Skip to main content
SpringerLink
Log in

Impact of arbuscular mycorrhizal fungi on the allergenic potential of tomato

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal (AM) fungi influence the expression of defence-related genes in roots and can cause systemic resistance in plants probably due to the induced expression of specific defence proteins. Among the different groups of defence proteins, plant food allergens were identified. We hypothesized that tomato-allergic patients differently react to tomatoes derived from plants inoculated or not by mycorrhizal fungi. To test this, two tomato genotypes, wild-type 76R and a nearly isogenic mycorrhizal mutant RMC, were inoculated with the AM fungus Glomus mosseae or not under conditions similar to horticultural practice. Under such conditions, the AM fungus showed only a very low colonisation rate, but still was able to increase shoot growth of the wild-type 76R. Nearly no colonisation was observed in the mutant RMC, and shoot development was also not affected. Root fresh weights were diminished in AM-inoculated plants of both genotypes compared to the corresponding controls. No mycorrhizal effects were observed on the biomass and the concentration of phosphate and nitrogen in fruits. Real-time quantitative polymerase chain reaction analysis revealed that six among eight genes encoding for putative allergens showed a significant induced RNA accumulation in fruits of AM-colonised plants. However, human skin reactivity tests using mixed samples of tomato fruits from the AM-inoculated and control plants showed no differences. Our data indicate that AM colonisation under conditions close to horticultural practice can induce the expression of allergen-encoding genes in fruits, but this does not lead necessarily to a higher allergenic potential.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 

  • Allen MF, Moore TS Jr, Christensen M (1980) Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae: I. Cytokinin increases in the host plant. Can J Bot 58:317–374

    Google Scholar 

  • Altmann F (2007) The role of protein glycosylation in allergy. Int Arch Allergy Immunol 142:99–115

    Article  CAS  PubMed  Google Scholar 

  • Anonymous (1992) Kleur-stadia tomaten. Centraal Bureau van de Tuinbouwveilingen in Nederland (ed) 2803 PE Gouda

  • Asero R, Mistrello G, Roncarolo D, De Vries SC, Gautier MF, Ciurana CLF, Verbeek E, Mohammadi T, Knul-Brettlova V, Akkerdaas JH, Bulder I, Aalberse RC, Van Ree R (2000) Lipid transfer protein: A pan-allergen in plant-derived foods that is highly resistant to pepsin digestion. Int Arch Allergy Immunol 122:20–32

    Article  CAS  PubMed  Google Scholar 

  • Ballmer-Weber BK, Hoffmann A, Wüthrich B, Lüttkopf D, Pompei C, Wangorsch A, Kästner M, Vieths S (2002) Influence of food processing on the allergenicity of celery: DBPCFC with celery spice and cooked celery in patients with celery allergy. Allergy 57:228–235

    Article  CAS  PubMed  Google Scholar 

  • Barker SJ, Stummer B, Gao L, Dispain I, Oconnor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization—isolation and preliminary characterisation. Plant J 15:791–797

    Article  CAS  Google Scholar 

  • Bolhaar STHP, van de Weg E, van Ree R, Gonzalez-Mancebo E, Zuidmeer L, Bruijnzeel-Koomen CAFM, Fernandez-Rivas M, Jansen J, Hoffmann-Sommergruber K, Knulst AC, Gilissen LJWJ (2005) In vivo assessment with prick-to-prick testing and double-blind, placebo-controlled food challenge of allergenicity of apple cultivars. J Allergy Clin Immunol 116:1080–1086

    Article  PubMed  Google Scholar 

  • Breiteneder H (2009) A classification of plant food allergens. Allergologie 32:375–382

    Article  Google Scholar 

  • Diaz-Perales A, Collada C, Blanco C, Sanchez-Monge R, Carrillo T, Aragoncillo C, Salcedo G (1999) Cross-reactions in the latex-fruit syndrome: A relevant role of chitinases but not of complex asparagine-linked glycans. J Allergy clin Immunol Volume 104, number 3, part 1

  • Drüge U, Schönbeck F (1990) Effect of vesicular-arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L) in relation to cytokinin levels. J Plant Physiol 141:40–48

