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Application of Arbuscular Mycorrhizal Fungi in Production of Annual Oilseed Crops

  • Mahaveer P. SharmaEmail author
  • Sushil K. Sharma
  • R. D. Prasad
  • Kamal K. Pal
  • Rinku Dey
Chapter
Part of the Soil Biology book series (SOILBIOL, volume 41)

Abstract

Nutrient mining through removal by crops, soil erosion and leaching is a major challenge for sustaining the productivity of oilseeds. Besides external application of fertilisers, a major contribution of nitrogen for legumes is addressed by nitrogen-fixing bio-inoculants. In the scenario of climate change, efforts should also be made to identify climate-resilient microbes to address the issue in the future. Within the constraints of available resources, a large number of plant growth-promoting microorganisms including AM fungi have been identified and found to enhance growth and yield of many oilseed crops. However, effective strains tolerant to abiotic stresses like salinity, high temperature and moisture-deficit stress are scanty. The quality inoculum production of AM fungi and its application in oilseeds have been discussed with consideration of the soil edaphic factors for identifying potential AM fungi and their management for higher oilseed crop yields yet maintaining the agroecosystem sustainability.

Keywords

Root Colonisation Mycorrhizal Colonisation Oilseed Crop Root Pathogen Preceding Crop 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are thankful to the Director of ICAR-Directorate of Soybean Research, Indore, India, for his kind support during the compiling of this task. Authors are also thankful to Prof Hamel Chantal, Agriculture and Agri-Food Canada, for making critical comments and suggestions on this review chapter.

References

  1. Abbott LK, Robson AD (1991) Factors influencing the occurrence of vesicular-arbuscular mycorrhizas. Agric Ecosyst Environ 35:121–150Google Scholar
  2. Abdalla ME, Abdel-Fattah GM (2000) Influence of the endomycorrhizal fungus Glomus mosseae on the development of peanut pod rot disease in Egypt. Mycorrhiza 10:29–35Google Scholar
  3. Abdel-Fattah GM, Shabanam YM (2002) Efficacy of the arbuscular mycorrhizal fungus Glomus clarum in protection of cowpea plants against root rot pathogen Rhizoctonia solani. J Plant Dis Prot 109:207–215Google Scholar
  4. Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12PubMedGoogle Scholar
  5. Adewole MB, Awotoye OO, Ohiembor MO, Salami AO (2010) Influence of mycorrhizal fungi on phytoremediating potential and yield of sunflower in Cd and Pb polluted soils. J Agric Sci 55:17–28Google Scholar
  6. Adholeya A, Tiwari P, Singh R (2005) Large-scale production of arbuscular mycorrhizal fungi on root organs and inoculation strategies. In: Declerck S, Strullu DG, Fortin JA (eds) In vitro culture of mycorrhizas. Springer, Heidelberg, pp 315–338Google Scholar
  7. Agricultural Statistics at a Glance (2004) Agricultural Statistics Division, Directorate of Economics & Statistics, Department of Agriculture & Cooperation Ministry of Agriculture, Government of India, India, p 221Google Scholar
  8. AICRPS (2009) Annual progress report, All India coordinated research project on soybean (2009-10). Directorate of Soybean Research (ICAR), Indore, p 251Google Scholar
  9. Al-Karaki GN, Al-Raddad A, Clark RB (1998) Water stress and mycorrhizal isolate effects on growth and nutrient acquisition of wheat. J Plant Nutr 21:891–902Google Scholar
  10. Al-Khaliel AS (2010) Effect of salinity stress on mycorrhizal association and growth response of peanut infected by Glomus mosseae. Plant Soil Environ 56:318–324Google Scholar
  11. An ZQ, Grove JH, Hendrix JW, Hershman DE, Henson GT (1990) Vertical distribution of endogonaceous mycorrhizal fungi associated with soybean, as affected by soil fumigation. Soil Biol Biochem 22:715–719Google Scholar
  12. Anil-Prakash, Vandana T (2002) Exploiting mycorrhiza for oilseed crop production. In: Rajak RC (ed) Biotechnology of microbes and sustainable utilization pages. Scientific Publishers, India, p 370Google Scholar
  13. Antunes PM, Rajcan I, Goss MJ (2006) Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max L.) Merr. Soil Biol Biochem 38:533–543Google Scholar
  14. Artursson V, Finlay RD, Jansson JK (2005) Combined bromodeoxyuridine immunocapture and terminal restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol 7:1952–1966PubMedGoogle Scholar
  15. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10PubMedGoogle Scholar
  16. Aryal UK, Shah SK, Xu HL, Fujita M (2006) Growth, nodulation and mycorrhizal colonization in Bean plants improved by rhizobial inoculation with organic and chemical fertilization. J Sustain Agric 29:71–83Google Scholar
