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Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L.

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Abstract

Individuals of Inula ensifolia L. (Asteraceae), a valuable xerothermic plant species with potential therapeutic value, were inoculated under laboratory conditions with different strains of arbuscular mycorrhizal fungi (AMF): (1) Glomus intraradices UNIJAG PL-Bot, (2) G. intraradices UNIJAG PL-Kap, (3) Glomus clarum UNIJAG PL13-2, and (4) AMF crude inoculum from natural stands of I. ensifolia. We found AMF species specificity in the stimulation of thymol derivative production in the roots of I. ensifolia. There was an increase in thymol derivative contents in roots after G. clarum inoculation and at the same time the decreased production of these metabolites in the G. intraradices treatments. Moreover, no correlation between the extent of AMF colonization and the effects of the fungal symbionts on the plant was observed. A multilevel analysis of chlorophyll a fluorescence transients (JIP test) permitted an evaluation of plant vitality, expressed in photosynthetic performance index, influenced by the applied AMF strains, which was found to be in good agreement with the results concerning thymol derivative production. The mechanisms by which AMF trigger changes in phytochemical concentration in plant tissues and their consequences for practice are discussed.

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References

  • Abu-Zeyad R, Khan AG, Khoo C (1999) Occurrence of arbuscular mycorrhiza in Castanospermum australe A. Cunn. & C. Fraser and effects on growth and production of castanospermine. Mycorrhiza 9:111–117

    CAS  Google Scholar 

  • Akiyama K, Hayashi H (2002) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotechnol Biochem 66:762–769

    Article  CAS  PubMed  Google Scholar 

  • Biró B, Köves-Péchy K, Tsimilli-Michael M, Strasser RJ (2006) Role of beneficial microsymbionts on the plant performance and plant fitness. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizosphere, vol 7, Soil biology series (Varma A—series editor). Springer-Verlag, Berlin, pp 265–296

    Chapter  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 

  • Dzwonko Z, Loster S (2008) Changes in plant species composition in abandoned and restored limestone grasslands—the effect of tree and shrub cutting. Acta Soc Bot Pol 77(1):67–75

    Google Scholar 

  • Feldmann F, Hallmann J, Wagner S, Long X-Q, Schneider C, Hutter I, Ceipek B, Fan J, Zheng X, Wang C, Feng G (2008) Mycorrhizal fungi as biological components of integrated cucumber production (BIOMYC)-promising results for mycorrhizal technology transfer to horticultural practice. In: Feldmann F, Kapulnik Y, Baar J (eds) Mycorrhiza works. Deutsche Phytomedizinische Gesellschaft Braunschweig, Germany, pp 25–38. ISBN 978-3-941261-01-3

    Google Scholar 

  • Feldmann F, Gillessen M, Hutter I, Schneider C (2009) Should we breed for effective mycorrhiza symbioses? In: Feldmann F, Alford DV, Furk C (eds) Crop plant resistance to biotic and abiotic factors. Current potential and future demands. Deutsche Phytomedizinische Gesellschaft Braunschweig, Germany, pp 507–522. ISBN 978-3-941261-05-1

    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

    Article  CAS  Google Scholar 

  • Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154

    Article  CAS  PubMed  Google Scholar 

  • Gemma JN, Koske RE, Habte M (2002) Mycorrhizal dependency of some endemic and endangered Hawaiian plant species. Am J Bot 89(2):337–345

    Article  Google Scholar 

  • Graham JH, Eissenstat DM, Drouillard DL (1991) On the relationship between a plant's mycorrhizal dependency and rate of vesicular-arbuscular mycorrhizal colonization. Funct Ecol 5:773–779

    Article  Google Scholar 

  • Hamel C (1996) Prospects and problems pertaining to the management of arbuscular mycorrhizae in agriculture. Agr Ecosyst Environ 60:197–210

    Article  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 doi:10.1007/s00572-009-0280-z

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

    Article  CAS  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2002b) Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J Sci Food Agr 82:339–342

    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 

  • 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 

  • Larose G, Chênevert R, Moutoglis P, Gagné S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339

    Article  CAS  Google Scholar 

  • Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185:241–251

    Article  CAS  Google Scholar 

  • Orłowska E, Ryszka P, Jurkiewicz A, Turnau K (2005) Effectiveness of arbuscular mycorrhizal fungal (AMF) strains in colonization of plants involved in phytostabilisation of zinc wastes. Geoderma 129:92–98

    Article  Google Scholar 

  • Perzanowska J, Grzegorczyk M (2009) Obszary Natura 2000 w Małopolsce (Natura 2000 network in Małopolska province). Instytut Ochrony Przyrody, Polska Akademia Nauk, Kraków, ISBN: 978-83-61191-16-2 (in Polish)

