cultivable endophytic mycobiont piriformospora indica in...

International Journal of Science, Engineering and Technology Research (IJSETR), Volume 3, Issue 7, July 2014

2033 ISSN: 2278 – 7798 All Rights Reserved © 2014 IJSETR

Cultivable Endophytic Mycobiont Piriformospora indica in Millet Growth Promotion

Krishnaveni. N1, Dipika.B

2, Geetha Ramani D

3, Cibi Chakravarthy

4

1. Assistant Professor, Department of Microbiology, PSG College of Arts & Science,

Coimbatore

2. Research Scholar, Department of Microbiology, PSG College of Arts & Science,

Coimbatore

3. Associate Professor, Department of Microbiology, Dr. NGP College of Arts and Science,

Coimbatore

4. Research Scholar, Department of Biotechnology, Bharathiar University, Coimbatore.

ABSTRACT

The novel endophytic fungi Piriformospora

indica has been proven to have vast applications as plant growth promoter. P. indica

significantly increases plant biomass, flowering

and yield, nutrient value etc., during its

colonization and proliferation in the roots of the host plants. Study plants were chosen to be

Sorghum (Sorghum bicolor), Pearl Millet

(Pennisetum glaucum) and Finger Millet (Eleusine coracana). Pot cultures of P. indica

colonized plants were compared for physical

parameters as root, shoot height, dry and fresh weight. The P.indica colonized plants have

shown comparatively higher level of

chlorophyll, protein, phosphate and calcium

content. Enzymic and non-enzymic antioxidants levels were higher in P.indica colonized plants.

Various metabolites produced by

Piriformospora indica was analysed by GC-MS analysis, depicting many medically important

compounds with anti-cancer, insecticidal,

nematicidal, anti parasitic, anti-bacterial and

anti-fungal properties. Thus the present study has added to the proof that Piriformospora

indica is a highly efficient plant growth

promoting endophytic fungi.

Keywords: endophytic fungi, millet endophyte,

Piriformospora indica, plant growth promoter.

INTRODUCTION

Piriformospora indica, the

mycorrhizae (AM)-like fungus, has been

extensively studied to be cultivable in axenic

cultures, where it forms chlamydospores

asexually [1]. The fugus Piriformospora

indica was discovered in the Thar Desert

(1988) from the rhizospheric soil of two

xerophytic plants, namely Prosopis juliflora

and Ziziphus nummularia [1]. It is the first

symbiotic fungus, which was proved to be

inoculated to the roots of a plants [2,3,4] and

found to have stimulated considerable

attention as they form endophytic

associations with most plant species

[22,23]. This is of great interest that they

possess plant growth-promoting

characteristics and contribute several other

benefits to their host plants [1,5, 6, 7, 8, 20,

22, 23]. P. indica colonizes the roots, grows

intracellularly, forming pear-shaped spores

that collect in the roots as well as on the root

surface. The endophyte mediates nutrient

uptake, stimulates growth and seed

production, allows plants to survive in less

water, confers resistance to toxins,

resistance to heavy metal ions, and promotes

salt stress [1, 13, 14, 15, 17, 19, 21]. It

significantly increases plant biomass,

flowering and yield, nutrient value etc.,

during its colonization and proliferation in

the roots of the host plants. [1,7, 14, 18].



Piriformospora indica as a mycofertilizer

has produced a greater keenness among

mycorrhizologists, due to being easily

culturable, plant-growth enhancer and

inducer. In the present work, the recently

discovered root endophytic-fungi

Piriformospora indica has been optimized

and tested for its growth enhancement.

METHODOLOGY

Culture of P.indica

P.indica was procured from the Department

of Microbial technology, Amity University,

Noida. The culture was maintained on Hill

and Kaefer medium [4]. The cultures were

incubated at 30±2°C in incubator for a week.

