The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii

Plant Signaling and Behavior

Volumn 7, Issue 1, 2012, Pages 103-112

  Das, Aparajita ^a   Kamal, Shwet ^b   Shakil, Najam Akhtar ^c   Sherameti, Irena ^d   Oelmüller, Ralf ^d   Dua, Meenakshi ^e   Tuteja, Narendra ^f   Johri, Atul Kumar ^e   Varma, Ajit ^a  

^a AMITY UNIVERSITY   (India)

^b National Research Centre for Mushroom India   (India)

^c INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e JAWAHARLAL NEHRU UNIVERSITY   (India)

^f INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Coleus forskohlii; P cymene; Piriformospora indica; Secondary metabolite

Indexed keywords

COLEUS; FUNGI; PIRIFORMOSPORA INDICA; PLECTRANTHUS BARBATUS;

ARTICLE; BASIDIOMYCETES; BIOMASS; COLEUS; FLOWER; MASS FRAGMENTOGRAPHY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT ROOT;

BASIDIOMYCOTA; BIOMASS; COLEUS; FLOWERS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; PLANT ROOTS;

EID: 84856763668     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.7.1.18472     Document Type: Article

References (78)

1. Chandel KPS, Sharma N. Micropropagation of Coleus forskohlii (Willd.) Briq. In: Bajaj YPS, ed. Biotechnology in Agriculture and Forestry. Hi Tech and Micropropagation. Berlin: Springer, 1997: 74-84.
2. Kurian A, Sankar A. Important medicinal plants in trade. In: Peter KV, ed. Medicinal Plants. Vol 2. New Delhi: New India Publishing Agency, 2007: 294-295.
3. Ahmed B, Viswakarma RA. Coleoside, a monoterpene glycoside from Coleus forskohlii. Phytochemistry 1988; 27:3309-3310. http://dx.doi.org/10.1016/0031-9422(88)80050-5
4. Ahmed B, Merotra R. Coleoside-B: a new phenolic glycoside from Coleus forskohlii. Pharmazie 1991; 46: 157-8.
5. Petersen M. Coleus spp: In vitro culture and the production of forskolin and Rosmarinic acid. In: Bajaj YPS, ed. Biotechnology in Agriculture and Forestry, Medicinal and Aromatic plants VI. Berlin: Springer, 1994: 69-85.
6. Ammon HPT, Muller AB. Forskolin: from an ayurvedic remedy to a modern agent. Planta Med 1985; 46:473-7. http://dx.doi.org/10.1055/s-2007-969566
7. De Souza NJ, Shah V. Forskolin - an adenylate cyclase activating drug from an Indian herb. Econ Med Plant Res 1988; 2:1-16.
8. Kavitha C, Rajamani K, Vadivel E. Coleus forskohlii: A comprehensive review on morphology, phytochemistry and pharmological aspects. J of Med Plants Res 2010; 4:278-85.
9. Patil S, Hulamani NC, Rokhade AK. Performance of genotype of Coleus forskohlii Briq. for growth, yield and essential oil content. Indian Perfumer 2001; 45: 17-21.
10. Misra LN, Tyagi BR, Ahmad A, Bahl JR. Variablity in the chemical composition of the essential oil of Coleus forskohlii genotypes. J Essent Oil Res 1994; 6:243-7.
11. Chowdhary AR, Sharma ML. GC-MS investigations on the essential oil from Coleus forskohlii Briq. Indian Perfumer 1998; 42:15-6.
12. Vishwakarma RA, Tyagi BR, Ahmed B, Hussain A. Variation in forskolin content in the roots of Coleus forskohlii. Planta Med 1988; 54:471-2. PMID: 17265327; http://dx.doi.org/10.1055/s-2006-962512
13. Boby VU, Bagyaraj DJ. Biological control of root-rot of Coleus forskohlii Briq. using microbial inoculants. World J Microbiol Biotechnol 2003; 19:175-80. http://dx.doi.org/10.1023/A:1023238908028
14. Sailo GL, Bagyaraj DJ. Influence of different AMfungi on the growth, nutrition and forskolin content of Coleus forskohlii. Mycol Res 2005; 109:795-8. PMID:16121565; http://dx.doi.org/10.1017/S0953756205002832
15. Oelmüller R, Sherameti I, Tripathi S, Varma A. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 2009; 49:1-17. http://dx.doi.org/10.1007/s13199-009-0009-y
16. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS USA 2005; 102:13386-91. PMID:16174735; http://dx.doi.org/10.1073/pnas.0504423102
17. Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, et al. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. PNAS USA 2006; 103:18450-7. PMID:17116870; http://dx.doi.org/10.1073/pnas.0605697103
