants leaf extracts (Krajnc et al., concentration of 1 mL L-1 and humic acid
2012). Also, SWE increases antioxidant was applied dissolved in irrigation water in
1506Seaweed Extract and Humic Acid on Fenugreek __________________________________
Table 1. Physical and chemical properties of experimental soil.
Available Available
Clay Silt Sand OM
Texture Phosphorus Potassium N (%) PH EC
(%) (%) (%) (%)
)ppm) )ppm)
Loam 31 35 34 12.7 145 0.08 0.71 7.4 2.31
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Table 2. Chemical properties of seaweed extract (SWE) fertilizer.
Amino S Zn P2O5 K2O N Fe Mn B Mg
C
acid -1
(%) (mg kg )
(%)
20 15 4000 50 800 4000 4000 400 150 20 1000
concentration of 500 mL L-1; and repeated (Salehi et al., 2013). Results are expressed
every 2 weeks until harvest, according to the as mg of gallic acid equivalents per g dry
manufacturer's directions. All amounts of matter of extract (mg GAE g-1 DM).
calcium super-phosphate (15% P2O5),
potassium sulfate (48% K2O), and half of
Total Flavonoid Content (TFC)
Urea (46% N) were applied during soil
preparation. The remaining half of urea was
applied 30 days after sowing. TFC was estimated by aluminum chloride
colorimetric method as previously described,
with a few modification (Marija et al.,
Determination of Morphological and 2014). The total flavonoid content was
Physiological Parameters expressed as mg quercetin per g dry matter
of extracts (mg QE g-1 DM) by comparison
Growth parameters including plant height, with the quercetin standard curve.
fresh and dry weight were measured at flowering
stage and numbers of fruits per plant, number of
seed per fruit, and 1,000 seeds weight at seed DPPH Radical Scavenging Activity
harvest stage. Photosynthetic pigments i.e. chl.
“a”, chl. “b”, total chlorophyll, and total The stable 1,1-DiPhenyl-2-PicrylHydrazyl
carotenoids were determined according to the radical (DPPH) was used for determination
methods described by Von Wettstein (1957). of free radical-scavenging activity of the
extracts. The DPPH radical-scavenging
Extraction of Plant Essential Oil activity was determined using the method
described by Zengin et al. (2015). The
results were expressed as equivalents of
Dried seeds of fenugreek (20 g, three times) trolox (mg TAE g-1 DM).
were subjected to hydro distillation for 3 hours
using a Clevenger-type apparatus to produce
oil according to the method recommended by Total Antioxidant Activity (TAC) by
the European pharmacopoeia, and essential oil Phosphomolybdenum Method
percentage was determined.
The TAC of fenugreek extracts was
Total Phenolic Content (TPC) spectrophotometrically determined by the
phosphomolybdenum assay using the
method described by Zengin et al. (2015).
The TPC of the fenugreek extract was The antioxidant activity of the extracts were
determined by the Folin-Ciocalteu reagent as
previously reported, with minor changes
1507______________________________________________________________ Mafakheri and Asghari
expressed as mg ascorbic acid equivalents RESULTS
per g of dry matter (mg AAE g-1 DM).
Growth Parameters
Alpha-Glucosidase Inhibition Assay
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From the data presented in Table 3, it is
The α-glucosidase inhibitory activity of clear that the plants height, fresh and dry
the extracts was assessed according to an weight, number of seeds per plant, and 1,000
earlier reported bioassay method (Asghari et seeds weight of fenugreek was highly
al., 2015). The results were expressed as increased as a result of SWE and chemical
percent of α-glucosidase inhibition. fertilizer treatments. SWE and chemical
fertilizer exhibited the highest shoot length
Statistical Analysis (24.93 and 22.95 cm), respectively,
compared to the control (19.3 cm). The plant
height increased 29% and 19% by the
All the data were subjected to statistical application of SWE and chemical fertilizers,
analysis using SPSS software (IBM SPSS respectively. Results showed that SWE
Statistics, version 22). Differences between fertilization increased plants fresh and dry
the treatments were performed by Duncan’s weights in fenugreek from 11.11 and 7.38 g
Multiple Range Test at 5% confidence (control), to 14.66 and 9.73 g, respectively
interval. Transformations were applied to (Table 3).