  17. Auge RM, Sylvia DM, Park S, Buttery BR, Saxton AM, Moore JL, Cho KH (2004) Partitioning mycorrhizal influence on water relations of Phaseolus vulgaris into soil and plant components. Can J Bot 82:503–514Google Scholar
  18. Awotoye OO, Adewole MB, Salami AO, Ohiembor MO (2009) Arbuscular mycorrhiza contribution to the growth performance and heavy metal uptake of Helianthus annuus L. in pot culture. J Environ Sci Technol 3:157–163Google Scholar
  19. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570PubMedGoogle Scholar
  20. Bagayoko M, Buerkert A, Lung G, Bationo A, Romheld V (2000) Cereal/legume rotation effects on cereal growth in Sudano-Sahelian West Africa: soil mineral nitrogen, mycorrhizae and nematodes. Plant Soil 218:103–116Google Scholar
  21. Barea JM, Andrade G, Bianciotto VV, Dowling D, Lohrke S, Bonfante P (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl Environ Microbiol 64:2304–2307PubMedCentralPubMedGoogle Scholar
  22. Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778PubMedGoogle Scholar
  23. Becard G, Piche Y (1992) Establishment of AM in root organ cultures review and proposed methodology. In: Norris J, Read D, Verma A (eds) Techniques for the study of mycorrhiza. Academic, New York, pp 89–108Google Scholar
  24. Bethlenflavay GJ, Schreiner RP, Mihara KL (1997) Mycorrhizal fungi effects on nutrient composition and yield of soybean seeds. J Plant Nutr 20:521–529Google Scholar
  25. Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010PubMedCentralPubMedGoogle Scholar
  26. Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological N fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11Google Scholar
  27. Budi SW, Van Tuinen D, Martinotti G, Gianinazzi S (1999) Isolation from Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soil-borne fungal pathogens. Appl Environ Microbiol 65:5148–5150PubMedCentralPubMedGoogle Scholar
  28. Calvet C, Pera J, Barea JM (1993) Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviride and Pythium ultimum in a peat-perlite mixture. Plant Soil 148:1–6Google Scholar
  29. Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosyst Environ 116:72–84Google Scholar
  30. Caris C, Hördt W, Hawkins H, Römheld V, George E (1998) Studies of iron transport by arbuscular mycorrhizal hyphae from soil to peanut and sorghum plants. Mycorrhiza 8:35–39Google Scholar
  31. Carling DE, Roncadori RW, Hussey RS (1995) Interactions of arbuscular mycorrhizae, Meloidogyne arenaria and phosphorus fertilization on peanut. Mycorrhiza 6:9–13Google Scholar
  32. Caron M, Fortin JA, Richard C (1986) Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can J Plant Pathol 8:12–16Google Scholar
  33. Chandrashekara CP, Patil VC, Sreenivasa MN (1995) VA-mycorrhiza mediated P effect on growth and yield of sunflower (Helianthus annuus L.) at different P levels. Plant Soil 176:325–328Google Scholar
  34. Clark RB, Zeto SK (1996) Iron acquisition by mycorrhizal maize grown on alkaline soil. J Plant Nutr 19:247–264Google Scholar
  35. Colozzi A, Cardoso EJBN (2000) Detecção de fungos micorrízicos arbusculares em raízes de cafeeiro e de crotalária cultivada na entrelinha. Pesqui Agropecu Bras 35:2033–2042Google Scholar
  36. Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonization patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced diseases in mycorrhizal tomato. Plant Soil 185:223–232Google Scholar
  37. Cranenbrouck S, Voets L, Bivort C (2005) Methodologies for InVitro cultivation of AM fungi with root organs. In: Declerck S, Strullu DG, Fortin A (eds) In Vitro culture of mycorrhizas. Springer, Berlin, pp 342–375Google Scholar
  38. Dalpé Y, de Souza FA, Declerck S (2005) Life cycle of Glomus species in monoxenic culture. In: Declerck S, Fortin JA, Strullu DG (eds) Dans: biology of arbuscular mycorrhizal fungi under in vitro culture. Springer, Germany, pp 49–71Google Scholar
  39. Damodaram T, Hegde DM (2010) Oilseeds situation: a statistical compendium 2010. Directorate of Oilseeds Research, Hyderabad, p 486Google Scholar
  40. Daniell T, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36:203–209PubMedGoogle Scholar
  41. Davis RM, Menge JA (1980) Influence of Glomus fasciculatus and soil phosphorus on Phytophthora root rot of citrus. Phytolopathology 7:447–452Google Scholar
  42. Dehne HW (1982) Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72:1114–1119Google Scholar
  43. Del Val C, Barea JM, Azcon-Aguilar C (1999) Assessing the tolerance of heavy metals of arbuscular mycorrhizal fungi isolated from sewage-sludge contaminated soils. Appl Soil Ecol 11:261–269Google Scholar
  44. Dev A, Gour RK, Jain RK, Bisen PS, Sengupta LK (1997) Effect of vesicular arbuscular mycorrhiza-Rhizobium inoculation interaction on heavy metal (Cu, Zn and Fe) uptake in soybean (Glycine max, var. JS-335) under variable P doses. Int J Tropic Agric 15:75–79Google Scholar
