Open Access
P. Suneeta , K. Eraivan Arutkani Aiyanathan and S. Nakkeeran
Department of Plant Pathology, Centre for Plant Protection Studies, Tamil Nadu Agricultural University, Coimbatore – 641 003, India.
J Pure Appl Microbiol. 2017;11(2):1161-1168
https://doi.org/10.22207/JPAM.11.2.63 | © The Author(s). 2017
Received: 12/02/2017 | Accepted: 10/04/2017 | Published: 30/06/2017
Abstract

An extensive study was undertaken to manage the most vigorous, polyphagous pathogen Sclerotium rolfsii causing collar rot disease in Gerbera by utilizing nine commercial fungicides and eight novel Trichoderma spp. Under in vitro conditions, there was 61.11 per cent reduction of pathogen (S. rolfsii) by T. harzianum NVTH2 and T. viride TV1 over control and was followed by T. citrinoviride NVTC1, T. citrinoviride NVTC2 and T. asperellum NVTA1 with per cent inhibition of 55.55, 54.44 and 53.33 respectively. On the other hand, commercial fungicides, tebuconazole 50%+ trifloxystrobin 25%, tebuconazole 250 EC, propioconazole 25% EC, fenamidone 10%+ mancozeb 50%WG and propineb 70WP reduced the growth of S. rolfsii to an extent of 100 per cent inhibition in all the tested concentrations. Combination of most effective Trichoderma spp. and fungicides had resulted in the best treatment T2 against the collar rot pathogen of Gerbera under protected cultivation.

Keywords

Fungicides, Gerbera, Trichoderma spp., collar rot.

Introduction

Floriculture is recognized as a highly competitive and a profitable sector. Indian flower export markets are estimated as 11 billion US dollars at present and expected to grow up to 20 billion US dollars by 2020 (Gian Aggarwal, 2011). India has a vast potential to grow good quality Gerbera. Area under Gerbera cultivation in Tamil Nadu is around 25 ha with production of 53 lakh cut flowers at an estimated value of Rs. 15 lakhs (INDIASTAT, 2013).

There is a continuous exploitation of the soils in polyhouses which makes Gerbera highly susceptible to soil borne diseases. Jamwal and Jamwal (2012) observed foot rot, wilt, root rot complex, blight and grey mold in Gerbera. In India, collar rot disease in Gerbera jamesonii Bolus ex Hook was recorded for the first time caused by Sclerotium rolfsii (Suneeta et al., 2016).

Biological control of soil borne pathogens by using antagonistic fungi, Trichodema spp. has been under investigations from several years. At the same time, chemical agents also carry the huge capacity to control the soil borne diseases with their quick mode of action. Integration of different treatments including seedling dip with carbendazim+mancozeb, addition of vermicompost, drenching with fungicide and application of Trichoderma harzianum (7%) were found to be effective in management of dry root rot (Sclerotium rolfsii) of chilli in comparison with individual treatments (Madhavi and Bhattiprolu, 2011). Seetharamulu et al. (2012) evaluated the efficacy of Trichoderma viride against Fusarium solani in in-vitro system while in in-vivo system it was effective against the disease in combination with fungicide Mancozeb. Comparison of bio-efficacy and combination of Trichoderma spp. and fungicidal molecules against collar rot pathogen (Sclerotium rolfsii) of Gerbera results in the better control of the pathogen.

Materials and Methods

Isolation of the collar rot pathogen
The isolation technique of Sclerotium rolfsii was adapted from Rangaswami and Mahadevan (1999). The infected crown bits were surface sterilised by using 0.1% mercuric chloride (HgCl2) for 30 seconds and placed on to the PDA medium amended with 100 ìg/ml of streptomycin sulphate which were incubated at temperature (20 ± 2°C) for 5 days.

Identification of the pathogen
The pathogen was identified according to the morphological characteristics based on size, shape and colour of sclerotia and mycelium growth.

