Beneficial Effects of Arbuscular Mycorrhizal Fungi and Trichoderma on Diseased Shallot

Abstract

Purple blotch and fusarium basal rot are important shallot diseases which have caused significant yield loss. An alternative control method for these diseases is the use of biocontrol agents, such as arbuscular mycorrhizal fungi (AMF) and Trichoderma. The objectives of this study were to determine the effects of AMF and Trichoderma sp. on
shallot growth and disease suppression. The experiment was set as a Complete Randomized Block Design with three treatments and three replications. The treatments were AMF, Trichoderma sp., and control. Each treatment was applied to a row and 15 shallot plants were taken as samples for observation. Disease severity of purple blotch and fusarium basal rot, plant height, number of leaves and shallot resistances to Fusarium solani were observed during this study. Results demonstrated that at seven weeks after planting, the application of AMF and Trichoderma sp. tended to suppress
fusarium basal rot to 0.89% and 1.78% respectively, but only the application of AMF that suppressed purple blotch disease to 0.44%. The application of AMF and Trichoderma sp. also tended to increase plant height, number of leaves, leaf fresh weight and dry weight, root length, and bulb weight. In addition, AMF and Trichoderma sp. application
increased shallot resistances against Fusarium solani.

Full text

INTRODUCTION
Production of shallot in 2015–2018 was
fluctuative. Production of shallot in 2015 decreased
by 0.39 percent compared to production in 2014.
Production growth of shallot in 2018 compared to
2017 increased by 2.26 percent (Badan Pusat Statistik,
2018). Fungal diseases, such as purple blotch
(Alternaria porri)and fusarium basal rot, are one of
the problems in shallot production. Continuous
disease control using chemical fungicides may have
detrimental effects to the environment by
contaminating soil and water (Sudirman et al., 2011).
Therefore, it is necessary to use alternative control
methods, such as biological control using Arbuscular
mycorrhizal fungi (AMF) and Trichoderma.
Arbuscular mycorrhizal fungi can increase water
and nutrient absorption; thus, increasing plant growth
(Salisbury & Ross, 1995). The fungi can also inhibit
Fusarium infection by colonizing roots and promoting
plant growth and root volume (Al-Hmoud & Al-
Momany, 2015). In addition to their effects on soil-
borne pathogen, AMF (Glomus intraradices) has
ability to inhibit air borne disease such as early
blight disease (Alternaria solani) on tomatoes (Jung
et al., 2012). Sari (2016) also reported that shallots
treated with AMF showed lower purple blotch
severity compared to the untreated control.
Another fungus that also has beneficial effect on
plant growth and suppresses fungal disease is
Trichoderma. Interaction of Trichoderma with the
host plants can increase plant growth, yield, nutrient
availability, and resistances to plant pathogens
(Naguleswaran et al., 2014). Trichoderma is
recognized as an antagonistic fungus against
several soil-borne pathogens, such as Fusarium,
Pythium, Sclerotinia, Rhizoctonia, Gaeumannomyces
(Howell, 2007). Trichoderma has been reported to
inhibit Alternaria sp. in vitro and the development
of purple blotch disease in onion (Ghanbarzadeh
et al., 2016). Combination between Trichoderma
harzianum and Glomus mosseae also decreased
severity fusarium basal rot and purple blotch
disease in shallots (Abo-Elyousr et al., 2014). The
objective of this study was to determine the effects
of AMF and Trichoderma sp. application on shallot
growth and disease suppression in the field.
ABSTRACT
Purple blotch and fusarium basal rot are important shallot diseases which have caused significant yield loss. An
alternative control method for these diseases is the use of biocontrol agents, such as arbuscular mycorrhizal fungi
(AMF) and Trichoderma. The objectives of this study were to determine the effects of AMF and Trichoderma sp. on
shallot growth and disease suppression. The experiment was set as a Complete Randomized Block Design with three
treatments and three replications. The treatments were AMF, Trichoderma sp., and control. Each treatment was applied
to a row and 15 shallot plants were taken as samples for observation. Disease severity of purple blotch and fusarium
basal rot, plant height, number of leaves and shallot resistances to Fusarium solani were observed during this study.
Results demonstrated that at seven weeks after planting, the application of AMF and Trichoderma sp. tended to suppress
fusarium basal rot to 0.89% and 1.78% respectively, but only the application of AMF that suppressed purple blotch
disease to 0.44%. The application of AMF and Trichoderma sp. also tended to increase plant height, number of leaves,
leaf fresh weight and dry weight, root length, and bulb weight. In addition, AMF and Trichoderma sp. application
increased shallot resistances against Fusarium solani.
Keywords: biocontrol agent; Fusarium basal rot; plant disease management; purple blotch
Jurnal Perlindungan Tanaman Indonesia, Vol. 24, No. 1, 2020: 105–114
DOI: 10.22146/jpti.53517
Available online at http://jurnal.ugm.ac.id/jpti
ISSN 1410-1637 (print), ISSN 2548-4788 (online)
Research Article
Beneficial Effects of Arbuscular Mycorrhizal Fungi and Trichoderma
on Diseased Shallot
Chaieydha Noer Afiefah1), Suryanti1), Tri Joko1), & Susamto Somowiyarjo1)
1)Department of Plant Protection, Faculty of Agriculture, Universitas Gadjah Mada
Jln. Flora No.1, Bulaksumur, Sleman,Yogyakarta 55281
*Corresponding author. E-mail: suryanti.faperta@ugm.ac.id
Received January 17, 2020; revised April 20, 2020; accepted July 27, 2020
ISSN 1410-1637 (print), ISSN 2548-4788 (online)