  45. Devi MC, Reddy MN (2002) Phenolic acid metabolism of groundnut (Arachis hypogaea L.) plants inoculated with VAM fungus and Rhizobium. Plant Growth Regul 37:151–156Google Scholar
  46. Diedhiou PM, Hallmann J, Oerke EC, Dehne HW (2003) Effects of arbuscular mycorrhizal fungi and a non-pathogenic Fusarium oxysporum on Meloidogyne incognita infestation of tomato. Mycorrhiza 13:199–204PubMedGoogle Scholar
  47. Doley K, Jite PK (2013a) Effect of arbuscular mycorrhizal fungi on growth of groundnut and disease caused by Macrophomina phaseolina. J Exp Sci 4:11–15Google Scholar
  48. Doley K, Jite PK (2013b) Disease management and biochemical changes in groundnut inoculated with Glomus fasciculatum and pathogenic Macrophomina phaseolina (Tassi) Goid. Plant Sci Feed 3:21–26Google Scholar
  49. Douds DD Jr (2002) Increased spore production by Glomus intraradices in the split-plate monoxenic culture system by repeated harvest, gel replacement, and re-supply of glucose to the mycorrhiza. Mycorrhiza 12:163–167PubMedGoogle Scholar
  50. Douds DD Jr, Nagahashi G, Pfeffer PE, Kayser WM, Reider C (2005) On-farm production and utilization of arbuscular mycorrhizal fungus inoculum. Can J Plant Sci 85:15–21Google Scholar
  51. Douds DD Jr, Nagahashi G, Pfeffer PE, Reider C, Kayser WM (2006) On-farm production of AM fungus inoculum in mixtures of compost and vermiculite. Bioresour Technol 97:809–818PubMedGoogle Scholar
  52. Dugassa GD, Vonalten H, Schnbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L infected by fungal pathogens. Plant Soil 185:173–182Google Scholar
  53. 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 116:297–303Google Scholar
  54. El-Azouni IM, Hussein Y, Shaaban LD (2008) The associative effect of VA mycorrhizae with Bradyrhizobium as biofertilizers on growth and nutrient uptake of Arachis hypogaea. Res J Agric Biol Sci 4:187–197Google Scholar
  55. Elsen A, Declerck S, De Waele D (2001) Effects of Glomus intraradices on the reproduction of the burrowing nematode Radopholus similis in dixenic culture. Mycorrhiza 11:49–51Google Scholar
  56. Elsheikh EAE, Mohamedzein EMM (1998) Effect of Bradyrhizobium, VA mycorrhiza and fertilisers on seed composition of groundnut. Ann Appl Biol 132:325–330Google Scholar
  57. Estaun V, Camprubi A, Joner EJ (2002) Selecting arbuscular mycorrhizal fungi for field application. In: Gianinazzi S, Schueep H, Barea JM, Haselwandter K (eds) Mycorrhiza technology in agriculture: from genes to bioproducts. Birkhauser, Basel, pp 249–259Google Scholar
  58. Fontem DA, Iroume RN, Aloleko F (1996) Effet de la résistance variétale et des traitements fongicides sur la cercosporiose de l’arachide. Cahier Agric 5:33–38Google Scholar
  59. Fortin JA, Becard G, Declerck S, Dalpe Y, St Arnaud M, Coughlan AP, Piche Y (2002) Arbuscular mycorrhiza on root-organ cultures. Can J Bot 80:1–20Google Scholar
  60. Garnett T, Conn V, Kaiser B (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283PubMedGoogle Scholar
  61. Gaur A, Adholeya A (2000) Effects of the particle size of soil-less substrates upon AM fungus inoculum production. Mycorrhiza 10:43–48Google Scholar
  62. Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122PubMedGoogle Scholar
  63. Gonçalves EJ, Muchojev JJ, Muchojev RMC (1991) Effect of kind and method of fungicidal seed treatment of bean seed on infections by VA-mycorrhizal fungus Glomus macrocarpum and by the pathogenic fungus Fusarium solani. I. Fungal and plant parameters. Plant Soil 132:41–46Google Scholar
  64. Grichar VJ, Bosweel TE (1987) Comparison of lorsban and tilt with terrachlor for control of southern blight on peanut. The Texas Agriculture Experiment Station, PR-4534Google Scholar
  65. Groth DE, Martinson CA (1983) Increased endomycorrhizal colonization of maize and soybeans after soil treatment with metalaxyl. Plant Dis 67:1377–1378Google Scholar
  66. Gupta R, Krishnamurthy KV (1996) Response of mycorrhizal and nonmycorrhizal Arachis hypogaea to NaCl and acid stress. Mycorrhiza 6:145–149Google Scholar
  67. Habte M, Zhang YC, Schmitt DP (1999) Effectiveness of Glomus species in protecting white clover against nematode damage. Can J Bot 77:135–139Google Scholar
  68. Hamel C, Strullu DG (2006) Arbuscular mycorrhizal fungi in field crop production: potential and new direction. Can J Plant Sci 86:941–950Google Scholar
  69. Harinikumar DM, Bagyaraj DJ (1988) Effect of crop rotation on native vesicular-arbuscular mycorrhizal propagules in soil. Plant Soil 110:77–80Google Scholar
  70. Harinikumar KM, Bagyaraj D (1989) Effect of cropping sequence, fertilizers and farmyard manure on vesicular-arbuscular mycorrhizal fungi in different crops over three consecutive seasons. Biol Fertil Soils 7:173–175Google Scholar