Pathogenicity test
The mycelium and sclerotia of the pathogen Sclerotium rolfsii were inoculated in the collar portion of 30 days old Gerbera (var. Donavan yellow and Bellwater white) plants and maintained in the polyhouse at 22 ± 2°C. After 7 days of inoculation typical symptoms of browning and rotting were observed and the pathogen was re-isolated. Similar methodology was followed to prove pathogenicity in tomato plants by Xie et al. (2014).

Collection of fungal antagonists (Trichoderma spp.)
Eight isolates of Trichoderma spp. were collected from the Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, India (Table 1).
Table (1):
List of Trichoderma spp. used in the study.

S.No.
Name of isolate
Name of antagonist
Accession number of the isolate in NCBI
1.
NVTA1
T. asperellum
KJ803854
2.
NVTA2
T. asperellum
KJ803855
3.
NVTH1
T. harzianum
KJ803856
4.
NVTH2
T. harzianum
KJ803857
5.
NVTE1
T. erinaceum
KJ813823
6.
NVTC1
T. citrinoviride
KJ813824
7.
NVTC2
T. citrinoviride
KJ813825
8.
TV1
T. viride
Commercial strain (not submitted)

In vitro screening by Trichoderma spp
The antagonistic activity of Trichoderma spp. against the test pathogen was evaluated by dual culture technique (Dennis and Webster, 1971). The radial growth of mycelium of antagonist in mm and pathogen were measured and Percent Inhibition (PI) was calculated: PI= C-T/C X 100

Where, C is the growth of test pathogen (mm) in the absence of the antagonist; T is the growth of test pathogen (mm) in the presence of the antagonist.

In vitro evaluation of fungicides
The efficacy of 9 commercial fungicides namely difenoconazole 25% EC (Score), tebuconazole 50% + trifloxystrobin 25% WG (Nativo), fenamidone 10% + mancozeb 50% WG (Sectin), propineb 70 WP (Antracol), fosetyl aluminium 50% WP (Alliete), propioconazole 25% EC (Tilt), tebuconazole 250 EC (Folicur), kresoxim-methyl 44.3% SC (Ergon) and carbendazim 50% WP (Benfil) at 25ppm, 50ppm, 100ppm, 250ppm, 500ppm, 1000ppm and 1500ppm concentrations were tested against the root pathogens by Poisoned food technique (Grover and Moore, 1962) using Potato dextrose agar medium. The treatments were replicated thrice and were incubated at room temperature (28±2oC) and the diameter of colonies were recorded on 7th day and expressed in centimeter (cm). The per cent inhibition (PI) of growth was calculated by using the formula:

PI = C-T/C x 100, Where I = Inhibition percentage, C = Rate of growth of pathogen in control and T = Rate of growth of pathogen in treatment.

Development of liquid formulation of Trichoderma spp.
The fungal antagonists (TV1, NVTH1 and NVTH2) were cultured on 1000ml of Potato Dextrose broth and incubated in an orbital shaker at 150 rpm at room temperature (28±2°C) for 48hr. Later the liquid biomass along with fungal mycelia were mixed with 1% glycerol (10ml), tween 20 (10ml) and poly vinyl pyrrolidone – 40000 ml. wt (10g) each separately (Somasegaran and Hoben, 1985). The resultant mixture was kept in orbital shaker at 200 rpm for 5 minutes to ensure uniform blending and was standardized to obtain one ml of formulation consists of 106cfu/ml. The liquid formulation was stored at 5°C for further study.

Integration of Trichoderma spp. and fungicides for the management of collar rot under protected cultivation
Field experiment was conducted during 2013-2014 in Gerbera (var. Donavan yellow) fields located at Spic Agro Biotech centre, Ooty, to assess the efficacy of liquid formulation of Trichoderma spp. (106 cfu/ ml) @ 5ml/litre individually and in combination with commercial fungicides @ 0.5 to 1ml/lit (moderate dosages) against collar rot under protected condition (polyhouse). Thirty days old plants of Gerbera were used and the experiment was laid out with 7 treatments and 3 replications in RBD. The bed size of each replication was 5m2 with 30 × 30 cm spacing (Table-2).
Table (2):
Treatment schedule of Trichoderma spp. and fungicides.

