Spore Associated Bacteria (SAB) of Arbuscular Mycorrhizal Fungi (AMF) and Plant Growth Promoting Rhizobacteria (PGPR) Increase Nutrient Uptake and Plant Growth Under Stress Conditions

다국어 초록 (Multilingual Abstract)

Microorganisms present in the rhizosphere soil plays a vital role in improving the plant growth and soil fertility. Many kinds of fertilizers including chemical and organic has been approached to improve the productivity. Though some of them showed significant improvement in yield, they failed to maintain the soil properties. Rather they negatively affected soil eventually, the land became unsuitable for agricultural. To overcome these problems, microorganisms have been used as effective alternative. For past few decades, plant growth promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) have been used as effective inoculants to enhance the plant growth and productivity. PGPR improves the plant growth and helps the plant to withstand biotic and abiotic stresses. AM fungi are known to colonize roots of plants and they increase the plant nutrient uptake. Spore associated bacteria (SAB) are attached to spore wall or hyphae and known to increase the AMF germination and root colonization but their mechanism of interaction is poorly known. Better understanding the interactions among AMF, SAB and PGPR are necessary to enhance the quality of inoculants as a biofertilizers. In this paper, current knowledge about the interactions between fungi and bacteria are reviewed and discussed about AMF spore associated bacteria.

목차 (Table of Contents)

• Introduction
• AMF and stress
• Interaction between AMF and plant root
• Spore Associated Bacteria (SAB)
• SAB role in mycorrhizosphere
• PGPR
• Combined inoculation of AMF, SAB and PGPR
• Conclusion
• References

참고문헌 (Reference)

1 Vivas, A., "Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity" 62 : 1523-1533, 2006

2 Tavares de Lima, A.S., "Triple inoculation with Bradyrhizobium, Glomus and Paenibacillus on cowpea (vigna unguiculata [L.] Walp.) development" 42 : 919-926, 2011

3 Zhang, H.X., "Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit" 19 : 765-768, 2001

4 Hildebrandt, U., "Towards growth of arbuscular mycorrhizal fungi independent of a plant host" 68 : 1919-1924, 2002

5 Cuartero, J., "Tomato and salinity" 78 : 83-125, 1999

6 Bhromsiri, C., "The effects of plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi on the growth, development and nutrient uptake of different vetiver ecotypes" 43 (43): 239-249, 2010

7 Merzaeva, O.V., "The Production of auxins by the endophytic bacteria of winter rye" 46 : 44-50, 2010

8 Paula, M.A., "Synergistic effects of vesicular-arbuscular mycorrhizal fungi and diazotrophic bacteria on nutrition and growth of sweet potato (Ipomoea batatas)" 14 : 61-66, 1992

9 Kim, K., "Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.)" 327 : 429-440, 2010

10 Liu, R., "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" 22 : 289-296, 2012

11 Tresner, H.D., "Sodium chloride tolerance of terrestrial fungi" 22 : 210-213, 1971

12 Parida, A.K., "Salt tolerance and salinity effects on plants: a review" 60 : 324-349, 2005

13 Khan, A.G., "Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation" 41 : 197-207, 2000

14 Zahran, H.H., "Rhizobium-legume symbiosis and nitrogen fixation under sever conditions and in an arid climate" 63 (63): 968-989, 1999

15 Zarei, M., "Responses of lentil to co-inoculation with phosphatesolubilizing rhizobial strains and arbuscular mycorrhizal fungi" 29 : 1509-1522, 2006

16 Bahrani, A., "Response of winter wheat to co-inoculation with Azotobacter and arbescular mycorrhizal fungi (AMF) under different sources of nitrogen fertilizer" 8 (8): 95-103, 2010

17 Abdel Rahman, S.S.A., "Response of three sweet basil cultivars to inoculation with Bacillus subtilis and arbuscular mycorrhizal fungi under salt stress conditions" 9 (9): 93-111, 2011

18 Meghvansi, M.K., "Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi and Bradyrhizobium japonicum in the alluvial soil" 44 : 316-323, 2008

19 Zubek, S., "Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria" 19 : 113-123, 2009

20 Cantrell, I.C., "Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity" 233 : 269-281, 2001

21 Aliasgharzadeh, N., "Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil" 11 : 119-122, 2001

22 Vivas, A., "Nickel-tolerant Brevibacillus brevis and arbuscular mycorrhizal fungus can reduce metal acquisition and nickel toxicity effects in plant growing in nickel supplemented soil" 38 : 2694-2704, 2006