  71. Harrier LA, Watson CA (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag Sci 60:149–157PubMedGoogle Scholar
  72. Hart MM, Reader RJ, Klironomos JN (2001) Life strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93:1186–1194Google Scholar
  73. Heinzemann J, Weritz J (1990) Rockwoola new carrier system for mass multiplication of vesicular-arbuscular mycorrhizal fungi. Angew Bot 64:271–274Google Scholar
  74. Hildebrandt U, Janetta K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919–1924PubMedCentralPubMedGoogle Scholar
  75. Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. University of California, College of Agriculture, Agriculture Experiment Station Circular 347, BerkeleyGoogle Scholar
  76. Ijdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21(1):1–16PubMedGoogle Scholar
  77. Ilbas AI, Sahin S (2005) Glomus fasciculatum inoculation improves soybean production. Acta Agric Scand Sect B Soil Plant Sci 55:287–292Google Scholar
  78. Iyer RM, Bhat N, Madhusudhanan K (2003) Effect of organic amendments on growth and colonization of Glomus fasciculatum native to oil palm. Int J Oil Palm Res 3(4):65–67Google Scholar
  79. Jackson RM, Mason PA (1984) Mycorrhiza. Edward Arnold, London, p 60. ISBN 0-7131-2876-3Google Scholar
  80. Jalaluddin M, Hamid M, Muhammad SE (2008) Selection and application of a AM-fungus for promoting growth and resistance to charcoal rot disease of sunflower var. Helico-250. Pak J Bot 40:1313–1318Google Scholar
  81. Jamal A, Ayub N, Usman M, Khan AG (2002) Arbuscular mycorrhizal fungi enhance zinc and nickel uptake from contaminated soil by soya bean and lentil. Int J Phytoremed 4:205–221Google Scholar
  82. Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AM fungi communities as affected by tillage in a temperate soil. Mycorrhiza 12(5):225–234PubMedGoogle Scholar
  83. Jansa J, Hans-Rudolf O, Egli S (2009) Environmental determinants of the arbuscular mycorrhizal fungal infectivity of Swiss agricultural soils. Eur J Soil Biol 45:400–440Google Scholar
  84. Jarstfer AG, Sylvia DM (1992) Inoculum production and inoculation strategies for vesicular-arbuscular mycorrhizal fungi. In: Meting B (ed) Soil microbial ecology; application in agriculture and environmental management. Marcel Dekker, New York, pp 349–377Google Scholar
  85. Jarstfer AG, Sylvia DM (1995) Aeroponic culture of AM fungi. In: Varma A, Hock B (eds) Mycorrhiza structure, function, molecular biology and biotechnology. Springer, Heidelberg, pp 521–559Google Scholar
  86. Johnson NC, Copeland PJ, Crookston RK, Pfleger FL (1992) Mycorrhizae: possible explanations for yield decline with continuous corn and soybean. Agron J 84:387–390Google Scholar
  87. Kabir Z (2005) Tillage or no-tillage: impact on mycorrhizae. Can J Plant Sci 85:23–29Google Scholar
  88. Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM utilization through reduced P fertilization II Field studies. Plant Soil 231:65–79Google Scholar
  89. Karagiannidis N, Bletsos F, Stavropoulos N (2002) Effect of Verticillium wilt (Verticillium dahlia Kieb.) and mycorrhizae (Glomus mosseae) on root colonization, growth and nutrient in tomato and eggplant seedlings. Sci Hortic 94:145–156Google Scholar
  90. Karasawa T, Kasahara Y, Takebe M (2001) Variable response of growth and arbuscular mycorrhizal colonization of maize plants to preceding crops in various types of soils. Biol Fertil Soils 33:286–293Google Scholar
  91. Kellam MK, Schenck NC (1980) Interaction between a vesicular-arbuscular mycorrhizal fungus and root knot nematode on soybean. Phytopathology 72:293–296Google Scholar
  92. Kennedy AC, Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant and Soil 170:75–86Google Scholar
  93. Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207PubMedGoogle Scholar
  94. Kjoller R, Rosendahl S (2000) Effects of fungicides in arbuscular mycorrhizal fungi: differential responses in alkaline phosphatases activity of external and internal hyphae. Biol Fertil Soils 31:361–365Google Scholar
  95. Kling M, Jakobsen I (1997) Direct application of carbendazim and propiconazole at field rates to the external mycelium of three arbuscular mycorrhizal fungi species: effect on 32P transport and succinate dehydrogenase activity. Mycorrhiza 7:33–37Google Scholar
  96. Kothari SK, Marschner H, Romheld V (1991) Effect of vesicular arbuscular fungus and rhizosphere microorganisms on manganese reduction in the rhizosphere and manganese concentration in maize (Zea mays L.). New Phytol 117:649–655Google Scholar
  97. Krishna KR, Bagyaraj DJ (1982) Influence of vesicular-arbuscular mycorrhiza on growth and nutrition of Arachis hypogaea L. Legume Res 5:18–22Google Scholar