S. No.
Treatment
Treatment details
1.
T1
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @ 5ml/lit+ SD-tebuconazole 250 EC @500ppm
2.
T2
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+SD-tebuconazole 50%+trifloxistrobin 25% WG @500ppm
3.
T3
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+SD-propioconazole 25% @500ppm
4.
T4
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+ SD-propineb 70 WP @500ppm
5.
T5
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+ SD-fenamidone 10%+mancozeb 50% WG @500ppm
6.
T6
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+ SD-difenoconazole 25%EC @500ppm
7.
T7
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit
8.
T8
Control

RD-Root dipping at the time of planting; **SD- Soil drenching at 15 days interval.
Statistical analysis
All the experiments were statistically analyzed independently. The treatment means were compared by Duncan’s Multiple Range-Test (DMRT) (Gomez and Gomez, 1984). The package used for analysis was IRRISTAT version 92-1 developed by the International Rice Research Institute, Biometrics unit, The Philippines.

RESULTS AND DISCUSSION

Symptomatology of collar rot
Initially, the infected plants exhibited brown necrotic lesions on the petioles near collar region. Subsequently, the affected leaves droop and resulted in death of the infected plants. Examination showed the presence of white cottony mycelium and plenty of round, brown sclerotial bodies on the affected collar portion. Similar symptomatology was described by Arunasri et al. (2011) in collar rot of crossandra.

Morphological characterization of the pathogen
Pathogen was isolated from Gerbera variety Donavan (yellow). The mycelium of the fungal culture on PDA medium was white and fluffy. Small white tufts were formed on mycelium which later turned to dark brown, round, sclerotia and measured 1-2 mm in diameter. Based on phenotypic characters, the pathogen was confirmed as Sclerotium rolfsii. Similar morphology was described by Sennoi et al. (2010) in the stem rot of Jerusalem artichoke (Sclerotium rolfsii).

Pathogenicity of S. rolfsii
Inoculation of S. rolfsii into the collar region of 30 days old healthy Gerbera plants (var. Bellwater white) expressed the typical symptoms within 5 days after inoculation. Typical rot in the collar portion with numerous brown, mustard seed like sclerotia, followed by blightening and girdling of the affected plants was seen.

In vitro screening of Trichoderma spp. against S. rolfsii
The efficacy of in vitro antagonism of different isolates of Trichoderma spp. against S. rolfsii by dual culture technique revealed that the growth of S. rolfsii was suppressed to an extent of 61.11 per cent by T. harzianum NVTH2 and T. viride TV1 over control and was followed by T. citrinoviride NVTC1, T. citrinoviride NVTC2 and T. asperellum NVTA1 with per cent inhibition of 55.55, 54.44 and 53.33 respectively (Table-3).
Table (3):
Antifungal activity of Trichoderma spp. against S. rolfsii under in vitro.

S. No.
Isolates
Mycelial growth (mm)*
Per cent Inhibition over control
1
T. erinaceum-NVTE1
43.00de
52.22de (46.27)
2
T. citriniviridae-NVTC1
40.00b
55.55b (48.18)
3
T. citrinoviridae-NVTC2
41.00bc
54.44bc (47.54)
4
T. asperellum-NVTA1
42.00cd
53.33cd (46.90)
5
T. asperellum-NVTA2
45.00f
49.99f (44.99)
6
T. harzianum-NVTH1
44.00ef
51.11ef (45.63)
7
T. harzianum-NVTH2
35.00a
61.11a (51.42)
8
T. viride (TV1)
35.00a
61.11a (51.42)
9
Control
90.00g

*Values are mean of three replications.
In a column, means followed by a common letter are not significantly different at the 5% level by DMRT
Values in parentheses are arc sine transformed values

Manu et al. (2012) observed the maximum inhibition of mycelial growth of 61.88% in T. harzianum, which was followed by T. viride (Tv-27 isolate) (57.77%) and T. harzianum (Th-55 isolate) (56.33%) against S. rolfsii causing foot rot of fingermillet. Patro and Madhuri (2013) evaluated the antagonistic effect of biocontrol agents viz., T. harzianum – 1, T. harzianum – 2, T. viride, Pseudomonas fluorescens and Bacillus subtilis against S. rolfsii causing foot rot of finger millet and observed maximum inhibition of mycelial growth (61.88%) in T. harzianum – 2, which was followed by T. viride (57.77%).

