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Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes

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Abstract

Arbuscular mycorrhizal (AM) fungi can affect many different micronutrients and macronutrients in plants and also influence host volatile compound synthesis. Their effect on the edible portions of plants is less clear. Two separate studies were performed to investigate whether inoculation by AM fungi (Rhizophagus irregularis, Funneliformis mosseae, or both) can affect the food quality of tomato fruits, in particular common minerals, antioxidants, carotenoids, a suite of vitamins, and flavor compounds (sugars, titratable acids, volatile compounds). It was found that AM fungal inoculation increased the nutrient quality of tomato fruits for most nutrients except vitamins. Fruit mineral concentration increased with inoculation (particularly N, P, and Cu). Similarly, inoculated plants had fruit with higher antioxidant capacity and more carotenoids. Furthermore, five volatile compounds were significantly higher in AM plants compared with non-AM controls. Taken together, these results show that AM fungi represent a promising resource for improving both sustainable food production and human nutritional needs.

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References

  • Akiyama K, Hayashi H (2002) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotech Biochem 66:763–769

    Google Scholar 

  • Al-Karaki GN, Clark RB (1999) Varied rates of mycorrhizal inoculum on growth and nutrient acquisition by barley grown with drought stress. J Plant Nutr 22:1775–1784

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Hammad R (2001) Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. J Plant Nutr 24:1311–1323

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Al-Raddad A, Clark RB (1998) Water stress and mycorrhizal isolate effects on growth and nutrient acquisition of wheat. J Plant Nutr 21:891–902

    Article  CAS  Google Scholar 

  • Allen MF, Smith WK, Moore TS, Christensen M, Allen F (1981) Comparative water relations and photosynthesis of mycorrhizal and non-mycorrhizal Bouteloua gracilis H.B.K. Lag Ex Steud. New Phytol 88:683–693

    Article  Google Scholar 

  • Anonymous (1992) Kleur-stadia tomaten. Central Bureau van de Tuibouwveilingen in Nederland (Ed.), 2803 PE Gouda

  • Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514

    Article  PubMed  Google Scholar 

  • Antunes PM, Franken P, Schwarz D, Rillig M, Cosme M, Scott M, Hart MM (2012) Linking soil biodiversity to human health: do arbuscular mycorrhizal fungi contribute to food nutrition? In: Wall D, Bardgett RD, Behan-Pelletier V, Herrick JE, Jones H, Ritz K, Six J, Strong DR, van der Putin WH (eds) Soil ecology and ecosystem services. Oxford University Press, Oxford, pp 153–172

    Chapter  Google Scholar 

  • Araim G, Saleem A, Arnason JT, Charest C (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus increases growth and secondary metabolism of purple coneflower, Echinacea purpurea (L.) Moench. J Agr Food Chem 57:2255–2258

    Article  CAS  Google Scholar 

  • Azcón R, Barea JM (1992) The effect of vesicular-arbuscular mycorrhizae in decreasing Ca acquisition by alfalfa plants in calcareous soils. Biol Fert Soils 13:155–159

    Google Scholar 

  • Azcón R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165:1137–1145

    Article  Google Scholar 

  • Baldwin EA, Scott JW, Einstein MA, Malundo TMM, Carr BT, Shewfelt RL, Tando KS (1998) Relationship between sensory and instrumental analysis of tomato flavor. J Am Soc Horti Sci 123:906–915

    CAS  Google Scholar 

  • Barea JM, Azcón R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351

    Article  CAS  PubMed  Google Scholar 

  • Baslam M, Goicoechea N (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22:347–359

    Article  CAS  PubMed  Google Scholar 

  • Baslam M, Garmendia I, Goicoechea N (2011a) Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. J Agr Food Chem 59:5504–5515

    Article  CAS  Google Scholar 

  • Baslam M, Pascual I, Sánchez-Díaz M, Erro J, García-Mina JM, Goicoechea N (2011b) Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition. J Agri Food Chem 59:11129–11140

    Article  CAS  Google Scholar 

  • Blee KA, Anderson AJ (1996) Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices Schenck and Smith. Plant Physiol 110:675–688

