Identification and Evaluation of Antifungal Compounds from Botanicals for the Control of Sugarcane Red Rot Pathogen, Colletotrichum falcatum

Identification and Evaluation of Antifungal Compounds from Botanicals

for the Control of Sugarcane Red Rot Pathogen, Colletotrichum falcatum

Keywords: Sugarcane Red Rot, Colletotrichum falcatum, Psoralea corylifolia, Antifungal Activity.

ABSTRACT: Red rot is a devastating disease in sugarcane caused by fungus, Colletotrichum falcatum. In this study, eighteen different botanicals were screened for identifying effective antifungal compound against C. falcatum. Among the plants screened, 15 per cent aqueous leaf extract of Psoralea corylifolia alone inhibited 100 per cent growth of both mycelium as well as spore germination under in vitro conditions. The extract did not exhibit any inhibitory effect to the beneficial microbes viz., Pseudomonas fluorescens, Bacillus megaterium and Gluconacetobacter diazotrophicus which are normally used in sugarcane. The effective plant extracts exhibiting 100 per cent antifungal activity was subjected to TLC, HPLC and GC-MS analysis to identify the bioactive antifungal compound. It revealed the presence of 7H-furo [3,2-G] (1) benzopyran-7-one as main bioactive compound which is thought to be the intermediate of antifungal compound, 8 – methoxypsoralen formed during biosynthesis.

164-172 | JRA | 2013 | Vol 2 | No 1

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Journal of Research in

Agriculture An International Scientific

Research Journal

Authors:

Rajkumar D* and

Murugesan R.

Institution:

Department of Agricultural

Microbiology, Tamil Nadu

Agricultural University,

Coimbatore, – 641 003,

Tamilnadu, India.

Corresponding author:

Rajkumar D.

Email:

Web Address:

http://www.jagri.info/

documents/AG0044.pdf.

Dates: Received: 11 May 2013 Accepted: 28 May 2013 Published: 13 June 2013

Article Citation: Rajkumar D and Murugesan R. Identification and Evaluation of Antifungal Compounds from Botanicals for the Control of Sugarcane Red Rot Pathogen, Colletotrichum falcatum. Journal of Research in Agriculture (2013) 2(1): 164-172

Original Research

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INTRODUCTION

Sugarcane is one of the most important cash

crops grown in India which contributes to the tune of

7.5 per cent of agricultural production of the country

(Viswanathan, 2010). But, sugarcane red rot disease

caused by fungus Colletotrichum falcatum is considered

as very serious disease and it was responsible for the

elimination of many elite sugarcane varieties such as Co

312, Co 658, Co 997, Co 1148, CoC 671 etc. Upto 100

per cent yield loss has been reported in severe

epiphytotics (Siddique et al., 1983). The use of chemical

fungicide bavistin is the common practice followed by

the sugarcane growers for the control of sugarcane red

rot. Practicing sett treatment with systemic fungicides

alone is not sufficient to protect such a long duration

crop. The use of synthetic fungicide leads to several

problems such as residue in food and feed, pathogen

resistance, toxicity to non target organism and

environmental pollution (Angelo et al. 2012). In addition

to these, elimination of soil born inoculum through

chemicals is difficult and costly. Development of

resistant varieties through breeding methods is a long

term endeavour. Therefore, with the increasing public

awareness of environmental safety and persistent

demand for ecofriendly products, we are forced to

produce quality products both for export and domestic

consumption. Hence, an alternative approach is the use

of botanicals in management of this disease which are

eco friendly in addressing the problem.

MATERIALS AND METHODS

Plants screened for antifungal study

Eighteen plants belonging to 14 families were

taken for screening antifungal activity against

Colletotrichum falcatum. All the plants were collected

from Medicinal Plant Section maintained at Botanical

Garden and agricultural fields of Tamil Nadu

Agricultural University, Coimbatore (Table 1). All the

experiments were done with three replications and the

data given are the mean of three replications. Since this

study is a preliminary qualitative screening study under

in vitro conditions quantitative data were not given and

so statistics was also not applied for the data.

Microbial cultures taken for study

Sugarcane red rot fungi, Colletotrichum falcatum

was obtained from Department of Plant Pathology,

Sugarcane Breeding Institute, ICAR, Coimbatore.