the data to ensure that the residuals had The highest numbers of pods per plant
normal distribution. Correlations were recorded were 12.12 and 11 in the plants that
performed using the Pearson’s correlation received SWE and NPK fertilizer, which
coefficient (r). were 63 and 48% higher than the control,
respectively. All fertilizer treatments
Table 3. Means comparison of morphological traits of fenugreek. a
Treatments Plant height Plant Plant Number of Number of 1000 Seeds
(cm) Fresh Weight Dry Weight (g) fruit per seed per weight (g)
(g) plant fruit
SWE 24.93 a 14.66 a 9.73 a 12.12 a 11.5 a 10.22 a
Humic acid 21.92 b 12.43 bc 8.19 bc 8.37 b 11.62 a 9.17 ab
NPK 22.95 ab 13.47 ab 8.62 b 11 ab 11.28 a 9.64 ab
Control 19.3 c 11.11 c 7.38 c 7.43 b 9.14 b 8.23 b
a
Means in each column followed by similar letter(s), are not significantly different at 5% probability level.
Table 4. Means comparison of biochemical traits of Fenugreek.a
Treatments Total Chlorophyll Chlorophyll Ascorbic acid Total Essential
chlorophyll “a” “b” (mg g-1 FW) carotenoids oil
(mg g-1 FW) (mg g-1 FW) (mg g-1 FW) (mg g-1 FW) (%)
SWE 1.98 a 1.30 a 0.68 a 0.0040 a 0.27 a 0.97 a
Humic acid 1.70 b 1.18 a 0.51 b 0.0034 ab 0.20 b 0.85 a
NPK 1.35 c 0.93 b 0.41 b 0.0032 b 0.16 b 0.88 a
Control 0.96 d 0.78 c 0.18 c 0.0030 b 0.08 c 0.69 b
a
Means in each column followed by similar letter(s), are not significantly different at 5% probability level.
1508Seaweed Extract and Humic Acid on Fenugreek __________________________________
increased number of seeds per pod but there of 0.97%.
were no significant differences between
treatments. SWE also caused 24% increase
Phytochemical Contents and
in 1,000 seeds weight over the control.
Antioxidant Activity
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Biochemical Traits As shown in Figure 1, total phenolic and
flavonoids contents of fenugreek extract
The obtained results showed that were influenced by fertilizer source (P≤
treatments had significant effect on total 0.05). It was observed that application of
chlorophyll, chlorophyll “a” and “b”, total SWE increased the production of total
carotenoids, and essential oil content of phenolics and flavonoids contents in
fenugreek (P≤ 0.05) (Table 4). The fenugreek. The TPC in the T. foenum-
maximum chlorophyll “a” content was graceum leaf extract were expressed as mg
obtained in plants that were treated with GAE g-1 extract and indicated that plants
SWE and humic acid, with the values of treated with SWE and NPK had the highest
1.30 and 1.18 mg g-1 fresh weight, amount of phenolic content (158.47 and
respectively, which were 66 and 51% 146.67 mg GAE g-1 extract, respectively).
increase over the control. The highest Also, humic acid treatment had no
chlorophyll “b”, total chlorophyll, ascorbic significant effect on TPC in comparison
acid and carotenoids contents were obtained with the control. According to the obtained
as 0.68, 1.98, 0.0040, and 0.27 mg g-1 FW, results, plants that received SWE, had the
respectively, in plants that received SWE. maximum amount of flavonoids (177.77 mg
An important point is that NPK treatment QE g-1 DM). So, total flavonoids were
exhibited significant positive effect on the enhanced 125% in the SWE treatment
amount of total chlorophyll, chlorophyll “a”, compared to the control. The TFC in the
chlorophyll “b” and total carotenoids of the plants cultivated with NPK treatment (89.23
plant, compared to the control, while its mg QE g-1 extract) was significantly lower
effect on ascorbic acid amount was not than SWE, however, this amount was
significant (Table 4). All of applied nutrition statistically higher than the control (52.33
treatments enhanced significantly the mg QE g-1 DM). In order to evaluate the
essential oil percentage in the plants. As can antioxidant activity of fenugreek extracts,
be seen in Table 4, the highest amount of DPPH and phosphomolybdenum assays
essential oil is related to SWE with the value were conducted. As can be seen in Figure 2,
Figure 1. Effect of treatments on total phenol and flavonoids of Fenugreek.
Figure 1. Effect of treatments on 1509
total phenol and flavonoids of fenugreek.
