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Development of a taxon-discriminating molecular marker to trace and quantify a mycorrhizal inoculum in roots and soils of agroecosystems

. 2021 Jun ; 66 (3) : 371-384. [epub] 20210203

Language English Country United States Media print-electronic

Document type Journal Article

Grant support
Edital nº 046/2013, project 213/13 Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
TEAM project Arbuscular mycorrhizal fungi as an efficient tool to improve the agricultural production of small scale local farmers in Cuba Vliruos-Belgium

Links

PubMed 33534036
DOI 10.1007/s12223-020-00844-y
PII: 10.1007/s12223-020-00844-y
Knihovny.cz E-resources

Crop inoculation with Glomus cubense isolate (INCAM-4, DAOM-241198) promotes yield in banana, cassava, forages, and others. Yield improvements range from 20 to 80% depending on crops, nutrient supply, and edaphoclimatic conditions. However, it is difficult to connect yield effects with G. cubense abundance in roots due to the lack of an adequate methodology to trace this taxon in the field. It is necessary to establish an accurate evaluation framework of its contribution to root colonization separated from native arbuscular mycorrhizal fungi (AMF). A taxon-discriminating primer set was designed based on the ITS nrDNA marker and two molecular approaches were optimized and validated (endpoint PCR and quantitative real-time PCR) to trace and quantify the G. cubense isolate in root and soil samples under greenhouse and environmental conditions. The detection limit and specificity assays were performed by both approaches. Different 18 AMF taxa were used for endpoint PCR specificity assay, showing that primers specifically amplified the INCAM-4 isolate yielding a 370 bp-PCR product. In the greenhouse, Urochloa brizantha plants inoculated with three isolates (Rhizophagus irregularis, R. clarus, and G. cubense) and environmental root and soil samples were successfully traced and quantified by qPCR. The AMF root colonization reached 41-70% and the spore number 4-128 per g of soil. This study demonstrates for the first time the feasibility to trace and quantify the G. cubense isolate using a taxon-discriminating ITS marker in roots and soils. The validated approaches reveal their potential to be used for the quality control of other mycorrhizal inoculants and their relative quantification in agroecosystems.

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Abbott LK (1982) Comparative anatomy of vesicular-arbuscular mycorrhizas formed on subterranean clover. Aust. J. Bot. 30:485–499

Abbott LK, Gazey C (1994) An ecological view of the formation of VA mycorrhizas. Plant Soil 159:69–78

Badri A, Stefani FO, Lachance G, Roy-Arcand L, Beaudet D, Vialle A, Hijri M (2016) Molecular diagnostic toolkit for Rhizophagus irregularis isolate DAOM-197198 using quantitative PCR assay targeting the mitochondrial genome. Mycorrhiza 26:721–733. https://doi.org/10.1007/s00572-016-0708-1 PubMed DOI

Barea JM, Pozo MJ, López-Ráez JA, Aroca R, Ruiz-Lozano JM, Ferrol N, Azcón R, Azcón-Aguilar C (2013) Arbuscular Mycorrhizas and their Significance in Promoting Soil-Plant System Sustainability against Environmental Stresses. In: Belén M, González-López J (eds) Beneficial Plant-microbial Interactions. Ecology and Applications. CRC Press, Taylor & Francis Group, Boca Raton London New York, pp 353–387

Bayrami S, Mirshekari B, Farahvash F (2012) Response of potato (Solanum tuberosum cv. Agria) to seed inoculation with mycorrhiza strains in different phosphorus fertilization. J Food Agric Environ 10:726–728

Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87:99–108. https://doi.org/10.1007/s00253-010-2585-4 PubMed DOI

Berruti A, Desirò A, Visentin S, Zecca O, Bonfante P (2017) ITS fungal barcoding primers versus 18S AMF-specific primers reveal similar AMF-based diversity patterns in roots and soils of three mountain vineyards. Environmental Microbiology Reports 9(5):658–667. https://doi.org/10.1111/1758-2229.12574 PubMed DOI

