Interaction between the plant growth-promoting fungus Phoma sp. GS8-2 and the arbuscular mycorrhizal fungus Glomus mosseae: Impact on biocontrol of soil-borne diseases, microbial population, and plant growth

Australasian Plant Pathology

Volumn 41, Issue 3, 2012, Pages 271-281

  Saldajeno, Mary Grace B ^a   Ito, Masanori ^a   Hyakumachi, Mitsuro ^a  

^a GIFU UNIVERSITY   (Japan)

Author keywords

Biocontrol; Disease severity; Plant growth enhancement; Root colonization; Soil borne pathogens

Indexed keywords

AGROSTIS; ARBUSCULAR; BACTERIA (MICROORGANISMS); CUCUMIS SATIVUS; FUNGI; FUSARIUM OXYSPORUM; GLOMUS MOSSEAE; LYCOPERSICON ESCULENTUM; PHOMA; THANATEPHORUS CUCUMERIS;

EID: 84863205258     PISSN: 08153191     EISSN: 14486032     Source Type: Journal    
DOI: 10.1007/s13313-011-0101-7     Document Type: Article

References (64)

1. 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
2. Azcón-Aguilar C, Jaizme-Vega M, Calvet C (2002) The contribution of arbuscularmycorrhizal fungi to control of soil-borne plant pathogens. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture: from genes to bioproducts. Birkhäuser Verlag, Basel, pp 187-197
3. Brundrett MC, Piché Y, Peterson RL (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can J Bot 62: 2128-2134
4. 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: 1-6 (Pubitemid 24408655)
5. Castro-Sowinski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of co-inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276: 1-11 (Pubitemid 47620451)
6. Chandanie WA, Kubota M, Hyakumachi M (2005) Interaction between arbuscular mycorrhizal fungus Glomus mosseae and plant growth promoting fungus Phoma sp. on their root colonization and growth promotion of cucumber. Mycoscience 46: 201-204 (Pubitemid 40865712)
7. Chandanie WA, Kubota M, Hyakumachi M (2006) Interactions between plant growth promoting fungi and arbuscular mycorrhizal fungus Glomus mosseae and induction of systemic resistance to anthracnose disease in cucumber. Plant Soil 286: 209-217 (Pubitemid 44411097)
8. Chandanie WA, Kubota M, Hyakumachi M (2009) Interactions between the arbuscular mycorrhizal fungus Glomus mosseae and plant growth promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). App Soil Ecol 41: 336-341
9. Datnoff LE, Nemec S, Pernezny K (1995) Biological control of Fusarium crown and root rot of tomato in Florida using Trichoderma harzianum and Glomus intraradices. Biol Control 5: 427-431
10. De Boer M, Bom P, Kindt F, Keurentjes JJB, van der Sluis I, van Loon LC, Bakker PAHM (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93: 626-632 (Pubitemid 36516868)
11. Défago G, Keel C (1995) Pseudomonads as biocontrol agents of diseases caused by soil-borne pathogens. In: Hokkanen HMT, Lynch JM (eds) Biological control: benefits and risks. University Press, Cambridge, pp 230-257
12. Edwards SG, Young JPW, Fitter AH (1998) Interactions between Pseudomonas flourescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol Lett 166: 297-303 (Pubitemid 128384174)
13. Fernández N, Patiño B, Vázquez C (1993) Pectin degrading enzymes secreted by six isolates of Fusarium oxysporum. Mycol Res 97: 461-466
14. Filion M, St-Arnaud M, Jabaji-Hare SH (2003) Quantification of Fusarium solani f. sp. phaseoli in mycorrhizal bean plants and surrounding mycorrhizosphere soil using real-time polymerase chain reaction and direct isolations on selective media. Phytopathology 93: 229-235 (Pubitemid 36108587)
15. Fracchia S, García-Romera I, Godeas A, Ocampo JA (2000) Effect of the saprophytic fungus Fusarium oxysporum on arbuscular mycorrhizal colonization and growth of plants in greenhouse and field trials. Plant Soil 223: 175-184
16. Garcia-Romera I, Garcia-Garrido JM, Martin J, Fracchia S, Mujica MT, Godeas A, Ocampo JA (1998) Interaction between saprophytic Fusarium strains and arbuscular mycorrhizas of soybean plants. Symbiosis 24: 235-246 (Pubitemid 28259533)
17. Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. App Environ Microbiol 65: 1428-1434 (Pubitemid 29173666)
18. Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91: 621-627 (Pubitemid 32665205)
19. Haggag WM, Abd-El latif FM (2001) Interaction between vesicular arbuscular mycorrhizae and antagonistic biocontrol microorganisms on controlling root rot disease incidence of geranium plants. Online J Biological Sci 1: 1147-1153
20. Haggag WM, Nofal MA (2006) Improving the biological control of Botryodiplodia disease on some Annona cultivars using single or multi-biogents in Egypt. Biological Cont 38: 341-349 (Pubitemid 44163823)
21. Hale MG, Moore LD (1979) Factors affecting root exudation II: 1970-1978. In: Brady NC (ed) Advances in agronomy, vol 31, Academic Press. Inc, New York, pp 93-124
22. Hart MM, Reader RJ (2002) Does percent root len gth colonization and soil hyphal length reflect the extent of colonization for all AMF? Mycorrhiza 12: 297-301 (Pubitemid 36087217)
23. Horinouchi H, Muslim A, Suzuki T, Hyakumachi M (2007) Fusarium equiseti GF191 as an effective biocontrol agent against Fusarium crown and root rot of tomato in rock wool systems. Crop Prot 26: 1514-1523 (Pubitemid 47379991)
24. Hyakumachi M (1994) Plant growth promoting fungi from turfgrass rhizosphere with potential for disease suppression. Soil Microorg 44: 53-68
25. Hyakumachi M, Kubota M (2004) Fungi as plant growth promoter and disease suppressor. In: Arora DK (ed) Fungal biotechnology in agricultural, food, and environmental applications, vol 21. Marcel Dekker, New York, pp 101-110
26. Jeffries P, Barea JM (2001) Arbuscular mycorrhiza: a key component of sustainable plant-soil ecocsystems. In: Hock B (ed) The Mycota: Vol IX: fungal associations. Springer, Berlin, pp 95-113
27. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37: 1-16 (Pubitemid 36260702)
28. Khaosaad T, García-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systematically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39: 727-734 (Pubitemid 44909227)
29. Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke N (2001) Induction of systemic resistance in cucumber against several diseases by plant growth promoting fungi: lignification and superoxide generation. Eur J Plant Pathol 107: 523-533 (Pubitemid 32763515)
30. Komada H (1975) Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Rev Plant Prot Res 8: 114-124
31. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78: 366-371
32. Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28: 23-36 (Pubitemid 39588385)
33. Marschner P, Crowley DE, Higashi RM (1997) Root exudation and physiological status of a root-colonizing fluorescent pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.). Plant Soil 189: 11-20 (Pubitemid 27236361)
34. Martin JP (1950) Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Sci 69: 215-232
35. Martinez A, Obertello M, Pardo A, Ocampo JA, Godeas A (2004) Interactions between Trichoderma pseudokoningii strains and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Mycorrhiza 14: 79-84 (Pubitemid 38641593)
36. Martínez-Medina A, Pascual JA, Lloret E, Roldán A (2009) Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedling nurseries. J Sci Food Agric 89: 1843-1850
37. Martínez-Medina A, Roldán A, Pascual JA (2011) Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: growth response and Fusarium wilt biocontrol. App Soil Ecol 47: 98-105
38. McAllister CB, Garcia-Garrido JM, García-Romera I, Godeas A, Ocampo JA (1997) Interaction between Alternaria alternata or Fusarium equiseti and Glomus mosseae and its effects on plant growth. Biol Fert Soil 24: 301-305
39. 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 115: 495-501
40. Meera MS, Shivanna MB, Kageyama K, Hyakumachi M (1994) Plant growth promoting fungi from zoysiagrass rhizosphere as potential inducers of systemic resistance in cucumbers. Phytopathology 84: 1399-1406
