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Mycorrhizal status of an ozone-sensitive poplar clone treated with the antiozonant ethylene diurea

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Abstract

The antiozonant ethylene diurea is proven to prevent growth reductions in forest trees induced by ozone. The community of mycorrhizal fungi could be useful indicator of environmental stress. In this study, response of mycorrhizal fungi and fine roots to a 4-year exposure to ambient ozone and treatment with antiozonant was investigated in ozone-sensitive poplar clone under field conditions. The community of ectomycorrhizal fungi and root length colonization with ectomycorrhizal, arbuscular mycorrhizal fungi, and root endophytic fungi was analyzed in antiozonant-treated poplar plants and in poplar plants irrigated with water. In general, plants protected by antiozonant showed higher total number of fine roots, number of ectomycorrhizal types, Shannon–Weaver diversity index, and Species richness index compared to the plants treated with water. The ectomycorrhizal community shifted from contact exploration type in the trees irrigated with water to short-distance exploration type in ethylene diurea-treated trees. Ozone protectant may beneficially affect the belowground community of mycorrhizal fungi colonizing roots of ozone-sensitive poplar clone.

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References

  • Abarenkov K, Nilsson RH, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186(2):281–285

    Article  PubMed  Google Scholar 

  • Agerer R (ed) (1987–2008) Colour atlas of ectomycorrhizae, 1st–13th edn. Einhorn-Verlag, Schwäbisch Gmünd

  • Agerer R (1991) Characterisation of ectomycorrhiza. Techniques for the study of mycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Methods Microbiol 23:25–72

  • Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ECM mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Agerer R, Rambold G (2004–2012) First posted on 2004-06-01; most recent update: 2012-09-18]. DEEMY—An Information System for Characterization and Determination of Ectomycorrhizae. www.deemy.de. München, Germany

  • Agerer R, Danielson RM, Egli S, Ingleby K, Luoma D, Treu R (eds) (2001–2006) Descriptions of ectomycorrhizae, 1st–10th edn. Einhorn-Verlag, Schwäbisch Gmünd

  • Andersen CP (2003) Source—sink balance and carbon allocation below ground in plants exposed to ozone (Tansley review). New Phytol 157:213–228

    Article  CAS  Google Scholar 

  • Andrew C, Lilleskov A (2009) Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3. Ecol Lett 12:813–822

    Article  PubMed  Google Scholar 

  • Atlas R, Bartha R (1981) Introduction to microbiology. Addison-Wesley Publishing Company, Reading, UK, pp 242–244

    Google Scholar 

  • Beauchamp VB, Stromberg JC, Stutz JC (2006) Arbuscular mycorrhizal fungi associated with PopulusSalix stands in a semiarid riparian ecosystem. New Phytol 170:369–380

    Article  PubMed  Google Scholar 

  • Coleman MD, Dickson RE, Isebrands JG, Karnosky DF (1995) Carbon allocation and partitioning in aspen clones varying in sensitivity to tropospheric ozone. Tree Physiol 15:593–604

    Article  CAS  PubMed  Google Scholar 

  • Coleman MD, Dickson RE, Isebrands JG, Karnosky DF (1996) Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone. Tree Physiol 16:145–152

    Article  CAS  PubMed  Google Scholar 

  • Cudlin P, Kieliszewska-Rokicka B, Rudawska M, Grebenc T, Alberton O, Lehto T, Akker MR, Børja I, Konopka B, Leski T, Kraigher H, Kuyper TW (2007) Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosyst 141:406–425

    Article  Google Scholar 

  • Eichhorn MP, Paris P, Herzog F, Incoll LD, Liagre F, Mantzanas K, Mayus M, Moreno G, Papanastasis VDJ, Pilbeam D, Pisanelli A, Dupraz C (2006) Silvoarable systems in Europe–past, present and future prospects. Agrofor Syst 67(1):29–50

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of ectomycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Grebenc T, Kraigher H (2007a) Types of ectomycorrhiza of mature beech and spruce at ozone-fumigated and control forest plots. Environ Monit Assess 128:47–59

    Article  CAS  PubMed  Google Scholar 

  • Grebenc T, Kraigher H (2007b) Changes in the community of ectomycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration. Plant Biol 9(2):279–287

