2 Egypt. J. Phytopathol., Vol. 32, No. 1-2, pp.

11-21 (2004)
Preliminary Evaluation of Salicylic Acid and
Acetylsalicylic Acid Efficacy for Controlling Root
Rot Disease of Lupin under Greenhouse Conditions
Nehal S. El-Mougy
Plant Pathol. Dept., National Res. Centre, Giza, Egypt.
alicylic acid (SA) and acetylsalicylic acid (ASA) in addition to
Rizolex-T were evaluated as seed dressing or soil drench against
lupin root rot pathogens under greenhouse conditions. No significant
reduction in seed germination was observed when lupin seeds were
treated with SA and ASA up to 2 and 3 g/kg, respectively. Raising the
applied dosages has reflected negatively on seed germination. SA,
ASA and Rizolex-T as well as seed dressing or soil drench at the rate
of 2, 3 and 3 g/kg, respectively, have significantly reduced the
percentage of root rot incidence at both pre-, and post-emergence
stages of lupin plants growth comparing with untreated control in
artificially infested soil with Fusarium solani, Rhizoctonia solani and
Sclerotium rolfsii. Seed dressing showed higher significant reduction
in disease incidence than soil drench treatment. Acetylsalicylic acid as
seed dressing or soil drench showed superior effect on root rot
incidence followed by SA and Rizolex-T, respectively. The
percentage of disease infection at these treatments where 4.0 &
12.5%; 12.0 & 22.7% and 24.0 & 31.6% at pre-emergence stage,
while the recorded infection at post-emergence stage were 16.0 &
19.6%; 16.0 & 23.8% and 20.0 & 25.0% for seed and soil treatments,
respectively. Furthermore, all the applied treatments significantly
increased the chitinase activity in treated lupin plants grown in soil
infested with F. solani, R. solani and S. rolfsii. Lupin plants treated
with SA and ASA showed more activity in chitinase than Rizolex-T
treatment. It is thus suggested that the usage of SA and ASA as seed
dressing or soil drench could be considered as fungicide alternatives
for controlling such soilborne diseases.
Key words: Acetylsalicylic acid, disease control, F. solani, R. solani,
root rot, S. rolfsii and salicylic acid.
Root rot diseases caused by several soilborne fungal pathogens are widespread
and serious in many crops cultivated in different soil types. Lupin (Lupinus termis
Forsk) is subjected to attack by many pathogenic organisms wherever the crop is
grown. Several root rot pathogens such as Rhizoctonia solani, Sclerotium rolfsii and
Fusarium solani are reported to attack lupin roots and stem base causing serious
losses in seed germination and plant stand as well (Fahim et al., 1983).
An investigation for controlling such diseases is considered important, especially
in view of their wide prevalence in Egypt. Several attempts to control root rot
diseases could be accepted. However, fungicides are considered one of several
factors involving in environmental pollution, in spite of their satisfactory results in
S
NEHAL S. EL-MOUGY
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
12
the control of plant diseases. In addition, control of disease with fungicides has
proven very difficult, and almost all fungicides are effective only at phytotoxic
levels (Jarvis, 1988). On the other hand, the application of biological control using
antagonistic microorganisms proved to be successful for controlling various plant
diseases in many countries. At the same time, it still not easy and costly in
application, however it can serve as a better control measure under greenhouse
conditions (Sivan and Chet, 1986). Recently, the growing concern over the use of
pesticides to human health and environment has brought increasing interest in the
use of alternatives characterized with negative impact on the environment.
Therefore, present activity focuses on finding compounds that are safe to human and
environment. An alternative to fungicidal application, it may be possible to utilize
a scheme of inducible plant defenses which provides protection against a broad
spectrum of diseasecausing organisms. Among synthetic inducers, salicylic acid
(SA) and acetylsalicylic acid (ASA) have been found to be active as antimicrobial
agents in various trials as disease resistance inducers. These have been reported for
inducing resistance against several plant pathogens, i.e. TMV (Marrero et al., 1990)
bacterial soft (El-Sayed, 1996) bacterial wilt (Abdel-Said et al., 1996) as well as
soilborne fungal root rot and wilt diseases (Chen-Chunquan et al., 1999 and
Mandavia et al., 2000), in addition to fungal foliar diseases (Srinivas et al., 1997).