    Article  Google Scholar 

  • Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131

    Article  PubMed  PubMed Central  Google Scholar 

  • Foetisch K, Son DY, Altmann F, Aulepp H, Conti A, Haustein D, Vieths S (2001) Tomato (Lycopersicon esculentum) allergens in pollen-allergic patients. Eur Food Res Tech 213:259–266

    Article  CAS  Google Scholar 

  • Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuhnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419

    Article  PubMed  Google Scholar 

  • Fuentes-Silva D, Mendoza-Hernandez G, Stojanoff V, Palomares LA, Zenteno E, Torres-Lariose A, Rodriguez-Romeroa A (2007) Crystallization and identification of the glycosylated moieties of two isoforms of the main allergen Hev b 2 and preliminary X-ray analysis of two polymorphs of isoform II Acta Cryst. F63:787–791

  • Gao LL, Delp G, Smith SE (2001) Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytol 151:477–491

    Article  Google Scholar 

  • Gao LL, Knogge W, Delp G, Smith FA, Smith SE (2004) Expression patterns of defense-related genes in different types of arbuscular mycorrhizal development in wild-type and mycorrhiza-defective mutant tomato. Mol Plant-Microb Interact 17:1103–1113

    Article  CAS  Google Scholar 

  • Garmendia I, Goicoechea N, Aguirreolea J (2004) Antioxidant metabolism in asymptomatic leaves of Verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J Phytopathol 152:593–599

    Article  CAS  Google Scholar 

  • Gerdemann JW (1968) Vesicular-arbuscular mycorrhiza and plant growth. Annu Rev Phytopathol 6:397–418

    Article  Google Scholar 

  • Gernns H, von Alten H, Poehling HM (2001) Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen—is a compensation possible? Mycorrhiza 11:237–243

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Diem HG (1982) Endomycorrhizae in the tropics. In: Dommergues YR, Diem HG (eds) Microbiology of tropical soils and plant productivity. Dr W. Junk Publishers, The Hague, pp 209–251

    Chapter  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochem 68:101–110

    Article  CAS  Google Scholar 

  • Heinzerling L, Frew AJ, Binslev-Jensen C, Bonini S, Bousquet J, Bresciani M, Carlsen KH, Van Cauwenberge P, Darsow U, Fokkens WJ, Haahtela T, Van Hoecke H, Jessberger B, Kowalski ML, Kopp T, Lahoz CN, Lodrup Carlsen KC, Papadopoulos NG, Ring J, Schmid-Grendelmeier P, Vignola AM, Wöhrl S, Zuberbier T (2005) Standard skin prick testing and sensitization to inhalant allergens across Europe—a survey from the GA2LEN network. Eur J Allergy Clin Immunol 60:1287–1300

    Article  CAS  Google Scholar 

  • Herrmann S, Munch JC, Buscot F (1998) A gnotobiotic culture system with oak microcuttings to study specific effects of mycobionts on plant morphology before, and in the early phase of, ectomycorrhiza formation by Paxillus involutus and Piloderma croceum. New Phytol 138:203–212

    Article  Google Scholar 

  • Heuvelink E (1996) Dry matter partitioning in tomato: validation of a dynamic simulation model. Ann Bot 77:71–80

    Article  Google Scholar 

  • Hoffmann-Sommergruber K (2002) Pathogenesis-related (PR)-proteins identified as allergens. Biochem Soc Trans 30:930–935

    Article  CAS  PubMed  Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen-Jarolim E, Santner B, Leitner A, Grimm R, Scheiner O, Ebner C, Breiteneder H (1998) Bell peppers (Capsicum annuum) express allergens (profilin, pathogenesis-related protein P23 and Bet v 1) depending on the horticultural strain. Int Arch Allergy Immunol 116:103–109

    Article  CAS  PubMed  Google Scholar 

  • Kondo Y, Urisu A, Tokuda R (2001) Identification and Characterization of the allergens in the tomato fruit by immunoblotting. Int Arch Allergy Immunol 126:294–299

    Article  CAS  PubMed  Google Scholar 

  • Lingua G, D’Agostino G, Massa N, Antosiano M, Berta G (2002) Mycorrhiza-induced differential response to a yellow disease in tomato. Mycorrhiza 12:191–198

    Article  PubMed  Google Scholar 

  • Liu JY, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ortolani C, Ispano M, Pastorello EA, Ansaloni R, Magri GC (1989) Comparison of results of skin prick tests (with fresh foods and commercial food extracts) and RAST in 100 patients with oral allergy syndrome. J Allergy Clin Immunol 83:683–690