    CAS  PubMed Central  PubMed  Google Scholar 

  • Böhm V (2012) Lycopene and heart health. Mol Nutr Food Res 56:296–303

    Article  PubMed  Google Scholar 

  • Buttery RG, Ling LC (1993) Volatile components of tomato fruit and plant parts: relationship and biogenesis. In Bioactive volatile compounds from Plants. American Chemical Society, Washington

    Book  Google Scholar 

  • Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R, Cárdenas-Navarro R (2010) Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria x ananassa Duch.) at different nitrogen levels. J Sci Food Agr 90:1774–1782

    CAS  Google Scholar 

  • Ceballos I, Ruiz M, Fernández C, Peña R, Rodríguez A, Sanders IR (2013) The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS One 8:e70633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cebolla-Cornejo J, Rosello S, Valcarcel M, Serrano E, Beltran J, Nuez F (2011) Evaluation of genotype and environment effects on taste and aroma flavor components of Spanish fresh tomato varieties. J Agr Food Chem 59:2440–2450

    Article  CAS  Google Scholar 

  • Chaudhary V, Kapoor R, Bhatnagar AK (2008) Effectiveness of two arbuscular mycorrhizal fungi on concentrations of essential oil and artemisinin in three accessions of Artemisia annua L. Appl Soil Ecol 40:174–181

    Article  Google Scholar 

  • Clark RB, Zeto SK (1996) Mineral acquisition by mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1495–1503

    Article  CAS  Google Scholar 

  • Conversa G, Lazzizera C, Bonasia A, Elia A (2012) Yield and phosphorus uptake of a processing tomato crop grown at different phosphorus levels in a calcareous soil as affected by mycorrhizal inoculation under field conditions. Biol Fert Soils 49:691–703

    Article  Google Scholar 

  • Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494

    Article  CAS  PubMed  Google Scholar 

  • Copetta A, Bardi L, Bertolone E, Berta G (2011) Fruit production and quality of tomato plants (Solanum lycopersicum L.) are affected by green compost and arbuscular mycorrhizal fungi. Plant Biosyst 145:106–115

    Article  Google Scholar 

  • Cosme M, Franken P, Mewis I, Baldermann S, Wurst S (2014) Arbuscular mycorrhizal fungi affect glucosinolate and mineral element composition in leaves of Moringa oleifera. Mycorrhiza. doi:10.1007/s00572-014-0574-7

    PubMed  Google Scholar 

  • Cunningham FX (2002) Regulation of carotenoid synthesis and accumulation in plants. Pure Appl Chem 74:1409–1417

    Article  CAS  Google Scholar 

  • Egea I, Waniping B, Barsan C, Jauneau A, Pech JC, Latche A, Li Z, Chervin C (2011) Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and line-lapse recording on intact live tissue. Ann Bot 108:291–297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Farmer MJ, Li X, Feng G, Zhao B, Chatagnier O, Gianinazzi S, Gianinazzi-Perason V, Van T (2007) Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl Soil Ecol 35:599–609

    Article  Google Scholar 

  • Farneti B, Cristescu SM, Costa G, Harren FJM, Woltering EJ (2012) Rapid tomato volatile profiling by using proton-transfer reaction mass spectrometry (PTR-MS). J Food Sci 77:C551–C559

    Article  CAS  PubMed  Google Scholar 

  • Fiorill V, Catoni M, Miozz L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987

    Article  Google Scholar 

  • Food and Agriculture Organization. 2012. Production of tomato by countries. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor. Accessed 21 Feb 2014

  • Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions : the importance of a community approach. Environ Entomol 38:93–102

    Article  PubMed  Google Scholar 

  • Gericke S, Kurmies B (1952) The colorimetric determination of phosphoric acid ammonium vanadate molybdate and its application in plant analysis. J Plant Nutr Soil Sci 159:11–21

    Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi : getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    Article  PubMed Central  PubMed  Google Scholar 

  • Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D et al (2012) Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Brit J Nutr 107:242–251

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Avio L, Sbrana C (2013) Improvement of nutraceutical value of food by plant symbionts. In: K.G. Ramawat, J.M. Me’rillon (eds) Natural Products. Springer, Berlin Heidelberg, p 2641–2662