Moreover, few attempts proved the direct inhibitor effect of SA and ASA on the
growth of phytopathogenic microorganisms (Dwivedi, 1990; Guo et al., 1993;
Srinivas et al., 1997; Matthew and Alexander, 1999; Mandavia et al., 2000 and
El-Mougy, 2002).
The purpose of the present study aimed to evaluate the efficacy of salicylic acid
and acetylsalicylic acid applied as seed or soil treatments for controlling root rot
disease of lupin under greenhouse conditions.
M a t e r i a l s a n d M e t h o d s
Root rot pathogens:
An aggressive isolate of Fusarium solani, Rhizoctonia solani and Sclerotium
rolfsii, obtained from Plant Pathol. Dept., National Res. Centre (NRC), were used in
the present study. These fungal isolates proved to be highly pathogenic to induce
root rot disease on various plants in previous works (El-Kazzaz and El-Mougy, 2001
and Abdel-Kader et al., 2002).
In vitro assay:
The influence of SA and ASA as seed dressing or soil drench on lupin seeds
germination was evaluated under in vitro conditions.
a) Seed dressing:
Lupin seeds (cv. Giza 2) were surface disinfected by immersing in sodium
hypochlorite (2%) for 2 min, and washed several times with sterilized water, then
dried between two sterilized layers of filter paper.
The disinfected lupin seeds were coated with either SA or ASA at the rate of 1,
2, 3, 4 and 5 g/kg seeds. Seed dressing was carried out by applying the tested SA
PRELIMINARY EVALUATION OF SALYCYLIC ACID .
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
13
and ASA individually to the moistened seeds in polyethylene bags and shaked well
to ensure even distribution of the added chemicals. The treated lupin seeds were
sown in 2x2 cm cells in polystyrene foam trays with 1x1 cm bottom holes for
drainage and root emergence. Mixture of autoclaved peat-moss and sand (1:1, v/v)
was used for sowing.
b) Soil drench:
Salicylic acid and acetylsalicylic acid were individually mixed thoroughly at
different rates, i.e. 1, 2, 3, 4 and 5 g/kg of soil mixture. The drenched peat-moss-
sand soil was filled into polystyrene foam trays, then sown with disinfected lupin
seeds.
The fungicide Rizolex-T at the recommended dose (3 g/kg) was applied either as
seed or soil treatment as stated before, in addition to disinfected lupin seeds sown in
autoclaved peat-moss-sand soil were used as comparison treatments.
Seventy two lupin seeds were sown for each particular treatment. All polystyrene
foam trays were kept under laboratory conditions (18-21C) and irrigated every two
days for three successive weeks, then the percentage of germinated lupin seeds was
calculated.
Greenhouse experiment:
Effect of SA and ASA on root rot disease incidence of lupin was studied. Pot
experiment was carried out in the greenhouse of Plant Pathology Dept., NRC. The
above mentioned lupin root rot pathogens were used in the present experiment.
Loamy soil was artificially infested individually (at the rate of 5% w/w) with the
inoculum of each fungus tested which previously grown for two weeks on sand
barley medium (1 : 1, w/w and 40% water) at 252C.
A set of varied infested soils were filled in plastic pots (20 cm in diameter) and
sown, with relevant to the specific treatment, with disinfected lupin seeds dressed
individually with SA and ASA at the rate of 2 or 3 g/kg seeds, respectively.
Another set of varied infested soil was thoroughly mixed individually with SA
and ASA at the rate of 2 or 3 g / kg soil weight, then filled in plastic pots (20-cm-
diameter) and sown with disinfected lupin seeds.
The fungicide Rizolex-T was applied to artificially infested soils, at the
recommended dose, as seed dressing or soil drench at the rate of 3 g/kg seeds or soil,
and used for comparison treatment.
A set of disinfected lupin seeds were sown in artificially infested soils and served
as general check treatment. Five lupin seeds (cv. Giza 2) were sown in each pot and
five replicated pots were used for each particular treatment.
Percentage of root rot disease incidence was calculated as pre- and post-
emergence damping-off after 20 and 40 days of sowing date, respectively.