Th r ee ben e f i c i a l m i c r oor gan i s m s v i z . ,

Pseudomonas fluorescens, Bacillus megaterium and

Gluconacetobacter diazotrophicus commonly applied for

sugarcane crop were obtained from Department of

Agricultural Microbiology, Tamil Nadu Agricultural

University, Coimbatore.

Preparation of plant extracts

Fresh plant parts of all botanicals were

thoroughly washed with running tap water followed by

rinsing twice with distilled water. The plant materials

were shade dried for 1 h. Weighed plant materials were

homogenized in mixer grinder with distilled water

(1:1 w/v). The slurry of plant extracts obtained was passed

through glass wool and the filtrate was then centrifuged at 5000

rpm for 10 min. Supernatant of botanicals thus obtained

were the standard aqueous plant extract solution (100

per cent). For methanol extract, weighed plant materials

were homogenized in mixer grinder with methanol

(1:3 w/v). The slurry samples collected in a beaker were

covered with aluminium foil and incubated in

refrigerator at 4°C for 24 h. After incubation period,

slurry was filtered using glass wool and subsequently

with Whatman No. 1 filter paper. The clear filtrate was

allowed to evaporate in petriplates and the residues were

dissolved in distilled water to obtain standard methanol

plant extract solution of all botanicals (Biri Singh, 2004).

In vitro testing of plant extracts against test pathogens

The antifungal effects of all the plant extracts

were screened by poison food technique (Horsefall,

1956). An appropriate amount of plant extracts were

added to sterilized potato dextrose agar (PDA) medium

165 Journal of Research in Agriculture (2013) 2(1): 164-172

Rajkumar and Murugesan , 2013

to obtain the desired concentration of 25 per cent. Then

the medium containing plant extracts were kept in water

bath at 45°C for 60 min to eliminate bacterial contamination

(Martinez et al., 1990) and plated after cooling it to luke

warm temperature. C. falcatum mycelial disc of 9 mm

diameter was taken from 3-5 days old culture plate and

placed to the centre of each plates and incubated at

28°C. After 5 days of incubation the diameter of

mycelial colony was measured and the per cent

inhibition for all botanicals was calculated by using the

formula (Vincent, 1927).

Where, C and T were mycelial growth (cm) of test

fungi in control and treatments, respectively. All treatments

were done in triplicates and average values were taken for

interpretation.

Minimum inhibitory concentration (MIC)

Minimum inhibitory concentration is the lowest

concentration at which 100 per cent inhibition of

mycelial growth is obtained. Among the different

botanicals screened, P. corylifolia aqueous leaf extract,

which exhibited effective inhibition over C. falcatum,

was tested at different concentrations (5, 10, 15 and

20 per cent) to find out MIC by poison food technique.

Evaluation of the effect of Psoralea corylifolia extract

on the spore germination of Colletotrichum falcatum

P. corylifolia extract of different concentrations

(5, 10, 15 and 20 per cent) were prepared in tubes for

checking its effect on spore germination of C. falcatum.

A loopful of conidia from sporulated culture in oatmeal

enriched PDA medium were transferred into extract

containing tubes. From each extract concentration, 100

μl was taken into the cavity slides along with the control

(without extract). These slides were kept in a moist

chamber for the period of 24 h for germination of spores

and the effect of P. corylifolia extract on spore

germination was determined by counting germinated

spores under microscope and it was compared with the

control (Jayakumar, 2007).