18. Kumar M, Yadav V, Tuteja N, Johri AK. Antioxidant enzyme activities in plants colonized with Piriformospora indica. Microbiology 2009; 155:780-90. PMID: 19246749; http://dx.doi.org/10.1099/mic.0.019869-0
19. Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, et al. A Phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in the phosphate transport to the host plant. J Biol Chem 2010; 285:26532-44. PMID:20479005; http://dx.doi.org/10.1074/jbc.M110.111021
20. Dolatabadi HK, Goltapeh EM, Jaimand K, Rohani N, Varma A. Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J Basic Microbiol 2011; a51:33-9. PMID:21259287; http://dx.doi.org/10.1002/jobm.201000214
21. Dolatabadi HK, et al. Effect of Piriformospora indica and Sebacina vermifera on plant growth and essential oil yield in Thymus vulgaris in vitro and in vivo experiments. Symbiosis 2011. b53:29-35. http://dx.doi.org/10.1007/s13199-010-0104-0
22. Varma A, Verma S. Sudha, Sahay NS, Franken P. Piriformospora indica, a cultivable plant growth promoting root endophyte. Appl Environ Microbiol 1999; 65:2741-4. PMID:10347070
23. Rai M, Acharya D, Singh A, Varma A. Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 2001; 11:123-8. http://dx.doi.org/10.1007/s005720100115
24. Rai MK, Varma A, Pandey AK. Antifungal potential of Spilanthes calva after inoculation of Piriformospora indica. Mycoses 2004; 47:479-81. PMID:15601453; http://dx.doi.org/10.1111/j.1439-0507.2004.01045.x
25. Peškan-Berghofer T, Shahollari B, Giong P, Hehl S, Market C, Blanke V, et al. 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 endoplasmatic reticulum and at the plasma membrane. Physiol Plant 2004; 122:465-77. http://dx.doi.org/10.1111/j.1399-3054.2004.00424.x
26. Rai MK, Varma A. Arbuscular mycorrhizae-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasica. Electron J Biotechnol ISSN 2005; 8:107-12.
27. Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, et al. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 2010; 20:191-200. PMID:19789897; http://dx.doi.org/10.1007/s00572-009-0279-5
28. Achatz B, von Rüden S, Andrade D, Neumann E, Pons-Kühnemann J, Franken P, et al. Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating early plant development. Plant Soil 2010; 333:59-70. http://dx.doi.org/10.1007/s11104-010-0319-0
29. Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, et al. Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 2008; 165:60-70. PMID:18031866; http://dx.doi.org/10.1016/j.jplph.2007.05.017
30. Varma A. Piriformospora indica: An axenically culturable mycorrhiza-like endosymbiotic fungus. In: Hock B, ed. The Mycota IX, Fungal Associations. Berlin: Springer-Verlag, 2001: 123-150.
31. Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R. 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 which binds to a conserved motif in their promoters. J Biol Chem 2005; 280:26241-7. PMID:15710607; http://dx.doi.org/10.1074/jbc.M500447200
32. Kumar M, Yadav V, Singh A, Tuteja N, Johri AK. Piriformospora indica enhances plant growth by transferring phosphate. Plant Signal Behav 2011; 6:723-5. PMID:21502815; http://dx.doi.org/10.4161/psb.6.5.15106
33. Shahollari B, Varma A, Oelmüller R. Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton X-100 insoluble plasma membrane microdomains. J Plant Physiol 2005; 162: 945-58. PMID:16146321; http://dx.doi.org/10.1016/j.jplph.2004.08.012
34. Barazani O, Benderoth M, Groten K, Kuhlemier C, Baldwin IT. Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuate. Oecologia 2005; 146:234-43. PMID:16032437; http://dx.doi.org/10.1007/s00442-005-0193-2
35. Schäfer P, Pfith S, Voll LM, Zajic D, Chandler PM, Waller F, et al. Phytohormones in plant root-Piriformospora indica mutualism. Plant Signal Behav 2009; 4:669-71. PMID:19820343; http://dx.doi.org/10.4161/psb.4.7.9038
36. Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, et al. Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 2009; 59:461-74. PMID:19392709; http://dx.doi.org/10.1111/j.1365-313X.2009.03887.x
37. Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, et al. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol. Plant-Microb Interact 2011; 24:421-31. http://dx.doi.org/10.1094/MPMI-05-10-0110
38. Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, et al. Piriformospora indica affects plant growth by auxin production. Physiol Plant 2007; 131:581-9. PMID:18251849; http://dx.doi.org/10.1111/j.1399-3054.2007.00983.x
39. Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, et al. The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 2008; 21:1371-83. PMID:18785832; http://dx.doi.org/10.1094/MPMI-21-10-1371
40. Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, et al. Root plasma membrane H1-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 2006; 57:1353-62. PMID:16547127; http://dx.doi.org/10.1093/jxb/erj111
41. Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, et al. Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and non beneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 2010; 185:1062-73. PMID:20085621; http://dx.doi.org/10.1111/j.1469-8137.2009.03149.x
42. Yano-Melo AM, Saggin Júnior OJ, Lima-Filho JM, Melo NF, Maiai LC. Effect of arbuscular mycorrhizal fungi on the acclimatization of micropropagated banana plantlets. Mycorrhiza 1999; 9:119-23. http://dx.doi.org/10.1007/s005720050009
43. Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M. Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 2010; 335:311-23. http://dx.doi.org/10.1007/s11104-010-0417-z
44. Jurkiewicz A, Ryszka P, Anielska T, Waligórski P, Białońska D, Góralska K, et al. Optimization of culture conditions of Arnica Montana L.: Effects of Mycorrhizal fungi and competing plants. Mycorrhiza 2010; 20:293-306. PMID:19838743; http://dx.doi.org/10.1007/s00572-009-0280-z
45. Lovato PE, Gianinazzi-Pearson V, Trouvelot A, Gianinazzi S. The state of art of mycorrhizas and micropropagation. Adv Hort Sci 1996; 10:46-52.
46. Tsang A, Maun MA. Mycorrhizal fungi increase salt tolerance of Strophostyles helvola in coastal foredunes. Plant Ecol 1999; 144:159-66. http://dx.doi.org/10.1023/A:1009844125905
47. Kumari R, Kisan H, Bhoon YK, Varma A. Colonization of cruciferous plants by Piriformospora indica. Curr Sci 2003; 85:1672-4.
48. Pham HG. Interaction of Piriformospora indica with diverse microorganisms and plants. In: Varma A, Abbott LK, Werner D, Hampp R, eds. Plant Surface Microbiology. Berlin: Springer-Verlag, 2004: 237-265.
49. Perner H, Schwarz D, Bruns C, Mäder P, George E. Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza 2007; 17:469-74. PMID:17318595; http://dx.doi.org/10.1007/s00572-007-0116-7
50. Aboul-Nasr A. Effects of vesicular-arbuscular mycorrhiza on Tagetes erecta and Zinnia elegans. Mycorrhiza 1996; 6:61-4. http://dx.doi.org/10.1007/s005720050107
51. Gaur A, Adholeya A. Diverse response of five ornamental plant species to mixed indigenous and single isolate arbuscular mycorrhizal inocula in marginal soil amended with organic matter. J Plant Nutr 2005; 28:707-23. http://dx.doi.org/10.1081/PLN-200052647
52. Long LK, Yao Q, Huang YH, Yang RH, Guo J, Zhu HI. Effects of arbuscular mycorrhizal fungi on zinnia and the different colonization between Gigaspora and Glomus. World J Microbiol Biotechnol 2010; 26: 1527-31. http://dx.doi.org/10.1007/s11274-010-0313-y
53. Poulton JL, Bryla D, Koide RT, Stephenson AG. Mycorrhizal infection and high soil phosphorus improve vegetative growth and the female and male functions in tomato. New Phytol 2002; 154:255-64. http://dx.doi.org/10.1046/j.1469-8137.2002.00366.x
54. Kapoor R, Giri B, Mukerji KG. Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L.) and Carum (Trachyspermum ammi (Linn.) Sprague. World J Microbiol Biotechnol 2002. a18:459-63. http://dx.doi.org/10.1023/A:1015522100497
55. Toussaint JP, Smith FA, Smith SE. Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 2007; 17:291-7. PMID:17273856; http://dx.doi.org/10.1007/s00572-006-0104-3