  98. Kucey RMN, Bonetti R (1988) Effect of vesicular-arbuscular mycorrhizal fungi and captan on growth and N2-fixation by Rhizobium-inoculated field beans. Can J Soil Sci 68:143–149Google Scholar
  99. Kuszala C, Gianinazzi S, Gianinazzi-Pearson V (2001) Storage conditions for the long-term survival of AM fungal propagules in wet sieved soil fractions. Symbiosis 30:287–299Google Scholar
  100. Lee YJ, George E (2005) Development of a nutrient film technique culture system for arbuscular mycorrhizal plants. Hortic Sci 40:378–380Google Scholar
  101. Lekberg Y, Koide RT (2005) Arbuscular mycorrhizal fungi, rhizobia, available soil P and nodulation of groundnut (Arachis hypogaea) in Zimbabwe. Agric Ecosyst Environ 110:143–148Google Scholar
  102. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153Google Scholar
  103. Linderman RG (1994) Role of AM fungi in biocontrol. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS Press, St. Paul, pp 1–26Google Scholar
  104. Lisette J, Xavier C, Germida JJ (2003) Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 37:261–267Google Scholar
  105. Liu A, Plenchette C, Hamel C (2007) Soil nutrient and water providers: how arbuscular mycorrhizal mycelia support plant performance in a resource limited world. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production. Haworth Food & Agricultural Products Press, Binghamton, pp 37–66Google Scholar
  106. Mäder P, Edenhofer S, Boller T, Wiemken A, Niggli U (2000) Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol Fertil Soils 31:150–156Google Scholar
  107. Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697PubMedGoogle Scholar
  108. Mahanta D, Rai RK (2008) Effects of sources of phosphorus and biofertilizers on productivity and profitability of soybean (Glycine max)–wheat (Triticum aestivum) system. Indian J Agron 53:279–284Google Scholar
  109. Malcova R, Vosatka M, Gryndler M (2003) Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaries L. Appl Soil Ecol 23:55–67Google Scholar
  110. Mallesha BC, Bagyaraj DJ, Pai G (1992) Perlite-soilrite mix as a carrier for mycorrhiza and rhizobia to inoculate Leucaena leucocephala. Leucaena Res Rep 13:32–33Google Scholar
  111. Mandhare VK, Kalbhor HB, Patil PL (1995) Effects of VA-Mycorrhiza, Rhizobium and phosphorus on summer groundnut. J Maharashtra Agric Univ 20:261–262Google Scholar
  112. Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur J Soil Biol 46:151–156Google Scholar
  113. Mansfeld-Giese K, Larsen J, Bodker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140PubMedGoogle Scholar
  114. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  115. Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445Google Scholar
  116. Martensson AM, Carlegren K (1994) Impact of phosphorus fertilization on VAM diaspores in two Swedish long-term field experiments. Agric Ecosyst Environ 47:327–334Google Scholar
  117. Mathur N, Vyas A (2000) Influence of arbuscular mycorrhizae on biomass production, nutrient uptake and physiological changes in Ziziphus mauritiana Lam. under water stress. J Arid Environ 45:191–195Google Scholar
  118. Matsubara Y, Ohba N, Fukui H (2001) Effect of arbuscular mycorrhizal fungus infection on the incidence of fusarium root rot in asparagus seedlings. J Jpn Soc Hortic Sci 70:202–206Google Scholar
  119. Mayo K, Davis RE, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78:426–431Google Scholar
  120. McGonigle TP, Miller MH (1993) Mycorrhizal development and phosphorus absorption in maize under conventional and reduced tillage. Soil Sci Soc Am J 57:1002–1006Google Scholar
  121. Meghvansia MK, Prasad K, Harwani D, Mahna SK (2008) Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi and Bradyrhizobium japonicum in the alluvial soil. Eur J Soil Biol 44:316–323Google Scholar
  122. Menendez AB, Scervino JM, Godeas AM (2001) Arbuscular mycorrhizal populations associated with natural and cultivated vegetation on a site of Buenos Aires province, Argentina. Biol Fertil Soils 33:373–381Google Scholar
  123. Menge JA, Steirle D, Bagyaraj DJ, Johnson ELV, Leonard RT (1978) Phosphorus concentrations in plants responsible for inhibition of mycorrhizal infection. New Phytol 80:575–578Google Scholar
  124. Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesiculararbuscular fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol Biochem 18:185–190Google Scholar
  125. Mirzakhani M, Ardakani MR, Band AA, Rejali F, Shirani Rad AH (2009) Response of spring safflower to co-inoculation with Azotobacter chroococum and Glomus intraradices under different levels of nitrogen and phosphorus. Am J Agric Biol Sci 4:255–261Google Scholar
  126. Mosse B (1962) The establishment of AM fungi under aseptic conditions. J Gen Microbiol 27:509–520PubMedGoogle Scholar
