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Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.)

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Abstract

A greenhouse experiment was conducted to examine the effects of inoculation with two Methylobacterium oryzae strains (CBMB20 and CBMB110) and a consortium of three arbuscular mycorrhizal (AM) fungi on the growth of red pepper (Capsicum annum L.). Inoculation of red pepper plants with the M. oryzae strains resulted in a significant increase in root length and root fresh weight compared to untreated control plants. The combined inoculation of M. oryzae strains and AM fungi significantly increased various plant growth parameters and chlorophyll content compared to uninoculated controls. Mycorrhizal colonisation and the number of AM fungal spores were higher in co-inoculation treatments. In addition, the combined inoculation of M. oryzae strains and AM fungi resulted in significantly higher nitrogen (N) accumulation in the roots and shoots of red pepper plants compared to uninoculated controls. The combined inoculation of M. oryzae strain CBMB110 and AM fungi increased the phosphorus (P) content by 23.3% compared to untreated controls. The micronutrient content of the red pepper plants also increased in most of the inoculation treatments. A perfect mutualism among CBMB100-AMF was found which was attributed to the improved macro- and micronutrient uptake along with higher chlorophyll content in red pepper. Further research on in-depth understanding of the co-operative microbial interactions will facilitate the successful application of Methylobacterium-AM fungi products in biotechnology.

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References

  • Alarcón A, Davies FT Jr, Egilla JN, Fox TC, Estrada-Luna AA, Ferrera-Cerrato R (2002) Short term effects of Glomus claroideum and Azospirillum brasilense on growth and root acid phosphatase activity of Carica papaya L. under phosphorus stress. Microbiologia 44:31–37

    Google Scholar 

  • Antunes V, Cardoso EJBM (1991) Growth and nutrient status of citrus plants as influenced by mycorrhiza and phosphorus application. Plant Soil 131:11–19

    CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  CAS  PubMed  Google Scholar 

  • Azcon R (1987) Germination and hyphal growth of Glomus mosseae in vitro: effect of rhizosphere bacteria and cell-free culture media. Soil Biol Biochem 19:417–419

    Article  Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Ant Van Leeuwen 81:343–351

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G (1998) Proposal for the division of plant growth promoting rhizobacteria into two classification: biocontrol-PGPB (Plant growth promoting bacteria) & PGPB. Soil Biol Biochem 30:1225–1228

    Article  CAS  Google Scholar 

  • Bianciotto V, Bonfante P (2002) Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric and endocellular bacteria. Ant Van Leeuwen 81:365–371

    Article  CAS  Google Scholar 

  • Boby VU, Balakrishna AN, Bagyaraj DJ (2008) Interaction between Glomus mosseae and soil yeasts on growth and nutrition of cowpea. Microbiol Res 163:693–700

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2000) Possible role of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Deka Boruah HP, Rabha BK, Saikia N, Dileep Kumar BS (2003) Fluorescent Pseudomonas influences palisade mesophyll development and spatial root development in Phaseolus vulgaris. Plant Soil 256:291–301

    Article  CAS  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190

    Article  CAS  PubMed  Google Scholar 

  • Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132

    Google Scholar 

  • Frey-Klett P, Pierrat JC, Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas Fir. Appl Environ Microbiol 63:139–144

    CAS  PubMed  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 endone species extracted from soil by wet sieving and decanting. Trans Brit Mycol Soc 46:235–244

    Article  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extracellular PRPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

  • He X, Nara K (2007) Element biofortification: can mycorrhizas potentially offer a more effective and sustainable pathway to curb human malnutrition? Trends Plant Sci 12:331–333

    Article  CAS  PubMed  Google Scholar 

  • Hebbern CA, Pedas P, Schjoerring JK, Knudsen L, Husted S (2005) Genotypic differences in manganese efficiency: a field trial with winter barley (Hordeum vulgare L.). Plant Soil 272:233–244

    Article  CAS  Google Scholar 

  • Hock B, Varma A (1995) Mycorrhiza structure, function, molecular biology and biotechnology. Springer, Berlin

    Google Scholar 

  • Kothari SK, Marschner H, Romhbeld V (1990) Direct and indirect effects of VA mycorrhiza and rhizosphere microorganisms on mineral nutrient acquisition by maize (Zea mays L.) in a calcareous soil. New Phytol 116:637–645

    Article  CAS  Google Scholar 

  • Kucey RM, Paul EA (1982) Carbon flow, photosynthesis and N2 fixation in mycorrhizal and odulated faba beans (Vicia faba. L.). Soil Biol Biochem 14:407–412

    Article  Google Scholar 

  • Kumar B, Trivedi P, Pandey A (2007) Pseudomonas corrugata: A suitable bioinoculant for maize grown under rainfed conditions of Himalayan region. Soil Biol Biochem 39:3093–3100

    Article  CAS  Google Scholar 

  • Madhaiyan M, Kim BY, Poonguzhali S, Kwon SW, Song MH, Ryu JH, Go SJ, Koo BS, Sa TM (2007) Methylobacterium oryzae sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, ACC deaminase producing bacterium isolated from field grown rice (Oryza sativa L. cv Nam-Pyeoung). Int J Syst Evol Microbiol 57:326–331

