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Synergy between Glomus fasciculatum and a beneficial Pseudomonas in reducing root diseases and improving yield and forskolin content in Coleus forskohlii Briq. under organic field conditions

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Abstract

Root rot and wilt, caused by a complex involving Fusarium chlamydosporum (Frag. and Cif.) and Ralstonia solanacearum (Smith), are serious diseases affecting the cultivation of Coleus forskohlii, a crop with economic potential as a source of the medicinal compound forskolin. The present 2-year field experiments were conducted with two bioinoculants (a native Pseudomonas monteilii strain and the exotic arbuscular mycorrhizal (AM) fungus Glomus fasciculatum) alone and in combination under organic field conditions in order to evaluate their potential in controlling root rot and wilt. Combined inoculation of P. monteilii with G. fasciculatum significantly increased plant height, plant spread, and number of branches; reduced disease incidence; and increased tuber dry mass of C. forskohlii, compared to vermicompost controls not receiving any bioinoculants. Increase in tuber yields was accompanied by an increase in plant N, P, and K uptake. Co-inoculation of P. monteilii with G. fasciculatum significantly improved the percent AM root colonization and spore numbers retrieved from soil. This suggests P. monteilii to be a mycorrhiza helper bacterium which could be useful in organic agriculture. The forskolin content of tubers was significantly increased by the inoculation treatments of P. monteilii, G. fasciculatum, and P. monteilii + G. fasciculatum.

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References

  • Ames RN, Reid CPP, Ingham ER (1984) Rhizospheric bacterial population response to root colonization by a vesicular–arbuscular mycorrhizal fungus. New Phytol 96:555–563

    Article  Google Scholar 

  • Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Darokar MP, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130

    Article  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Bansal M, Mukerjii KG (1994) Positive correlation between VAM-induced changes in root exudation and mycorrhizal mycoflora. Mycorrhiza 5:39–44

    Article  Google Scholar 

  • Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bomfante P, O'Gara F, Azcón-Aguilar C (1998) Impact on arbuscular mycorrhizal function formation of Pseudomonas strains used as inoculants for the biocontrol of soil-borne plant pathogens. Appl Environ Microbiol 64:2304–2307

    PubMed  CAS  Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (2005) Interaction between mycorrhizal fungi and bacteria to improve plant nutrient cycling and soil structure. In: Buscot F, Varma S (eds) Microorganism in soils: roles in genesis and functions. Springer, Heidelberg, pp 351–371

    Google Scholar 

  • Bharadwaj DP, Alström S, Lundquist P-O (2011) Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions. Mycorrhiza. doi:10.1007/s00572-011-0418-7

  • Boby BU, Bagyaraj DJ (2003) Biological control of root-rot of Coleus forskohlii Briq. using microbial inoculants. World J Microbiol Biotechnol 19:175–180

    Article  CAS  Google Scholar 

  • Chachaty E, Saulnier P (2000) Isolating chromosomal DNA from bacteria. In: Rapley R (ed) The nucleic acid protocols handbook, vol 1. Humana, Totowa, pp 29–32

    Chapter  Google Scholar 

  • Coelho Netto RA, Assis LAG (2002) Coleus barbatus: Um Novo Hospedeiro De Ralstonia solanacearum. Fitopatol Brasil 27:266

    Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka AE (2005) Use of plant growth promoting bacteria for biocontrol of plant diseases: principles, mechanism of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  PubMed  CAS  Google Scholar 

  • Cook D, Sequeira L (1991) Genetic and biochemical characterization of a Pseudomonas solanacearum gene cluster required for extracellular polysaccharide production and for virulence. J Bacteriol 173:1654–1662

    PubMed  CAS  Google Scholar 

  • De Souza NJ, Dohandwalla AN, Rupp RH (eds) (1986) Forskolin: its chemical, biological and medical potential. Hoechst India Limited, Bombay, p 77

    Google Scholar 

  • Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13:85–91

    Article  PubMed  CAS  Google Scholar 

  • Edwards SG, Young JPW, Fitter AH (1998) Interactions between Pseudomonas fluorescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol Lett 166:297–303

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Brit Mycol Soc 46:235–246

    Article  Google Scholar 

  • Gianinazzi S, Huchette O, Gianinazzi-Pearson V (2008) New outlooks in mycorrhiza applications. In: Baar J, Estaun V, Ortas I, Orfanoudakis M, Alifragis D (eds) Proceedings of the COST870meeting “Mycorrhiza application in sustainable agriculture and natural systems”, 17–19 September 2008. Thessaloniki, Greece, pp 20–22

  • Gianinazzi S, Gollotte A, Binet M-N, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Harrier AL, Watson AC (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic/or other sustainable farming system. Pest Manag Sci 60:149–157

    Article  PubMed  CAS  Google Scholar 

  • Hemashenpagam N, Selvaraj T (2011) Effect of arbuscular mycorrhizal (AM) fungus and plant growth promoting rhizomicroorganisms (PGPR’s) on medicinal plant Solanum viarum seedlings. J Environ Biol 32:579–583

