Combined Use of Beneficial Bacteria and Arbuscular Mycorrhizal Fungi for the Biocontrol of Plant Cryptogamic Diseases: Evidence, Methodology, and Limits

Krzyzaniak, Yuko; Magnin-Robert, Maryline; Randoux, Béatrice; Fontaine, Joël; Lounès-Hadj Sahraoui, Anissa

doi:10.1007/978-3-030-51916-2_24

Combined Use of Beneficial Bacteria and Arbuscular Mycorrhizal Fungi for the Biocontrol of Plant Cryptogamic Diseases: Evidence, Methodology, and Limits

Yuko Krzyzaniak⁵,
Maryline Magnin-Robert⁵,
Béatrice Randoux⁵,
Joël Fontaine⁵ &
Anissa Lounès-Hadj Sahraoui⁵

Chapter
First Online: 31 October 2020

488 Accesses
1 Citations

Part of the Soil Biology book series (SOILBIOL,volume 60)

Abstract

Keeping up agricultural production, while reducing chemical inputs, under biotic and abiotic stresses, falls within a considerable challenge. Among the solutions, developing more sustainable strategies to protect crops by using biocontrol agents is a promising alternative. Several beneficial microorganisms can limit pathogen development by direct (antibiosis, competition) and/or indirect effects (plant growth promotion and resistance induction) thanks to nutritional and hormonal balance regulations. A great deal of research articles have already reported the beneficial roles of rhizobacteria or arbuscular mycorrhizal fungi (AMF) on reducing the development of fungal pathogens when applied alone, or on plant nutrition when co-inoculated; while fewer of them reviewed the co-inoculation as a mean to protect against fungal pathogens. Hence, this review aims to present recent developments on the effectiveness of the co-inoculation with beneficial bacteria and AMF for fungal disease management. Firstly, main mechanisms beneath the beneficial effects of bacterial or AMF inoculation alone on plants are recalled. Secondly, results relating their combined inoculation on disease severity are presented and sorted according to their outcomes (synergistic, neutral, or antagonistic interactions), along with the possible underlying mechanisms. Finally, we gathered the main methodologies employed in tripartite interaction experiment and brought to light future challenges for practical use.

Keywords

Arbuscular mycorrhizal fungi
Plant growth-promoting rhizobacteria
Mycorrhiza helper bacteria
Tripartite interactions
Fungal diseases
Biocontrol

This is a preview of subscription content, access via your institution.

Chapter: USD 29.95; Price excludes VAT (USA)

eBook: USD 149.00; Price excludes VAT (USA)

Softcover Book: USD 199.99; Price excludes VAT (USA)

Hardcover Book: USD 199.99; Price excludes VAT (USA)