Characterization of Piriformospora

indica:

Morphological characteristics-Fungal

Wet mount technique

Lacto phenol cotton blue technique was

carried to identify the morphological

structure of the fungi. A small block of

fungal culture from the surface of agar plate

was taken and placed on a clean glass slide.

A drop of Lacto phenol cotton blue was

added on the block. The cover slip was

placed on the culture block with a gentle

press. The slide was viewed under

microscope at 45X, to observe the

morphological features of the fungi.

Cultural characteristics

The fungal isolates were inoculated in

different culture media like Nutrient agar,

Malt extract, Malt yeast extract agar,

Sabouraud’s Dextrose agar medium, MYP

Medium, Hill and Kafer medium and Brain

Heart Infusion agar medium to observe its

colony morphology and various cultural

characteristics.

Optimization of Piriformospora indica

To optimize the various growth parameters

of the fungus in laboratory conditions,

several physical parameters such as

Temperature, Incubation time required for

optimum growth, Heavy metals

concentrations, different salt concentrations,

different carbon sources, nitrogen sources,

vitamin sources and growth in various media

have been studied.

Determination of extracellular enzyme

formation by P.indica

To resolve the extracellular enzyme

produced by P.indica, various enzyme

activity such as amlyolytic activity, cellulase

activity, proteolytic activity, laccace activity

and lipolytic activity were performed [10,

21].

Germination studies

In the present study, tissue culture technique

has been used for studying the ability of

Piriformospora indica in pre-determined

conditions to check the plant growth

promoting ability of the fungal

endosymbiont and for this study the Millet

varieties of Sorghum, Pearl Millet

(Pennisetum glaucum) and Finger Millet

(Eleusine coracana) seeds were used for the

growth determination.

The selected seeds of the test plants were

surface-sterilized with sterile distilled water

for three times and rinsed in 0.1% HgCl2 for

about 1 min and finally washed for three

times with sterile distilled water [1,2] to

eliminate the naturally occurring surface

microorganism. The Murashige and Skoog

medium was prepared and dispensed in

sterile petriplates. After solidification the

surface sterilized seeds were aseptically

transferred to Murashige and Skoog medium

[12] and the plates were incubated at room

temperature in presence of light, to observe

the germination of plantlet in tissue culture

media.



Pot culture studies

In pot study, the seeds of chosen plants were

allowed to germinate by inoculating

P.indica on a hard substratum which

contains sand and soil in 3:1 ratio. The soil

was autoclaved thrice on alternate days and

air dried. Riverbed sand was soaked in 10%

HCl overnight and then washed under

running tap water until the pH has reached

near neutrality (pH 6-7 as standardized in

the present study) [8]. This sterile soil has

been used as substratum in pots. Pots were

also surface-sterilized by 70% ethanol and

were then half-filled with this sterile soil

mixture and the fungal inoculum has been

added in the volume as variying

concentrations of 3%, 5% and 7%to the soil

content that is filled in the pot. The fungal

inoculum was mixed well with the sterile

soil so as to enhance even distribution of the

fungal inoculum in the soil in pot. Equal

number of surface sterilized seeds was sown and also in sterile soil for control plants

(without addition of P. indica).The pot study

experiments were carried out in controlled

conditions.

Root Colonization by fungus -

Microscopic Observation

Roots of randomly chosen plants were

washed thoroughly in running tap water, cut

into about 1-cm pieces, transferred to 10%

KOH, boiled for 10 min, then acidified with

1 M HCl for 10 min, and finally stained with

0.02% of Trypan blue in lactophenol

overnight [9, 11]. Samples were destained

with lactic acid:glycerol:water solution in

the ratio of 14:1:1(Volumetric ratio). The

stained root samples were observed under

microscope.

Estimation of plant growth

For assessment of plant growth promotion of

endosymbiotic sorghum, pearl millet and

finger millet plants; shoot and root length,

fresh and dry weight, total protein

estimation and increase in chlorophyll

pigmentation, phosphate content, calcium

content, enzymic and non enzymic

antioxidants were measured. The parameters

were compared with the values in control

plants.