Determination of chitinase activity:
The effect of usage the inducers SA and ASA as seed or soil treatment in
addition to untreated control on chitinase activity was determined in lupin plants as
follows:
NEHAL S. EL-MOUGY
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
14
(a) Extraction of enzyme:
Plant tissues (g), relevant to each particular treatment, were homogenized in 0.2
M Tris HCL buffer (pH 7.8) containing 14mM -mercaptoethanol at the rate of 1 :
3 (w/v). The homogenate was centrifuged at 3000 rpm for 15 min. The supernatant
was used to determine enzyme activity (Tuzum et al., 1989).
(b) Chitinase assay:
The substrate, colloidal chitin was prepared from chitin powder according to the
method described by Ried and Ogryd-Ziak (1981). Twenty five grams of chitin was
milled, suspended in 250ml of 85% phosphoric acid and stored at 4C for 24 hr, then
blended in 2 liters of distilled water using a waring blender and the suspension was
centrifuged. The washing procedure was repeated twice. In the final wash, the
colloidal chitin suspension was adjusted to pH 7.0 with (1 N) NaOH, separated by
centrifugation, then stored at 4C. Determination of the enzyme activity was carried
out according to the method of Monreal and Reese (1969), 1 ml of 1% colloidal
chitin in 0.05 M citrate phosphate buffer (pH 6.6) in test tubes, 1 ml of enzyme
extract was added and mixed by shaking. Tubes were kept in a water bath at 37C
for 60 min, then cooled and centrifuged before assaying. Reducing sugar was
determined in 1 ml of the supernatant by dinitrosalicylic acid (DNS). Optical density
was determined at 540nm. Chitinase activity was expressed as mM N-acetylglucos-
amine equivalent released / gram fresh weight tissue / 60 min.
Statistical analysis:
Tukey test for multiple comparisons among means was utilized (Neler et al.,
1985).
R e s u l t s a n d D i s c u s s i o n
In vitro assay:
The effect of SA and ASA application as seed or soil treatment on lupin seed
germination was tested under in vitro conditions. Data presented in Table (1) show
that usage of salicylic acid and acetylsalicylic acid as seed dressing or soil drench up
to 2g/kg had no inhibitory effect on lupin seed germination. Raising the used dosage
more than 2 or 3 g/kg for SA and ASA, respectively caused significant reduction in
the percentage of lupin seed germination, while no inhibitory effect was observed
with Rizolex-T when applied at the recommended dose (3g/kg) as seed dressing or
soil drench treatment.
In this regard, many investigators recorded the effect of SA and ASA on seed
germination. Sushma-Negi et al. (2001) studied the effect of different concentrations
of SA and ASA on seed germination of soybean. They found that percentage of seed
germination was decreased with the increasing level used of SA. Zhang-ShiGong et
al. (1999) stated that wheat seeds treated with 1 g/l salicylic acid or 2 g/l aspirin
increased their germination rate. They added that the addition of SA and ASA not
only increase germination rate but also increase germination and activities of alpha-
amylase and proteinase in endosperm and their contents of soluble sugars, protein
and free amino acids. Moreover, Elangovan et al. (1995) reported that treatment of
seeds
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Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
15
Table 1. I n vitro effect of Salicylic acid (SA) and Acetylsalicylic acid (ASA) on
lupin (cv. Giza 2) seed germination
SA ASA Tested dose
(g/kg) Seed dressing Soil drench Seed dressing Soil drench
1 98.6 a
*
97.2 a 98.6 a 98.6 a
2 95.8 a 94.4 a 97.2 a 95.8 a
3 84.7 b 81.4 b 95.8 a 94.4 a
4 81.9 b 79.2 b 83.3 b 83.3 b
5 77.8 b 76.4 b 80.5 b 80.5 b
Comparison treatment:
Rizolex-T seed dressing
Soil drench (3g/kg)
Check treatment
98.6 a
98.6 a
97.2 a
* Percentage of lupin seed germination.
Figures with the same letters are not significantly different (P= 0.05).
with 1 and 2 mM salicylic acid induced 25% and 16% higher in seed germination,
respectively, of Phaseolus aureus (Vigna radiata), while treatment with 5 mM SA
inhibited the growth of seedlings. These reports are in agreement with the present
data that concentrations of SA and ASA positively affect seed germination up to
certain concentration, then inhibition in germination rate starts. On the other hand,
several workers recorded the positive effect on germination of seeds treated with
different concentrations of various fungicides (Siddique et al., 1996; Shalaby, 1997
and Vyakarnahal et al., 2000).