Learn about institutional subscriptions

References

Aalipour H, Nikbakht A, Etemadi N et al (2019) Biochemical response and interactions between arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria during establishment and stimulating growth of Arizona cypress (Cupressus arizonica G.) under drought stress. Sci Hortic (Amsterdam) 261:108923. https://doi.org/10.1016/j.scienta.2019.108923
CAS CrossRef Google Scholar
Abbass Z, Okon Y (1993) Plant growth promotion by Azotobacter paspali in the rhizosphere. Soil Biol Biochem 25:1075–1083. https://doi.org/10.1016/0038-0717(93)90156-6
CrossRef Google Scholar
Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular-arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32(5):401–409. https://doi.org/10.1007/s003740000269
CrossRef Google Scholar
Agler MT, Ruhe J, Kroll S et al (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352. https://doi.org/10.1371/JOURNAL.PBIO.1002352
CrossRef Google Scholar
Akhtar MS, Siddiqui ZA (2008) Glomus intraradices, Pseudomonas alcaligenes, and Bacillus pumilus: effective agents for the control of root-rot disease complex of chickpea (Cicer arietinum L.). J Gen Plant Pathol 74:53–60. https://doi.org/10.1007/s10327-007-0062-4
CrossRef Google Scholar
Akköprü A, Demir S (2005) Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. J Phytopathol 153:544–550. https://doi.org/10.1111/j.1439-0434.2005.01018.x
CrossRef Google Scholar
Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant Pathol 114:329–341
CrossRef Google Scholar
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
CAS CrossRef Google Scholar
Arya N, Rana A, Rajwar A et al (2018) Biocontrol efficacy of siderophore producing indigenous pseudomonas strains against Fusarium wilt in tomato. Natl Acad Sci Lett 41:133–136. https://doi.org/10.1007/s40009-018-0630-5
CAS CrossRef Google Scholar
Azcón-Aguilar C, Jaizme-Vega MC, Calvet C (2002) The contribution of arbuscular mycorrhizal fungi to the control of soil-borne plant pathogens. In: Mycorrhizal technology in agriculture. Birkhäuser, Basel, pp 187–197
CrossRef Google Scholar
Baar J, Paradi I, Lucassen ECHET, Hudson-Edwards KA, Redecker D, Roelofs JGM, Smolders AJP (2011) Molecular analysis of AMF diversity in aquatic macrophytes: a comparison of oligotrophic and utraoligotrophic lakes. Aquat Bot 94(2):53–61. https://doi.org/10.1016/j.aquabot.2010.09.006
CAS CrossRef Google Scholar
Bach E, Dos Santos Seger GD, de Carvalho Fernandes G et al (2016) Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Appl Soil Ecol 99:141–149. https://doi.org/10.1016/j.apsoil.2015.11.002
CrossRef Google Scholar
Barratt BIP, Moran VC, Bigler F, van Lenteren JC (2018) The status of biological control and recommendations for improving uptake for the future. BioControl 63:155–167. https://doi.org/10.1007/s10526-017-9831-y
CrossRef Google Scholar
Basu M, Santhaguru K (2009) Impact of Glomus fasciculatum and fluorescent pseudomonas on growth performance of Vigna radiata (l.) wilczek challenged with phytopathogens. Journal of Plant Protection Research 49(2):190–194. https://doi.org/10.2478/v10045-009-0028-y
CrossRef Google Scholar
Battini F, Grønlund M, Agnolucci M et al (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci Rep 7:4686. https://doi.org/10.1038/s41598-017-04959-0
CAS CrossRef Google Scholar
Baysal Ö, Silme RS (2019) The beneficial influence of microbial interactions on plant diseases and plant growth promoting effect. In: Mycorrhizosphere and pedogenesis. Springer, Singapore, pp 151–166
CrossRef Google Scholar
Bedini S, Pellegrino E, Avio L et al (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496. https://doi.org/10.1016/j.soilbio.2009.04.005
CAS CrossRef Google Scholar
Begum N, Qin C, Ahanger MA et al (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
CrossRef Google Scholar
Benjamin EO, Wesseler JHH (2016) A socioeconomic analysis of biocontrol in integrated pest management: a review of the effects of uncertainty, irreversibility and flexibility. NJAS-Wageningen J Life Sci 77:53–60. https://doi.org/10.1016/j.njas.2016.03.002
CrossRef Google Scholar
Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18
CAS CrossRef Google Scholar
Berta G, Sampo S, Gamalero E et al (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur J Plant Pathol 111:279–288. https://doi.org/10.1007/s10658-004-4585-7
CrossRef Google Scholar
Bolton MD (2009) Primary metabolism and plant defense–fuel for the fire. Mol Plant-Microbe Interact 22:487–497. https://doi.org/10.1094/MPMI-22-5-0487
CAS CrossRef Google Scholar
Bona E, Cantamessa S, Massa N et al (2017) Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza 27:1–11. https://doi.org/10.1007/s00572-016-0727-y
CAS CrossRef Google Scholar
Bonfante P (2003) Plants, mycorrhizal fungi and endobacteria: a dialog among cells and genomes. Biol Bull 204:215–220. https://doi.org/10.2307/1543562
CAS CrossRef Google Scholar
Bonfante P, Anca I-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504
CAS CrossRef Google Scholar
Borah SN, Goswami D, Sarma HK et al (2016) Rhamnolipid biosurfactant against fusarium verticillioides to control stalk and ear rot disease of maize. Front Microbiol 7:1505. https://doi.org/10.3389/fmicb.2016.01505
CrossRef Google Scholar
Boutheina Z-E, Aya H, Naima B, Ahmed N (2019) Responses of date palm seedling to co-inoculation with phosphate solubilizing bacteria and mycorrhizal arbuscular fungi. Int J Environ Agric Biotechnol 4:581–588. https://doi.org/10.22161/ijeab/4.2.43
Google Scholar
Brauer VS, Rezende CP, Pessoni AM et al (2019) Antifungal agents in agriculture: friends and foes of public health. Biomol Ther 9:521. https://doi.org/10.3390/biom9100521
CAS CrossRef Google Scholar
Budi SW, Van Tuinen D, Martinotti G, Gianinazzi S (1999) Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Appl Environ Microbiol 65:5148–5150
CAS CrossRef Google Scholar
Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545
CAS CrossRef Google Scholar
Cely MVT, Siviero MA, Emiliano J et al (2016) Inoculation of Schizolobium parahyba with mycorrhizal fungi and plant growth-promoting Rhizobacteria increases wood yield under field conditions. Front Plant Sci 7:1708. https://doi.org/10.3389/fpls.2016.01708
CrossRef Google Scholar
Comby M, Mustafa G, Magnin-Robert M et al (2017) Arbuscular mycorrhizal fungi as potential bioprotectants against aerial phytopathogens and pests. In: Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 195–223
CrossRef Google Scholar
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.1016/J.SOILBIO.2009.11.024
CAS CrossRef Google Scholar
Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119. https://doi.org/10.1146/annurev-phyto-080614-120132
CAS CrossRef Google Scholar
Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonisation patterns of root tissues by Phytophthora nicotianae var. Parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232
CAS CrossRef Google Scholar
Davies J (2013) Specialized microbial metabolites: functions and origins. J Antibiot (Tokyo) 66:361–364
CAS CrossRef Google Scholar
De Bona GS, Adrian M, Negrel J et al (2019) Dual mode of action of grape cane extracts against Botrytis cinerea. J Agric Food Chem 67:5512–5520. https://doi.org/10.1021/acs.jafc.8b07098
CAS CrossRef Google Scholar
De Curtis F, de Felice DV, Ianiri G, De Cicco V, Castoria R (2012) Environmental factors affect the activity of biocontrol agents against ochratoxigenic Aspergillus carbonarius on wine grape. Int J Food Microbiol 159(1):17–24. https://doi.org/10.1016/j.ijfoodmicro.2012.07.023
CrossRef Google Scholar
De Vleesschauwer D, Höfte M (2009) Rhizobacteria-induced systemic resistance. In: Van Loon L (ed) Advances in botanical research, vol 51, pp 223–281
Google Scholar
del Jaizme-Vega CM, Rodríguez-Romero AS, Antonio L, Núñez B (2006) 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. Effect of the combined inoculation of arbuscular mycorrhiz. Fruits 61:162. https://doi.org/10.1051/fruits:2006013
CrossRef Google Scholar
Desai S, Kumar GP, Daniel Amalraj L et al (2016) Exploiting PGPR and AMF biodiversity for plant health management. In: Microbial inoculants in sustainable agricultural productivity, Research perspectives, vol 1. Springer, India, New Delhi, pp 145–160
CrossRef Google Scholar
Deveau A, Labbé J (2016) Mycorrhiza helper bacteria. In: Martin F (ed) Molecular mycorrhizal symbiosis. John Wiley, New York, pp 437–450
CrossRef Google Scholar
Dixit R, Agrawal L, Gupta S et al (2016) Southern blight disease of tomato control by 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing Paenibacillus lentimorbus B-30488. Plant Signal Behav 11:e1113363. https://doi.org/10.1080/15592324.2015.1113363
CAS CrossRef Google Scholar
Doubková P, Vlasáková E, Sudová R (2013) Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil 370:149–161. https://doi.org/10.1007/s11104-013-1610-7
CAS CrossRef Google Scholar
Dugassa GD, Von Alten H, Schönbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182
CAS CrossRef Google Scholar
Duijff BJ, Bakker PAHM, Schippers B (1994) Suppression of fusarium wilt of carnation by pseudomonas putida WCS358 at different levels of disease incidence and iron availability. Biocontrol Sci Tech 4:279–288. https://doi.org/10.1080/09583159409355336
CrossRef Google Scholar
Duponnois R (2006) Bacteria Helping Mycorrhiza Development. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial Activity in the Rhizoshere, Soil Biology, vol 7. Springer, Heidelberg, Berlin, pp 297–310
Google Scholar
Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13:85–91. https://doi.org/10.1007/s00572-002-0204-7
CAS CrossRef Google Scholar
El Guilli M, Hamza A, Clément C et al (2016) Effectiveness of postharvest treatment with chitosan to control citrus green mold. Agriculture 6:12. https://doi.org/10.3390/agriculture6020012
CAS CrossRef Google Scholar
Escudero V, Mendoza R (2005) Seasonal variation of arbuscular mycorrhizal fungi in temperate grasslands along a wide hydrologic gradient. Mycorrhiza 15(4):291–299. https://doi.org/10.1007/s00572-004-0332-3
CrossRef Google Scholar
Espidkar Z, Yarnia M, Ansari MH et al (2017) Differences in nitrogen and phosphorus uptake and yield components between barley cultivars grown under arbuscular mycorrhizal fungus and pseudomonas strains Co-inoculation in rainfed condition. Appl Ecol Environ Res 15:195–216. https://doi.org/10.15666/aeer/1504_195216
CrossRef Google Scholar
Fagard M, Launay A, Clément G et al (2014) Nitrogen metabolism meets phytopathology. J Exp Bot 65:5643–5656. https://doi.org/10.1093/jxb/eru323
CAS CrossRef Google Scholar
FAO (2016) Integrated Pest Management (IPM). EU Com
Google Scholar
Fedele G, Bove F, González-Domínguez E, Rossi V (2020) A Generic Model Accounting for the Interactions among pathogens, host plants, biocontrol agents, and the environment, with parametrization for Botrytis cinerea on Grapevines. Agronomy 10(2):222. https://doi.org/10.3390/agronomy10020222
CrossRef Google Scholar
Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Curr Opin Microbiol 32:103–112
CrossRef Google Scholar
Fester T, Maier W, Strack D (1999) Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8:241–246. https://doi.org/10.1007/s005720050240
CAS CrossRef Google Scholar
Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533. https://doi.org/10.1046/j.1469-8137.1999.00366.x
CrossRef Google Scholar
Flint ML, Dreistadt SH, Clark JK, University of California Integrated Pest Management Program (1998) Natural enemies handbook : the illustrated guide to biological pest control. UC Division of Agriculture and Natural Sciences
Google Scholar
Flor-Peregrín E, Azcón R, Martos V et al (2014) Effects of dual inoculation of mycorrhiza and endophytic, rhizospheric or parasitic bacteria on the root-knot nematode disease of tomato. Biocontrol Sci Tech 24:1122–1136. https://doi.org/10.1080/09583157.2014.925091