RESULTS AND DISCUSSION

Piriformospora indica cultures were

obtained from Dr. Varma’s laboratory at

Department of Microbial Biotechnology,

Amity University, Noida, India. The culture

was reviewed by using the selective medium

of Hill and Kafer and in this medium the

growth pattern has been shown (Fig 1). P.

indica showed the morphology of pear-

shaped chlamydospores at hyaline hyphae

was examined under light microscope at

45X (Fig 2).

Fig 1

Fig 2

Fig 1- Colonies of Piriformospora indica on

Hill & Kafer medium

Fig 2-Fungal culture showing hyphae with

spores on Fungal mount technique

The cultural characteristics of the P. indica

was determined in different types of

medium, showed puffed white chalky

powdery appearance with the pointed tip at



the centre of the each colony in the different

medium (Fig 3) .

Nutrient agar SDA

Brain heart infusion agar Malt extract agar

Malt yeast extract agar MYP agar

Hill & Kafer agar

Fig 3- Growth of Piriformospora indica on

different medium

Optimization of Piriformospora indica

The cultures were revived and optimized to

grow in laboratory conditions. P. indica

showed optimum growth at a temperature of

270C and dry weight of 1.2 g/l, the optimum

incubation time for the initiation of growth

was found to be 3 days and it was also noted

that the maximum level of growth was

obtained on the 33rd

day and dry weight of

0.48g/5ml, Hill and Kafer medium have

shown to demonstrate better growth among

all the other nutrient media which showed a

maximum growth of 0.66g/5ml dry weight.

P.indica culture showed more resistance to

Nickel and Lead when compared to that of

Zinc and Cadmium, this proves that only

minimal amount of Heavy metal tolerance

has been observed in P.indica culture. The

culture showed a reduced growth when the

concentration of heavy metal and salt was

increased but there was still a viability of the

culture observed at lowest concentration of

heavy metals and salt used for the present

study, which shows that they are tolerant to

heavy metals and salt stress may be at more

lower concentrations which has to be

explored.

The fungal culture has the ability to grow in

the high concentration of glucose in which,

the dry weight was higher in the

concentration of 5% and the poor carbon

source was straw, in this it shows less

amount of dry weight when compared to

other carbon sources, has ability to grow in

the high concentration of peptone in which,

the dry weight was higher in the

concentration of 1% and lesser growth was

observed when nitrogen source was casein

and also has the ability to grow in the high

concentration of nicotinamide in which, the

dry weight was higher in the concentration

of 1% and the poor growth was observed

when vitamin source was riboflavin, it

shows less amount of dry weight when

compared to other vitamin sources.

Determination of extracellular enzyme

production by P.indica

The extracellular enzyme activity produced

by Piriformospora indica culture were

studied and found to be amylolytic,

cellulase, laccase and lipolytic activity

which were positive. Proteolytic activity was

not positive for the fungi and the results

were shown (Fig 4).



Amylolytic activity Cellulase activity

Proteolytic activity Laccase activity

Lipolytic activity

Fig 4- Enzyme production by

Piriformospora indica

Germination and Pot culture studies

Germination studies of P. indica in MS

medium have shown considerable

advancement in growth compared to control

plant (Fig 5a. & 5b and Table 1). Pot

culture studies have also revealed better

plant growth promotion which is evidenced

by comparing the physical parameters of

endosymbiotic plant with the control plant

(Fig 6). In all the three types of plants the

growth rate was excellent in P.indica

colonized plants in pot culture.