Greenhouse experiment:
The efficacy of salicylic acid and acetylsalicylic acid in addition to Rizolex-T as
seed dressing or soil drench on lupin root rot incidence was evaluated in pots
experiment using soil artificially infested with the disease agents under greenhouse
conditions.
Data in Table (2) reveal that all the tested treatments have significantly reduced
the percentage of root rot incidence at both pre- and post-emergence stages of lupin
plant growth comparing with the check treatment. The highest percentage of root rot
infection was observed in lupin plants grown in infested soil with R. solani followed
by these grown soil infested with S. rolfsii and F. solani. The corresponding disease
percentages were 64.0 & 55.5%; 56.0 & 54.5% and 36.0 & 43.8% at pre- and post-
emergence stages of plant growth, respectively.
Data also show that all treatments varied in their effect on disease incidence.
Seed treatments showed higher significant reduction on disease incidence than soil
treatments. In infested soil with F. solani, ASA as seed dressing or soil drench
showed superior effect on disease incidence followed by SA and Rizolex-T,
respectively. Disease incidence (%), for these treatments, recorded 4.0 & 12.5%;
12.0 & 22.7% and 24.0 & 31.6% at pre-emergence stage for seed and soil
treatments, respectively. Meanwhile, at post-emergence stage the recorded root rot
NEHAL S. EL-MOUGY
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
16
Table 2. Percentage of lupin root rot incidence in response to seed dressing or
soil drench with SA, ASA and Rizolex-T under greenhouse conditions
Treatment
SA ASA Rizolex-T
Tested fungus Disease incidence
(%)
Check*
Seed Soil Seed Soil Seed Soil
Pre-emergence 36.0 b** 12.0 e 22.7 d 4.0 f 12.5 e 24.0 d 31.6 b F. solani
Post-emergence 43.8 a 16.0 e 23.8 d 16.0 e 19.6 d 20.0 d 25.0 c
Pre-emergence 64.0 a 28.0 c 27.7 c 24.0 d 31.3 b 8.0 f 26.0 c R. solani
Post-emergence 55.5 a 32.0 b 29.4 c 28.0 c 33.3 b 16.0 e 28.5 c
Pre-emergence 56.0 a 20.0 d 25.0 c 16.0 e 28.6 c 16.0 e 28.5 c S. rolfsii
Post-emergence 54.5 a 24.0 d 26.3 c 20.0 d 30.0 b 20.0 d 30.0 b
* Lupin plants grown in artificially infested soil with root rot pathogens.
** Figures with the same letters are not significantly different (P= 0.05).
infection was 16.0 & 19.6%; 16.0 & 23.8% and 20.0 & 25.0% for the same
treatment, in a respective order. Furthermore, in infested soil with R. solani and
S. rolfsii another feature of tested treatments on lupin root rot incidence was
observed. Rizolex-T occupied the first order for reduction of root rot incidence at
both damping-off stages followed by ASA and SA treatments especially when used
for seed dressing. It is interesting to note that, more reduction in disease incidence
was observed at pre-emergence stage of plant growth than at post-emergence. This
observation was also recorded by Abdel-Kader (1997) who reported that Rizolex-T
as seed dressing decreased bean root rot incidence to a lower extent at post-
emergence stage in comparison with the biocide treatments. He concluded that this
may be due to the expected degradation of fungicide when introduced into the soil
and exposed to the environmental conditions. This conclusion is in harmony with
the present results that treated lupin seeds with SA; ASA or Rizolex-T provide such
protection to seed bed region against soilborne pathogens reflected on the observed
lower disease incidence at pre-emergence stage before exposure to degradation
factors. The efficacy of SA and ASA for decreasing disease incidence on various
plants was recorded by many investigators. Palva et al. (1994) reported that the
addition of SA to the growth medium of tobacco seedlings made them almost fully
resistant to infection by soft rot bacteria. They stated that the molecular mechanism
of the SA-induced resistance to Erwinia carotovora subsp. carotovora appears to
involve inhibition of plant cell wall-degrading enzymes secreted by the pathogen.
Okey and Sreenivasan (1996) recorded that seed treatment, plant spray and soil
drench with SA reduced infection with Phytophthora palmivora of cacao. They add
that these results indicated that SA induces systemic resistance in cacao and should
be considered as a potential chemical for control of the pathogen.