MATERIALS AND METHODS
Field study was conducted at Gotakan Village,
Panjatan, Kulon Progo; while other work was done
at the glass house and Laboratory of Plant Pathology,
Faculty of Agriculture, Universitas Gadjah Mada
during January–November 2019. Field study used
a Complete Randomized Block Design (RCBD)
with three blocks and three treatments, which were
AMF, Trichoderma sp., and control. Each block
was in one row and 15 shallot plants were taken as
samples for observation. Crok Kuning shallot variety
was planted with spacing 10 cm in row and 20 cm
between rows. Ten grams of AMF (Glomus spp.) in
zeolite formulation were applied into each planting
hole before planting; whereas 20 g for Trichoderma
sp. in caolin formulation was applied one day before
planting. Before applying biological agents, cow
manure at a dose of 1 t/ha was applied in the soil.
Disease Severity and Plant Growth Observation
Plant height and number of leaves were observed
every week. The shallot bulbs were harvested at
seven weeks after planting. The variables observed
were: fresh and dry weight of shoot, root length, and
bulbs weight. Disease severity was observed as soon
as the symptom appeared and it was repeated weekly.
Fusarium basal rot and purple blotch were observed
using the following formula (Ismiyatuningsih et al.,
2016):
DS = Disease severity
n = number of plants or leaves infected
v = disease score
N = number of observed plants or leaves
Z = highest score used
Purple blotch disease was scored using scoring
used by Putrasemedja et al. (2012) with slight
modifications :
Score 0 = Healthy plants (no symptoms)
Score 1 = the infected tissues are 0–10% of the leaf
Score 2 = the infected tissues are 11–20% of the leaf
Score 3 = the infected tissues are 21–40% of the leaf
Score 4 = the infected tissues are 41–60% of the leaf
Score 5 = the infected tissues are 61–100% of the leaf
The score used for fusarium basal rot were
(Nugroho et al., 2015):
Score 0 = No symptoms
Score 1 = Some leaves turn yellow but not dry
Score 2 = Some leaves are dry but not withered
Score 3 = Plants are wither but not yet rotten
Score 4 = Roots are rotten
Score 5 = Plants die
The shallot crops were harvested at seven weeks
after planting. The variables observed were fresh
and dry weight of shallot shoot and and bulbs, as
well as the root length. In addition, the shallot bulbs
were further tested for their resistances to Fusarium
solani. Harvested shallot bulbs were inoculated by
spraying the pathogen conidial suspension with
concentration of 106 conidia/ml. Fusarium solani
used in this disease resistance test was a collection
of Plant Disease Laboratory, Faculty of Agriculture,
Universitas Gadjah Mada. Fusarium basal rot
disease is caused by 3 species of fusarium: Fusarium
oxysporum, Fusarium solani, and Fusarium acutatum
(Lestiyani, 2015).
Pathogen-inoculated shallot bulbs were then
incubated in a sterile container at room temperature
for 7 days. Disease incidence was determined by
counting the percentage of bulbs with necrotic
symptom:
RESULTS AND DISCUSSION
Disease Severity and Plant Growth
Disease severity of fusarium basal rot was
started to appear at the first week after shallots were
planted. Shallots treated with AMF and Trichoderma
sp. had lower disease severity of fusarium basal rot
(Figure 1).
At seven weeks after planting the severity of
fusarium basal rot in shallot treated with AMF and
Trichoderma sp. was 0.89% and 1.78%, compared
with control which 4% (Figure 1). Lower disease
severity of fusarium basal rot in shallots treated with
AMF implied interaction between AMF and the
shallot roots. Mycorrhizal fungi provide an effective
alternative method of disease control especially for
the pathogens which affect the below ground of the
plant. Zeng (2006) stated that interactions between
pathogens, AMF, and host plant are able to reduce
disease severity of soil-borne pathogens. This research
proved that lower disease severity of fusarium basal
rot at shallots treated with AMF implied interaction
between AMF and shallot roots. Previous
research showed that AMF suppress the progress of
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106
Disease Severity = ∑(n×v) × 100%
N × Z
Infection percentage = ∑ bulb with necrosis × 100%
∑ total bulb incubated

