Skip to main content
Log in

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

  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

The influence of the interaction between Phoma sp. GS8-2 (GS8-2) and the arbuscular mycorrhizal fungus Glomus mosseae (Gm) on the development of soil-borne diseases, microbial population, and plant growth in cucumber, bentgrass and tomato plants was investigated under controlled conditions. The composite inoculation of GS8-2 and Gm yielded varied effects on suppression of symptoms of soil-borne pathogens depending on the host-pathogen combination involved. The GS8-2 + Gm had neutral effect in reducing damping-off disease of cucumber caused by Rhizoctonia solani AG-4 and the crown and root rot disease of tomato caused by Fusarium oxysporum f. sp. radicis-lycopersici (Forl), but exacerbated the brown patch disease caused by R. solani AG2-2 in bentgrass. In tomato plants, Forl populations in the roots and rhizosphere were significantly reduced by GS8-2 + Gm. Results also show that the composite inoculation of GS8-2 and Gm resulted to a synergistic effect on the reduction of fungal and bacterial populations in roots and rhizosphere of the plants. Plant growth enhancement was due to the individual effect of GS8-2 or Gm but not their interaction. GS8-2 root colonization of cucumber and tomato plants decreased significantly in dual inoculated plants compared to plants inoculated with GS8-2 alone; while no significant differences were found in the Gm root colonization of the three plant species indicating that GS8-2 had no effect on Gm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig 2

Similar content being viewed by others

References

  • 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 

  • Azcón-Aguilar C, Jaizme-Vega M, Calvet C (2002) The contribution of arbuscular mycorrhizal 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

    Chapter  Google Scholar 

  • Brundrett MC, Piché Y, Peterson RL (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can J Bot 62:2128–2134

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fernández N, Patiño B, Vázquez C (1993) Pectin degrading enzymes secreted by six isolates of Fusarium oxysporum. Mycol Res 97:461–466

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91:621–627

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hyakumachi M (1994) Plant growth promoting fungi from turfgrass rhizosphere with potential for disease suppression. Soil Microorg 44:53–68

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Komada H (1975) Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Rev Plant Prot Res 8:114–124

    Google Scholar 

  • Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Martin JP (1950) Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Sci 69:215–232

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhizal-induced resistance. Curr Opinion Plant Biol 10:393–398

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Raupach GS, Kloepper JW (1998) Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158–1164

    Article  PubMed  CAS  Google Scholar 

  • Ravnskov S, Jensen B, Knudsen IMB, Bødker L, Jensen DF, Karliński 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rousseau A, Benhamou N, Chet I, Piché Y (1996) Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86:434–443

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, Great Britain

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgment

We would like to thank F. Kawane (Idemitsu Kosan Co. Ltd., Tokyo, Japan) for the kind provision of G. mosseae inoculum and to the two anonymous reviewers for their suggestions in improving the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mitsuro Hyakumachi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saldajeno, M.G.B., Ito, M. & Hyakumachi, M. 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 Pathol. 41, 271–281 (2012). https://doi.org/10.1007/s13313-011-0101-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-011-0101-7

Keywords

Navigation