    Article  CAS  PubMed  Google Scholar 

  • Petersen A, Vieths S, Aulepp H, Schlaak M, Becker WM (1996) Ubiquitous structures responsible for IgE cross-reactivity between tomato fruit and grass pollen allergens. J Allergy Clin Immunol 98:805–815

    Article  CAS  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant-Microb Interact 13:238–241

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Subramanian KS, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 107:245–253

    Article  Google Scholar 

  • Taylor J, Harrier L (2003) Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Mol Biol 51:619–629

    Article  CAS  PubMed  Google Scholar 

  • Trouvelot A, Fardeau JC, Planchette C, Gianinazzi S, Gianinazzi-Pearson V (1986) Nutritional balance and symbiontic expression in mycorrhizal wheat. Physiol Veg 24:300

    Google Scholar 

  • Vieths S, Hoffmann A, Holzhauser T, Muller U, Reindl J, Haustein D (1998) Factors influencing the quality of food extracts for in vitro and in vivo diagnosis. Allergy 53:65–71

    Article  CAS  PubMed  Google Scholar 

  • Wagner S, Breiteneder H (2002) The latex-fruit syndrome. Biochem Soc Trans 30:935–940

    Article  CAS  PubMed  Google Scholar 

  • Westphal S, Kolarich D, Foetisch K, Lauer I, Altmann F, Conti A, Crespo JF, Rodriguez J, Enrique E, Vieths S, Scheurer S (2003) Molecular characterization and allergenic activity of Lyc e 2 (b-fructofuranosidase), a glycosylated allergen of tomato. Eur J Biochem 270:1327–1337

    Article  CAS  PubMed  Google Scholar 

  • Westphal S, Kempf W, Foetisch K, Retzek M, Vieths S, Scheurer S (2004) Tomato profilin Lyc e 1: IgE cross-reactivity and allergenic potency. Allergy 59:526–532

    Article  CAS  PubMed  Google Scholar 

  • Wigotzki M, Steinhart H, Paschke A (2000) Influence of varieties, storage and heat treatment on IgE-binding proteins in hazelnuts (Corylus avellana). Food Agric Immunol 12:217–229

    Article  CAS  Google Scholar 

  • Yagami T (2002) Features and mode of action of cross-reactive plant allergens relevant to latex-fruit syndrome. Food Agric Immunol 14:241–253

    Article  CAS  Google Scholar 

  • Zacharisen MC, Elms NP, Kurup VP (2002) Severe tomato allergy (Lycopersicon esculentum). Allergy Asthma Proc 23:149–152

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Ministries of Consumer Protection, Food and Agriculture of the Federal Republic of Germany, of the Land Brandenburg and of the Land Thüringen. The authors express their thanks to Kerstin Fischer (IGZ), Gundula Aust (IGZ) and Eva-Maria Fiedler (Charité) for their valuable help in conducting and analyzing the experiments.

Author information

Authors and Affiliations

  1. Leibniz-Institute of Vegetable and Ornamental Crops, Großbeeren/Erfurt e.V., Theodor Echtermeyer Weg, 14979, Grossbeeren, Germany

    Dietmar Schwarz, Saskia Welter, Eckhard George & Philipp Franken

  2. Proteome Factory AG, Magnusstr. 11, 12489, Berlin, Germany

    Karola Lehmann

  3. Department Molecular Systems Biology, Faculty of Life Science, University of Vienna, Althanstr. 14, 1090, Vienna, Austria

    Wolfram Weckwerth

  4. Department of Dermatology and Allergology, Charité—Universitätsmedizin Berlin, Charitéplatz 1, 10117, Berlin, Germany

    Sabine Dölle & Margitta Worm

Authors
  1. Dietmar Schwarz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saskia Welter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eckhard George
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philipp Franken
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karola Lehmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolfram Weckwerth
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sabine Dölle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Margitta Worm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dietmar Schwarz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwarz, D., Welter, S., George, E. et al. Impact of arbuscular mycorrhizal fungi on the allergenic potential of tomato. Mycorrhiza 21, 341–349 (2011). https://doi.org/10.1007/s00572-010-0345-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-010-0345-z

Keywords

Search

Navigation