fusarium wilt in shallots with the longest disease
incubation period in 21 days and decreasing disease
incidence up to 40 % (Fitriani et al., 2019).
The mycorrhizal symbiosis involves several
mechanisms in controlling plant disease such as
creating mechanical barrier hindering the pathogen
penetration and subsequent spread; thickening of
cell wall through lignification and production of
other polysaccharides which in turn hinder the entry
of root pathogen; producing antibiotics and toxins
that inhibit the pathogen; compensating the nutrient
absorption in roots (Zeng, 2006).
The benefits of Trichoderma sp. have been
reported in controlling fusarium basal rot in onion.
The antagonistic mechanisms of Trichoderma
against fungal pathogen can be divided into three
types, which are antibiosis, parasitism, and
competition for space and nutrition (Baker & Cook,
1982). Trichoderma can produce secondary metabolites,
such as polyketides, alkyl pyrones, isonitriles,
alametichin, tricholin, peptaibols, 6-penthyl- α-pyrone,
massoilactone, viridin, gliovirin, glisoprenins, and
heptelidic acids (Raaijmakers et al., 2009). Several
Trichoderma spp. produce iron chelating siderophores
which hinder growth of other fungi (Ghosh et al.,
2017). Trichoderma can also parasites other fungi
and causes vacuolar enlargement and lysis of the
host cells. Trichoderma penetrates host cell walls
by excreting degrading enzymes, such as protease,
chitinase, and glukanase (Harjono & Widyastuti,
2001).
In this study, purple blotch disease was started
to appear at five weeks after planting. The disease
severity was very low. At seven weeks after planting,
the disease severity in the control was only 0.89%.
It may caused by the relative humidity is low. The
field is located in lowland at altitude 7 masl (Badan
Pusat Statistik Kabupaten Kulon Progo, 2019).
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Figure 1. Disease severity of fusarium basal rot in all treatments during seven weeks of observation with vertical bars
representing standard errors
Afiefah et al.: Beneficial Effects of Arbuscular Mycorrhizal Fungi and Trichoderma on Diseased Shallot 107
Figure 2. Disease severity of purple blotch in all treatments during seven weeks of observation with vertical bars
representing standard errors

