Abstract
Aims
The aim of this study was to elucidate the effects of the interactions between the arbuscular mycorrhizal fungus Glomus mosseae (Gm) and Fusarium equiseti GF18-3 on cucumber growth and the biocontrol of the yellow strain of Cucumber mosaic virus (CMV-Y).
Methods
Cucumber plants were pre-inoculated with Gm and GF18-3 for 4 weeks before the leaves were inoculated with CMV. CMV accumulation in cucumber leaves was determined using an indirect enzyme-linked immunosorbent assay (ELISA) at 1, 2, and 3 weeks post-inoculation (WPI). An RT-PCR analysis was performed to evaluate the expression levels of defence-related genes.
Results
The co-inoculation of cucumber plants with Gm and GF18-3 or GF18-3 alone resulted in effective control of CMV disease severity, though no significant reduction was observed in the Gm-alone treatment. CMV accumulation was significantly decreased in cucumber plants treated with combined inoculation or with GF18-3 alone at 1, 2, and 3 WPI. The RT-PCR results revealed higher expression levels of SA-inducible genes in all treatments, while only Gm treatment of plants induced JA-inducible genes.
Conclusion
The dual inoculation treatment and inoculation with GF18-3 alone have the potential to reduce disease severity and increase plant growth. Moreover, modulation of plant defence responses in the shoots may contribute to this protection.
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Abbreviations
- CMV:
-
Cucumber mosaic virus
- BGI:
-
barley grain inoculum
- BTH:
-
benzothiadiazole
- ISR:
-
induced systemic resistance
- JA:
-
jasmonic acid
- PDA:
-
potato dextrose agar
- PDB:
-
potato dextrose broth
- PGPF:
-
plant growth-promoting fungi
- PGPR:
-
plant growth-promoting rhizobacteria
- PR:
-
pathogenesis related
- DPI:
-
days post inoculation
- WAP:
-
weeks after planting
- RT-PCR:
-
reverse transcription-PCR
- SA:
-
salicylic acid
- SAR:
-
systemic acquired resistance.
References
Al-Karaki GB, McMichael JZ (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269
Arpana J, Bagyaraj DJ (2007) Response of kalmegh to an arbuscular mycorrhizae fungus and a growth promoting rhizomicroorganism at two levels of phosphorus fertilizer. Am-Euras J Agric Environ Sci 2:33–38
Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10
Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740
Benhamou N, Nicole M (1999) Cell biology of plant immunization against microbial infection: The potential of induced resistance in controlling plant diseases. Plant Physiol Biochem 37:703–719
Bhromsiri C (2009) Use of soil microbial inoculation for improving the effectiveness of vetiver grass and the effect on natural soil microbial ecology. Dissertation, Chiang Mai University
Bi HH, Song YY, Zeng RS (2007) Biochemical and molecular responses of host plants to mycorrhizal infection and their roles in plant defence. Allelopathy J 20:15–28
Blilou I, Ocampo JA, Garcia-Garrido JM (2000) Induction of Ltp (Lipid transfer protein) and Pal (Phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977
Brundrett MC, Piché Y, Peterson RL (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can J Bot 62:2128–2134
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
Camprubí A, Calvet C, Estaún V (1995) Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial population and enzyme activity in potting mixes. Plant Soil 173:233–238
Casal JJ, Mella RA, Ballare CL, Maldonado S (1994) Phytochrome-mediated effects on extracellular peroxidase activity, lignin content and bending resistance in etiolated Vicia faba epicotyls. Physiol Plant 92:555–562
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
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
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.). Appl Soil Ecol 41:336–341
Compant S, Duffy B, Nowak J, Clement C, Ait Barka E (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959
Cools HJ, Ishii H (2002) Pre-treatment of cucumber plants with acibenzolar-S-methyl systemically primes a phenylalanine ammonia lyase gene (PAL) for enhanced expression upon attack with a pathogenic fungus. Physiol Mol Plant Pathol 61:273–280
