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Mycorrhiza of Linden (Tilia spp.) in Artificial Plantings in St. Petersburg

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Abstract—This study is devoted to the mycorrhizal colonization of three linden species (Tilia cordata, T. platyphyllos, and T. × europaea) in the urban environment of St. Petersburg. The study was conducted on three model territories: the Summer Garden, Botanical Garden, and Duderhof Heights. During the study, data was obtained on the morphology and anatomy of the mycorrhizal structures in linden trees, molecular identification of the mycorrhizal symbionts, and the influence of certain soil characteristics on the diversity of ectomycorrhizal fungi (EMF). Light microscopy confirmed the double mycorrhizal colonization characteristic of the genus Tilia: arbuscular mycorrhiza (AM) and ectomycorrhiza (EM). In all the studied trees, the root tips had intensive mycorrhizal colonization. EM colonization rates varied depending on the linden species, but only slightly on the season and location, while AM colonization rates varied with the season, place and linden species. In some of the studied trees, the presence of fine root endophytes was found. nrITS was used for molecular identification of EM symbionts of linden trees. As a result, 58 EMF taxa were identified. The main ectomycorrhizal symbionts identified for Tilia were basidiomycetes Inocybe, Tomentella, Sebacina and Entoloma, and ascomycetes Tuber and Peziza. Among the identified EMF taxa, 13 taxa were observed for the first time for T. cordata; 12, for T. platyphyllos; and 8, for T. × europaea. The taxonomic diversity of EMF varied depending on the species of linden, season, and location of trees. To study the influence of soil characteristics on the composition of EMF communities, soil was analyzed for the concentration of nitrate nitrogen (N\({\text{O}}_{3}^{ - }\)) and mobile phosphorus (P2O5) and pH. Among the studied soil parameters, EMF biodiversity was mainly affected by changes in the mobile phosphorus and nitrate nitrogen values, and an increase in soil pH led to a depletion in the diversity of EMF taxa.

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REFERENCES

  1. Angiosperm Phylogeny Group, An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV, Bot. J. Linn. Soc., 2016, vol. 181, no. 1, pp. 1–20.

    Article  Google Scholar 

  2. Bainard, L., Klironomos, J., and Gordon, M.A., The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments, Mycorrhiza, 2011, vol. 21, no. 2, pp. 91–96. https://doi.org/10.1007/s00572-010-0314-6

    Article  PubMed  Google Scholar 

  3. Beck, A., Kottke, I., and Oberwinkler, F., Two members of the Glomeromycota form distinct ectendomycorrhizas with Alzatea verticillata, a prominent tree in the mountain rain forest of southern Ecuador, Mycol. Progress, 2005, vol. 4, no. 1, pp. 11–22.

    Article  Google Scholar 

  4. Beck, A., Haug, I., Oberwinkler, F., and Kottke, I., Structural characterization and molecular identification of arbuscular mycorrhiza morphotypes of Alzatea verticillata (Alzateaceae), a prominent tree in the tropical mountain rain forest of South Ecuador, Mycorrhiza, 2007, vol. 17, pp. 607–625.

    Article  PubMed  Google Scholar 

  5. Bondartseva, M.A., Kotkova, V.M., Zmitrovich, I.V., et al., Aphyllophoroid and heterobasidioid fungi of the Peter the Great Botanical Garden of the Komarov Botanical Institute of RAS (St. Petersburg), in Botanika: Istoriya, Teoriya, Praktika (k 300-letiyu osnovaniya Botanicheskogo instituta im. V.L. Komarova Rossiyskoy akademii nauk): trudy mezhdunarodnoi nauchnoi konferentsii (Botany: History, Theory, Practice (To the 300th Anniversary of the Founding of the V.L. Komarov Botanical Institute of the Russian Academy of Sciences): Proc. Int. Sci. Conf., St. Petersburg, 2014, pp. 23–30.

  6. Brundrett, M. C. and Tedersoo, L., Evolutionary history of mycorrhizal symbioses and global host plant diversity, New Phytol., 2018, p. 220.