    Article  CAS  PubMed  Google Scholar 

  • Gregg JW, Jones CG, Dawson TE (2003) Urbanization effects on tree growth in the vicinity of New York City. Nature 424:183–187

    Article  CAS  PubMed  Google Scholar 

  • Hoshika Y, Omasa K, Paoletti E (2012) Whole-tree water use efficiency is decreased by ambient ozone and not affected by O3-induced stomatal sluggishness. PLoS ONE 7(6):e39270. doi:10.1371/journal.pone.0039270

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoshika Y, Pecori F, Conese I, Bardelli T, Marchi E, Manning WJ, Badea O, Paoletti E (2013) Effects of a three-year exposure to ambient ozone on biomass allocation in poplar using ethylenediurea. Environ Pollut 180:299–303

    Google Scholar 

  • Hrynkiewicz K, Baum C, Leinweber P, Weih M, Dimitriou I (2010) The significance of rotation periods for mycorrhiza formation in Short Rotation Coppice. For Ecol Manage 260(11):1943–1949

    Article  Google Scholar 

  • Hu JL, Lin XG, Wang JH, Cui XC, Wu S, Zhang J, Zhu JG (2009) Arbuscular mycorrhizal fungal effects on wheat growth in response to elevated tropospheric O3 concentration. Huan Jing Ke Xue 30(11):3393–3398

    PubMed  Google Scholar 

  • Jakucs E (2002) Ectomycorrhizae of Populus alba L. in South Hungary. Phyton 42:199–210

    Google Scholar 

  • Jakucs E, Kovacs GM, Agerer R, Romsics C, Erös-Honti Z (2005) Morphological-anatomical characterization and molecular identification of Tomentella stuposa ectomycorrhizae and related anatomotypes. Mycorrhiza 15(4):247–258

    Article  PubMed  Google Scholar 

  • Kaldorf M, Renker C, Fladung M, Buscot F (2004) Characterization and spatial distribution of ectomycorrhizas colonizing aspen clones released in an experimental field. Mycorrhiza 14:295–306

    Article  PubMed  Google Scholar 

  • Karliński L, Rudawska M, Kieliszewska-Rokicka B, Leski T (2010) Relationship between genotype and soil environment during colonization of poplar roots by mycorrhizal and endophytic fungi. Mycorrhiza 20:315–324

    Article  PubMed  Google Scholar 

  • Katanić M, Grebenc T, Hrenko M, Štupar B, Galić Z, Orlović S, Kraigher H (2008) Prva identifikacija tipova ektomikorize u zasadu belih topola (Populus alba L.) kod Novog Sada. Topola 181(182):49–59

    Google Scholar 

  • Katanić M, Orlović S, Grebenc T, Štupar B, Galić Z, Kovačević B, Kraigher H (2010) Identification of ectomycorrhizal types in a white poplar (Populus alba L.) plantation near Novi Sad. Les 62(5):155–159

    Google Scholar 

  • Katanić M, Orlović S, Grebenc T, Bajc M, Galić Z, Kebert M, Kraigher H (2011) Mycorrhizal fungi on poplars from a pyrite contaminated site. In: Proceedings book of “STREPOW” international workshop, February 23–24, 2011. Andrevlje-Novi Sad, Serbia, pp 305–312

  • Khan AG (2006) Mycorrhizoremediation—an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7(7):503–514

    Article  PubMed Central  PubMed  Google Scholar 

  • Khasa DP, Chakarvarty P, Robertson B, Thomas R, Danick BP (2002) The mycorrhizal status of selected poplar clones introduced in Alberta. Biomass Bioenergy 22:99–104

    Article  Google Scholar 

  • Klašnja B, Orlović S, Galić Z, Drekić M (2006) Poplar biomass of short rotation plantations as renewable energy raw material. In: Columbus F (ed) Biomass and bioenergy new research. Nova Science Publishers, INC. New York, USA, pp 35–66. ISBN 1-59454-865-X

  • Klopfenstein NB, Chun YW, Kim MS, Ahuja MR, Dillon MC, Carman RC, Eskew LG (1997) Micropropagation, genetic engineering, and molecular biology of Populus. Rocky Mountain Forest and Range Experiment Station, USDA Forest Service. 326 pp