Moreover, Voget and Buchenauer (1997) reported that both SA and ASA
reduced the percentage of cucumber damping off when applied as soil drench.
Also, Wisniewska and Chelkowski (1999) confirmed the above mentioned reports.
They stated that the application of SA as seed treatment at different concentrations
from 1-10 g/l reduced the Fusarium blight disease on cucumber seedlings
as 38 up to 66%.
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Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
17
These results are in a harmony with those obtained in the present study, as SA
and ASA, either used as seed dressing or soil drench, had the ability to reduce lupin
root rot incidence. The recorded effect might be attributed to the act of SA and ASA
as plant defense inducers or to their direct effect on soilborne plant pathogens as
stated by El-Mougy (2002).
Dressing lupin seed or soil drench with Sa, ASA and Rizolex-T were applied to
evaluate their effect on chitinase activity in lupin plants grown in soil artificially
infested with root rot pathogens. Data in Table (3) indicate that all treatments have
significantly increased the chitinase activity. Lupin seeds treated with SA and ASA
showed more activity of chitinase enzyme than Rizolex-T treatment. In this concern,
seeds treated with ASA showed superior effect followed by SA and Rizolex-T, in
a respective order. These treatments increased the chitinase activity up to 8.1, 150.0
and 142.3% and to 56.9, 94.8 and 67.7% as well as to 8.1, 93.5 and 15.2% in lupin
plants grown in infested soil with F. solani, R. solani and S. rolfsii, respectively.
Table 3. Chitinase activity in lupin plants treated with SA, ASA and Rizolex-T
as seed dressing or soil drench under greenhouse conditions
Treatment
SA ASA Rizolex-T
Tested
Fungus
Chitinase
measure
Check *
Seed Soil Seed Soil Seed Soil
Activity 0.86a** 1.35 c 1.21 c 1.79 c 1.11 c 0.93 ab 0.89 ab F. solani
Increase (%) ------ 56.9 40.6 108.1 29.0 8.1 3.4
Activity 0.75a 1.52 c 1.10 c 1.95 c 1.07 c 1.52 c 1.01 c R. solani
Increase (%) ------ 94.8 41.0 150.0 37.1 93.5 29.4
Activity 0.59a 0.99 ab 0.71 ab 1.43 c 1.08 c 0.68 ab 0.77 ab S. rolfsii
Increase (%) ------ 67.7 20.3 142.3 83.0 15.2 30.5
* Lupin plants grown in artificial infested soil with root rot pathogens.
** Figures with the same letters are not significantly different (P= 0.05).
In case of soil drench, the highest increase in chitinase activity was observed in
plants grown in soil infested with F. solani, R. solani and S. rolfsii then drenched
with SA (being 40.6, 41.0 and 20.0 %, respectively) as more than in check
treatment. These figures followed by 29.0, 37.1, 83.0% and 3.4, 29.4, 30.5%
increase in chitinase activity resulted for treatments of ASA and Rizolex-T,
respectively. Meanwhile, the lowest chitinase activities (being 0.86, 0.75 and 0.59%)
was recorded in untreated lupin plants grown in infested soil with the same
pathogens, respectively.
In this regard, many investigators reported that induced resistance in various
plants is associated with enhancing the activities of chitinase and -1,3-glucanase
which hydrolyse hyphal cell wall of fungi (Matta et al., 1988). Also, Sathiyabama
and Balasubramanian (1999) reported that prior treatment of groundnut leaves with
salicylic acid showed a reduction in the number of rust pustules caused by Puccinia
NEHAL S. EL-MOUGY
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
18
arachidis. They concluded that enhanced activities of intercellular chitinase and
glucanase of treated leaves might be associated with induced resistance responses in
treated groundnut with SA against rust disease.
Promising applicable technique could be suggested in the light of the results
obtained in the present study. The usage of salicylic acid and acetylsalicylic acid as
seed dressing or soil drench might be considered as safe, cheap and easily applied
method for controlling soilborne plant pathogens taking into consideration the
avoidance of environmental pollution.
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(Received 11/02/2004;
in revised form 14/04/2004)
PRELIMINARY EVALUATION OF SALYCYLIC ACID .
Egypt. J. Phytopathol., Vol. 32, No, 1-2 (2004)
21
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