Alternaria porri on onion occured following a long
period of relative humidity (>90%) or dew deposition
and temperatures ranges between 20º–25º C (Gupta
& Pathak, 1986; Evert & Lacy, 1996). High humidity
was not the only factor caused disease infection,
but it has to be supported by the presence of thin
film water on the leaf surface at least for 4 hours
since the attachment of the conidia on the leaves
(Hadisutrisno et al., 1996).
At seven weeks after planting disease severity of
purple blotch was observed on shallots treated with
Trichoderma sp. and control (0.89%), while shallots
treated with AMF showed 0.44% (Figure 2). The
interaction between AMF and host plants has been
reported to inhibit proliferation of necrotrophic
pathogens and decrease disease symptoms, such as
Alternaria solani and Botrytis cinerea on tomatoes
(Pozoet al., 2010; de la Noval et al., 2007) and
Magnaporthegrisea on rice (Campos-Soriano et al.,
2012). Interaction between AMF and host plant may
lead to systemic protection including protection of
above-ground organs as the fungi can activate local
and systemic resistance (Xavier & Boyetchko,
2004). Decrease in disease severity may also due to
lignification of plant cell wall as a result of AMF
colonization. Lignification is considered an important
mechanism for disease resistance and it may contribute
to reducing proliferation in vascular tissues in root
plant that use AMF (Kapulnik & Douds, 2000).
AMF-inoculated plants had increased disease
resistance possibly due to morphological alterations,
such as thickening of the cell wall by lignification
(Al-Raddad, 1987). Thickening of the cell wall through
lignification and production of other penetration and
growth of pathogens like Fusarium oxysporum,
Phomaterrestris and Meloidogyne incognita have
been demonstrated (Bagyaraj, 2014).
Purple blotch disease is a foliar disease. In this
study, purple blotch disease severity in shallots
treated with Trichoderma sp. were similar with control.
In this case, Trichoderma sp. was not able to induce
plant resistant to purple blotch disease. Another
study also reported that Trichoderma sp. was not
able to induce plant resistance. Bahramisharif &
Rose (2018) reported that the application of T.
harzianum and oak-bark compost in planting
medium increased disease severity of tomato late
blight. The application of T. harzianum combined
with oak-bark compost negatively affected the root
growth and resulted in significantly higher disease
severity in both whole plant and detached assays. In
contrast, application of B. subtilis subsp. subtilis
combined with oak-bark compost effectively reduced
the disease severity.
The Effects of Trichoderma and AMF on the Growth
and Yield of Shallot
Application of Trichoderma sp. resulted more
higher plant than AMF and control at five week
after planting (Figure 3). Trichoderma sp. and AMF
application tended to increase plant height and
number of leaves than control between at five and
four weeks. Number of leaves was different among
all treatments (Figure 4). Application of AMF resulted
in more number of leaves than Trichoderma sp. and
control at four weeks after planting. This was
probably due to the fungal effects on shallot roots
and the increased in nutrition absorption.
The ability of Trichoderma to increase plant
growth was reported in other studies. Doni et al.
(2014) reported that Trichoderma spp. were able to
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Figure 3. Plant height in all treatments during seven weeks of observation with vertical bars representing standard
errors
Jurnal Perlindungan Tanaman Indonesia Vol. 24 No. 1
108

enhance rice growth components including plant
height, and also leaf number, tiller number, root
length and root fresh weight. The application of
Trichoderma as shallot seed treatment increased
plant height, the leaf area index, extensive root, net
assimilation rate (NAR), plant growth rate, Nitrate
Reductase Activities (NRA), total chlorophyll, and
fresh bulb weight (Darsan et al., 2016).
Several studies have also reported that AMF
were able to increase plant height and number of
leaves (Shuab et al. 2014). Balliu et al. (2015) found
that AMF increased N, P, K, Ca absorption, leaf
area and tomato plant growth. The symbiosis of AMF
with root of their host plant allows mycorrhizae to
obtain essential nutrients in exchange of N, P, K,
Ca, Zn, & S for plant. Arbuscular mycorrhizal fungi
produce arbuscular structures which help increase
inorganic minerals, carbon compounds, and phosphor
exchanges (Li et al., 2016; Prasad et al., 2017).
Therefore, they significantly boost the phosphorus
concentration in both root and shoot systems (Al-
Hmoud & Al-Momany, 2017). Under phosphorus
limited condition, AMF root association improves
phosphorus supply (Bucher, 2007).
This research showed that the AMF application
tended to result in higher shoot fresh and dry
weight, bulb weight, and root length then those in
control (Figure 5). Widi et al., (2010) also found an
increase of tuber weight of shallot after AMF
application. In addition, AMF was also reported to
increase shallot bulb diameter, bulb weight, and
bulb fresh weight per cluster (Hidayat et al., 2018).
Mycorrhizal fungi colonization causes more
effective macro nutrient absorption which increases
photosynthetic products and hence results in biomass
accumulation (Begum et al., 2019).
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Figure 4. Number of leaves in all treatments during seven weeks of observation with vertical bars representing
standard errors
Figure 5. Root length, shoot fresh and dry weight, bulb weight in all treatments after seven weeks of observation with
vertical bars representing standard errors
Afiefah et al.: Beneficial Effects of Arbuscular Mycorrhizal Fungi and Trichoderma on Diseased Shallot 109