CrossRef Google Scholar
Fones H, Preston GM (2013) The impact of transition metals on bacterial plant disease. FEMS Microbiol Rev 37:495–519. https://doi.org/10.1111/1574-6976.12004
CAS CrossRef Google Scholar
Frey-Klett P, Garbaye J (2005) Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytol 168:4–8. https://doi.org/10.1111/j.1469-8137.2005.01553.x
CAS CrossRef Google Scholar
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
CAS CrossRef Google Scholar
Fuentes-Ramirez LE, Caballero-Mellado J (2006) Bacterial biofertilizers. In: PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 143–172
CrossRef Google Scholar
Gao X, Lu X, Wu M et al (2012) Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7:e33977. https://doi.org/10.1371/journal.pone.0033977
CAS CrossRef Google Scholar
Gao P, Li Y, Guo Y, Duan T (2018) Co-inoculation of lucerne (Medicago sativa) with an AM fungus and a rhizobium reduces occurrence of spring black stem and leaf spot caused by Phoma medicaginis. Crop Pasture Sci 69:933. https://doi.org/10.1071/CP18135
CrossRef Google Scholar
Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210. https://doi.org/10.1111/j.1469-8137.1994.tb04003.x
CrossRef Google Scholar
García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386. https://doi.org/10.1093/jexbot/53.373.1377
CrossRef Google Scholar
García-Gutiérrez L, Zeriouh H, Romero D et al (2013) The antagonistic strain Bacillus subtilisUMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defence responses. Microb Biotechnol 6:264–274. https://doi.org/10.1111/1751-7915.12028
CAS CrossRef Google Scholar
Gianinazzi S, Gollotte A, Binet MN et al (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530
CrossRef Google Scholar
Gill KH, Garg H (2014) Pesticides: environmental impacts and management strategies. In: Pesticides-toxic aspects. InTech, Croatia, pp 187–230
Google Scholar
Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
CrossRef Google Scholar
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
CAS CrossRef Google Scholar
Hage-Ahmed K, Moyses A, Voglgruber A et al (2013) Alterations in root exudation of intercropped tomato mediated by the Arbuscular Mycorrhizal fungus Glomus mosseae and the soilborne pathogen Fusarium oxysporum f.sp. lycopersici. J Phytopathol 161:763–773. https://doi.org/10.1111/jph.12130
CAS CrossRef Google Scholar
Haggag WM, Faten M, Faten A (2001) Interaction between vesicular arbuscular mycorrhizae and antagonistic biocontrol micro-organisms on controlling root-rot disease incidence of geranium plants. J Biol Sci 1:1147–1153. https://doi.org/10.3923/jbs.2001.1147.1153
CrossRef Google Scholar
Hashem A, Abd_Allah EF, Alqarawi AA et al (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089. https://doi.org/10.3389/fmicb.2016.01089
CrossRef Google Scholar
Hassan Dar G, Zargar MY, Beigh GM (1997) Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and rhizobium leguminosarum. Microb Ecol 34:74–80. https://doi.org/10.1007/s002489900036
CAS CrossRef Google Scholar
Hayat R, Ali S, Amara U et al (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598
CrossRef Google Scholar
Heil M (2001) The ecological concept of costs of induced systemic resistance (ISR). Eur J Plant Pathol 107:137–146. https://doi.org/10.1023/A:1008793009517
CrossRef Google Scholar
Heimpel GE, Mills NJ (2017) Biological control: ecology and applications. Cambridge University Press, Cambridge
CrossRef Google Scholar
Hernández-Montiel LG, Rueda-Puente EO, Cordoba-Matson MV, Holguín-Peña JR, Zulueta-Rodríguez R (2013) Mutualistic interaction of rhizobacteria with arbuscular mycorrhizal fungi and its antagonistic effect on Fusarium oxysporum in Carica papaya seedlings. Crop Prot 47:61–66. https://doi.org/10.1016/J.CROPRO.2013.01.008
CrossRef Google Scholar
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146
CAS CrossRef Google Scholar
Holland T, Bowen P, Kokkoris V et al (2019) Does inoculation with arbuscular mycorrhizal fungi reduce trunk disease in grapevine rootstocks? Horticulturae 5:61. https://doi.org/10.3390/horticulturae5030061
CrossRef Google Scholar
Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287
CAS CrossRef Google Scholar
Jaffuel G, Imperiali N, Shelby K et al (2019) Protecting maize from rootworm damage with the combined application of arbuscular mycorrhizal fungi, Pseudomonas bacteria and entomopathogenic nematodes. Sci Rep 9:3127. https://doi.org/10.1038/s41598-019-39753-7
CAS CrossRef Google Scholar
Jones P, Garcia BJ, Furches A et al (2019) Plant host-associated mechanisms for microbial selection. Front Plant Sci 10:862
CrossRef Google Scholar
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664. https://doi.org/10.1007/s10886-012-0134-6
CAS CrossRef Google Scholar
Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agron 2019:1–7
CrossRef CAS Google Scholar
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151
CrossRef Google Scholar
Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29. https://doi.org/10.1016/j.tplants.2004.12.003
CAS CrossRef Google Scholar
Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480. https://doi.org/10.1046/j.1365-2672.2003.02161.x
CAS CrossRef Google Scholar
Khan MS, ZAIDI A (2007) Synergistic effects of the inoculation with plant growth-promoting Rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turkish J Agric For 31:355–362
CAS Google Scholar
Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9:2732
CrossRef Google Scholar
Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845
CrossRef Google Scholar
Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252. https://doi.org/10.1016/J.ENVEXPBOT.2008.09.008
CAS CrossRef Google Scholar
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92(4):486–488
CrossRef Google Scholar
Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecol Lett 8:61–69. https://doi.org/10.1111/j.1461-0248.2004.00690.x
CrossRef Google Scholar
Kundan R, Pant G, Jadon N, Agrawal PK (2015) Plant growth promoting rhizobacteria: mechanism and current prospective. J Fertil Pestic 6:155. https://doi.org/10.4172/2471-2728.1000155
CrossRef Google Scholar
Larsen J, Ravnskov S, Jakobsen I (2003) Combined effect of an arbuscular mycorrhizal fungus and a biocontrol bacterium against Pythium ultimum in soil. Folia Geobot 38:145–154. https://doi.org/10.1007/BF02803147
CrossRef Google Scholar
Latha P, Karthikeyan M, Rajeswari E (2019) Endophytic bacteria: prospects and applications for the plant disease management. In: Plant health under biotic stress. Springer, Singapore, pp 1–50
Google Scholar
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349. https://doi.org/10.1111/j.1574-6941.2008.00531.x
CAS CrossRef Google Scholar
Lee B, Farag MA, Park HB et al (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS One 7:e48744. https://doi.org/10.1371/journal.pone.0048744
CAS CrossRef Google Scholar
Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - a meta-analysis. Soil Biol Biochem 81:147–158. https://doi.org/10.1016/j.soilbio.2014.11.013
CAS CrossRef Google Scholar
Lenoir I, Fontaine J, Lounès-Hadj Sahraoui A (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15
CAS CrossRef Google Scholar
Lerat S, Lapointe L, Gutjahr S et al (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595. https://doi.org/10.1046/j.1469-8137.2003.00691.x
CrossRef Google Scholar
Li Y, Héloir M, Zhang X et al (2019) Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defence stimulation. Mol Plant Pathol 20:1037. https://doi.org/10.1111/mpp.12809
CAS CrossRef Google Scholar
Liu J, Maldonado-Mendoza I, Lopez-Meyer M et al (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. https://doi.org/10.1111/j.1365-313X.2007.03069.x
CAS CrossRef Google Scholar
Liu Y, Feng X, Gao P et al (2018) Arbuscular mycorrhiza fungi increased the susceptibility of astragalus adsurgens to powdery mildew caused by erysiphe pisi. Mycology 9:223–232. https://doi.org/10.1080/21501203.2018.1477849
CAS CrossRef Google Scholar
Lowe A, Rafferty-McArdle SM, Cassells AC (2012) Effects of AMF- and PGPR-root inoculation and a foliar chitosan spray in single and combined treatments on powdery mildew disease in strawberry. Agric Food Sci 21:28–38. https://doi.org/10.23986/afsci.4997
CAS CrossRef Google Scholar
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918
CAS CrossRef Google Scholar
Ma Y, Látr A, Rocha I et al (2019) Delivery of inoculum of Rhizophagus irregularis via seed coating in combination with Pseudomonas libanensis for cowpea production. Agronomy 9:33. https://doi.org/10.3390/agronomy9010033
CAS CrossRef Google Scholar
Mahmoudi N, Mahdhi M, Abdedaiem R et al (2017) Growth response and drought tolerance of lens culinaris inoculated with arbuscular mycorrhizal fungi. Int J Pure App Biosci 5:674–685. https://doi.org/10.18782/2320-7051.6063
CrossRef Google Scholar
Mamatha G, Bagyaraj DJ, Jaganath S (2002) Inoculation of field-established mulberry and papaya with arbuscular mycorrhizal fungi and a mycorrhiza helper bacterium. Mycorrhiza 12:313–316. https://doi.org/10.1007/s00572-002-0200-y
CAS CrossRef 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(11):1843–1850. https://doi.org/10.1002/jsfa.3660
CAS CrossRef Google Scholar
Martínez-Viveros O, Jorquera MA, Crowley DE et al (2010) Mechanisms and practical considerations involved in plant growth promotion by Rhizobacteria. J Soil Sci Plant Nutr 10:293–319. https://doi.org/10.4067/S0718-95162010000100006
CrossRef 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(3):495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
CrossRef Google Scholar
McNeely D, Chanyi RM, Dooley JS et al (2017) Biocontrol of Burkholderia cepacia complex bacteria and bacterial phytopathogens by Bdellovibrio bacteriovorus. Can J Microbiol 63:350–358
CAS CrossRef Google Scholar
Mejri S, Siah A, Coutte F et al (2018) Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis. Environ Sci Pollut Res 25:29822–29833. https://doi.org/10.1007/s11356-017-9241-9
CAS CrossRef Google Scholar
Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569
CAS Google Scholar
Mohan V, Nivea R, Menon S (2015) Evaluation of ectomycorrhizal fungi as potential bio-control agents against selected plant pathogenic fungi. J Acad Ind Res 3:408
CAS Google Scholar
Mustafa G, Khong NG, Tisserant B et al (2017) Defence mechanisms associated with mycorrhiza-induced resistance in wheat against powdery mildew. Funct Plant Biol 44:443–454. https://doi.org/10.1071/FP16206
CAS CrossRef Google Scholar
Nadeem SM, Ahmad M, Zahir ZA et al (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448. https://doi.org/10.1016/J.BIOTECHADV.2013.12.005
CrossRef Google Scholar
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract pseudomonas putida to the rhizosphere. PLoS One 7:e35498. https://doi.org/10.1371/journal.pone.0035498
CAS CrossRef Google Scholar
Neeraj, Singh K (2011) Organic amendments to soil inoculated arbuscular mycorrhizal fungi and Pseudomonas fluorescens treatments reduce the development of root-rot disease and enhance the yield of Phaseolus vulgaris L. Eur J Soil Biol 47:288–295. https://doi.org/10.1016/J.EJSOBI.2011.07.002
CrossRef Google Scholar
Nicot PC, Alabouvette C, Bardin M, Blum B, Köhl J, Ruocco M (2012) Review of factors influencing the success or failure of biocontrol: technical, industrial and socio-economic perspectives. IOBC-WPRS Bulletin 78:95–98. http://ec.europa.eu/sanco_pesticides/
Google Scholar
Norman JR, Atkinson D, Hooker JE (1996) Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant Soil 185:191–198
CAS CrossRef Google Scholar
Ojiambo PS, Scherm H (2006) Mini-review biological and application-oriented factors influencing plant disease suppression by biological control: a meta-analytical review. Phytopathology 96(11):1168–1174. https://doi.org/10.1094/PHYTO-96-1168