  • Gonzalez-Chavez C, Haen JD, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240:287–297

    Article  CAS  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Gupta ML, Prasad A, Ram M, Kumar S (2002) Short communication effect of the vesicular ± arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis). Bioresource Technol 81:2001–2003

    Article  Google Scholar 

  • Hamel C, Dalpe Y, Lapierre C, Simard RR, Smith DL (1996) Endomycorrhizae in a newly cultivated acidic meadow: effects of three years of barley cropping, tillage, lime, and phosphorus on root colonization and soil infectivity. Biol Fert Soils 21:160–165

    Article  Google Scholar 

  • Hart MM, Forsythe JA (2012) Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; benefits in addition to phosphorus. Sci Hortic 148:206–214

    Article  CAS  Google Scholar 

  • He X, Nara K (2007) Element biofortification: can mycorrhizas potentially offer a more effective and sustainable pathway to curb human malnutrition? Trends Plant Sci 12:331–333

    Article  CAS  PubMed  Google Scholar 

  • Jackson LE, Miller D, Smith SE (2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Sci Hortic 94:205–218

    Article  Google Scholar 

  • Jansa J, Ozafar AM, Rossard EF (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488

    Article  CAS  Google Scholar 

  • Jurkiewicz A, Ryszka P, Anielska T, Waligórski P, Białońska D, Góralska K, Tsimilli-Michael M, Turnau K (2010) Optimization of culture conditions of Arnica montana L.: effects of mycorrhizal fungi and competing plants. Mycorrhiza 20:293–306

    Article  PubMed  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2002) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L) and Carum (Trachyspermum ammi Linn). World J Microb Biot 18:459–463

    Article  CAS  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil yield and quality in Foeniculum vulgare mill on mycorrhizal inoculation supplemented with P-fertilizer. Bioresource Technol 93:307–311

    Article  CAS  Google Scholar 

  • Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587

    Article  CAS  PubMed  Google Scholar 

  • Kaya C, Higgs D, Kirnak H, Tas I (2003) Mycorrhizal colonisation improves fruit yield and water use efficiency in watermelon (Citrullus lanatus Thunb.) grown under well-watered and water-stressed conditions. Plant Soil 253:287–292

    Article  CAS  Google Scholar 

  • Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446

    Article  CAS  PubMed  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kothari SK, Marschner H, Romheld V (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L.) in a calcareous soil. New Phytol 116:637–645

    Article  CAS  Google Scholar 

  • Krumbein A, Auerwald H (1998) Characterization of aroma volatiles in tomatoes by sensory analysis. Nahrung/Food 42:395–399

    Article  CAS  Google Scholar 

  • Krumbein A, Schwarz D (2013) Grafting: a possibility to enhance health-promoting and flavor compounds in tomato fruits of shaded plants? Sci Hortic 149:97–107

    Article  CAS  Google Scholar 

  • Krumbein A, Peters P, Brückner B (2004) Flavour compounds and a quantitative descriptive analysis of tomatoes (Lycopersicon esculentum Mill.) of different cultivars in short-term storage. Postharvest Biol Tech 32:15–28

    Article  CAS  Google Scholar 

  • Krumbein A, Schwarz D, Kläring HP (2006) Effects of environmental factors on carotenoid content in tomato (Lycopersicon esculentum Mill.) grown in a greenhouse. J Appl Bot Food Qual 80:160–164

    CAS  Google Scholar 

  • Latef AAH, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127:228–233

    Article  Google Scholar 

  • Lee J, Scagel CF (2009) Chicoric acid found in basil (Ocimum basilicum L.) leaves. Food Chem 115:650–656

    Article  CAS  Google Scholar 

  • Li X, Marschner H, George E (1991) Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 136:49–57

    Article  CAS  Google Scholar 

  • Li H, Smith FA, Dickson S, Holloway RE, Smith SE (2008) Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol 178:852–862

    Article  PubMed  Google Scholar 

  • Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, Cantamessa S, Copetta A, D’Agostino G, Gamalero E, Berta G (2013) Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads increases anthocyanin concentration in strawberry fruits (Fragaria x ananassa var. Selva) in conditions of reduced fertilization. Int J Mol Sci 14:16207–16225