Pearl millet plant

Sorghum plant

Finger millet plant

Fig 5a- Germination studies on the study

plant in plates

Pi

Pi C

Pi c

c

C

C

Pi

C



PI

Pearl millet plant Sorghum plant Finger millet plant

Fig 5b- Germination studies on the study plant in bottles

Table 1-Shows the difference in germination between the inoculated and uninoculated plants

Sorghum plant Pearl millet plant Finger millet plant

Fig 6- Pot culture studies in the study plants

S.No

Study

Plants

Day of germination

Measurement of germination

in cm

P.indica

Inoculated

Control P.indica

Inoculated

Control

1 Sorghum 2nd

day 3rd

day 0.6 0.4

2 Pearl

Millet

4th day 5

thday 0.3 0.05

3 Finger

millet

2nd

day 4thday 0.4 0.15

Pi Pi Pi

C C C

Control 3%

5% 7% Control 33%

5% 7% Control 3%

33% 5%



Microscopic Observation of Root

Colonization by Fungus

The stained root samples were observed under

light microscope (100X). The colonization of root by P. indica in the study plants has been

shown in Plate 6, Figure 4.15.This shows the

difference between the P.indica colonized study

plants with that of control plants.

Control root Pi colonized root

Fig 7- Root staining of the study plants

showing SEM picture of Pi colonization

Estimation of physical parameters

The colonization of the study plants

by P.indica has led to its increased growth.

Due to the growth promotional activities in

the study plants when compared to un-

inoculated plants, plants inoculated with

P.indica showed greater increase in root and

shoot length and increase in fresh and dry

weight. In all the three plants the

endosymbiont colonized plants have shown

excellent growth, and gain in weight and

length when compared to that of control

plants in pot studies and their differences

have been shown in Table 2a &2b and Fig

8a & 8b.

Table 2a- Fresh and Dry weight of plants

studied with Piriformospora indica

Table 2b- Shoot and Root length of plants

studied with Piriformospora indica

1

2

Plants

Sorghum

Pearl millet

Finger millet

Control

plants

Fresh

weight

in gms

Dry

weight

in gms

Fresh

weight

in gms

Dry

weight

in gms

Fresh

weight

in gms

Dry

weight

in gms

5.06

1.92

3.45

1.05

4.23

0.93

P.indica

colonized

plants

7.94

2.53

5.5

1.85

6.09

1.34

1

2

Plants

Sorghum

Pearl millet

Finger millet

Control

plants

Shoot

length

in cms

Root

length

in cms

Shoot

length

in cms

Root

length

in cms

Shoot

length

in cms

Root

length

in cms

34

3.5

26

2.8

30

3.1

P.indica

colonized

plants

49

4.6

32

3.7

43

4.2



Fig 8a- Shoot length of the Pi colonized

study plants with control plants

Sorghum plant Finger millet plant

Pearl millet plant

Sorghum plant Finger millet plant

Pearl millet plant

Fig 8b- Root length of the Pi colonized

study plants with control plants

The P.indica colonized plants have

shown comparatively higher chlorophyll

content when compared to that of control

plants which indicates that P.indica helps to

enhance the chlorophyll production in the

plants, there is net gain in total protein

content in P. indica colonized plants which

might help for the various plant growth

promoting and protecting characteristics of

the fungus that has been demonstrated

earlier. The proteins were further

characterized by Native-PAGE to determine

the difference in molecular weight of the

proteins present in P. indica colonized and

control plants, when compared to control

plants there is net gain in total phosphate

content in P. indica colonized plants which

might help for diverse regulatory, structural,

and energy transfer roles the various plant

growth promoting and protecting

characteristics of the fungus, increasing

amount of calcium content present in

P.indica colonized plant when compared to

that of control plants which helps for the

plant growth promotional and building

activities.

P.indica colonized plants showed

increasing level of ascorbic acid which helps

in protecting the plants and also helps in

plant growth promoting properties, increased proline content which helps the

plants to grow under stress conditions and

also helps in plant growth promoter, increased reduced glutathione content which

favours the plant–fungal association and

increases resistance to the pathogen and

also promotes plant growth, increased level

of catalase content which responsible for

preventing and neutralizing the free radical

induced damages on tissues. This result has

been shown (Table 3).