CAS CrossRef Google Scholar
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987
CAS CrossRef Google Scholar
Perazzolli M, Roatti B, Bozza E, Pertot I (2011) Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine. Biol Control 58:74–82. https://doi.org/10.1016/j.biocontrol.2011.04.006
CrossRef Google Scholar
Pérez-de-Luque A, Tille S, Johnson I et al (2017) The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Sci Rep 7:16409. https://doi.org/10.1038/s41598-017-16697-4
CAS CrossRef Google Scholar
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158–IN18. https://doi.org/10.1016/S0007-1536(70)80110-3
CrossRef Google Scholar
Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316
CAS CrossRef Google Scholar
Pieterse CMJ, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
CAS CrossRef Google Scholar
Pliego C, De Weert S, Lamers G et al (2008) Two similar enhanced root-colonizing pseudomonas strains differ largely in their colonization strategies of avocado roots and Rosellinia necatrix hyphae. Environ Microbiol 10:3295–3304. https://doi.org/10.1111/j.1462-2920.2008.01721.x
CrossRef Google Scholar
Pozo MJ, Jung SC, Martínez-Medina A et al (2013) Root allies: Arbuscular mycorrhizal fungi help plants to cope with biotic stresses. In: Aroca R (ed) Soil biology. Springer, Berlin, pp 289–307
Google Scholar
Ratzke C, Gore J (2018) Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biol 16:e2004248. https://doi.org/10.1371/journal.pbio.2004248
CAS CrossRef Google Scholar
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53
CAS CrossRef Google Scholar
Rilling JI, Acuña JJ, Nannipieri P et al (2019) Current opinion and perspectives on the methods for tracking and monitoring plant growth–promoting bacteria. Soil Biol Biochem 130:205–219. https://doi.org/10.1016/J.SOILBIO.2018.12.012
CAS CrossRef Google Scholar
Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. https://doi.org/10.1016/S0734-9750(99)00014-2
CrossRef Google Scholar
Rosier A, Medeiros FHV, Bais HP (2018) Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil 428:35–55
CAS CrossRef Google Scholar
Rouphael Y, Franken P, Schneider C et al (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic (Amsterdam) 196:91–108
CrossRef Google Scholar
Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596. https://doi.org/10.1128/AEM.02775-08
CAS CrossRef Google Scholar
Rupp S, Weber RWS, Rieger D et al (2017) Spread of Botrytis cinerea strains with multiple fungicide resistance in German horticulture. Front Microbiol 7:2075. https://doi.org/10.3389/fmicb.2016.02075
CrossRef Google Scholar
Ryan RP, Germaine K, Franks A et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9
CAS CrossRef Google Scholar
Ryu CM, Farag MA, Hu CH et al (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. https://doi.org/10.1104/pp.103.026583
CAS CrossRef Google Scholar
Saldajeno MGB, Hyakumachi M (2011a) Arbuscular mycorrhizal interactions with Rhizobacteria or saprotrophic fungi and its implications to biological control of plant diseases. In: Fulton SM (ed) Mycorrhizal fungi: soil, agriculture and environmental implications. Nova Science Publishers, New York, pp 1–28
Google Scholar
Saldajeno MGB, Hyakumachi M (2011b) 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. https://doi.org/10.1111/j.1744-7348.2011.00471.x
CrossRef Google Scholar
Sanchez-Bel P, Troncho P, Gamir J et al (2016) The nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato. Front Microbiol 7:1598. https://doi.org/10.3389/FMICB.2016.01598
CrossRef Google Scholar
Sannazzaro AI, Ruiz OA, Albertó EO, Menéndez AB (2006) Alleviation of salt stress in lotus glaber by Glomus intraradices. Plant Soil 285:279–287. https://doi.org/10.1007/s11104-006-9015-5
CAS CrossRef Google Scholar
Sarma RK, Saikia R, Talukdar NC (2017) Mitochondrial DNA based molecular markers in arbuscular mycorrhizal fungi (amf) research. Springer, Cham, pp 243–250
Google Scholar
Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280
CrossRef Google Scholar
Singh R, Soni SK, Kalra A (2013) Synergy between Glomus fasciculatum and a beneficial Pseudomonas in reducing root diseases and improving yield and forskolin content in Coleus forskohlii Briq. Under organic field conditions. Mycorrhiza 23:35–44. https://doi.org/10.1007/s00572-012-0447-x
CrossRef Google Scholar
Singh R, Kumar M, Mittal A, Mehta PK (2017) Microbial metabolites in nutrition, healthcare and agriculture. 3 Biotech 7(1):15
CrossRef Google Scholar
Singh S, Bhatnagar S, Choudhary S et al (2018) Fungi as biocontrol agent: an alternate to chemicals. In: Fungi and their role in sustainable development: current perspective. Springer, Singapore, pp 23–33
CrossRef Google Scholar
Smith S, Read D (2008) Mycorrhizal Symbiosis. Elsevier Ltd, Amsterdam
Google Scholar
Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O’Gara F, Doohan FM (2011) In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol 111(3):683–692. https://doi.org/10.1111/j.1365-2672.2011.05079.x
CAS CrossRef Google Scholar
Song YY, Cao M, Xie LJ et al (2011) Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza 21:721–731. https://doi.org/10.1007/s00572-011-0380-4
CAS CrossRef Google Scholar
Song Y, Chen D, Lu K et al (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. https://doi.org/10.3389/fpls.2015.00786
CrossRef Google Scholar
Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104:18842–18847. https://doi.org/10.1073/pnas.0708139104
CrossRef Google Scholar
Srivastava R, Khalid A, Singh USS, Sharma AKK (2010) Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. sp. lycopersici for the management of tomato wilt. Biol Control 53:24–31. https://doi.org/10.1016/j.biocontrol.2009.11.012
CrossRef Google Scholar
Sumathi S, Thangavelu R (2016) Co-inoculation of arbuscular mycorrhizal fungi (AMF) and their mycorrhizae helper bacteria (MHB) effectively suppresses fusarium wilt in banana. Plant Archives 16(1):365–375