In vitro screening of fungicides against S. rolfsii
Among the nine fungicides, tebuconazole 50% + trifloxystrobin 25%, tebuconazole 250 EC, propioconazole 25% EC, fenamidone 10%+mancozeb 50%WG and propineb70WP recorded 100 per cent inhibition of pathogen growth in all the concentrations tested. Difenoconazole 25% EC recorded 100 per cent inhibition of pathogen at 500, 1000 and 1500ppm concentrations. Other fungicides like carbendazim 50% WP, fosetyl aluminium 80% WP and kresoxim-methyl 44.3% SC were not so effective in inhibiting the mycelial growth of S. rolfsii (Table-4).
Table (4):
In vitro antagonism of fungicides against S. rolfsii.

S. No. Fungicides Percent inhibition over control
25ppm 50ppm 100ppm 250ppm 500ppm 1000ppm 1500ppm
1 Tebuconazole 250 EC 86.67
(68.32)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
2 Propioconazole 25% EC 100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
3 Difenoconazole 25% EC 70.00
(57.18)
74.44
(59.51)
78.89
(62.43)
86.67
(68.60)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
4 Fenamidone 10%+Mancozeb 50% WG 100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
5 Propineb70 WP 80.00
(63.91)
83.33
(65.91)
88.89
(69.74)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
6 Fosetylaluminium
50% WP
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
7 Kresoxim-Methyl
44.3% SC
4.44
(12.01)
7.78
(15.70)
16.67
(24.27)
20.00
(27.03)
23.33
(28.87)
40.00
(39.42)
42.22
(40.45)
8 Tebuconazole 50% +Trifloxystrobin 25%WG 100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
100.0
(89.53)
9 Carbendazim 50% WP 0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
8.89
(16.75)
13.33
(21.55)
10 Control 0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)
0.00
(0.46)

*Values are mean of three replications. **SD-soil drenching at 15 days interval. In a column, means followed by a common letter are not significantly different at the 5% level by DMRT Values in parentheses are arc-sine transformed values

Arunasri et al. (2011) reported that the combi products containing triazoles viz., avatar, merger and nativo were highly inhibitive to the growth of Sclerotium rolfsii in crossandra. Sangeetha and Jahagirdar (2013) reported that mancozeb, carbendazim, thiophanate methyl, hexaconazole, propioconazole completely inhibited the growth of S. rolfsii, R. bataticola and Fusarium sp. causing root rot and wilt complex in soybean.

Effect of Trichoderma spp. and fungicides on management of collar rot and plant growth promotion of Gerbera
Field experiment resulted in T2 as best treatment module in reducing collar rot incidence, growth and yield parameters of Gerbera which was a combination of most effective Trichoderma spp. strains @ 5ml/lit and commercialized combi fungicide, Nativo @ 0.5ml/lit applied at 10ml/plant in the polyhouse. This was followed by treatment T1 which was significantly effective against collar rot disease and improved the plant growth parameters of Gerbera either over the control (Table 5 & 6).
Table (5):
Effect of Trichoderma spp. and fungicides on collar rot incidence, growth characters and flower yield under protected cultivation.

S. No.
Treatment module
Collar rot incidence*
Root length (cm)*
Plant height (cm)*
No. of flowers/m2*
T1
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-tebuconazole250 EC@500ppm
4.30a (56.52)
20.23a
41.46b
50.10b
T2
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-tebuconazole50%+trifloxistrobin25%WG@500ppm
4.00a (59.55)
20.40a
42.11a
51.80a
T3
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-propioconazole25%@500ppm
5.53b (45.99)
19.22b
39.20c
48.60c
T4
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-propineb70WP@500ppm
6.11c (38.22)
18.12c
37.23e
46.10e
T5
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-fenamidone10%+mancozeb50%WG@500ppm
5.69b (42.46)
18.70c
38.27d
47.30d
T6
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-difenoconazole25%EC@500ppm
7.91d (20.02)
17.82d
36.71f
45.20f
T7
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit
8.23e (16.78)
17.22d
36.36f
44.10g
T8
Control
9.89f
16.83e
34.69g
39.30h