  127. Mosse B, Thompson JP (1984) Vesicular-arbuscular endomycorrhizal inoculum production. I. Exploratory experiments with beans (Phaseolus vulgaris) in nutrient flow culture. Can J Bot 62:1523–1530Google Scholar
  128. Mostafavian SR, Pirdashti H, Ramzanpour MR, Andarkhor AA, Shahsavari A (2008) Effects of mycorrhizae, Thiobacillus and sulphur nutrition on the chemical composition of soybean. Pak J Biol Sci 11:826–835PubMedGoogle Scholar
  129. Mulligan MF, Smucker AJM, Safir GF (1985) Tillage modifications of dry edible bean root colonization by AM fungi. Agron J 77:140–144Google Scholar
  130. Murillo-Williams A, Pedersen P (2008) Arbuscular mycorrhizal colonization response to three seed-applied fungicides. Agron J 100:795–800Google Scholar
  131. Nogueira MA, Magelhaes GC, Cardoso EJBN (2004) Manganese toxicity in mycorrhizal and phosphorus-fertilized soybean plants. J Plant Nutr 27:141–156Google Scholar
  132. Oehl F, Sieverding E, Ineichen K, Mader P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824PubMedCentralPubMedGoogle Scholar
  133. Osunde AO, Bala A, Gwam MS, Tsado PA, Sanginga N, Okugun JA (2003) Residual benefits of promiscuous soybean to maize (Zea mays L.) grown on farmers’ fields around Minna in the southern Guinea savanna zone of Nigeria. Agric Ecosyst Environ 100:209–220Google Scholar
  134. Ozgonen H, Akgul DS, Erkilic A (2010) The effects of arbuscular mycorrhizal fungi on yield and stem rot caused by Sclerotium rolfsii Sacc. in peanut. Afr J Agric Res 5:128–132Google Scholar
  135. Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant and Soil 141(13–39):1992Google Scholar
  136. Pinochet J, Calvet C, Camprubí A, Fernandez C (1996) Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops. Plant Soil 185:183–190Google Scholar
  137. Powell JR, Gulden RH, Hart MM, Campbell RG, Levy-Booth DJ, Dunfield KE, Pauls KP, Swanton CJ, Trevors JT, Klironomos JN (2007) Mycorrhizal and rhizobial colonization of genetically modified and conventional soybeans. Appl Environ Microbiol 73:4365–4367PubMedCentralPubMedGoogle Scholar
  138. Powell JR, Campbell RG, Dunfield KE, Gulden RH, Hart MM, Levy-Booth DJ, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Antunes PM (2009) Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobium japonicum, and genetically modified soybean. Appl Soil Ecol 41:128–136Google Scholar
  139. Pozo MJ, Azcon-Aguilar C, Dumas-Gaudot E, Barea JM (1999) β-1,3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141:149–157Google Scholar
  140. Price NS, Roncadori RW, Hussey RS (1995) The growth of nematode tolerant and intolerant soybeans as affected by phosphorus, Glomus intraradices and light. Plant Pathol 44:597–603Google Scholar
  141. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715Google Scholar
  142. Quilambo OA (2002) Minimising the effects of drought stress on growth of two peanut cultivars, using arbuscular mycorrhiza (AM) inoculants. J Trop Microbiol Biotechnol 1:22–28Google Scholar
  143. Raju PS, Clark RB, Ellis JR, Maranville JW (1990) Effects of species of VA-mycorrhizal fungi on growth and mineral uptake of sorghum at different temperatures. Plant Soil 121:165–170Google Scholar
  144. Redecker D, Thierfelder H, Werner D (1995) A new cultivation system for arbuscular-mycorrhizal fungi on glass beads. Angew Bot 69:189–191Google Scholar
  145. Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339Google Scholar
  146. Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363Google Scholar
  147. Rodriguez-Kabana R, Curl EA (1980) Non-target effects of pesticides on soilborne pathogens and disease. Annu Rev Phytopathol 18:311–332Google Scholar
  148. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317PubMedGoogle Scholar
  149. Saito M, Marumoto T (2002) Inoculation with arbuscular mycorrhizal fungi: the status quo in Japan and the future prospects. Plant Soil 244:273–279Google Scholar
  150. Sanchez L, Weidmann S, Brechenmacher L, Batoux M, van Tuinen D, Lemanceau P (2004) Common gene expression in Medicago truncatula roots in response to Pseudomonas fluorescens colonization, mycorrhiza development and nodulation. New Phytol 161:855–863Google Scholar
  151. Sanginga N, Carsky RJ, Dashiell K (1999) Arbuscular mycorrhizal fungi respond to rhizobial inoculation and cropping systems in farmers’ fields in the Guinea savanna. Biol Fertil Soils 30:179–186Google Scholar
  152. Savary S (1991) Approche de la pathologie des cultures tropicales: I exemple de I arachide en Afrique de I Ouest. Karthala-Orstom, ParisGoogle Scholar
  153. Schreiner RP, Bethlenfalvay GJ (1997) Mycorrhizae, biocides, and biocontrol. 3. Effects of three different fungicides on developmental stages of three AM fungi. Biol Fertil Soils 24:18–26Google Scholar