23 Tester, M., "Na+ tolerance and Na+ transport in higher plants" 91 : 503-527, 2003

24 Peterson, R.L., "Mycorrhizas: Anatomy and Cell Biology" National Research Council of Canada 2004

25 Giri, B., "Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake" 14 : 307-312, 2004

26 Weissenhorn, I., "Mycorrhiza and salt tolerance of trees" 2002

27 Siddikee, M. A., "Isolation, Characterization, and Use for Plant Growth Promotion Under Salt Stress, of ACC Deaminase-Producing Halotolerant Bacteria Derived from Coastal Soil" 한국미생물·생명공학회 20 (20): 1577-1584, 2010

28 Cruz, A.F., "Isolation and analysis of bacteria associated with spores of Gigaspora margarita" 104 : 1711-1717, 2007

29 Poonguzhali, Selvaraj, "Isolation and Identification of Phosphate Solubilizing Bacteria from Chinese Cabbage and Their Effect on Growth and Phosphorus Utilization of Plants" 한국미생물·생명공학회 18 (18): 773-777, 2008

30 Levy, A., "Invasion of spores of the arbuscular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp" 69 : 6250-6256, 2003

31 Artursson, V., "Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth" 8 (8): 1-10, 2006

32 Edwards, S.G., "Interactions between Pseudomonas fluorescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus within the rhizosphere" 166 : 297-303, 1998

33 Bharadwaj, D.P., "Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions" 22 : 437-447, 2011

34 Rydlová, J., "Interaction of arbuscular mycorrhizal fungi and rhizobia: Effects on flax yield in spoil-bank clay" 174 : 128-134, 2011

35 McMillen, B.G., "Inhibition of hyphal growth of a vesicular arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores" 30 (30): 1639-1646, 1998

36 Rabie, G.H., "Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater" 15 : 225-230, 2005

37 Azcon, R., "Influence of arbuscular mycorrhizae and phosphorus fertilization on growth, nodulation and N2 fixation (15N) in Medicago sativa at four salinity levels" 24 : 81-86, 1997

38 Vivas, A., "Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress" 13 : 249-256, 2003

39 Behn, O., "Influence of Pseudomonas fluorescens and arbuscular mycorrhiza on the growth, yield, quality and resistance of wheat infected with Gaeumannomyces graminis" 115 (115): 4-8, 2008

40 Feng, G., "Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots" 12 : 185-190, 2002

41 Horii, S., "Identification and function of Gigaspora margarita growth-promoting microorganisms" 41 : 135-141, 2006

42 Gallagher, J.L., "Halophytic crops for cultivation at seawater salinity" 89 : 323-336, 1985

43 Chabot, R., "Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar, phaseoli" 184 : 311-321, 1996

44 Pfeiffer, C.M., "Growth and nutrition of guayule (Parthenium argentatum) in a saline soil as influenced by vesicular-arbuscular mycorrhiza and phosphorus fertilization" 108 : 315-321, 1988

45 Kloepper, J.W., "Free-living bacterial inocula for enhancing crop productivity" 7 : 39-43, 1989

46 Anandham, R., "Evaluation of shelf life and rock phosphate solubilization of Burkholderia sp. in nutrient-amended clay, rice bran and rock phosphatebased granular formulation" 23 : 1121-1129, 2007

47 Ma, J.H., "Ethylene inhibitors enhance in vitro root formation from apple shoot cultures" 17 : 211-214, 1998

48 Siddikee, M.A., "Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity" 49 : 427-434, 2011

49 Adesemoye, A.O., "Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system" 54 : 876-886, 2008

50 Chen, B. C., "Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings" 147 : 374-380, 2007

51 Wu, S. C., "Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea" 140 : 124-135, 2006

52 Cekic, F.O., "Effects of arbuscular mycorrhizal inoculation on biochemical parameters in Capsicum annuum grown under long term salt stress" 36 : 63-72, 2012

53 Jaizme-Vega, M.C., "Effect of the combined inoculation of arbuscular mycorrhizal fungi and plant- growth promoting rhizobacteria on papaya (Carica papaya L.) infected with the root-knot nematode Meloidogyne incognita" 61 : 1-7, 2006

54 Al-Khaliel, A.S., "Effect of salinity stress on mycorrhizal association and growth response of peanut infected by Glomus mosseae" 56 : 318-324, 2010