Binet MN, van Tuinen D, Souard F et al (2017) Responses of above- and below-ground fungal symbionts to cessation of mowing in subalpine grassland. Fungal Ecol 25:14–21. https://doi.org/10.1016/j.funeco.2016.10.001 DOI

Börstler B, Thiéry O, Sýkorová Z, Berner A, Redecker D (2010) Diversity of mitochondrial large subunit rDNA haplotypes of Glomus intraradices in two agricultural field experiments and two semi-natural grasslands. Mol Ecol 19:1497–1511. https://doi.org/10.1111/j.1365-294X.2010.04590.x PubMed DOI

Brito I, Goss MJ, Carvalho M, Chatagnier O, van Tuinen D (2012) Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil Till Res 121:63–67. https://doi.org/10.1016/j.still.2012.01.012 DOI

Brito I, Goss MJ, Alho L, Brígido C, van Tuinen D, Félix MR, Carvalho M (2018) Agronomic management of AMF functional diversity to overcome biotic and abiotic stresses - the role of plant sequence and intact extraradical mycelium. Fungal Ecol. https://doi.org/10.1016/j.funeco.2018.06.001

Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

Buysens C, Alaux PL, César V, Huret S, Declerck S, Cranenbrouck S (2017) Tracing native and inoculated Rhizophagus irregularis in three potato cultivars (Charlotte, Nicola and Bintje) grown under field conditions. Appl Soil Ecol 115:1–9

Cesaro P, van Tuinen D, Copetta A, Chatagnier O, Berta G, Gianinazzi S, Lingua G (2008) Preferential Colonization of Solanum tuberosumL. roots by the Fungus Glomus intraradicesin Arable Soil of a Potato Farming Area. Appl Environ Microbiol 74:5776–5783. https://doi.org/10.1128/AEM.00719-08 PubMed DOI PMC

Crossay T, Antheaume C, Redecker D, Bon L, Chedri N, Richert C, Guentas L, Cavaloc Y, Amir H (2017) New method for the identification of arbuscular mycorrhizal fungi by proteomic-based biotyping of spores using MALDI-TOF-MS. Sci Rep 7:14306. https://doi.org/10.1038/s41598-017-14487-6 PubMed DOI PMC

Davison J, Moora M, Öpik M et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.1126/science.aab1161 PubMed DOI

Demir S, Sipahioglu HM, Kaya I, Usta M, Savur OB (2011) Detection of arbuscular mycorrhizal fungi within colonised roots of the Gramineae family members by nested-polymerase chain reaction (PCR). Archives of Phytopathology and Plant Protection 44:1061–1067. https://doi.org/10.1080/03235401003755221 DOI

Farmer MJ, Li X, Feng G, Zhao B et al (2007) Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl Soil Ecol 35:599–609

Furrazola E, Covacevich F, Torres-Arias Y, et al (2015) Functionality of arbuscular mycorrhizal fungi in three plant communities in the Managed Floristic Reserve San Ubaldo-Sabanalamar, Cuba. Rev Biol Trop 63:341–356. ISSN-0034–7744

Furrazola E, Ojeda L, Hernández C (2016) Mycorrhizal colonization and species of arbuscular mycorrhizal fungi in grasses from the Cuenca Pecuaria “El Tablón”, Cienfuegos. Cuba. Cuban J Agr Sci 50:321–331

Gamper H, Leuchtmann A (2007) Taxon-specific PCR primers to detect two inconspicuous arbuscular mycorrhizal fungi from temperate agricultural grassland. Mycorrhiza 17:145–152 PubMed

Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes – application to the identification of mycorrhizae and rusts. Mol Ecol Not 2:113–118 PubMed

Gerdemann JW, Nicolson TH (1963) Spore of mycorrhizae endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244. ISSN 0007–1536

Giovannetti M, Mosse B (1980) An evaluation of techniques to measure vesicular-arbuscular infection in roots. New Phytol 84:489–500

Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117 PubMed

González PJ, Ramírez JF, Rivera R, Hernández A, Crespo G (2016a) Effectiveness of inoculation of two forage legumes grown on two soil types with arbuscular mycorrhizal fungi. Tropical Grasslands-Forrajes Tropicales 4:82–90