Please put labels for the axes______________________________________________________________ Mafakheri and Asghari
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Figure 2. Effect of treatments on DPPH radical scavenging total antioxidant activities of fenugreek
extract.
all fertilizer treatments increased significantly μg mL-1) in comparison with the control
DPPH radical scavenging activity of the plants (IC50= 38.07 μg mL-1).
by 11 to 78.5% in comparison to the control.
The highest DPPH radical scavenging activity Simple Correlation
was revealed to occur in plants that were
treated with SWE indicating 304.33 μg TEs g-1
extract. Simple correlation results showed that plant
height had significant positive correlation with
fresh weight (r=0.810**), dry weight (r=
Enzyme Inhibitory Activity
0.786**), number of pods per plant (r= 0.426*),
number of seeds per pod (r= 0.448*), total
Inhibitory activity of fenugreek extract on chlorophyll (r= 0.545**), chlorophyll “a” and
α-glucosidase is presented in Figure 3. “b” (r= 0.551** and r= 0.480**), total
Alpha-glucosidase inhibitors could be used carotenoids (r= 0.519**), essential oil
as the remedies of diabetes. According to the percentage (r= 0.541**), DPPH (r= 0.866**),
obtained data, plants treated with SWE phosphomol (r= 0.905**), and glucosidase (r=
showed significantly stronger activity 0.883**). Other correlation results can be seen
against α-glucosidase (IC50 values of 171.37 in Table 5.
Figure 3. Effect of treatments on α-glucosidase inhibitory effect of fenugreek extract.
1510Seaweed Extract and Humic Acid on Fenugreek __________________________________
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1511______________________________________________________________ Mafakheri and Asghari
DISCUSSION esculentus (Thirumaran et al, 2009). The
increase in chlorophyll content was a result
In the present investigation, plants treated of reduction in chlorophyll degradation,
with SWE showed better response in terms which might be caused in part by betaines in
of vegetative parameters. These results are the SWE (Whapham et al., 1993). Seaweed
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in good agreement with previous studies extracts contain cytokinins as well, which
where growth and seedling vigor of maize, induce the physiological activities and
mungbean, and cabbage were enhanced by increase the total chlorophyll in the plant.
SWE treatment (Rengasamy et al., 2015; Also, this will positively reflect on the
Kannan et al., 2016). The stimulatory effect activity of photosynthesis and the
of SWE on cabbage plant may be the result synthesized materials, which will show on
of synergistic interactions between SWE and shoots characteristics (Janick and Whipkey,
endogenous growth hormones (Teixeira da 2002). Regarding the biochemical traits
Silva et al., 2013). It was speculated that the application of SWE showed a significant
increase in plant height may have been a effect on the content of plant essential oil
result of macronutrients found in NPK compared to the control. This result is in a
fertilizer and N-containing plant growth good line with the findings of Golzadeh et
regulators (auxins and cytokinins) within the al. (2011) on Matricarai recutita and Rafiee
SWE that were absorbed by the plants. An et al. (2013) on Calendula officinalis L..
alternative explanation is that organic Ardebili et al. (2012) indicated that foliar
molecules such as organic acids, methionine application of SWE as a source of amino
and even aminoacids in SWE can increase acids, at suitable concentrations, had
nutrient absorption in plants by chelating the positive effects on the content of secondary
available nutrients, thereby increasing their metabolites, antioxidants, and antioxidant
absorbance (Papenfus et al., 2013). Seaweed activity. They reported that increasing the
extracts can equilibrate growth as a result of phytochemical constituents of Aloe vera
auxin and gibberellin acid presence, which plants by using amino acids could
will increase vitamins and hormones demonstrate which of these compounds was
producing in the treated plants (O’ Dell, involved in stimulating plant metabolic
2003). This increase in shoots characteristics pathways. El-Sharabasy et al. (2012)
might be also due to the macronutrients reported that amino acids have a significant
content in seaweed extracts (Table 2). effect on the production of secondary
Macronutrients like nitrogen, potassium, and metabolites. SWE applications significantly
phosphorous are very essential for growth influenced the phenolic and flavonoids
and development of the plant (Attememe, contents and antioxidant potential of the
2009). The observation of SWE treated studied fenugreek leaves. The contents of
Arachis hypogea plants suggested that the phenolic and flavonoids in leaves obtained
growth and biochemical characteristics in the treated plants were higher than for the
might be promoted by micro and macro controls. Phenolic compounds are a class of
elements and growth promoting hormones antioxidant agents that act as free radical
present in the SWE (Ganapathy-selvam and scavengers and are responsible for
Sivakumar, 2014). Our findings coincide antioxidant activity in medicinal plants. Free
with those of earlier studies carried out on radicals may cause many disease conditions
soybean (Rathore et al., 2009) where there such as cancer and coronary heart disease in
was an increase in vegetative growth by the human (Alizadeh et al., 2010; Javanmardi et
application of SWE. Similar results were al., 2003) Many plants extracts containing
also observed in Cajanus cajan (L.) Millsp. bioactive compounds, including phenolics
(Mohan et al., 1994), Vigna sinensis L. and flavonoid, exhibit efficient antioxidant
(Sivasankari et al., 2006), and Abelmoschus properties and prevent free radical damages
(Koleva et al., 2002). High antioxidant
1512Seaweed Extract and Humic Acid on Fenugreek __________________________________
amounts/activities following SWE treatment are of the leaf extracts. Hence, the application of
important for improving the nutritional value of SWE on Fenugreek might be useful in
medicinal plants as well as prolonging their shelf increasing the yield and medicinal value of
life, thus enhance the overall quality and these plants and help produce an essential oil
marketable value of fresh produce. Increases in content from fenugreek seeds.