41. Meera MS, Shivanna MB, Kageyama K, Hyakumachi M (1995a) Persistence of induced systemic resistance in cucumber in relation to root colonization by plant growth promoting fungal isolates. Crop Prot 14: 123-130
42. Meera MS, Shivanna MB, Kageyama K, Hyakumachi M (1995b) Responses of cucumber cultivars to induction of systemic resistance against anthracnose by plant growth promoting fungi. Eur J Plant Pathol 101: 421-430
43. Müller AK, Westergaard K, Christensen S, Sørensen SJ (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol 36: 11-19 (Pubitemid 32476855)
44. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S ribosomal RNA. Appl Environ Microbiol 59: 695-700 (Pubitemid 23072343)
45. Norman JR, Hooker JE (2000) Sporulation of Phytophthora fragariae shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol Res 104: 1069-1073
46. Ozgonen H, Erkilic A (2007) Growth enhancement and Phytophthora blight (Phytophthora capsici Leonian) control by arbuscular mycorrhizal fungal inoculation in pepper. Crop Prot 26: 1682-1688 (Pubitemid 47488545)
47. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhizal-induced resistance. Curr Opinion Plant Biol 10: 393-398
48. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón- Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53: 525-534 (Pubitemid 34196683)
49. Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik J (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Heidelberg, pp 193-208
50. Raupach GS, Kloepper JW (1998) Mixtures of plant growthpromoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88: 1158-1164 (Pubitemid 28496950)
51. Ravnskov S, Jensen B, Knudsen IMB, Bøker L, Jensen DF, Karli?ski L, Larsen J (2006) Soil inoculation with the biocontrol agent Clonostachys rosea and the mycorrhizal fungus Glomus intraradices results in mutual inhibition, plant growth promotion and alteration of soil microbial communities. Soil Biol Biochem 38: 3453-3462 (Pubitemid 44573291)
52. Roberts DP, Lohrke SM, Meyer SLF, Buyer JS, Bowers JH, Baker CJ, Li W, de Souza JT, Lewis JA, Chung S (2005) Biocontrol agents applied individually and in combination for suppression of soilborne diseases of cucumber. Crop Prot 24: 141-155 (Pubitemid 40256931)
53. Rousseau A, Benhamou N, Chet I, Piché Y (1996) Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86: 434-443 (Pubitemid 126629964)
54. Saldajeno MGB, Hyakumachi M (2011) The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae stimulate plant growth and reduce severity of anthracnose and damping-off diseases in cucumber (Cucumis sativus L.) seedlings. Ann Appl Biol 159: 28-40
55. Scheffknecht S, Mammerler R, Steinkellner S, Vierheilig H (2006) Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Mycorrhiza 16: 365-370 (Pubitemid 44078604)
56. Shivanna MB, Meera MS, Kageyama K, Hyakumachi M (1996) Growth promotion ability of zoysiagrass rhizosphere fungi in consecutive plantings of wheat and soybean. Mycoscience 37: 163-168 (Pubitemid 27015373)
57. Shivanna MB, Meera MS, Kubota M, Hyakumachi M (2005) Promotion of growth and yield in cucumber by zoysiagrass rhizosphere fungi. Microbes Environ 20: 34-40
58. Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant- Microbe Interact 13: 238-241
59. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, Great Britain
60. Toyota K, Kitamura M, Kimura M (1995) Suppression of Fusarium oxysporum f. sp. raphani PEG-4 in soil following colonization by other Fusarium spp. Soil Biol Biochem 27: 41-46 (Pubitemid 26446908)
61. Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104: 927-936
62. Vázquez MM, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15: 261-272
63. Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82: 1166-1176 (Pubitemid 39501021)
64. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82: 1198-1227 (Pubitemid 39501024)