*Values are mean of three replications. **SD-soil drenching at 15 days interval Means followed by a common letter are not significantly different at 5% level by DMRT
Data in the parenthesis are per cent reduction over control

Table (6):
Effect of Trichoderma spp. and fungicides on flower characters of Gerbera under protected cultivation.

S. No.
Treatments
Days taken for flower bud initiation*
Days taken for flower bud opening*
Length of flower stalk (cm)*
Flower diameter (cm)*
T1
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+SD-tebuconazole 250 EC @500ppm
83.40b
106.00bc
36.20bc
8.80b
T2
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+SD-tebuconazole 50%+trifloxistrobin 25% WG @500ppm
81.10a
104.33a
36.40ab
9.00a
T3
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-propioconazole 25% EC @500ppm
84.00bc
107.66cd
35.60ef
8.60c
T4
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-propineb 70 WP@500ppm
85.66cd
110.00f
34.80gh
8.00e
T5
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-fenamidone 10%+mancozeb 50% WG@500ppm
86.20de
108.00de
35.90de
8.40d
T6
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit+
SD-difenoconazole 25% EC @500ppm
88.30f
112.00g
34.60hi
7.90fg
T7
RD-NVTH2+ TV1 @5ml/lit
**SD- NVTH2+ TV1 @5ml/lit
90.10g
115.33h
34.40ij
7.80gh
T8
Control
92.33h
119.00i
32.20k
7.10i

*Values are mean of three replications
Means followed by a common letter are not significantly different at 5% level by DMRT
Triazole compounds are generally used as fungicides for the management of both soil borne and foliar diseases of crop plants, which also have plant growth regulating properties (Fletcher et al., 1986). In the triazole fungicide (difenoconazole), thirteen novel triazole analogs containing 1, 3-dioxolane rings have been synthesized and they express plant-growth regulatory activity similar to those of a difenoconazole (Xu et al., 2004).

There are several reports demonstrating control of a wide range of plant pathogens including Sclerotium rolfsii by Trichoderma spp. by elicitation of induced systemic or localized resistance which occur due to the interaction of bioactive molecules such as proteins avr-like proteins and cell wall fragments released by the action of extracellular enzymes during mycoparasitic reaction (Thangavelu & Mustaffa, 2010). The possible mechanisms involved in the reduction of collar rot severity of Gerbera due to Trichoderma spp. treatment might be the mycoparasitism, spatial and nutrient competition, antibiosis by enzymes and secondary metabolites, and induction of plant defense system.

Integration of different treatments like carbendazim + metalaxyl, captan + metalaxyl+ G. virens 3 and captan + metalaxyl + T. viride 2 was confirmed as higher disease reduction of wilt complex caused by four wilt pathogens viz, Fusarium oxysporum, Phytopthora capsici, Rhizoctonia solani and Sclerotium rolfsii to 59.8, 58.6 and 58.0 % over control and maximum yield of 138.6, 137.0 and 135.6 q/ha was observed respectively in Bell pepper (Rather et al., 2012).

Hence, the combination of the efficient Trichoderma spp. and fungicidal molecules resulted in the collar rot disease reduction significantly and subsequently increased the plant growth parameters in Gerbera jamesonii.

CONCLUSION

S. rolfsii is a polyphagous, highly vigourous and destructive soil borne pathogen and is a difficult task to control this pathogen once established. This study was undertaken to obtain the efficient strains of Trichoderma spp. and the effective fungicides in order to get a novel integrated management module against the most destructive collar rot pathogen of Gerbera under polyhouse. This occurrence of collar rot in Gerbera jamesonii is a first report in Tamil Nadu, India. This might be due to the unknowing transmission of propagules through implements and tools used in the soils of polyhouse. 

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