  154. Scullion J, Eason WR, Scott EP (1998) The effectivity of arbuscular mycorrhizal fungi from high input conventional and organic grassland and grass-arable rotations. Plant Soil 204:243–254Google Scholar
  155. Shalaby AM, Hanna MM (2000) Interactions between VA mycorrhizal fungus Glomus mosseae, Bradyrhizobium japonicum and Pseudomonas syringae in soybean plants. Egypt J Microbiol 35:199–209Google Scholar
  156. Sharifia M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151Google Scholar
  157. Sharma MP, Adholeya A (2011) Developing prediction equations and optimizing production of three AM fungal inocula under on-farm conditions. Exp Agric 47:529–537Google Scholar
  158. Sharma MP, Sharma SK (2006) Arbuscular mycorrhizal fungi an emerging bio-inoculant for production of soybean. SOPA Digest III(IX):10–16Google Scholar
  159. Sharma MP, Sharma SK (2008) On-farm production of arbuscular mycorrhizal fungi. Biofertilizer Newslett 16:3–7Google Scholar
  160. Sharma MP, Sharma SK, Alok Dwivedi (2010) Liquid biofertilizer application in soybean and regulatory mechanisms. Agric Today April issue: 44–45Google Scholar
  161. Sharma MP, Gupta S, Sharma SK, Vyas AK (2012a) Effect of tillage and crop sequences on arbuscular mycorrhizal symbiosis and soil enzyme activities in soybean (Glycine max L. Merril) rhizosphere. Indian J Agric Sci 82:25–30Google Scholar
  162. Sharma MP, Jaisighani K, Sharma SK, Bhatia VS (2012b) Effect of native soybean rhizobia and AM fungi in the improvement of nodulation, growth, soil enzymes and physiological status of soybean under microcosm conditions. Agric Res 1:346–351Google Scholar
  163. Sieverding E (1991) Vesicular–arbuscular mycorrhiza management in tropical agrosystems. Deutsche Gesellschaft für Technische Zusammansabeit (GT2) GmbH. Eschbon, GermanyGoogle Scholar
  164. Singh AL, Chaudhari V (1996) Use of zincated and boronated superphosphates and mycorrhizae in groundnut grown on a calcareous soil. J Oilseeds Res 13:61–65Google Scholar
  165. Singh S, Basappa H, Singh SK (2006) Status and prospects of integrated pest management strategies in selected crops Oilseeds. In: Singh A, Sharma OP, Garg DK (eds) Integrated pest management principles and applications, vol 2. CBS Publishers and Distributors, New Delhi, p 656Google Scholar
  166. Smith S, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, LondonGoogle Scholar
  167. Sreenivasa MN, Bagyaraj DJ (1989) Use of pesticide for mass production of vesicular-arbuscular mycorrhizal inoculums. Plant Soil 119:127–132Google Scholar
  168. Srinivasulu Y, Lakshman HC (2002) Response of Guizotia abyssinica Cass. (Niger) and Linum usitattissimum (Linseed) to VA-mycorrhizal inoculation in an unsterile soil. Karnataka J Agric Sci 15:405–407Google Scholar
  169. Strullu DG, Romand C, Plenchette C (1991) Axenic culture and encapsulation of the intraradical forms of Glomus spp. World J Microbiol Biotechnol 7:292–297PubMedGoogle Scholar
  170. Sugavanam V, Udaiyan K, Manian S (1994) Effect of fungicides on vesicular-arbuscular mycorrhizal infection and nodulation in groundnut (Arachis hypogeae L.). Agric Ecosyst Environ 48:285–293Google Scholar
  171. Sulochana T, Manoharachary C (1989) Vesicular-arbuscular mycorrhizal associations of castor and safflower. Curr Sci 58:459–461Google Scholar
  172. Sylvia DM, Hubbell DH (1986) Growth and sporulation of vesicular-arbuscular mycorrhizal fungi in aeroponic and membrane systems. Symbiosis 1:259–267Google Scholar
  173. Sylvia DM, Neal LH (1990) Nitrogen affects the phosphorus response of VA mycorrhiza. New Phytol 115:303–310Google Scholar
  174. Tain CY, Feng G, Li XI, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148Google Scholar
  175. Taiwo LB, Adegbite AA (2001) Effect of arbuscular mycorrhiza and Bradyrhizobium inoculation on growth, N2 fixation and yield of promiscuously nodulating soybean (Glycine max). J Agric Res 2:110–118Google Scholar
  176. Tepfer D (1989) Ri t-DNA from Agrobacterium rhizogenes. A source of genes having applications in rhizosphere biology and plant development, ecology and evolution. In: Kosuge T, Nester EW (eds) Plant-microbe interactions, vol 3. McGraw-Hill, New York, pp 294–342Google Scholar
  177. Tester M, Smith SE, Smith FA (1987) The phenomenon of “nonmycorrhizal” plants. Can J Bot 65:419–431Google Scholar
  178. Thompson JP (1987) Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower. Aust J Agric Res 38:847–867Google Scholar
  179. Thompson JP (1996) Correction of dual phosphorus and zinc deficiencies of linseed (Linum usitatissimum L.) with cultures of vesicular–arbuscular mycorrhizal fungi. Soil Biol Biochem 28:941–951Google Scholar
  180. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677PubMedGoogle Scholar