Daft MJ, Okusanya BO (1973) Effect of Endogone mycorrhiza on plant growth. V1. Influence of infection on the anatomy and reproductive development in four hosts. New Phytol 72:1333–1339
Dalisay RF, Kuc JA (1995a) Persistence of induced resistance and enhanced peroxidase and chitinase activities in cucumber plants. Physiol Mol Plant Pathol 47:315–327
Dalisay RF, Kuc JA (1995b) Persistence of reduced penetration by Colletotrichum lagenarium into cucumber leaves with induced systemic resistance and its relation to enhanced peroxidase and chitinase activities. Physiol Mol Plant Pathol 47:329–338
DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci USA 101:9927–9932
Dehne HW (1982) Interaction between vesicular mycorrhizal fungi and plant pathogens. Phytopathology 72:1115–1119
Donald F, Cipollini JR (1998) The induction of soluble peroxidase activity in bean leaves by wind induced mechanical perturbation. Am J Bot 85:1586–1591
Duponnois R, Colombet A, Hien V, Thioulouse J (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460–1468
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 isolation on selective media. Phytopathology 93:229–235
Fracchia S, Mujica MT, García-Romera I, García-Garrido JM, Martin J, Ocampo JA (1998) Interactions between Glomus mosseae and arbuscular mycorrhizal sporocarp-associated saprophytic fungi. Plant Soil 200:131–137
Fracchia S, Garcia-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
Gallou A, Cranenbrouck S, Declerck S (2009) Trichoderma harzianum elicits defence response genes in roots of potato plantlets challenged by Rhizoctonia solani. Eur J Plant Pathol 124:219–230
Garcia-Romera I, Garcia-Garrido JM, Martin J, Fracchia S, Mujica MT, Godeas A, Ocampo JA (1998) Interactions between saprotrophic Fusarium strains and arbuscular mycorrhizas of soybean plants. Symbiosis 24:235–246
Gerhardson B (2002) Biological substitutes for pesticides. Trends Biotechnol 20:338–343
Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activated gene expression and disease resistance in wheat. Plant Cell 8:629–643
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. Appl Environ Microbiol 65:1428–1434
Hammerschmidt R (1999) Phytoalexins: what have we learned after 60 years? Annu Rev Phytopathol 37:285–306
Horinouchi H, Muslim A, Suzuki T, Hyakumachi M (2007) Fusarium equiseti GF19-1 as an effective biocontrol agent against Fusarium crown and root rot of tomato in rock wool systems. Crop Prot 26:1514–1523
Hossain MM, Sultana F, Kubota M, Koyama H, Hyakumachi M (2007) The plant growth-promoting fungus Penicillium simplicissimum GP17-2 induces resistance in Arabidopsis thaliana by activation of multiple defence signals. Plant Cell Physiol 48:1724–1736
Hyakumachi M (1994) Plant-growth-promoting fungi from turfgrass rhizosphere with potential for disease suppression. Soil Microorganisms 44:53–68
Ipper NS, Lee SH, Suk JK, Shrestha A, Seo DU, Park DH, Cho JM, Park DS, Hur JH, Lim CK (2008) Antiviral activity of the expolysaccharaide produced by Serratia sp. strain Gsm01 against Cucumber mosaic virus. J Microbiol Biotechnol 18:67–73
Jeffries P, Barea JM (2001) Arbuscular mycorrhiza – a key component of sustainable plant–soil ecosystems. In: Hock B. Springer (ed) Fungal Associations, Vol. IX of The Mycota, Berlin, pp 95–113
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 Fert Soils 37:1–16
Kjoller R, Rosendahl S (1997) Polyacrylamide gel electrophoresis (PAGE) and densiometric measurement of enzyme activity of the pea root pathogen Aphanomyces euteiches in pea roots. J Phytopathol 145:253–256
Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82
Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544
Maciá-Vicente JG, Jansson HB, Talbot NJ, Lopez-Llorca LV (2009) Real-time PCR quantification and live-cell imaging of endophytic colonization of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. New Phytol 182:213–228
Martínez 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
McAllister CB, García-Romera I, Godeas A, Ocampo JA (1994) Interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae: effects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol Biochem 26:1363–1367