González PJ, Ramírez JF, Rivera R, Hernández A, Crespo G (2016b) Critical levels of phosphorus in the soil for forage legumes, inoculated with arbuscular mycorrhizal fungi. Technical Note, Cuban J Agr Sci 50:315–300

González PJ, Ramírez JF, Rivera R et al (2015) Management of arbuscular mycorrhizal inoculation for the establishment, maintenance and recovery of grasslands. Cuban J Agr Sci 49:535–540

Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35

Grace C, Stribley D (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162. https://doi.org/10.1016/S0953-7562(09)80005-1 DOI

Hamel C, Strullu DG (2006) Arbuscular mycorrhizal fungi in field crop production: potential and new direction. Can J Plant Sci 86:941–950

Herrera-Peraza RA, Hamel Ch, Fernández F, Ferrer RL, Furrazola E (2011) Soil-strain compatibility: the key to effective use of arbuscular mycorrhizal inoculants? Mycorrhiza 21:183–193. https://doi.org/10.1007/s00572-010-0322-6 PubMed DOI

Herrera-Peraza RA, Ferrer RL, Sieverding E (2003) Glomus brohultii: a new species in the arbuscular mycorrhizal forming glomerales. J Appl Bot 77:37–40

Hijri M (2016) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26:209–214 PubMed

Jacquemyn H, Deja A, De hert K, Cachapa Bailarote B, Lievens B, (2012) Variation in mycorrhizal associations with tulasnelloid fungi among populations of five Dactylorhiza species. PLoS ONE 7:e42212. https://doi.org/10.1371/journal.pone.0042212 PubMed DOI PMC

Janoušková M, Krak K, Vosátka M, Püschel D, Štorchová H (2017) Inoculation effects on root-colonizing arbuscular mycorrhizal fungal communities spread beyond directly inoculated plants. PLoS ONE 12:1–21. https://doi.org/10.1371/journal.pone.0181525 DOI

Joao JP, Rivera R, Martín G, Riera M, Simó J (2017) Integrated nutrition system with AMF, green manure and mineral fertilizer in Manihot esculenta Crantz. Cultivos Tropicales 38:117–128

Johansen RB, Vestberg M, Burns BR, Park D, Hooker JE, Johnston PR (2015) A coastal sand dune in New Zealand reveals high arbuscular mycorrhizal fungal diversity. Symbiosis 66:111–121. https://doi.org/10.1007/s13199-015-0355-x DOI

Köhl L, Oehl F, van der Heijden MGA (2014) Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecol Appl 24:1842–1853 PubMed

Köhl L, Lukasiewicz CE, van der Heijden MGA (2015) Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant, Cell Environ 39:136–146

Krak K, Janoušková M, Caklová P, Vosátka M, Štorchová H (2012) Intraradical dynamics of two coexisting isolates of the arbuscular mycorrhizal fungus Glomus intraradices sensu lato as estimated by real-time PCR of mitochondrial DNA. Appl Environ Microbiol 78:3630–3637. https://doi.org/10.1128/AEM.00035-12 PubMed DOI PMC

Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984 PubMed

Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223. https://doi.org/10.1111/j.1469-8137.2009.02835.x PubMed DOI

Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874 PubMed PMC

Manter DK, Vivanco JM (2007) Use of the ITS primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. J of Microbiol Meth 71:7–14

Martín GM, Tamayo Y, Ramírez JF, Varela M, Rivera R (2017) Relación entre la respuesta de Canavalia ensiformis a la inoculación micorrízica y algunas propiedades químicas del suelo. Cultivos Tropicales 38:24–29

Martín GM, Arias L, Rivera R (2010) Selección de las cepas de hongos micorrízicos arbusculares (HMA) más efectivas para la Canavalia ensiformis cultivada en suelo Ferralítico Rojo. Cultivos Tropicales 31:27–31

Millner PD, Mulbry WW, Reynolds SL (2001) Taxon-specific oligonucleotide primers for detection of two ancient endomycorrhizal fungi, Glomus occultum and Glomus brasilianum. FEMS Microbiol Let 196:165–170