    Article  PubMed Central  PubMed  Google Scholar 

  • Lisiewska Z, Kmiecik W (2000) Effect of storage period and temperature on the chemical composition and organoleptic quality of frozen tomato cubes. Food Chem 70:167–173

    Article  CAS  Google Scholar 

  • Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336

    Article  CAS  Google Scholar 

  • Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 109:465–470

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizai symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • McGonigle T, Miller M (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 

  • Medeiros CAB, Clark RB, Ellis JR (1994) Growth and nutrient uptake of sorghum cultivated with vesicular-arbuscular mycorrhiza isolates at varying pH. Mycorrhiza 4:185–191

    Article  Google Scholar 

  • Nair A, Bhargava S (2012) Reduced mycorrhizal colonization (rmc) tomato mutant lacks expression of SymRK signaling pathway genes. Plant Signal Behav 7:1578–1583

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nzanza B, Marais D, Soundy P (2012) Yield and nutrient content of tomato (Solanum lycopersicum L.) as influenced by Trichoderma harzianum and Glomus mosseae inoculation. Sci Hortic 144:55–59

    Article  CAS  Google Scholar 

  • Orujei Y, Shabani L, Sharifi-Tehrani M (2013) Induction of glycyrrhizin and total phenolic compound production in licorice by using arbuscular mycorrhizal fungi. Russ J Plant Physl 60:855–860

    Article  CAS  Google Scholar 

  • Oyarzun P, Gerlagh M, Hoagland AE (1993) Pathogenic fungi involved in root-rot of peas in the Netherlands and their physiological specialization. Neth J Plant Pathol 99:23–33

    Article  Google Scholar 

  • Perner H, Schwarz D, Krumbein A, Li X, George E (2007) Influence of nitrogen forms and mycorrhizal colonization on growth and composition of Chinese bunching onion. J Plant Nutr Soil Sci 170:762–768

    Article  CAS  Google Scholar 

  • Perner H, Rohn S, Driemel G, Batt N, Schwarz D, Kroh LW, George E (2008) Effect of nitrogen species supply and mycorrhizal colonization on organosulfur and phenolic compounds in onions. J Agr Food Chem 56:3538–3545

    Article  CAS  Google Scholar 

  • Philips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesiculararbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–61

  • Poiroux-Gonord F, Fanciullino AL, Poggi I, Urban L (2012) Carbohydrate control over carotenoid build up in conditional on fruit ontogeny in clementine fruits. Physiol Plant 147:417–431

    Article  PubMed  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124

    Article  CAS  Google Scholar 

  • Raju PS, Clark RB, Ellis JR, Maranville JW (1990) Effects of species of VA-mycorrhizal fungi on growth and mineral uptake of sorghum at different temperatures. Plant Soil 121:165–170

    Article  CAS  Google Scholar 

  • Rasouli-Sadaghiani M, Hassani A, Barin M, Danesh YR, Sefidkon F (2010) Effects of arbuscular mycorrhizal fungi on growth, essential oil production and nutrients uptake in basil. J Med Plants Res 4:2222–2228

    CAS  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Royal Society (2009) Reaping the benefits: Science and the sustainable intensification of global agriculture. Royal Society Policy document 11/09.

  • Rubio R, Borie F, Schalchli C, Castillo C, Azcón R (2002) Plant growth responses in natural acidic soil as affected by arbuscular mycorrhizal inoculation and phosphorus sources. J Plant Nutr 25:1389–1405

    Article  CAS  Google Scholar 

  • Russo V, Perkins-Veazie P (2010) Yield and nutrient content of bell pepper pods from plants developed from seedlings inoculated, or not, with microorganisms. Hort Sci 45:352–358

    Google Scholar 

  • Salvioli A, Zouari I, Chalot M, Bonfante P (2012) The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biol 12:44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santos J, Mendiola JA, Oliveira MB, Ibáñez E, Herrero M (2012) Sequential determination of fat- and water-soluble vitamins in green leafy vegetables during storage. J Chromatogr 1261:179–188