McAllister CB, García-Garrido JM, García-Romera I, Godeas A, Ocampo JA (1996) In vitro interactions between Alternaria alternata, Fusarium equiseti and Glomus mosseae. Symbiosis 20:163–174
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 Fertil Soils 24:301–305
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
Meddad-Hamza A, Beddiar A, Gollotte A, Lemoine MC, Kuszala C, Gianinazzi S (2010) Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. Afr J Biotechnol 9:1159–1167
Morkunas I, Gmerek J (2007) The possible involvement of peroxidase in defence of yellow lupine embryo axes against Fusarium oxysporum. J Plant Physiol 164:185–94
Nemec S, Myhre D (1984) Virus-glomus etunicatum interactions in citrus root stocks. Plant Dis 68:311–314
Postma J, Montanari V, Van den Boogert PHJF (2003) Microbial enrichment to enhance the disease suppressive activity of compost. Eur J Soil Biol 39:157–163
Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398
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
Punja ZK, Wan A, Rahman M (2008) Growth, population dynamics, and diversity of Fusarium equiseti in ginseng fields. Eur J Plant Pathol 121:173–184
Roossinck MJ (1999) Cucumoviruses (Bromoviridae)—general features. In: Granoof L, Webster RG (eds) Cucumoviruses (Bromoviridae)—general features. Encyclopedia of Virology, 2nd edn. Academic, San Diego, pp 315–320
Ryu C-M, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1- independent and jasmonic acid-dependent signaling pathway. Plant J 39:381–392
Ryu C-M, Kang BR, Han SH, Cho SM, Kloepper JW, Anderson AJ, Kim YC (2007) Tobacco cultivars vary in induction of systemic resistance against Cucumber mosaic virus and growth promotion by Pseudomonas chlororaphis O6 and its gacS mutant. Eur J Plant Pathol 119:383–390
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) seedlings. Ann Appl Biol 159:28–40
Selosse MA, Baudoin E, Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. C R Biol 327:639–648
Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628
Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-Induced Changes in Disease Severity and PR Protein Expression in Tobacco Leaves. Mol Plant-Microbe Interact 12:1000–1007
Shivanna MB, Meera MS, Kubota M, Hyakumachi M (2005) Promotion of growth and yield in cucumber by zoysiagrass rhizosphere fungi. Microb Environ 20:34–40
Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84
Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic, San Diego
Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Ann Rev Phytopathol 35:235–270
Suzuki Y, Kawazu T, Koyama H (2004) RNA isolation from siliques, dry seeds and other tissues of Arabidopsis thaliana. Biotechniques 37:542–544
Van Loon LC (1997) Induced resistance in plants and the role of pathogenesis related proteins. Eur J Plant Pathol 103:753–765
Van Loon LC, Bakker RPAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Ann Rev Phytopathol 36:453–483
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 rizosphere of maize plants. Appl Soil Ecol 15:261–272
Wang S, Wu H, Qiao J, Ma L, Liu J, Xia Y, Gao X (2009) Molecular mechanism of plant growth promotion and induced systemic resistance to Tobacco mosaic virus by Bacillus spp. J Microbiol Biotechnol 19:1250–1258
Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511
Zehnder GW, Yao C, Murphy JF, Sikora ER, Kloepper JW (2000) Induction of resistance in tomato against Cucumber mosaic cucumovirus by plant growth promoting rhizobacteria. BioControl 45:127–137
Acknowledgements
This work was supported by the Egyptian Government and a grant (KAKEN (B) 22380177) from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (Monbukagakusho).
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Elsharkawy, M.M., Shimizu, M., Takahashi, H. et al. The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae induce systemic resistance against Cucumber mosaic virus in cucumber plants. Plant Soil 361, 397–409 (2012). https://doi.org/10.1007/s11104-012-1255-y
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DOI: https://doi.org/10.1007/s11104-012-1255-y