Evaluation of the effect of P. corylifolia extract on

growth pattern of beneficial organisms

In vitro testing of the P. corylifolia plant extract

was carried out on beneficial microflora to assess its

influence on their growth. Twenty four hour old cultures

of Pseudomonas fluorescens, and Bacillus megaterium

were streaked on the nutrient agar medium

con t a in in g sp eci f i c p l an t ex t r act a n d

Journal of Research in Agriculture (2013) 2(1): 164-172 166


Table 1. List of medicinal plants screened for its antifungal activity

S.No Family Botanical name Parts used

1. Amaranthaceae Achyranthes aspera Leaf

2. Malvaceae Abelmoschus esculentus Leaf

3. Papilionaceae Abrus precatorius Leaf

4. Annonaceae Annona squamosa Leaf

5. Nyctaginaceae Bougainvillea spectabilis Leaf

6. Asclepiadaceae Calotropis gigantea Leaf

7. Verbenaceae Clerodendrum inerme Leaf

8. Caesalpiniaceae Caesalpinia bonduc Bark

9. Sapindaceae Cardiospermum halicacabum Leaf

10. Asteraceae Eclipta alba Leaf

11. Verbenaceae Lantana camara Leaf

12. Moringaceae Moringa oleifera Leaf

13. Meliaceae Melia azadirachta Leaf

14. Fabaceae Prosopis juliflora Leaf, Stem

15. Papilionaceae Psoralea corylifolia Leaf, Stem

16. Apiaceae Trachyspermum ammi Leaf, Stem

17. Verbenaceae Vitex negundo Leaf

18. Asteraceae Wedelia urticaefolia Leaf

Inhibition (%) = (C – T)

X 100 C

Gluconacetobacter diazotrophicus was streaked on the

potato dextrose agar medium containing plant extract and

suitable control (without plant extracts) was also maintained.

The plates inoculated with Pseudomonas fluorescens, and

Bacillus megaterium were incubated for two days whereas

Gluconacetobacter diazotrophicus plates were incubated

for five days. The growth of the organism was observed

visually, compared with that of the control and given the

remark as – for no growth, + for very less growth, ++ for

moderate growth and +++ for growth equivalent to control.

Control indicates petri plates containing PDA medium

without plant extracts. It was taken to check whether there is

any difference in the growth pattern of beneficial microbes

inoculated in PDA medium with plant extracts and without

plant extracts.

Identification of the fungitoxic principles through

TLC, HPLC and GC-MS analysis

Thin layer chromatographic study was carried

out to identify the nature of active principle in the

effective plant extracts. The solvent systems used were

ethyl acetate: methanol: ammonia solution (17:5:1),

chloroform: acetic acid (9:1) and ethyl acetate: formic

acid: acetic acid: water (100:11:11:27) for alkaloids,

phenols and flavonoids, respectively. Dragendroff’s

r e a g en t , F o l i n - C i o c a l t e u r ea g en t a n d

Diphenylboryloxyethylamine (1 per cent) with 5 per cent

polyethylene glycol 4000 were used as spray reagents.

The dried TLC plate was exposed to UV light (254 nm)

and observed for fluorescent spots. The compounds

separated in TLC were checked for its antifungal activity

against C. falcatum by poison food technique. The active

compounds which exerted antifungal activity were

subjected to HPLC analysis.

HPLC analysis

HPLC – shimadzu model L 6200 (Varian) diode

array detector in combination with Beckman ultrasphere

supelco ODS column (250 x 4.6 mm) was used for

analysis. The analysis was performed at a flow rate of

0.35ml min-1 using Methanol: Water (40:60) as mobile

phase. The UV detector was set at 260nm wavelength for

psoralen (Murali et al. 2002). Psoralen standard solutions

(0.5, 1.0, 1.5 and 2.0 percent) were prepared and 20 µl of

the solution was injected to record the retention time.

The individual peaks separated in HPLC was collected

through fraction collector and evaluated for its antifungal

activity by poison food technique. The peak which

exerted antifungal activity was again subjected to

GC-MS analysis.

GC-MS analysis

GC-MS JEOL GC mate – Hitachi model L 6200

(Varian) photo array detector in combination with

Beckman Ultrasphere supelco ODS column (250 x 4.6

mm) was used for analysis. The analysis was performed

at a flow rate of 0.35ml min-1. The UV detector was set

at 260nm wavelength for Psoralen. The peaks obtained in

chromatogram were analysed for its mass spectrum to

identify the compounds by comparing its molecular

weight with the compounds present in MS library.

RESULTS AND DISCUSSION

Antifungal activity of different botanicals

Among 18 plants tested for the antifungal

activity against C. falcatum, 15 per cent aqueous leaf

extract of P. corylifolia inhibited 100 per cent growth of

both mycelium as well as spore germination under

laboratory conditions (Plate 1and 2). None of the plant

extracts other than P. corylifolia were able to exhibit

comparatively appreciable inhibition over C. falcatum.