Google Scholar
Sundram S, Meon S, Seman IA, Othman R (2015) Application of arbuscular mycorrhizal fungi with Pseudomonas aeruginosa UPMP3 reduces the development of Ganoderma basal stem rot disease in oil palm seedlings. Mycorrhiza 25(5):387–397. https://doi.org/10.1007/s00572-014-0620-5
CAS CrossRef Google Scholar
Tabassum B, Khan A, Tariq M, Ramzan M, Iqbal Khan MS, Shahid N, Aaliya K (2017) Bottlenecks in commercialisation and future prospects of PGPR. In: Applied Soil Ecology Vol. 121, Elsevier, pp 102–117. https://doi.org/10.1016/j.apsoil.2017.09.030
Tahmatsidou V, O’Sullivan J, Cassells AC et al (2006) Comparison of AMF and PGPR inoculants for the suppression of Verticillium wilt of strawberry (Fragaria×ananassa cv. Selva). Appl Soil Ecol 32:316–324. https://doi.org/10.1016/j.apsoil.2005.07.008
CrossRef Google Scholar
Thioye B, van Tuinen D, Kane A, de Faria SM, Ndiaye C, Duponnois R, Sylla SN, Bâ AM (2019) Tracing Rhizophagus irregularis isolate IR27 in Ziziphus mauritiana roots under field conditions. Mycorrhiza 29(1):77–83. https://doi.org/10.1007/s00572-018-0875-3
CAS CrossRef Google Scholar
Tisserant B, Brenac V, Requena N et al (1998) The detection of Glomus spp. (arbuscular mycorrhizal fungi) forming mycorrhizas in three plants, at different stages of seedling development, using mycorrhiza-specific isozymes. New Phytol 138:225–239. https://doi.org/10.1046/j.1469-8137.1998.00112.x
CAS CrossRef Google Scholar
Todeschini V, Ait Lahmidi N, Mazzucco E et al (2018) Impact of beneficial microorganisms on strawberry growth, fruit production, nutritional quality, and volatilome. Front Plant Sci 9:1611. https://doi.org/10.3389/fpls.2018.01611
CrossRef Google Scholar
Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515. https://doi.org/10.1046/j.1469-8137.2002.00470.x
CrossRef Google Scholar
Trouvelot A, Kough J, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification functionnelle. In: Gianninazzi-Pearson V, Gianinazzi S (eds) Physiol Genet Asp mycorrhizae. INRA, Paris, pp 217–221
Google Scholar
Trouvelot S, Héloir M-C, Poinssot B et al (2014) Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front Plant Sci 5:1–14. https://doi.org/10.3389/fpls.2014.00592
CrossRef Google Scholar
Tsukanova KA, Сhеbоtаr V, Meyer JJM, Bibikova TN (2017) Effect of plant growth-promoting Rhizobacteria on plant hormone homeostasis. S Afr J Bot 113:91–102
CAS CrossRef Google Scholar
Vacheron J, Desbrosses G, Bouffaud ML et al (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. https://doi.org/10.3389/fpls.2013.00356
CrossRef Google Scholar
Van Rhijn P, Vanderleyden J (1995) The rhizobium-plant symbiosis. Microbiol Rev 59:124–142
CrossRef Google Scholar
Van Tuinen D, Jacquot E, Zhao B et al (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25s rDNA-targeted nested PCR. Mol Ecol 7:879–887. https://doi.org/10.1046/j.1365-294x.1998.00410.x
CrossRef Google Scholar
Vandenkoornhuyse P, Quaiser A, Duhamel M et al (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206
CrossRef Google Scholar
Verma SK, Kingsley K, Bergen M et al (2018) Bacterial endophytes from rice cut grass (Leersia oryzoides L.) increase growth, promote root gravitropic response, stimulate root hair formation, and protect rice seedlings from disease. Plant Soil 422:223–238. https://doi.org/10.1007/s11104-017-3339-1
CAS CrossRef Google Scholar
Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido JM (2008) The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? In: Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Berlin, pp 307–320
CrossRef Google Scholar
Vigo C, Norman JR, Hooker JE (2000) Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol 49:509–514. https://doi.org/10.1046/j.1365-3059.2000.00473.x
CrossRef Google Scholar
Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280. https://doi.org/10.1093/jxb/ert026
CAS CrossRef Google Scholar
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
CAS CrossRef Google Scholar
Wang W, Wang Z-Y (2014) At the intersection of plant growth and immunity. Cell Host Microbe 15:400–402. https://doi.org/10.1016/j.chom.2014.03.014
CAS CrossRef Google Scholar
Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790. https://doi.org/10.1016/j.cub.2007.09.025
CAS CrossRef Google Scholar
Wehner J, Antunes PM, Powell JR et al (2010) Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia (Jena) 53:197–201. https://doi.org/10.1016/j.pedobi.2009.10.002
CrossRef Google Scholar
Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. In: Canadian Journal of Botany. NRC Research Press, Ottawa, Canada, pp 1198–1227
Google Scholar
Wipf D, Krajinski F, Tuinen D et al (2019) Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytol 223:1127–1142. https://doi.org/10.1111/nph.15775
CAS CrossRef Google Scholar
Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478. https://doi.org/10.1016/S0038-0717(03)00003-8
CAS CrossRef Google Scholar
Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608. https://doi.org/10.1007/s11356-014-3396-4
CAS CrossRef Google Scholar
Yoder OC, Whalen ML (1975) Factors affecting postharvest infection of stored cabbage tissue by Botrytis cinerea. Can J Bot 53:691–699. https://doi.org/10.1139/b75-085
CrossRef Google Scholar
Zhao Q, Shen Q, Ran W et al (2011) Inoculation of soil by Bacillus subtilis Y-IVI improves plant growth and colonization of the rhizosphere and interior tissues of muskmelon (Cucumis melo L.). Biol Fertil Soils 47:507–514. https://doi.org/10.1007/s00374-011-0558-0
CAS CrossRef Google Scholar
Zhao X, Yuan S, Song H, Su X, Mao H, Shen W, Qu X, Dong J (2016) Arbuscular mycorrhizal and dark septate fungal associations in riparian plants of the three gorges reservoir region, Southwest China. Aquat Bot 133:28–37. https://doi.org/10.1016/j.aquabot.2016.05.003
CrossRef Google Scholar