the phenolic content of the leaves of
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Pelargonium were observed in plants treated
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تاثیر کاربرد عصاره جلبک ،هیومیک اسید و کود شیمیایی بر صفات مورفولوژیکی،
فیزیولوژیکی و بیوشیمیایی شنبلیله ()Trigonella foenum-graecum
س .مفاخری ،و ب .اصغری
چکیده
کطاٍرسی هذرى بِ دًبال دستیابی بِ رٍش ّای سیستی ٍ هذرًی است کِ بِ ٍاسطِ آى بتَاى هصزف
کَدّای ضیویایی را بذٍى تاثیز هٌفی در هیشاى هحصَل ٍ درآهذ کطاٍرساى ،کاّص داد .عصارُ جلبک
دریایی ٍ اسیذ َّهیک بِ عٌَاى هکولّای تغذیِای ٍ یا کَدّای بیَلَصیک در کطاٍرسی ٍ باغباًی بِ
هٌظَر افشایص رضذ ٍ عولکزد گیاُ استفادُ هیضَد .بِ هٌظَر بزرسی تاثیز عصارُ جلبکّ ،یَهیک اسیذ
ٍ کَد ضیویایی بز رضذ ٍ ًوَ ٍ فاکتَرّای فیشیَلَصیکی ٍ بیَضیویایی ضٌبلیلِ ،آسهایطی گلخاًِای در
سال 5931اجزا گزدیذً .تایج ًطاى داد کِ ،هحلَلپاضی با عصارُ جلبک ،فاکتَرّای رضذی گیاُ را
بْبَد بخطیذ .در بیي تیوارّای هختلف ،گیاّاًی کِ با عصارُ جلبک تیوار ضذًذ ،بیطتزیي هقذار ارتفاع
بَتٍِ ،سى تز ٍ خطک ،تعذاد ًیام در گیاُ ،هقذار کلزٍفیلّای ،b ٍ aکلزٍفیل کل ٍ کارتٌَئیل کل را
دارا بَدًذّ .وچٌیي کاربزد عصارُ جلبک هقذار تزکیبات فٌَلی ٍ فالًٍَئیذی را ًیش افشایص دادّ .وِ
تیوارّای کَدی در هقایسِ با ضاّذ ،بِ طَر هعٌیداری سبب افشایص قذرت ضذ رادیکالی گیاّاى در
هقابل رادیکالّای DDPHضذًذ .گیاّاًی کِ با عصارُ جلبک هحلَل پاضی ضذًذ ،فعالیت قَیتزی
در هقابلِ با آًشین آلفا-گلَکَسیذاس با هقذار 535/93 ، IC50هیکزٍگزم در هیلیلیتز در هقایسِ با
آکاربَس (با 53/3 ،IC50هیکزٍگزم در هیلیلیتز) بِ عٌَاى هْارکٌٌذُ آلفا گلیکَسیذاس رفزًس،
داضتِاًذ .دادُّای بِ دست آهذُ اس ایي هطالعًِ ،طاى داد کِ هیتَاى اس هحلَلپاضی عصارُ جلبک،
بزای بِ دست آٍردى حذاکثز کویت ٍ کیفیت هحصَل ضٌبلیلِ استفادُ ًوَد.
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