    PubMed  CAS  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice Hall of India, New Delhi

    Google Scholar 

  • Johansson PM, Johansson L, Gerhardson B (2003) Suppression of wheat-seedlings disease caused by Fusarium culmorum and Microdochium nivale using bacterial seed treatment. Plant Pathol 52:219–227

    Article  Google Scholar 

  • Kalra A, Chandra M, Awasthi A, Singh AK, Khanuja SPS (2010) Natural compound enhancing growth and survival of rhizobial inoculants in vermicompost-based formulation. Biol Fertil Soil 46:521–524

    Article  Google Scholar 

  • Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587

    Article  PubMed  CAS  Google Scholar 

  • Kataoka R, Futai K (2009) A new mycorrhizal helper bacterium, Ralstonia species, in the ectomycorrhizal symbiosis between Pinus thunbergii and Suillus granulates. Biol Fertil Soils 45:315–320

    Article  Google Scholar 

  • Kavitha C, Rajamani K, Vadivel E (2010) Coleus forskohlii: a comprehensive review on morphology, phytochemistry and pharmacological aspects. J Med Plants Res 4:278–285

    CAS  Google Scholar 

  • Kelman A (1954) The relationship of pathogenicity in Pseudomonas solanacearum to colony appearance on a tetrazolium medium. Phytopathology 44:693–695

    Google Scholar 

  • Khatun S, Chatterjee NC (2011) Glomus fasciculatum in defense responses to fusarial wilt of Coleus forskohlii. Acta Agr Scand B–Pl Sc 61:136–142

    CAS  Google Scholar 

  • Khatun S, Chatterjee NC, Cakilcioglu U (2011) The strategies for production of forskolin vis-a-vis protection against soil borne diseases of the potential herb Coleus forskohlii Briq. Europ J Med Pl 1:1–9

    Google Scholar 

  • King EO, Ward MK, Raney DE (1954) A simple media for the demonstration of pyocyanin and fluorescein. J Laborat Clinl Med 44:301–307

    CAS  Google Scholar 

  • Kloepper JW (1996) Host specificity in microbe-microbe interactions. Bioscience 46:406–409

    Article  Google Scholar 

  • Krishnaraj PU, Sreenivasa MN (1992) Increased root colonization by bacteria due to inoculation of vesicular arbuscular mycorrhiza fungus in chilli (Capsicum annuum). Zentral Mikrobiol 147:131–133

    Google Scholar 

  • Liu RJ, Luo XS (1994) A new method to quantify the inoculums potential of arbuscular mycorrhizal fungi. New Phytol 128:89–92

    Article  Google Scholar 

  • Liu R, Dai M, Wu X, Li M, Liu X (2012) Suppression of the root-knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood] on tomato by dual inoculation with arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Mycorrhiza. doi:10.1007/s00572-011-0397-8

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 11:495–501

    Article  Google Scholar 

  • Mohan V, Verma N (1996) Interaction of VA mycorrhizal fungi and rhizosphere microflora of forest tree species in arid and semi arid regions. Proceedings of IUFRO. In: An impact of diseases and insect pests in tropical forests, pp 222–223

  • Naik PR, Raman G, Narayanan KB, Sakthivel N (2008) Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiol 8:230. doi:10.1186/1471-2180-8-230

    Article  PubMed  Google Scholar 

  • Nash SM, Snyder WC (1962) Quantitative estimations by plate counts of propagules of the bean root-rot Fusarium in field soils. Phytopathologist 52:567–572

    Google Scholar 

  • Nautiyal CS (1997) Selection of chick pea rhizosphere competent Pseudomonas fluorescens NBR 11303 antagonistic to Fusarium oxysporum f. sp. ciceris, Rhizoctonia bataticola, Pythium spp. Curr Microbiol 35:52–58

    Article  CAS  Google Scholar 

  • Pal KK, Gardener BM (2006) Biological control of plant pathogens. Plant Health Instruct 1–25

  • Pandey R, Kalra A (2010) Inhibitory effects of vermicompost produced from agro-waste of medicinal and aromatic plants on egg hatching in Meloidogyne incognita (Kofoid and White) Chitwood. Curr Sci 98:833–835

    Google Scholar 

  • Prashanthi SK, Kulkarni S, Srenivasa MN, Kulkarni S (1997) Integrated management of root–rot disease of safflower caused by Rhizoctonia bataticola. Environ Ecol 15:800–802

    Google Scholar 

  • Ramesh R, Joshi AA, Ghanekar MP (2009) Pseudomonads: major antagonistic endophytic bacteria to suppress bacterial wilt pathogen, Ralstonia solanacearum in the egg plants (Solanum melongena L.). World J Microbiol Biotechnol 25:47–55

    Article  Google Scholar 

  • Rani A, Souche YS, Goel R (2009) Comparative assessment of in situ bioremediation potential of cadmium resistant acidophilic Pseudomonas putida 62BN and alkalophilic Pseudomonas monteilii 97AN strains on soybean. Int Biodet Biodeg 63:62–66