    Article  CAS  Google Scholar 

  • Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546

    Article  CAS  PubMed  Google Scholar 

  • Schreiner M, Mewis I, Huyskens-Keil S, Jansen M, Zrenner R, Winkler J, O’Brien N, Krumbein A (2012) UV-B-induced secondary plant metabolites—potential benefits for plant and human health. Crit Rev Plant Sci 31:229–240

    Article  CAS  Google Scholar 

  • Smith SE, Smith FAA, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  • Stewart LI, Hamel C, Hogue R, Moutoglis P (2005) Response of strawberry to inoculation with arbuscular mycorrhizal fungi under very high soil phosphorus conditions. Mycorrhiza 15:612–619

    Article  CAS  PubMed  Google Scholar 

  • Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34

    Article  CAS  PubMed  Google Scholar 

  • Toussaint J, St. Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices and Ri T-DNA roots of Daucus carota in an in vitro compartmented system. Can J Microbiol 50:251–260

    Article  CAS  PubMed  Google Scholar 

  • Toussaint J-P, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297

    Article  CAS  PubMed  Google Scholar 

  • Ulrichs C, Fische G, Büttner C, Mewis I (2008) Comparison of lycopene, β-carotene and phenolic contents of tomato using conventional and ecological horticultural practices, and arbuscular mycorrhizal fungi (AMF). Agron Colomb 26:1–12

    Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vierheilig H, Gagnon H, Strack D, Maier W (2000) Accumulation of cyclohexenone derivatives in barley, wheat and maize roots in response to inoculation with different arbuscular mycorrhizal fungi. Mycorrhiza 9:291–293

    Article  CAS  Google Scholar 

  • Wahb-Allah M, Abdel-Razzak H, Aslsdon A, Ibrahim A (2014) Growth, yield, fruit quality and water use efficiency of tomato under arbuscular mycorrhizal inoculation and irrigation level treatments. Life Sci J 11:109–117

    Google Scholar 

  • Watts-Williams SJ, Turney TW, Patti AF, Cavagnaro TR (2014) Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant Soil 376:165–175

    Article  CAS  Google Scholar 

  • Zeng Y, Guo L-P, Chen B-D, Hao Z-P, Wang J-Y, Huang L-Q, Yang G, Cui X-M, Yang L, Wu Z-X et al (2013) Arbuscular mycorrhizal symbiosis and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23:253–265

    Article  CAS  PubMed  Google Scholar 

  • Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2012) Arbuscular mycorrhizal fungal inoculation Increases phenolic synthesis in clover roots via hydrogen peroxide, salicyclic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79

    Article  PubMed  Google Scholar 

  • Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542

    Article  CAS  Google Scholar 

  • Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, Bagnaresi P, Bonfante P (2014) From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15:221

    Article  PubMed Central  PubMed  Google Scholar 

  • Zubek S, Stojakowska A, Anielska T, Turnau K (2010) Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L. Mycorrhiza 20:497–504

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank NSERC (Discovery Grants) and the Alexander von Humboldt Foundation (Early Researchers) for funding (MMH). Thank you to Alicia Tymstra for help with references. Thanks also to Tom Helmer and Katie Axwik for technical assistance.

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Authors and Affiliations

  1. Biology, University of British Columbia Okanagan, Kelowna, BC, V1V 1 V7, Canada

    Miranda Hart & Connie Leung

  2. Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, Agassiz, BC, V0M 1A0, Canada

    David L. Ehret

  3. Leibniz-Institute of Vegetable and Ornamental Crops (IGZ), Theodor-Echtermeyer-Weg 1, 14979, Großbeeren, Germany

    Angelika Krumbein & Philipp Franken

  4. Chemistry, University of British Columbia Okanagan, Kelowna, Canada

    Susan Murch & Christina Turi

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  1. Miranda Hart
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  2. David L. Ehret
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  4. Connie Leung
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  5. Susan Murch
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Correspondence to Miranda Hart.

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Hart, M., Ehret, D.L., Krumbein, A. et al. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 25, 359–376 (2015). https://doi.org/10.1007/s00572-014-0617-0

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  • DOI: https://doi.org/10.1007/s00572-014-0617-0

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