Morejón M, Herrera JA, Ayra C, González PJ, Rivera R, Fernández Y, Peña E, Téllez P, Rodríguez-de la Noval C, de la Noval-Pons BM (2017) Alternatives in nutrition of transgenic maize FR-Bt1 (Zea mays L.): response in growth, development and production. Cultivos Tropicales 38:146–155

Morgan BST, Egerton-Warburton LM (2017) Barcoded NS31/AML2 primers for sequencing of arbuscular mycorrhizal comm unities in environmental samples. Applications in Plant Sciences 5(8):1700017. https://doi.org/10.3732/apps.1700017 DOI

Öpik M, Davison J (2016) Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecol 24B:106–113. https://doi.org/10.1016/j.funeco.2016.07.005 DOI

Pellegrino E, Opik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217. https://doi.org/10.1016/j.soilbio.2015.02.020 DOI

Pellegrino E, Turrini A, Gamper HA, Cafà G, Bonari E, Young JPW, Giovannetti M (2012) Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822 PubMed

Pivato B, Mazurier S, Lemanceau P, Siblot S, Berta G, Mougel C, van Tuinen D (2007) Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol 176:197–210. https://doi.org/10.1111/j.1469-8137.2007.02151.x PubMed DOI

Plenchette C, Clermont-Dauphin C, Meynard JM, Fortin JA (2005) Managing arbuscular mycorrhizal fungi in cropping systems. Can J Plant Sci 85:31–40

Priyadharsini P, Muthukumar T (2015) Insight into the Role of Arbuscular Mycorrhizal Fungi in Sustainable Agriculture. In: Thangavel P, Sridevi G (eds), Environmental Sustainability, Springer India, pp 3–37. https://doi.org/10.1007/978-81-322-2056-5-1

Redecker D (2000) Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10:73–80. https://doi.org/10.1007/s005720000061 DOI

Řezáčová V, Gryndler M, Bukovská P, Šmilauer P, Jansa J (2016) Molecular community analysis of arbuscular mycorrhizal fungi - Contributions of PCR primer and host plant selectivity to the detected community profiles. Pedobiologia - International J Soil Biol 59:179–187. https://doi.org/10.1016/j.pedobi.2016.04.002 DOI

Rivera R, Fernández F (2006) Inoculation and management of mycorrhizal fungi within tropical agroecosystems. In: Uphoff N, Ball AS, Fernandes E et al (eds) Biological approaches to sustainable soil systems, CRC Press, Taylor & Francis Group. Boca Raton, Florida, USA, pp 479–489

Rivera R, Fernández F, Fernández K, Ruiz L, Sánchez C, Riera M (2007) Advances in the management of effective arbuscular mycorrhizal symbiosis in tropical ecosystems. In: Hamel Ch, Plenchette C (eds) Mycorrhizae in Crop Production. Haworth Press, Binghamton, NY, pp 151–196

Rodríguez Y, Dalpé Y, Séguin S, Fernández K, Fernández F, Rivera RA (2011) Glomus cubense sp. nov., an arbuscular mycorrhizal fungus from Cuba. Mycotaxon 118:337–347

Rosales PR, González PJ, Ramírez JF, Arzola J (2017) Selección de cepas eficientes de hongos micorrízicos arbusculares para el pasto guinea (Megathyrsus maximus cv. Likoni). Cultivos Tropicales 38:24–30

Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New York

Sánchez-Castro I, Ferrol N, Barea JM (2012) Analyzing the community composition of arbuscular mycorrhizal fungi colonizing the roots of representative shrubland species in a Mediterranean ecosystem. J of Arid Environments 80:1–9

Schenck NC, Spain JL, Sieverding E, Howeler RH (1984) Several new and unreported vesicular-arbuscular mycorrhizal fungi (Endogonaceae) from Colombia. Mycologia 76:685–699

Schmidt PA, Bálint M, Greshake B, Bandowa C, Römbke J, Schmitt I (2013) Illumina metabarcoding of a soil fungal community. Soil Biol Biochem 65:128–132