  7. Busetti, L., Sulle micorrize dei tigli (About mycorrhizas of Tilia), Allionia, 1962, vol. 8, pp. 45–54.

    Google Scholar 

  8. Ceruti, A. and Busetti, L., Sulla simbiosi micorrhizica tra tigli e Boletus subtomentosus, Russula grisea, Balsamia platysporae, Hysterangium clathroides (About mycorrhizal symbiosis of Tilia trees and Boletus subtomentosus, Russula grisea, Balsamia platyspora and Hysterangium clathroides), Allionia, 1962, vol. 8, pp. 55–66.

    Google Scholar 

  9. Chilvers, G., Lapeyrie, F., and Horan, D., Ectomycorrhizal vs endomycorrhizal fungi within the same root system, New Phytol., 1987, vol. 107, no. 2, pp. 441–448. https://www.jstor.org/stable/2433068?seq=1.

    Article  CAS  PubMed  Google Scholar 

  10. Courty, P.E., Doidy, J., Garcia, K., et al., The transportome of mycorrhizal systems, in Molecular Mycorrhizal Symbiosis, Martin, F., Ed., Wiley, 2016, pp. 239–256. https://doi.org/10.1002/9781118951446.ch14.

  11. Crous, P.W., Luangsa-Ard, J.J., Wingfield, M.J., et al., Fungal Planet description sheets: 785–867, Persoonia, 2018, vol. 41, pp. 238–417. https://doi.org/10.3767/persoonia.2018.41.12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dodd, J.C., Boddington, C.L., Rodriguez, A., et al., Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: Form, function and detection, Plant Soil, 2000, vol. 226, pp. 131–151.

    Article  CAS  Google Scholar 

  13. Dudka, V.A., Mycorrhizal status of Tilia cordata in the Summer Garden and Peter the Great Botanical Garden (St. Petersburg): Diversity of fungal partners and type of mycorrhizal colonization, in Materialy IV (XII) Mezhdunarodnoi Botanicheskoi Konferentsii Molodykh Uchenykh v Sankt-Peterburge 22–28 aprelya 2018 g. (Proc. IV (XII) Int. Bot. Conf. of Young Scientists in St. Petersburg, April 22–28, 2018), St. Petersburg, 2018a, pp. 208–209.

  14. Dudka, V.A., Malysheva, E.F., Malysheva, V.F., et al., Mycorrhizal status of Tilia cordata in the Summer Garden (St. Petersburg): Diversity of fungal symbionts and type of mycorrhizal colonization, Mikol. Fitopatol., 2018b, vol. 52, no. 4, pp. 243–251.

    Google Scholar 

  15. Entry, J.A., Rygiewicz, P.T., Watrud, L.S., et al., Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas, Adv. Environ. Res., 2002, vol. 7, pp. 123–138.

    Article  CAS  Google Scholar 

  16. Fini, A., Piero, F., Amoroso, G., et al., Effect of controlled inoculation with specific mycorrhizal fungi from the urban environment on growth and physiology of containerized shade tree species growing under different water regimes, Mycorrhiza, 2011, vol. 21, no. 8, pp. 703–719. https://doi.org/10.1007/s00572-011-0370-6

    Article  PubMed  Google Scholar 

  17. Garbaye, J. and Churin, J.L., Effect of ectomycorrhizal inoculation at planting on growth and foliage quality of Tilia tomentosa, J. Arboric., 1996, vol. 22, pp. 29–34.

    Google Scholar 

  18. Gardes, M. and Bruns, T.D., ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts, Mol. Ecol., 1993, vol. 2, pp. 113–118.

    Article  CAS  PubMed  Google Scholar 

  19. Giomaro, G., Sisti, D., Zambonelli, A., et al., Comparative study and molecular characterization of ectomycorrhizas in Tilia americana and Quercus pubescens with Tuber brumale, FEMS Microbiol., 2002, vol. 216, pp. 9–14.

    Article  CAS  Google Scholar 

  20. Gonçalves, S.C., Martins-Loução, M.A., and Freitas, H., Evidence of adaptive tolerance to nickel in isolates of Cenococcum geophilum from serpentine soils, Mycorrhiza, 2009, vol. 19, no. 4, pp. 221–230.

    Article  PubMed  Google Scholar 

  21. Guo, D., Xia, M., Wei, X., et al., Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species, New Phytol., 2008, vol. 180, pp. 673–683.