The presence of antifungal compounds in medicinal

plants has long been recognized as an important factor to

disease resistance (Mahadevan, 1982; Kurucheve et al., 1997).

Such compounds, being biodegradable and selective in

their toxicity are considered valuable for controlling

different plant diseases (Singh and Dwivedi, 1987).

Rajendra Prasad et al., (2004) reported the antifungal

activity of extracts obtained from P. corylifolia seeds

against dermatophytic fungi such as Trichophyton

rubrum, Trichophyton mentagrophytes, Epidermophyton



floccosum and Microsporum gypseum. Mazzuca et al.

(2003) also observed antifungal activity of its seed

extracts against some fungi causing infection in humans.

Sindhan et al., (1999) reported that 10 per cent leaf

extracts (aqueous) of Allium cepa, Zingiber officinale,

Azadirachta indica, Allium sativum, Mentha arvensis,

Eucalyptus globulens, Ocimum sanctum and Datura alba

were effective in inhibiting the mycelial growth of R.

solani to the extent of 40 – 60 per cent. The inhibitory

effect of the extract of Prosopis juliflora leaves was

studied against Gloeosporium piperatum (Gomathi and

Kannabiran, 2000) and against R. solani (Girija Shankar

and Thayumanavan, 2000). It is already known from the studies of

Khursheed et al. (1986) and Aqeel Ahmad et al., (1997) that

juliflorine, an alkaloid obtained from Prosopis juliflora

leaves, is the actual compound which is responsible for

antifungal activity. Available reports on P. corylifolia

suggest that the antifungal activity has been tested only

in seeds, not with other plant parts. But the present study

indicated that antifungal principles are also present in

leaves of P. corylifolia which exhibited more antifungal

activity. However, the results of the present study



Plate 1. Effect of Psoralea corylifolia leaf extract on mycelia growth of C. falcatum

Control 15 % leaf extract

Control

Plate 2. Effect of Psoralea corylifolia leaf extract on spore germination of C. falcatum

15 % leaf extract

pertaining to the antifungal activity of P. juliflora are

fully in corroboration with the earlier reports as

discussed above.

Compatibility studies of effective concentration

(15%) of P. corylifolia leaf extract against beneficial

bacteria

In vitro testing of the effective plant extract was

carried out on beneficial microflora to assess whether

plant extract is inhibitory or non –inhibitory to their

growth. The effective concentration (15 per cent) of leaf

extract of Psoralea corylifolia was taken for testing the

compatibility assessment with beneficial bacteria

Pseudomonas fluorescens, Bacillus megaterium, and

Gluconacetobacter diazotrophicus. The extract showed

no inhibitory effect and found to be compatible with all

beneficial microflora tested (Table 2). The results in the

present study were not in agreement with that of

Parimala and Sabitha Doraisamy (2000) who examined

the compatibility of six plant extracts viz., Azadirachta

indica, Abrus precatorius, Vitex negundo, Nerium

oleander and Catharanthus roseus for Trichoderma

viride strains (MNT 5 and MG 6), Pseudomonas

fluorescens and Bacillus subtilis, but found that these

plant extracts were non-compatible to the tested

antagonists. This may be due to the reason that the tested

plant extracts may be possessing different type of

compounds which are of inhibitory nature to the

beneficial antagonists. Literature on compatibility testing of

plant extracts with beneficial microflora viz., Bacillus

megaterium, Pseudomonas fluorescens and

Gluconacetobacter diazotrophicus had not been reported

earlier.