56. Rajeshkumar S, Nisha MC, Selvaraj T. Variability in growth, nutrition and phytochemical constituents of Plectranthus amboinicus (Lour) Spreng. as influenced by indigenous arbuscular mycorrhizal fungi. Mj Int J Sci Tech 2008; 2:431-9.
57. Abu-Zeyad A, Khan AG, Khoo C. Occurrence of arbuscular mycorrhiza in Castanospermum australe A. Cunn. & C. Fraser and effects on growth and production of castanospermine. Mycorrhiza 1999; 9:111-7.
58. Fester T, Maier W, Strack D. Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 1999; 8:241-6. http://dx.doi.org/10.1007/s005720050240
59. Copetta A, Lingua G, Berta G. Effects of three AMfungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 2006; 16:485-94. PMID:16896796; http://dx.doi.org/10.1007/s00572-006-0065-6
60. Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J. Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 2006; 16:443-6. PMID:16909287; http://dx.doi.org/10.1007/s00572-006-0062-9
61. Kapoor R, Giri B, Mukerji KG. Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J Sci Food Agric 2002; b88:1-4.
62. Kapoor R, Chaudhary V, Bhatnagar AK. Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 2007; 17:581-7. PMID:17578608; http://dx.doi.org/10.1007/s00572-007-0135-4
63. Schliemann W, Ammer C, Strack D. Metabolic profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 2008; 69:112-46. PMID:17706732; http://dx.doi.org/10.1016/j.phytochem.2007.06.032
64. Zubek S, Stojakowska A, Anielska T, Turnau K. Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L. Mycorrhiza 2010; 20:497-504. PMID:20177715
65. Rao YR, Rout PK. Geographical location and harvest time dependent variation in the composition of essential oils of Jasminum sambac (L) Aiton. J Essent Oil Res 2003; 15:398-401.
66. Graven EH, Webber L, Benias G, Venter M, Gardner JB. Effect of soil type and nutrient status on the yield and composition of Tagetes oil (Tagetes minuta L). J Essent Oil Res 1991; 3: 303-307.
67. Arrebola ML. Variation in the yield and composition of the essential oil of Thymus serphylloides Bory subsp gadorensis (Pau) Jalas. J Essent Oil Res 1995; 7:369-74.
68. Hill TW, Kaefer E. Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solution. Fungal Genet Newsl 2001; 48:20-1.
69. Pham HG, Kumari R, Singh A, Malla R, Verma A, Kaldorf M, et al. Axenic culture of symbiotic fungus Piriformospora indica. In: Varma A, Abbott LK, Werner D, Hampp R, eds. Plant Surface Microbiology. Germany: Springer-Verlag, 2004b: 593-613.
70. Varma A, Schuepp H. Positive influence of arbuscular mycorrhizal fungus on in vitro raised hortensia plantlets. Angew Bot 1994; 68:108-13.
71. Arnon DI. A copper enzyme is isolated chloroplast polyphenol oxidase in Beta vulgaries. Plant Physiol 1949; 24:1-15. PMID:16654194; http://dx.doi.org/10.1104/pp.24.1.1
72. Irving GCJ, Bouma D. Phosphorus compounds measured in a rapid and simple leaf test for the assessment of the phosphorus status of subterranean clover. Aust J Exp Agric Anim Husb 1984; 24:213-8. http://dx.doi.org/10.1071/EA9840213
73. Irving GCJ, McLaughlin MJ. A rapid and simple field test for phosphorus in Olsen and Bray No.1 extracts of soil. Commun Soil Sci Plant Anal 1990; 21:2245-65. http://dx.doi.org/10.1080/00103629009368377
74. Dickson S. Mandeep, Smith SM. Evaluation of vesicular arbuscular mycorrhizal colonization by staining. In: Varma A, ed. Mycorrhiza Manual. Germany: Springer-Verlag, 1998: 77-84.
75. Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and VAM fungi for rapid assessment of infection. Trans Br Mycol Soc 1970; 55:158-61. http://dx.doi.org/10.1016/S0007-1536(70)80110-3
76. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 1990; 115:495-501. http://dx.doi.org/10.1111/j.1469-8137.1990.tb00476.x
77. Khare P, Sashidhara KV, Yadav A, Garg SN, Khanuja SPS. Chemical composition of the inflorescence essential oil of Coleus forskohlii. Indian Perfumer 2007; 51:47-8.
78. Mukherjee S, Ghosh B, Jha S. Forskolin synthesis in in vitro cultures of Coleus forskohlii Briq transformed with Agrobacterium tumefaciens. Plant Cell Rep 1996; 15:691-4. http://dx.doi.org/10.1007/BF00231926