Download references

Acknowledgments

The authors wish to thank the “Université du Littoral Côte d’Opale (ULCO)” for providing financial supports for Y. Krzyzaniak post-doctoral fellowship. This work has been carried out in the framework of TRIPLET project which was supported by the partnership A2U (Artois, UPJV, ULCO) and in the framework of CPER ALIBIOTECH project which was financed by European Union, French State and the French Region of Hauts-de-France.

Author information

Authors and Affiliations

Université du Littoral Côte d’Opale, Unité de Chimie Environnementale et Interactions sur le Vivant (UCEIV) UR 4492, Calais Cedex, France
Yuko Krzyzaniak, Maryline Magnin-Robert, Béatrice Randoux, Joël Fontaine & Anissa Lounès-Hadj Sahraoui

Authors

Yuko Krzyzaniak
View author publications
You can also search for this author in PubMed Google Scholar
Maryline Magnin-Robert
View author publications
You can also search for this author in PubMed Google Scholar
Béatrice Randoux
View author publications
You can also search for this author in PubMed Google Scholar
Joël Fontaine
View author publications
You can also search for this author in PubMed Google Scholar
Anissa Lounès-Hadj Sahraoui
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anissa Lounès-Hadj Sahraoui .

Editor information

Editors and Affiliations

Amity Institute of Microbial Technology, Amity University Uttar Pradesh (AUUP), Noida, Uttar Pradesh, India
Neeraj Shrivastava
Amity Institute of Microbial Technology, Amity University Uttar Pradesh (AUUP), Noida, Uttar Pradesh, India
Shubhangi Mahajan
Amity Institute of Microbial Technology, Amity University Uttar Pradesh (AUUP), Noida, Uttar Pradesh, India
Ajit Varma

Ethics declarations

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

Copyright information

About this chapter

Cite this chapter

Krzyzaniak, Y., Magnin-Robert, M., Randoux, B., Fontaine, J., Lounès-Hadj Sahraoui, A. (2021). Combined Use of Beneficial Bacteria and Arbuscular Mycorrhizal Fungi for the Biocontrol of Plant Cryptogamic Diseases: Evidence, Methodology, and Limits. In: Shrivastava, N., Mahajan, S., Varma, A. (eds) Symbiotic Soil Microorganisms. Soil Biology, vol 60. Springer, Cham. https://doi.org/10.1007/978-3-030-51916-2_24

Download citation

DOI: https://doi.org/10.1007/978-3-030-51916-2_24
Published: 31 October 2020
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-51915-5
Online ISBN: 978-3-030-51916-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)