Pi C Pi

C

Pi C

Pi C

Pi

C

Pi C



Table 3 - Biochemical, Enzymic and non-enzymic antioxidant studies on Pi colonized plants

Gas Liquid Chromatography-Mass Spectrometry

Piriformospora indica was subjected to gas liquid chromatography mass spectrometry analysis.

The identification of compounds is based on the peak area, molecular weight and molecular

formula. Peak area is directly proportional to quantity of the compound present in the culture.

S.No

Estimations

Sorghum plant

Pearl millet plant

Finger millet plant

1

Chlorophyll

content

Control plant

Pi colonized

plant

Control plant

Pi colonized

plant

Control plant

Pi colonized

plant

1.42 g/tissue

2.11 g/tissue

0.86 g/tissue

1.33 g/tissue

1.27 g/tissue

2.06 g/tissue

2

Protein content

0.7mg/g

0.9 mg/g

0.2 mg/g

0.5 mg/g

0.4 mg/g

0.7 mg/g

3

Phosphate content

7.5µg/tissue

10 µg/tissue

3.5 µg/tissue

5 µg/tissue

5 µg/tissue

8.5 µg/tissue

4

Calcium content

180mg/g

220 mg/g

120 mg/g

170 mg/g

150 mg/g

190 mg/g

5

Non enzymic

aantioxidants

Ascorbic acid

0.46mg/g

0.6 mg/g

0.32 mg/g

0.42 mg/g

0.36 mg/g

0.48 mg/g

6

Proline

11.08µmoles /g

of tissue

15.93 µmoles

/g of tissue

5.19µmoles /g

of tissue

919µmoles /g

of tissue

9.35 µmoles /g

of tissue

13.16 µmoles

/g of tissue

7

Enzymic

antioxidants

Reduced

glutathione

0.48mg/g

0.72 mg/g

0.36 mg/g

0.6 mg/g

0.24 mg/g

0.48 mg/g

8

Catalase

860units/ml of

extract

1220 units/ml

of extract

503 units/ml of

extract

719 units/ml of

extract

647 units/ml

of extract

1000 units/ml

of extract



The GC-MS results shows the various metabolites produced by the fungi, there are many

medically important compounds that have been referred to show ant-bacterial, anti-fungal, anti-

parasitic, anti-cancer, insecticidal, nematicidal properties etc., shown in the Table 4. This study

gives a better understanding of the protective effect that it confers on its host plant against

invading pathogenic organisms. The components may further be analyzed to establish a better

understanding about these secondary metabolites produced by the fungi.

Library Search Results



Compound Name Probabilit

y

Molecular

Formula

Molecular

Weight Structure Commen Comments

Cholestan-3-ol,

2-methylene-,

(3á,5à)- (CAS)

4.73 C28H48O 400

Antimicrobial Antiinflammatory

Anticancer Diuretic

Antiasthma Antiarthritic

Ergosta-5,7,22-

trien-3-ol,

(3á,22E)- (CAS)

12.89 C28H44O 396

Synaptogenin R 0.68 C30H48O3 456 Anti fungal Property

Lanosta-

7,9(11),20(22)-

triene-3á,18-diol,

diacetate

(CAS)

9.08 C34H52O4 524

A plant derived secondary

metabolite with anti-Tuberculosis

product, anti-cancer properties

7-Oxogedunin 3.89 C26H30O6 438 Anti fungal Property & Insecticidal

activity

Neurosporaxanth

in methyl ester

6.19 C36H48O2 512 Major carotenoid product in F.

fujikuroi is neurosporaxanthin (b-

apo-4¢-carotenoic acid), a

carboxylic

xanthophyll formerly identified in

Neurosporacrassa

8-Norurs-9(11)-

en-12-one-28-oic

acid, 3-acetoxy-,

methyl ester (14á,20á)

7.00 C32H48O5 512 Cytotoxic activity

6,7-

Isopropylidenedi

oxy-1,15-

dihydroxy-8,15-

seco-mao

erystals A

3.62 C23H36O5 392

Herbicidal and Nematicidal

Property

Cholic acid 9.08 C24H40O5 408

An elicitor of defence response

expressed in plants

Cyclotrisiloxane, hexaphenyl-

6.62

C36H30O3 Si3

594

Plant active compound

Hexatriacontane 11.34 C36H74 506

Antioxidant Property



Table 4- Compounds present in the fungal culture was analyzed by GC-MS.