    Article  PubMed  Google Scholar 

  22. Hall, I.R., Species and mycorrhizal infections of New Zealand Endogonaceae, Trans. Br. Mycol. Soc., 1977, vol. 68, pp. 341–356.

    Article  Google Scholar 

  23. Ishida, T.A., Nara, K., and Hogetsu, T., Host effects on ectomycorrhizal fungal communities: Insight from eight host species in mixed conifer–broadleaf forests, New Phytol., 2007, vol. 174, pp. 430–440.

    Article  CAS  PubMed  Google Scholar 

  24. Jany, J.L., Martin, F., and Garbaye, J., Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests, Plant Soil, 2003, vol. 255, no. 2, pp. 487–494.

    Article  CAS  Google Scholar 

  25. Kõljalg, U., Nilsson, R.H., Abarenkov, K., et al., Towards a unified paradigm for sequence-based identification of fungi, Mol. Ecol., 2013, vol. 22, pp. 5271–5277.

    Article  PubMed  Google Scholar 

  26. Koske, R.E. and Gemma, J.N., A modified procedure for staining roots to detect VA mycorrhizas, Mycol. Res., 1989, vol. 92, no. 4, pp. 486–488.

    Article  Google Scholar 

  27. Kuhns, L.J., Potential benefits of mycorrhizae in the urban environment, Metro Tree Improvement Alliance, 1980, vol. 3, pp. 77–82.

    Google Scholar 

  28. Kumar, S., Stecher, G., Li, M., et al., MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, pp. 1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lang, C., Seven, J., and Polle, A., Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in a mixed Central European forest, Mycorrhiza, 2011, vol. 21, pp. 297–308.

    Article  PubMed  Google Scholar 

  30. Lapin, P.I., Botanicheskie Sady SSSR (Botanical Gardens of the USSR), Moscow: Kolos, 1984.

  31. Letniy Sad. Vozrozhdenie (Summer Garden. Revival), St. Petersburg: Severoslavyanskoe Byuro Reklamy, 2012.

  32. McLean, E.O., Soil pH and lime requirement, in Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties, American Society of Agronomy, 1982, pp. 199–209.

    Google Scholar 

  33. Melnikov, V.Yu., Historical range of plants for the Summer Garden, in Tezisy Dokladov XV Konferentsii Sadov Sankt-Peterburga (Proc. XV Conf. of Gardens of St. Petersburg), St. Petersburg, 2014, pp. 106–109.

  34. Morozova, O.V., Kovalenko, A.E., Rebriev, Yu.A., et al., Agaricoid and gasteroid fungi in the park of the Botanical Garden of the Komarov Botanical Institute, in Botanika: istoriya, teoriya, praktika (k 300-letiyu osnovaniya Botanicheskogo instituta im. V.L. Komarova Rossiyskoy akademii nauk): trudy mezhdunarodnoi nauchnoi konferentsii (Botany: History, Theory, Practice (To the 300th Anniversary of the Founding of the V.L. Komarov Botanical Institute): Proc. International Sci. Conf.), St. Petersburg, 2014, pp. 142–149.

  35. Nielsen, J. and Rasmussen, H., Mycorrhizal status and morphotype diversity in Tilia cordata—A pilot study of nurseries and urban habitats, Acta Hortic., 1999, vol. 496, pp. 451–459.

  36. Nilsson, R.H., Tedersoo, L., Abarenkov, K., et al., Five simple guidelines for establishing basic authenticity and reliability of newly generated fungal ITS sequences, MycoKeys, 2012, vol. 4, pp. 37–63.

    Article  Google Scholar 

  37. Obase, K., Douhan, G.W., Matsuda, Y., et al., Progress and challenges in understanding the biology, diversity, and biogeography of Cenococcum geophilum, in Biogeography of Mycorrhizal Symbiosis. Ecological Studies (Analysis and Synthesis), Tedersoo, L., Ed., Springer, 2017, vol. 230.

    Google Scholar 

  38. Oksanen, J., Blanchet, F.G., Friendly, M., et al., Vegan: Community ecology package, R package version 2.5–1, 2018. https://CRAN.R-project.org/package1/4vegan. Accessed September 1, 2018.