    Article  CAS  Google Scholar 

  • Sailo GL, Bagyaraj DJ (2005) Influence of different AM-fungi on the growth, nutrition and forskolin content of Coleus forskohlii. Mycol Res 109:795–798

    Article  PubMed  CAS  Google Scholar 

  • Sampangi RK, Bagyaraj DJ (1989) Root diseases and mycorrhizae. J Phytol Res 2:1–6

    Google Scholar 

  • Sarvanakumar D, Lavanya N, Muthumeena K, Raguchander T, Samiyappan R (2009) Fluorescent pseudomonads mixtures mediate disease resistance in rice plants against sheath rot (Sarocladium oryzae) disease. BioControl 54:273–286

    Article  Google Scholar 

  • Sastry MSR, Sharma AK, Johri BN (2000) Effect of an AM fungal consortium and Pseudomonas on the growth and nutrient uptake of Eucalyptus hybrid. Mycorrhiza 10:55–61

    Article  Google Scholar 

  • Schaneberg BT, Khan IA (2003) Quantitative analysis of forskolin in Coleus forskohlii (Lamiaceae) by reversed phase liquid chromatography. J AOAC Internat 86:467–470

    CAS  Google Scholar 

  • Seamon KB (1984) Forskolin and adenylate cyclase, new opportunities in drug design. Ann Rep Med Chem 19:293–302

    Article  CAS  Google Scholar 

  • Shah V, Bhat SV, Bajwa BS, Domacur H, De Souza NJ (1980) The occurrence of forskolin in Labiatae. Plant Med 39:183–185

    Article  CAS  Google Scholar 

  • Shivkumar BS, Manjunath R, Chandrashekhar ANS, Suresh CK (2006) Biocontrol of Fusarium infected Coleus using enriched compost. J Med Arom Plant Sci 28:589–592

    Google Scholar 

  • Shyla M (1998) Etiology and management of root rot of Coleus forskohlii. M.Sc. Thesis, University of Agricultural Sciences, Bangalore

  • Singh R, Paramaeswarn TN, Prakasa Rao EVS, Puttanna K, Kalra A, Srinivas KVNS, Bagyaraj DJ, Divya S (2009) Effect of arbuscular mycorrhizal fungi and Pseudomonas fluorescens on root-rot/wilt, growth and yield of Coleus forskohlii. Biocontrol Sci Technol 19:835–841

    Article  Google Scholar 

  • Singh R, Gangwar SP, Singh D, Singh R, Pandey R, Kalra A (2011) Medicinal plant Coleus forskohlii Briq.: disease and management (mini review). Med Plants 3:1–7

    Google Scholar 

  • Singh R, Soni SK, Awasthi A, Kalra A (2012) Evaluation of vermicompost doses for management of root rot disease complex in Coleus forskohlii under organic field conditions. Australasian Plant Pathol. doi:10.1007/s13313-012-0134-6

  • Snedecor GW, Cochran WG (1989) Statistical methods, 8th edn. Iowa State University Press, Ames

    Google Scholar 

  • Srinath J, Bagyaraj DJ, Satyanarayana BN (2003) Enhanced growth and nutrition of micropropagated Ficus benjamina to Glomus mosseae co-inoculated with Trichoderma harzianum and Bacillus coagulans. World J Microbiol Biotechnol 19:69–72

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Vanitha SC, Niranjana SR, Mortensen CN, Umesha S (2009) Bacterial wilt of tomato in Kranataka and its management by Pseudomonas fluorescens. BioControl 54(5):685–695. doi:10.1007/s10526-009-9217-x

    Article  Google Scholar 

  • Weller DM (1988) Biological control of soil borne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:398–407

    Article  Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  Google Scholar 

  • Wood J, Scott KP, Avgustin G, Newbold CJ, Flint HJ (1998) Estimation of the relative abundance of different Bacteroides and Prevotella ribotypes in gut samples by restriction enzyme profiling of PCR-amplified 16S rRNA gene sequences. Appl Environ Microbiol 64:3683–3689

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the National Medicinal Plants Board, New Delhi for providing financial support; the Council of Scientific and Industrial Research (CSIR), New Delhi, India for providing facilities; and Dr. K.V.N.S. Srinivas (Phyto-chemist, CIMAP, Research Centre, Hyderabad, India) for forskolin estimation; scientist-in-charge, CIMAP Research Centre, Bangalore; and Director, CSIR-Central Institute of Medicinal and Aromatic Plants, Lucknow, India, for encouragement and facilities.

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Correspondence to Alok Kalra.

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Singh, R., Soni, S.K. & Kalra, A. Synergy between Glomus fasciculatum and a beneficial Pseudomonas in reducing root diseases and improving yield and forskolin content in Coleus forskohlii Briq. under organic field conditions. Mycorrhiza 23, 35–44 (2013). https://doi.org/10.1007/s00572-012-0447-x

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