CONCLUSION

Endophytic fungi are an excellent model

organism for plant growth promotion studies

and the most widespread symbionts on earth

are receiving attention because of the

increasing range of their application in

sustainable agriculture and ecosystem

management. Development of P.indica may

not only complement crop-growth

promotion strategies but will also serve as

model representation to study its

physiological functions, molecular behaviors

that result in disease resistance against biotic

and abiotic stress including root and leaf

infecting pathogens, insect invaders, grain

yielders and production of many additional

growth mediating component as

biofertilizers in nutrient deficient soils. All

these impressive traits make P. indica very

valuable for applied research and also can be

easily proliferated on a large scale in axenic

culture in the absence of host plant. It could

thus be suggested to consider this endophyte

as a tool for endless sustainable agriculture.

ACKNOWLEDGMENT

The authors acknowledge Dr.Varma’s

laboratory, AMITY University, for the

culture and the Management PSG College of

Arts And Science, Coimbatore, for the

laboratory facilities.

BIBILIOGRAPHY

1. Ajit Varma, Savita Verma, Sudha,

Nirmal Sahay, Britta Bütehorn and

Philipp Franken. (1999). Piriformospora

indica, a Cultivable Plant-Growth-

Promoting Root Endophyte. Appl.

Environ. Microbiol. 1999, 65(6):2741.

2. Anjana Singh, Archana Singh, Meera

Kumari, Mahendra K. Rai and Ajit

Varma. (2003). Biotechnological

importance of Piriformospora indica

Verma et al – A Novel Symbiotic

Mycorrhiza-like Fungus: An Overview.

Indian Journal of Biotechnology. Vol. 2.

January, pp 65-75.

3. Archana Singh, Jyotika Sharma, Karl-

Heinz Rexer and Ajit Varma. (2000).

Plant productivity determinants beyond

minerals, water and light:

Pirifiormospora indica – A

revolutionary plant growth promoting

fungus. Current Science, Vol. 79, No.11.

1548-1555.

Nonacosane 10.90 C29H60 408 Nematicidal activity

Pentatriacontane 8.57 C35H72 492

Anti-bacterial and antifungal

activity

Octacosane

6.22 C28H58 394 Mosquitocidal activities

Tetracontane

6.22 C40H82 562 Antimicrobial, antitumor and

anticancer properties

Triacontane

(CAS)

5.98 C30H62 422 Antimicrobial, antitumor and


Hentriacontane 5.51 C31H64 436 Antimicrobial, antitumor and




4. Anjana Singh, Giang Huong Pham, Rina

Kumari, Rajani Malla, Ram Prasad,

Minu Sachdev, Michael Kaldorf,

François Buscot, Ralf Oelmüller,

Rüdiger Hampp, Anil Kumar Saxena,

Karl-Heinz Rexer, Gerhard Kost, Dr.

Ajit Varma. (2004). Axenic Culture of

Symbiotic Fungus Piriformospora

indica . Plant Surface Microbiology. pp

593-613.

5. Bagde. U. S., Ram Prasad and Ajit

Varma. (2010). Interaction of

Mycobiont: Piriformospora Indica with

Medicinal plants and plants of Economic

importance, African Journal of

Biotechnology Vol. 9 (54), pp. 9214-

9226.

6. Bahtiyar Yilmaz. (2013). Optimization

of Piriformospora indica application and

observation of Piriformospora indica

induced disease resistance against

various plant pathogens in wheat and

barley. A thesis submitted to the

graduate school of natural and applied

sciences of Middle East technical

university.