  181. Tisdale SI, Nelson WI, Baton JD (1995) Soil fertility and fertilizers. Macmillan, New YorkGoogle Scholar
  182. Todd TC, Winkler HE, Wilson GWT (2001) Interaction of Heterodera glycines and Glomus mosseae on soybean. J Nematol 33:306–310PubMedCentralPubMedGoogle Scholar
  183. Toro M, Azcon R, Barea JM (1997) Improvement of arbuscular mycorrhizal development by inoculation with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63:4408–4412PubMedCentralPubMedGoogle Scholar
  184. Torres-Barragan A, Zavaleta-Mejia E, Gonzalez-Chavez C, Ferrera-Cerrato R (1996) The use of arbuscular mycorrhizae to control onion white rot (Sclerotium cepivorum Berk.) under field conditions. Mycorrhiza 6:253–258Google Scholar
  185. Trappe JM, Molina R, Castellano M (1984) Reactions of mycorrhizal fungi and mycorrhiza formation to pesticides. Annu Rev Phytopathol 22:331–359Google Scholar
  186. Troeh ZI, Loynachan TE (2003) Endomycorrhizal fungal survival in continuous corn, soybean, and fallow. Agron J 95:224–230Google Scholar
  187. Turk MA, Assaf TA, Hameed KM, Al-Tawaha AM (2006) Significance of mycorrhizae. World J Agric Sci 2:16–20Google Scholar
  188. Tylka GL, Hussey RS, Roncadori RW (1991) Interactions of vesicular-arbuscular mycorrhizal fungi, phosphorus, and Heterodera glycines on soybean. J Nematol 23:122–133PubMedCentralPubMedGoogle Scholar
  189. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72Google Scholar
  190. Vivekanandan M, Fixen PE (1991) Cropping system effects on mycorrhizal colonization, early growth and phosphorus uptake of corn. Soil Sci Soc Am J 55:136–140Google Scholar
  191. Waceke JW (2003) A short communication: response of Soybean to concomitant inoculation with Arbuscular Mycorrhizal fungi and Rhizobium. J Tropic Microbiol 2:35–39Google Scholar
  192. Walley FL, Germida JJ (1996) Failure to decontaminate Glomus clarum NT4 spores is due to spore wall-associated bacteria. Mycorrhiza 6:3–49Google Scholar
  193. Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181PubMedGoogle Scholar
  194. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedGoogle Scholar
  195. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227Google Scholar
  196. Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol Fertil Soils 31:249–253Google Scholar
  197. Wright SF, Starr JL, Paltineanu IC (1999) Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci Soc Am J 63:1825–1829Google Scholar
  198. Wu CG, Liu YS, Hung LL (1995) Spore development of Entrophospora kentinensis in an aeroponic system. Mycologia 87:582–587Google Scholar
  199. Wu SC, Cheung KC, Luo YM, Wong MH (2004) Metal accumulation by Brassica juncea sharing rhizosphere with Zea mays: effect of mycorrhizal and beneficial bacterial inoculation. In: Proceedings of the fifth international conference on environmental geochemistry in the tropics, Haiko, Hainan, China, Nanjing, PR China: Institute Soil Science, Chinese Academy of Science, p 72Google Scholar
  200. Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478Google Scholar
  201. Xie Z, Staehelin C, Vierheili H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T, Xie ZP (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of undulating and non-nodulating soybeans. Plant Physiol 108:1519–1525PubMedCentralPubMedGoogle Scholar
  202. Yao MK, Tweddell RJ, Desilets H (2002) Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micro-propagated potato plantlets and on the extent of disease caused by Rhizoctonia solani. Mycorrhiza 12:235–242PubMedGoogle Scholar
  203. Zachee A, Bekolo N, Bime, Dooh N, Yalen M, Godswill N (2008) Effect of mycorrhizal inoculum and urea fertilizer on diseases development and yield of groundnut crops (Arachis hypogaea L.). Afr J Biotechnol 7:2823–2827Google Scholar
  204. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedCentralPubMedGoogle Scholar
  205. Zambolim L, Schenck NC (1983) Reduction of the effects of pathogenic, root-infecting fungi on soybean by the mycorrhizal fungus, Glomus mosseae. Phytopathology 73:1402–1405Google Scholar
  206. Zhang F, Shen J, Li L, Liu X (2004) An overview of rhizosphere processes related with plant nutrition in major cropping systems in China. Plant Soil 260:89–99Google Scholar
  207. Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Mahaveer P. Sharma
    • 1
    Email author
  • Sushil K. Sharma
    • 2
  • R. D. Prasad
    • 3
  • Kamal K. Pal
    • 4
  • Rinku Dey
    • 4
  1. 1.Microbiology SectionICAR-Directorate of Soybean Research (ICAR-DSR)IndoreIndia
  2. 2.NAIMCCICAR-National Bureau of Agriculturally Important Microorganisms (ICAR-NBAIM)UPIndia
  3. 3.ICAR-Directorate of Oilseeds Research (ICAR-DOR)HyderabadIndia
  4. 4.ICAR-Directorate of Groundnut Research (ICAR-DGR)JunagadhIndia

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