55 Sandhya, V., "Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress" 62 : 21-30, 2010

56 Gryndler, M., "Effect of dual inoculation with arbuscular mycorrhizal fungi and bacteria on growth and mineral nutrition of strawberry" 25 (25): 1341-1358, 2002

57 사동민, "Effect of co-inoculation of methylotrophic Methylobacterium oryzae with Azospirillum brasilense and Burkholderia pyrrocinia on the growth and nutrient uptake of tomato, red pepper and rice" KLUWER ACADEMIC PUBL 328 : 71-82, 201003

58 Bisht, R., "Effect of arbuscular mycorrhizal fungi, Pseudomonas fluorescens and Rhizobium leguminosarum on the growth and nutrient status of Dalbergia sissoo Roxb" 50 (50): 231-242, 2009

59 Abdel Latef, A.A.H., "Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress" 127 : 228-233, 2011

60 Sastry, M. S. R., "Effect of an AM fungal consortium and Pseudomonas on the growth and nutrient uptake of Eucalyptus hybrid" 10 : 55-61, 2000

61 Alexander, T., "Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L" 110 : 363-370, 1988

62 Brundrett, M., "Diversity and classification of mycorrhizal associations" 79 : 473-495, 2004

63 Tian, C.Y., "Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants" 26 : 143-148, 2004

64 Bianciotto, V., "Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae" 66 : 4503-4509, 2000

65 Rai, M.K., "Current advances in mycorrhization in micropropagation" 37 : 158-167, 2001

66 Jastrow, J.D., "Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie" 30 (30): 905-916, 1998

67 Miransari, M., "Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress" 12 : 563-569, 2009

68 Zahir, Z.A., "Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil" 47 : 457-465, 2011

69 Mahajan, S., "Cold, salinity and drought stresses: An overview" 444 : 139-158, 2005

70 Tajini, F., "Co-inoculation with Glomus intraradices and Rhizobium tropici CIAT899 increases P use efficiency for N2 fixation in the common bean (Phaseolus vulgaris L.) under P deficiency in hydroaeroponic culture" 53 : 123-129, 2011

71 Joseph, B., "Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.)" 2 : 141-152, 2007

72 Bianciotto, V., "Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria" 193 : 123-131, 1996

73 Bago, B., "Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi" 139 : 375-388, 1998

74 Akkopru, A., "Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria" 153 : 544-550, 2005

75 Li, B., "Biocontrol of Pythium damping-off in cucumber by arbuscular mycorrhizaassociated bacteria from the genus Paenibacillus" 52 : 863-875, 2007

76 Mansfeld-Giese, K., "Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices" 41 : 133-140, 2002

77 González-Chávez, M.C.A., "Bacteria associated with the extraradical mycelium of an arbuscular mycorrhizal fungus in an As/Cu polluted soil" 42 : 1-10, 2008

78 Roesti, D., "Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum" 71 : 6673-6679, 2005

79 Xavier, L.J.C., "Bacteria associated with Glomus clarum spores influence mycorrhizal activity" 35 : 471-478, 2003

80 Kumar, P., "Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens" 167 : 493-499, 2012

81 Toljander, J.F., "Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species" 254 : 34-40, 2005

82 Levy, A., "Association between Burkholderia species and arbuscular mycorrhizal fungus spores in soils" 41 : 1757-1759, 2009

83 Evelin, H., "Arbuscular mycorrhizal fungi in alleviation of salt stress: a review" 104 : 1263-1280, 2009

84 Cruz, A.F., "Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soilborne plant pathogens" 1 : 2011

85 Bharadwaj, D.P., "Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens" 40 : 2494-2501, 2008

86 Marulanda, A., "An indigenous drought-tolerant strain of Glomus intraradices associated with a native bacterium improves water transport and root development in Retama sphaerocarpa" 52 : 670-678, 2006

87 Nautiyal, C.S., "An efficient microbiological growth medium for screening phosphate solubilizing microorganisms" 170 : 265-270, 1999

88 Wu, Q.S., "Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems" 56 (56): 470-475, 2010

89 Sannazzaro, A.I., "Alleviation of salt stress in Lotus glaber by Glomus intraradices" 285 : 279-287, 2006

90 Colla, G., "Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration" 44 : 501-509, 2008

91 Daei, G., "Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions" 166 : 617-625, 2009

92 Wright, S. F., "A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi" 198 : 97-107, 1998

93 Glick, B.R., "A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria" 190 : 63-68, 1998