    Article  CAS  PubMed  Google Scholar 

  • Manjula G, Pfeffer PE, Hairu J, Jehad A, Douds DD, Allen JW, Buching H, Peter JL, Yair SH (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 453:819–823

    Google Scholar 

  • Medina A, Probanza A, Manero FJG, Azcon R (2003) Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol 22:15–28

    Article  Google Scholar 

  • Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol. Biochem 18:191–196

    Article  Google Scholar 

  • Nautiyal CS, Mehta S, Singh HB (2006) Biological control and plant-growth promotion by Bacillus strains from milk. J Microbiol Biotechnol 16:184–192

    Google Scholar 

  • Ortas I, Ortakci D, Kaya Z, Cinar A, Onelge N (2002) Mycorrhizal dependency of sour orange in relation to phosphorus and zinc nutrition. J Plant Nutr 25:1263–1279

    Article  CAS  Google Scholar 

  • Pedas P, Ytting CK, Fuglsanag AT, Jahn PT, Schjoerring JK, Husted S (2008) Manganese efficiency in Barley: identification and characterization of the metal ion transport HvIRT11[OA]. Plant Phy 148:455–466

    Article  CAS  Google Scholar 

  • Poonguzhali S, Madhaiyan M, Thangaraju M, Ryu JH, Chung KY, Sa TM (2005) Effects of co-cultures, containing N-fixer and P-solubilizer, on the growth and yield of Pearl millet (Pennisetum glaucum (L.) R. Br.) and Blackgram (Vigna mungo L.). J Microbiol Biotechnol 15:903–908

    CAS  Google Scholar 

  • Poonguzhali S, Madhaiyan M, Sa TM (2008) Isolation and identification of phosphate solubilizing bacteria from chinese cabbage and their effect on growth and phosphorus utilization of plants. J Microbiol Biotechnol 18:773–777

    CAS  PubMed  Google Scholar 

  • Raushch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470

    Article  Google Scholar 

  • Roseti D, Gaur R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M (2006) Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungiand plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biol Bioche 38:1111–1120

    Article  CAS  Google Scholar 

  • Ryu JH, Madhaiyan M, Poonguzhali S, Yim WJ, Indiragandhi P, Kim KA, Anandham R, Yun JC, Sa TM (2006) Plant growth substances produced by Methylobacterium spp. and their effect on the growth of tomato (Lycopersicon esculentum L.) and red pepper (Capsicum annuum L.). J Microbiol Biotechnol 16:1622–1628

    CAS  Google Scholar 

  • SAS Institute Inc (2004) SAS user's guide, version 9.1. SAS Institute Inc, Cary

    Google Scholar 

  • Sen R, Nurmiaho-Lassila K, Haahtela K, Korhonen K (1996) Specificity and mode of primary attachment of Pseudomonas fluorescens strains to the cell walls of ectomycorrhizal fungi. In: Azcón-Aguilar C, Barea JM (eds) Mycorrhizas in integrated systems: from genes to plant development. ECSC-EC-EAEC, Brussels

    Google Scholar 

  • Schmidt W, Tittel J, Schikora A (2000) Role of hormone in induction of iron deficiency responses in Arabidopsis roots. Plant Phy 122:1109–1118

    Article  CAS  Google Scholar 

  • Shaharoona B, Jamro GM, Zahiri ZA, Arshad M, Memon KS (2007) Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.). J Microbiol Biotechnol 17:1300–1307

    CAS  PubMed  Google Scholar 

  • Weller DM (1988) Biological control of soil borne plant pathogens in the rhizosphere with bacteria. Ann Rev Phytopathol 26:379–407

    Article  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial support form Korea Research Foundation (KRF), Brain Korea (BK21) and Rural Development Administration (RDA), Republic of Korea, is duly acknowledged.

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Authors and Affiliations

  1. Department of Agricultural Chemistry, Chungbuk National University, Cheongju, Chungbuk, 361-763, Republic of Korea

    Kyounga Kim, Woojong Yim, Pankaj Trivedi, Munusamy Madhaiyan, Hari P. Deka Boruah, Md. Rashedul Islam, Gillseung Lee & Tongmin Sa

  2. Korea Science & Engineering Foundation, 180-1 Gajeong-dong, Yuseong-gu, Deajeon, 305-350, Korea

    Gillseung Lee

Authors
  1. Kyounga Kim
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  2. Woojong Yim
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  3. Pankaj Trivedi
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  4. Munusamy Madhaiyan
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  5. Hari P. Deka Boruah
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  6. Md. Rashedul Islam
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  7. Gillseung Lee
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  8. Tongmin Sa
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Correspondence to Tongmin Sa.

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Responsible Editor: Peter A.H. Bakker.

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Kim, K., Yim, W., Trivedi, P. et al. Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.). Plant Soil 327, 429–440 (2010). https://doi.org/10.1007/s11104-009-0072-4

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  • DOI: https://doi.org/10.1007/s11104-009-0072-4

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