Schoch C, Seifert K, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241–6246 PubMed

Schütz L, Gattinger A, Meier M, Müller A, Boller T, Mäder P, Mathimaran N (2018) Improving crop yield and nutrient use efficiency via biofertilization-A global meta-analysis. Frontiers in Plant Science 8:2204. https://doi.org/10.3389/fpls.2017.02204 PubMed DOI PMC

Shrivastava A, Gupta VB (2011) Methods for the determination of limit of detection and limit of quantitation of the analytical methods. Chron Young Sci 2:21–25

Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295 PubMed PMC

Smith S, Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London

Spatafora JW, Chang Y, Benny GL et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042 PubMed DOI PMC

Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474 PubMed

Sýkorová Z, Börstle B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, Redecker D (2012) Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalarisarun dinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers. Mycorrhiza 22:69–80. https://doi.org/10.1007/s00572-011-0375-1 PubMed DOI

Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174

Thiéry O, Vasar M, Jairus T et al (2016) Sequence variation in nuclear ribosomal small subunit, internal transcribed spacer and large subunit regions of Rhizophagus irregularis and Gigaspora margarita is high and isolate-dependent. Mol Ecol 25:2816–2832. https://doi.org/10.1111/mec.13655 PubMed DOI

Thioye B, van Tuinen D, Kane A et al (2019) Tracing Rhizophagus irregularis isolate IR27 in Ziziphus mauritiana roots under field conditions. Mycorrhiza 29:77–83. https://doi.org/10.1007/s00572-018-0875-3 PubMed DOI

Thonar C, Erb A, Jansa J (2012) Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities-marker design, verification, calibration and field validation. Mol Ecol Resour 12:219–232. https://doi.org/10.1111/j.1755-0998.2011.03086.x PubMed DOI

Torres-Arias Y, Ortega R, Nobre C, Furrazola E, Louro-Berbara RL (2017) Production of native arbuscular mycorrhizal fungi inoculum under different environmental conditions. Braz J Microbiol 48:87–94 PubMed

Torres-Arias Y, Ortega R, González S, Furrazola E (2015) Diversidad de hongos micorrizógenos arbusculares (Glomeromycota) en bosques semicaducifolios de la Ciénaga de Zapata. Cuba. Revista del Jardín Botánico Nacional 36:195–200

Trouvelot A, Kough J, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’ un systeme radiculaire. Recherche de methodes d’estimation ayantune significantion fonctionnelle. Proceedings of the 1st European Symposium on Mycorrhizae: Physiological and Genetical Aspects of Mycorrhizae, Dijón, 1–5 July, 1985. (Gianinazzi-Pearson V, Gianinazzi S (Eds). INRA, Paris. p. 217–222

van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998a) Characterization of root colonization profiles by a microcosm of arbuscular mycorrhizal fungi using 25S rDNA targeted nested PCR. Mol Ecol 7:879–887

van Tuinen D, Zhao B, Gianinazzi-Pearson V (1998b) PCR in studies of AM fungi: from primers to application. In: Varma AK (ed) Mycorrhiza Manual. Springer-Verlag, Heidelberg, pp 387–400

Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109. https://doi.org/10.1111/j.1469-8137.2012.04348.x PubMed DOI

Voříšková A, Jansa J, Püschel D, Krüger M, Cajthaml T, Vosátka M, Janoušková M (2017) Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference? Mycorrhiza 27:577–585. https://doi.org/10.1007/s00572-017-0777-9 PubMed DOI

Wang Y, Huang Y, Qiu Q, Xin G, Yang Z, Shi S (2011) Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS ONE 6:e24512. https://doi.org/10.1371/journal.pone.0024512 PubMed DOI PMC

White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand H, Sninsky JS, White TJ (eds) PCR-Protocols and Applications-A Laboratory Manual. Academic Press, New York, pp 315–322

Yang C, Ellouze W, Navarro-Borrell A et al (2014) Management of the arbuscular mycorrhizal symbiosis in sustainable crop production. In: Solaiman Z, Abbott L, Varma A (eds) Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration. Springer, Berlin, pp 89–117

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