AMF colonization is widely believed to stimulate
nutrient uptake in plants. It is evident that inoculation
of AMF can enhance the concentration of various
micro-nutrients and micro-nutrients significantly,
which leads to increase photosynthate production
and hence increase biomass accumulation (Chen et
al., 2017; Mitra et al., 2019). Evelin et al. (2012)
stated that AMF improve the uptake of almost all
essential nutrients and contrarily decrease the uptake
of Na and Cl, leading to growth stimulation.
Arbuscular mycorrhizal fungi facilitate uptake of
soil nutrients, especially of N & P, which can
effectively promote the growth of host plant (Smith
et al., 2011).
The application of Trichoderma sp. also tended
to increase the shoot fresh and dry weight and the
root length (Figure 5). The direct beneficial effects
of Trichoderma sp. on plants are promoting and
improving plant root growth and structure, improving
seed vigor and growth, and decomposing, recycling,
and utilizing soil nutrients (Harman, 2011; Howell
et al., 2000; Shoresh et al., 2010). According to Levy
et al. (2004) Trichoderma directly affects plant growth
by producing plant growth-regulating hormones.
Trichoderma can also break down organic matter in
soils, so it is easily being absorbed by the plants.
Inoculation of Trichoderma asperellum produced
better leaf greenness, stomata opening width, number
of roots, plant height, number of plant leaves, fresh
bulb weight per plant (Setyaningrum et al., 2019).
Sutarman et al. (2018) also found that Trichoderma
formulated in spent substrate of oyster mushroom
increased the height and the number of leaves on
shallot.
Effects of Arbuscular Mycorrhiza Fungi and
Trichoderma Application on Disease Resistances
of Shallot Bulb
The result showed that AMF and Trichoderma
sp. treatments showed lower infection of F. solani
than control. The lowest disease infection was
observed in AMF treatment (Figure 6). Fusarium
solani infection caused necrotic symptoms on shallot
basal plate resulting in death and brown color of
plant tissue. Shallots treated with AMF and
Trichoderma sp. resulted in lower infection compared
to the control. This will be beneficial for shallot
bulb used for planting material which may carry
seed-borne pathogen, such as F.solani. This result
was consistent with Niemira et al. (1996) that
reported a suppression of postharvest damages
caused by Fusarium sambucinum on potato minitubers,
in AMF inoculated plants.
Sari (2016) stated that one of mechanisms of
AMF in suppressing the disease development is by
inducing natural plant protection mechanisms, such
as the accumulation of salicylic acid in leaves, cell
wall lignification, narrower stomata openings, and
increase of nutrient absorption. Salicylic acid is a
compound which signals plant protective mechanism
(Pozo & Azcon-Aguilar, 2007). AMF can also
indirectly induce lignification that acts as barrier on
cell walls which inhibits pathogen penetration (Sari,
2016). Lignin is believed to disrupt hydraulic
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Figure 6. Percentage of infected shallot bulb in all treatments with vertical bars representing standard errors
Jurnal Perlindungan Tanaman Indonesia Vol. 24 No. 1
110

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enzymatic processes, pathogen penetration mechanism,
also water and molecule exchange between plants
and pathogen (Nicholson & Hammerschmidt, 1992).
Lignin are able to iimprove disease resistance and
enhance the mechanical strength by cell wall
thickening (Yang et al., 2018). Mycorrhiza can also
stimulate plant resistance-related enzymes, such as
polyphenol oxidase and peroxidase (Al-Askar &
Rashad, 2010).
CONCLUSION
The application of AMF and Trichoderma sp.
tended suppress the development of fusarium basal
rot and increase shallot bulb weight. Only the
application of AMF tended suppress the development
of purple blotch diseases. The application of AMF
and Trichoderma sp. also tended to result in better
plant growth and the yield. The antagonist also
increased root length, fresh weight, and bulb weight.
In addition, the application of AMF and Trichoderma
sp. was able to increase shallot bulb resistances
against infection of F. solani.
ACKNOWLEDGEMENT
This study was funded by the Excellent Research
2019 budget (contract number 1683/PN/PT/2019),
Faculty of Agriculture, Universitas Gadjah Mada.
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