7. Barazani O, M. Benderoth, K. Groten, C.

Kuhlemeier, I. T. Baldwin, (2005).

Piriformospora indica and Sebacina

vermifera increase growth performance

at the expense of herbivore resistance in

Nicotiana attenuata. Oecologia, 146:

234–243.

8. Deshmukh S.D & K.-H. Kogel. (2007).

Piriformospora indica protects barley

from root rot caused by Fusarium

graminearum. Journal of Plant Diseases

and Protection, 114 (6), 263–268, 2007,

ISSN 1861-3829. © Eugen Ulmer KG,

Stuttgart.

9. Dickson, S., Mandeep & Smith, S. M.

(1998). Evaluation of vesicular

arbuscular mycorrhizal colonization by

staining In Mycorrhiza Manual, Edited

by A. Varma. Berlin/Heidelberg:

Springer Verlag. pp. 77–84.

10. Fatemah Karimi, Mozhgan Sepheri,

Majid Afyuni and Hajabbasi M.A.

(2011). Role of Piriformospora indica in

Barley (Hordeum vulgare L) resistance

to Cadmium, Lead and Copper.

International Conference of

Environmental Science and Technology,

Rhodes, Greece, 8-10. Pp-B-467- 475.

11. Kumar, M, R. Sharma, A. Jogawat, P.

Singh, M. Dua, S.S. Gill, D. Trivedi, N.

Tuteja, A. Verma, R. Oelmuller, A.

Johri, (2012). Piriformospora indica, a

root endophytic fungus, enhances abiotic

stress tolerance of the host plant. In: N.

Tuteja, S.S. Gill, A.F. Tiburcio, R.

Tuteja (eds) Improving crop resistance

to abiotic stress. Weinheim, Wiley-

Blackwell, pp 543-548

12. Murashige, T., and F. Skoog. (1962). A

revised medium for rapid growth and

bioassay with tobacco tissue cultures.

Physiol. Plant 15:431–487

13. Oelmüller Ralf, Iris Camehl, Corinna

Drzewiecki, Jyothilakshmi Vadassery,

Bationa Shahollari, Irena Sherameti,

Celine Forzani, Teun Munnik, Heribert

Hirt,. (2011). The OXI1 kinase pathway

mediates Piriformospora indica-induced

growth promotion in Arabidopsis. PLoS

Pathogens. 05/2011; 7(5):e1002051.

14. Peskan-Berghofer, T., Shahollari, B.,

Giong, P. H., Hehl, S., Markert, C.,

Blanke, V., et al. (2004). Association of

Piriformospora indica with Arabidopsis

thaliana roots represents a novel system

http://www.researchgate.net/researcher/39992199_Ralf_Oelmueller

http://www.researchgate.net/researcher/38778699_Iris_Camehl

http://www.researchgate.net/researcher/33717630_Corinna_Drzewiecki



http://www.researchgate.net/researcher/38440105_Jyothilakshmi_Vadassery

http://www.researchgate.net/researcher/38892404_Bationa_Shahollari

http://www.researchgate.net/researcher/38444122_Irena_Sherameti

http://www.researchgate.net/researcher/14690196_Celine_Forzani

http://www.researchgate.net/researcher/20625850_Teun_Munnik

http://www.researchgate.net/researcher/39418086_Heribert_Hirt



http://www.researchgate.net/journal/1553-7374_PLoS_Pathogens





to study beneficial plant-microbe

interactions and involves early plant

protein modifications in the endoplasmic

reticulum and at the plasma membrane.

Physiologia Plantarum, 122(4), 465-477.

15. Pham Huong Giong, Tatjana Peskan-

Berghofera, Bationa Shahollaria, Solveig

Hehl, Christine Markerta, Verena

Blanke, Gerhard Kost, Ajit Varma and

Ralf Oelmuller. (2004). Association of

Piriformospora indica with Arabidopsis

thaliana roots represents a novel system

to study beneficial plant–microbe

interactions and involves early plant

protein modifications in the endoplasmic

reticulum and at the plasma membrane.