Identification of antifungal compound from

Psoralea corylifolia extract

Different chromatographic studies such as TLC,

HPLC and GC-MS were carried out to identify the

specific compounds in P. corylifolia responsible for

antifungal activity against C. falcatum. In TLC study,

three different solvent systems were used for identifying

alkaloids, phenols and flavonoids. Among which the

flavonoid compounds which were well separated in the

ethyl acetate: formic acid: acetic acid: water

(100:11:11:27) solvent system alone exhibited antifungal

activity against C. falcatum which was confirmed by

poison food technique. The flavonoid compounds

separated in TLC were subjected to HPLC analyses, in

which it revealed three major peaks upon separation

(Figure 1). Among these, the compound showing second

peak exerted antifungal activity against C. falcatum which

was again confirmed by poison food technique. The

effective peak was collected through fractional collector

in HPLC and it was subjected to GC-MS analysis. GC-

MS analysis revealed five major peaks upon separation

(Figure 2 ) and these peaks were identified as, 2-[1-

cyclohexylethyl)carbamoyl] methyl ester propanoic acid (RT

2.551 min.), N-methyl-2-methoxy-1-propanamine (RT 3.360

min.), 2-propoxy ethanol (RT 3.451 min.), 1,2-

dimethylbenzene (RT 4.570 min.) and 7H-furo[3,2-G](1)

benzopyran-7-one (RT 25.062 min.). There is no report about

the fungicidal effect of 7H-furo[3,2-G] (1) benzopyran-7

-one. However, there are reports about the antifungal

nature of 9-methoxy-7H-furo [3,2-G](1) benzopyran-

7-one / 8-methoxypsoralen known to present in

P. corylifolia. The antifungal activity of


Rajkumar and Murugesan, 2013

Table 2. Compatability of effective leaf extract with beneficial organisms

S.No Name of Organism Control 15% extract

1 Bacillus megaterium (phosphorus solubilizer) +++ +++

2 Pseudomonas fluorescens (biocontrol agent) +++ +++

3 Glucanoacetobacter diazotrophicus (nitrogen fixer) +++ +++

+ - low compatible, ++ - Moderately compatible, +++ - Highly compatible

8-methoxypsoralen was studied already against

Fusarium oxysporum (Oliva et al., 2003) and against

dermatophytic fungi (Kundsen, 1980). Hence, it can be

presumed that resulting fungitoxicity of P. corylifolia

may be due to 8-methoxypsoralen, a furanocoumarin

which might be formed via 7H-furo [3,2-G](1)

benzopyran-7-one during biosynthesis. Antifungal effect

of 8-methoxypsoralen is reported due to its

photosensitizing potency (Young and Barth, 1982) and its

binding with nuclear DNA (Bredberg et al., 1977).



Figure 2. Mass spectrum of the compound

Minutes

0 2 4 6 8 10 12 14 16 18 20 22 24

mA

U

0

500

1000

1500

2000

2500

3000

3500

mA

U

0

500

1000

1500

2000

2500

3000

3500

0.1

92

487

195

0.5

33

439

194

1.1

41

1451

195

1.3

33

255

206

1.4

51

290

195

3.0

29

1793628

201

5.1

31

36540145

249

6.7

52

96165738

259

12.1

28

36279585

239

16.0

96

125730

191

17.7

39

62867

194

18.7

73

2169

191

19.4

03

3545

191

19.5

95

19349

203

24.1

39

2428

194

24.3

09

1647

193

24.7

79

388

195

1: 262 nm, 8 nm

Psoralen extract-r2

run2

Retention Time

Area

Lambda Max

Figure 1. HPLC of the compound

CONCLUSION

Various chemical fungicides have been

recommended for the control of different diseases.

However, their use cause several adverse effects and

have posed various problems like residues in feed and

food, pathogen resistance, toxicity to non-target

organisms, environmental pollution in different

agricultural ecosystems and hence it has become

necessary to use eco-friendly formulations which can fit

into integrated disease management. This study screened

different botanicals for the control of C. falcatum,

sugarcane red rot pathogen. It was found that the 15 %

leaf extract of P. corylifolia possess strong fungitoxic

properties under in vitro conditions worth exploiting for

the biomanagement of the sugarcane red rot disease.

Further studies are needed to test the fungitoxic effect

under field conditions, their thermostability, stability to

storage and also their phytotoxicity towards the host plant.

This study also confirmed the compatibility of fungitoxic

principles of plants with beneficial microbes. Therefore,

the present study augurs well for the establishment of the

fact that they should possess both the properties ie.,

toxicity to pathogenic fungi and safety to beneficial

microbes for their application in sustainable agriculture.

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Identification and Evaluation of Antifungal Compounds from Botanicals for the Control of Sugarcane Red Rot Pathogen, Colletotrichum falcatum