  • Kormanik PP, McGraw AC (1982) Quantification of vesicular–arbuscular mycorrhizae in plant roots. In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathology Society, St. Paul, pp 37–45

    Google Scholar 

  • Kraigher H (1996) Tipi mikorize: taksonomija, pomen, aplikacija. Zbornik gozdarstva in lesarstva 49:33–66

    Google Scholar 

  • Kraigher H (1999) Diversity of types of ectomycorrhizae on Norway spruce in Slovenia. Phyton 39(3):199–202

    Google Scholar 

  • Kraigher H, Al Sayegh-Petkovšek S (2011) Mycobioindication of stress in forest ecosystems. V: RAI, Mahendra (ur.), VARMA, Ajit (ur.). Diversity and biotechnology of ectomycorrhizae (Soil biology, vol 25). Springer, Heidelberg, NY, cop. 2011, str. 301–322

  • Kraigher H, Al Sayegh-Petkovšek S, Grebenc T, Simončič P (2007) Types of ectomycorrhiza as pollution stress indicators: case studies in Slovenia. Environ Monit Assess 128(1):31–45

    Article  CAS  PubMed  Google Scholar 

  • Krpata D, Peintner U, Langer I, Walter JF, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112(9):1069–1079

    Article  PubMed  Google Scholar 

  • Manning WJ, Paoletti E, Sandermann H Jr, Ernst D (2011) Ethylenediurea (EDU) a research tool for assessment and verification of the effects of ground level ozone on plants under natural conditions. Environ Poll 159:3283–3293

    Article  CAS  Google Scholar 

  • Marzuoli R, Gerosa G, Desotgiu R, Bussotti F, Ballarin-Denti A (2009) Ozone fluxes and foliar injury development in the ozone-sensitive poplar clone Oxford (Populus maximowiczii × Populus berolinensis): a dose-response analysis. Tree Physiol 29(1):67–76

    Article  CAS  PubMed  Google Scholar 

  • Matyssek R, Wieser G, Ceulemans R, Rennenberg H, Pretzsch H, Haberer K, Löw M, Nunn AJ, Werner H, Wipfler P, Oßwald W, Nikolova P, Hanke DE, Kraigher H, Tausz M, Bahnweg G, Kitao M, Dieler J, Sandermann H, Herbinger K, Grebenc T, Blumenröther M, Deckmyn G, Grams TEE, Heerdt C, Leuchner M, Fabian P, Häberle K-H (2010) Enhanced ozone strongly reduces carbon sink strength of adult beech (Fagus sylvatica)—resume from the free-air fumigation study at Kranzberg Forest. Environ Poll 158(8):2527–2532. doi:10.1016/j.envpol.2010.05.009

    Article  CAS  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 115:495–501

    Article  Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical applications. In: Allen MF (ed) Mycorrhizal functioning. Chapman and Hall, New York, pp 357–423

    Google Scholar 

  • Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216

    Article  Google Scholar 

  • Newman LA, Strand SE, Choe N, Duffy J, Ekuan G, Ruszaj M, Shurleff BB, Wilmoth J, Heilman P, Gordon MP (1997) Uptake and biotransformation of trichloroethylene by hybrid poplars. Environ Sci Technol 31:1062–1067

    Article  CAS  Google Scholar 

  • Paoletti E, Contran N, Manning WJ, Tagliaferro F (2007a) Ethylenediurea (EDU) Affects the growth of ozone-sensitive and tolerant Ash (Fraxinus excelsior) trees under ambient O3. Conditions short communication proceedings: impacts of air pollution and climate change on forest ecosystems. Sci World J 7(S1):128–133

    Article  CAS  Google Scholar 

  • Paoletti E, Manning WJ, Spaziani F, Tagliaferro F (2007b) Gravitational infusion of ethylenediurea (EDU) into trunks protected adult European ash trees (Fraxinus excelsior L.) from foliar ozone injury. Environ Poll 145:869–873

    Article  CAS  Google Scholar 

  • Paoletti E, Contran N, Manning WJ, Castagna A, Ranieri A, Tagliaferro F (2008) Protection of ash (Fraxinus excelsior) trees from ozone injury by ethylenediurea (EDU): roles of biochemical changes and decreased stomatal conductance in enhancement of growth. Environ Poll 155:464–472