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

    Article  Google Scholar 

  • Pinior A, Grunewaldt-Stöcker G, von Alten H, Strasser RJ (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyl a fluorescence, proline content and visual scoring. Mycorrhiza 15:596–605

    Article  CAS  PubMed  Google Scholar 

  • Réthy B, Csupor-Löffler B, Zupkó I, Hajdú Z, Máthé I, Hohmann J, Rédei T, Falkay G (2007) Antiproliferative activity of Hungarian Asteraceae species against human cancer cell lines. Part I. Phytother Res 21:1200–1208

    Article  PubMed  Google Scholar 

  • Rojas-Andrade R, Cerda-Garcia-Rojas CM, Frias-Hernández JT, Dendooven L, Olalde-Portugal V, Ramos-Valdivia AC (2003) Changes in the concentration of trigonelline in a semi-arid leguminous plant (Prosopis laevigata) induced by an arbuscular mycorrhizal fungus during the presymbiotic phase. Mycorrhiza 13:49–52

    Article  CAS  PubMed  Google Scholar 

  • Shimoda K, Kondo Y, Nishida T, Hamada H, Nakajima N, Hamada H (2006) Biotransformation of thymol, carvacrol, and eugenol by cultured cells of Eucalyptus perriniana. Phytochemistry 67:2256–2261

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London. ISBN 13: 978-0-1237-0526-6

    Google Scholar 

  • Stojakowska A, Kędzia B, Kisiel W (2005) Antimicrobial activity of 10-isobutyryloxy-8, 9-epoxythymol isobutyrate. Fitoterapia 76:687–690

    Article  CAS  PubMed  Google Scholar 

  • Stojakowska A, Michalska K, Malarz J (2006) Simultaneous quantification of eudesmanolides and thymol derivatives from tissues of Inula helenium and I. royleana by reversed-phase high-performance liquid chromatography. Phytochem Anal 17:157–161

    Article  CAS  PubMed  Google Scholar 

  • Stojakowska A, Malarz J, Zubek S, Turnau K, Kisiel W (2010) Terpenoids and phenolics from Inula ensifolia. Biochem Syst Ecol. doi:10.1016/j.bse.2009.12.011

    Google Scholar 

  • Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical and molecular aspects. J Chem Ecol 29:1955–1979

    Article  CAS  PubMed  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M (ed) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 445–483

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee C (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19, Advances in photosynthesis and respiration series (Govindjee—Series Editor). Kluwer Academic Publishers, Rotterdam, pp 321–362

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Dangre D, Rai M (2007) Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. In: Varma A, Oelmuller R (eds) Advanced techniques in soil biology, Soil biology series. Springer, Germany, pp 220–221

    Google Scholar 

  • Toussaint JP (2007) Investigating physiological changes in the aerial parts of AM plants: what do we know and where should we be heading? Mycorrhiza 17:349–353

    Article  PubMed  Google Scholar 

  • Toussaint JP, 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 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un systeme radiculaire. Recherche de methodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants' vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Dordrecht, pp 679–703

    Google Scholar 

  • Tsimilli-Michael M, Eggenberg P, Biró B, Köves-Pechy K, Vörös I, Strasser RJ (2000) Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen-fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P. Appl Soil Ecol 15:169–182

    Article  Google Scholar 

  • Turnau K, Haselwandter K (2002) Arbuscular mycorrhizal fungi, an essential component of soil microflora in ecosystem restoration. In: Gianinazzi S, Schűepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. From genes to mycorrhiza application. Birkhauser Verlag, Switzerland, pp 137–149

    Google Scholar 

  • Vierheilig H, Bennett R, Kiddle G, Kaldorf M, Ludwig-Müller J (2000) Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol 146:343–352

    Article  CAS  Google Scholar 

  • Zubek S, Błaszkowski J (2009) Medicinal plants as hosts of arbuscular mycorrhizal fungi and dark septate endophytes. Phytochem Rev 8:571–580

    Article  CAS  Google Scholar 

  • Zubek S, Turnau K, Błaszkowski J (2008) Arbuscular mycorrhiza of endemic and endangered plants from the Tatra Mts. Acta Soc Bot Pol 77(2):149–156

    Google Scholar 

  • Zubek S, Turnau K, Tsimilli-Michael M, Strasser RJ (2009) Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria. Mycorrhiza 19:113–123

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Prof. S. Loster (Institute of Botany, Jagiellonian University, Kraków) for providing us with the useful information concerning I. ensifolia. M.Sc. Eng. B. Szczepanowicz (Institute of Botany, Jagiellonian University) is acknowledged for her assistance during the soil samples analysis. The present research was financially supported by the Polish Ministry of Science and Higher Education (project no. 197/N-COST/2008/0).

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Zubek, S., Stojakowska, A., Anielska, T. et al. Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L.. Mycorrhiza 20, 497–504 (2010). https://doi.org/10.1007/s00572-010-0306-6

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