Physiologia Plantarum 122: 465–477.

16. Prasad. R., Bagde. U S., Pushpagandan P

and Varma A. (2008). Bacopa

monniera.: Pharmacological Aspects and

case study involving Piriformospora

indica. International Journal of

Integrative Biology. Submitted: 25 April

2008: Revised: 15 July 2008. Accepted:

15 Aug. 2008. Vol. 3., No.2, 100-110.

17. Shahollari, B., J. Vadassery, A.

Varma and R. Oelmüller (2007). A

leucin-rich repeat protein is required for

growth promotion and enhanced seed

production mediated by the endophytic

fungus Piriformospora

indica in Arabidopsis thaliana. Plant

J, 50: 1–13.

18. Shailendra Vyas., Rakhi Nagori and

Sunil Dutta Purohit. (2008). Root

Colonization and growth enhancement

of micropropagated Feronia limonia (L)

swingle by Piriformospora indica – A

Cultivable Root Endophyte.

International Journal of Plant

Dervelopmental Biology. Vol. 2 (2),

128-132.

19. Sherameti I, Shahollari B, Venus Y,

Altschmied L, Varma A, et al. (2005)

The endophytic fungus Piriformospora

indica stimulates the expression of

nitrate reductase and the starch-

degrading enzyme glucan-water dikinase

in tobacco and Arabidopsis roots

through a homeodomain transcription

factor that binds to a conserved motif in

their promoters. J Biol Chem 280:

26241–26247.

20. Sita R. Ghimire, Nikki D. Charlton,

Kelly D. Craven. (2009). The

Mycorrhizal Fungus, Sebacina

vermifera, Enhances Seed Germination

and Biomass Production in Switchgrass

(Panicum virgatum L). BioEnergy

Research, Volume 2, Issue 1-2, pp 51-

58.

21. Sunitha V.H., D. Nirmala Devi and C.

Srinivas. (2013). Extracellular

Enzymatic Activity of Endophytic

Fungal Strains Isolated from Medicinal

Plants. World Journal of Agricultural

Sciences 9 (1): 01-09.

22. Vikas Yadav, Manoj Kumar, Narendra

Tuteja and Atul Kumar Johri. (2009).

Antioxidant enzyme activities in maize

plants colonized with Piriformospora

indica. Microbiology, vol. 155 no. 3

780-790.

23. Waller F, Beate Achatz, Sibylle von

Rüden, Diana Andrade, Elke Neumann,

Jörn Pons-Kühnemann, Karl-Heinz

Kogel, Philipp Franken. (2010). Root

colonization by Piriformospora indica

enhances grain yield in barley under

diverse nutrient regimes by accelerating

plant development. Plant and Soil.

Volume 333, Issue 1-2, pp 59-70

http://link.springer.com/journal/12155



http://link.springer.com/journal/12155/2/1/page/1

http://mic.sgmjournals.org/search?author1=Manoj+Kumar&sortspec=date&submit=Submit

http://mic.sgmjournals.org/search?author1=Narendra+Tuteja&sortspec=date&submit=Submit



http://mic.sgmjournals.org/search?author1=Atul+Kumar+Johri&sortspec=date&submit=Submit


http://link.springer.com/journal/11104/333/1/page/1



24. Weiß M, M. A. Selosse, K. H. Rexer, A.

Urban, F. Oberwinkler, (2004).

Sebacinales: a hitherto overlooked cosm

of heterobasidiomycetes with a broad

mycorrhizal potential. Mycol Res, 108:

1003–1010.

Corresponding Author:

Krishnaveni. N - Assistant Professor,

Department of Microbiology, PSG College

of Arts & Science, Coimbatore, Tamil nadu,

India.

cultivable endophytic mycobiont piriformospora indica in...

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