    Article  CAS  Google Scholar 

  • Paoletti E, Contran N, Manning WJ, Ferrara AM (2009) Use of the antiozonant ethylenediurea (EDU) in Italy: verification of the effects of ambient ozone on crop plants and trees and investigation of EDU’s mode of action. Environ Pollut 157:1453–1460

    Article  CAS  PubMed  Google Scholar 

  • Qiu Z, Chappelka AH, Somers GL, Lockaby BG, Meldahl RS (1992) Effects of ozone and simulated acidic precipitation on above- and below-ground growth of loblolly pine (Pinus taeda L.). Can J For Res 22:582–587

    Article  CAS  Google Scholar 

  • Qiu Z, Chappelka AH, Somers GL, Lockaby BG, Meldahl RS (1993) Effects of ozone and simulated acidic precipitation on ectomycorrhizal formation on loblolly pine seedlings. Environ Exp Bot 33:423–431

    Article  CAS  Google Scholar 

  • Regvar M, Likar M, Piltaver A, Kugonič N, Smith JE (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330:345–356

    Article  CAS  Google Scholar 

  • Rudawska M, Leski T, Stasińska M (2011) Species and functional diversity of ectomycorrhizal fungal communities on Scots pine (Pinus sylvestris L.) trees on three different sites. Ann For Sci 68:5–15

    Article  Google Scholar 

  • Saravesi K, Markkola A, Rautio P, Tuomi J (2011) Simulated mammal browsing and host gender effects on dual mycorrhizal Salix repens Botany 89(1):35–42. doi:10.1139/B10-081

    Google Scholar 

  • Serengil Y, Augustaitis A, Bytnerowicz A, Grulke N, Kozovitz AR, Matyssek R, Müller-Starck G, Schaub M, Wieser G, Coskun AA, Paoletti E (2011) Adaptation of forest ecosystems to air pollution and climate change: a global assessment on research priorities. iFor Biogeosci For 4:44–48

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier-Academic Press, London

    Google Scholar 

  • Snedecor W, Cochran WG (1976) Statistical methods, 6th edn. The Iowa State University Press, Ames, pp 327–329

    Google Scholar 

  • Takásc T, Radimszky L, Németh T (2005) The arbuscular mycorrhizal status of poplar clones selected for phytoremediation of soils contaminated with heavy metals. Z Naturforsch 60c:357–361

    Google Scholar 

  • Vingarzan R (2004) A review of surface ozone background levels and trends. Atmos Environ 38:3431–3442

    Article  CAS  Google Scholar 

  • WHO (2000) Air quality guidelines for Europe, Reg. Publ. Eur. Ser., WHO Reg. Off. Eur., Copenhagen, 2nd edn, 91, 288 pp

  • Železnik P, Hrenko M, Then Ch, Koch N, Grebenc T, Levanič T, Kraigher H (2007) CASIROZ: root parameters and types of ectomycorrhiza of young beech plants exposed to different ozone and light regimes. Plant Biol 9:298–308

    Article  PubMed  Google Scholar 

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Acknowledgments

The study was carried out under COST-STSM-FP0903, the Research Programme P4-0107 of the Slovenian Forestry Institute and project III43007 “Studying climate change and its influence on the environment: impacts, adaptation and mitigation” financed by the Ministry of Education, Science and Technological Development of the Republic of Serbia, within the framework of integrated and interdisciplinary research.

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The authors declare that they have no conflict of interest.

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Correspondence to Marina Katanić.

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Communicated by R. Matyssek.

This article originates from the IUFRO Conference “Biological Reactions of Forests to Climate Change and Air Pollution,” held in Kaunas/Lithuania during May 18–27, 2012, as organized by IUFRO Research Group 7.01.00 in cooperation with COST Action FP 0903 “MAFor,” North American Air Pollution workshop ENVeurope and ICP monitoring task force (local organizer: Algirdas Augustaitis).

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Katanić, M., Paoletti, E., Orlović, S. et al. Mycorrhizal status of an ozone-sensitive poplar clone treated with the antiozonant ethylene diurea. Eur J Forest Res 133, 735–743 (2014). https://doi.org/10.1007/s10342-013-0751-9

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