  39. Orchard, S., Standish, R., Dickie, I., et al., Fine root endophytes under scrutiny: A review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina, Mycorrhiza, 2017, vol. 27, no. 7, pp. 619–638. https://doi.org/10.1007/s00572-017-0782-z

    Article  PubMed  Google Scholar 

  40. Pigott, C.D., Survival of mycorrhiza formed by Cenococcum geophilum Fr. in dry soils, New Phytol., 1982, vol. 92, pp. 513–517.

    Article  Google Scholar 

  41. Pigott, C.D., Tilia cordata Miller, J. Ecol., 1991, vol. 79, pp. 1147–1207.

    Article  Google Scholar 

  42. Pigott, C.D., Lime-Trees and Basswoods: A Biological Monograph of the Genus Tilia, Cambridge and New York: Cambridge University Press, 2012. https://doi.org/10.1017/CBO9781139033275

  43. Popov, E.S., Discomycetes of the Peter the Great Botanical Garden, in Botanika: istoriya, teoriya, praktika (k 300-letiyu osnovaniya Botanicheskogo instituta im. V.L. Komarova Rossiyskoy akademii nauk): Trudy mezhdunarodnoy nauchnoy konferentsii (Botany: History, Theory, Practice (To the 300th Anniversary of the Komarov Botanical Institute): Proc. Int. Sci. Conf.), St. Petersburg, 2014, pp. 166–169.

  44. R Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2012. http://www.R-project.org/.

  45. RStudio Team, RStudio: Integrated Development for R, Boston, MA: RStudio, Inc., 2017. URL https://rstudio.com/.

  46. Saleh-Rastin, N., Salt tolerance of the mycorrhizal fungus Cenococcum graniforme (Sow.) Ferd., Eur. J. Forest Pathol., 1976, vol. 6, no. 3, pp. 184–187.

    Article  CAS  Google Scholar 

  47. Shubin, V.I., Mikotrofnost’ drevesnykh porod. Znachenie pri razvedenii lesa v taezhnoi zone (Mycotrophy of Tree Species. Value for Forest Cultivation in the Taiga Zone), Leningrad: Nauka, 1973.

  48. Smith, M.E., Gryganskyi, A., Bonito, G., et al., Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales, Fungal Genet. Biol., 2013, vol. 61, pp. 61–68.

    Article  PubMed  Google Scholar 

  49. Smith, S.E. and Read, D.J., Mycorrhizal Symbiosis, London: Academic Press Ltd, 2008, 3rd ed., p. 800.

    Google Scholar 

  50. Smith, S.E. and Smith, F.A., Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales, Annu. Rev. Plant Biol., 2011, vol. 62, pp. 227–250.

    Article  CAS  PubMed  Google Scholar 

  51. Strullu-Derrien, C., Kenrick, P., and Selosse, M.A., Origins of the mycorrhizal symbioses, in Molecular Mycorrhizal Symbiosis, Martin, F., Ed., Wiley, 2016, pp. 1–20.

    Google Scholar 

  52. Tedersoo, L., May, T.W., and Smith, M.E., Ectomycorrhizal lifestyle in fungi: Global diversity, distribution, and evolution of phylogenetic lineages, Mycorrhiza, 2010, vol. 20, pp. 217–263.

    Article  PubMed  Google Scholar 

  53. Timonen, S. and Kauppinen, P., Mycorrhizal colonisation patterns of Tilia trees in street, nursery and forest habitats in southern Finland, Urban Forestry and Urban Greening, 2008, vol. 7, pp. 265–276.

    Article  Google Scholar 

  54. Trouvelot, A., Kough, J., and Gianinazzi-Pearson, V., Evaluation of VA infection levels in root systems. Research for estimation methods having a functional significance, in Physiological and Genetical Aspects of Mycorrhizae, Gianinazzi-Pearson, V. and Gianinazzi, S., Eds., Paris: INRA Press, 1986, p. 217.

    Google Scholar 

  55. Tyburska, J., Frymark-Szymkowiak, A., Kulczyk-Skrzeszewska, M., et al., Mycorrhizal status of forest trees grown in urban and rural environments in Poland, Ecological Questions, 2013, pp. 49–57.

  56. Vasiliev, I.V., Family Tiliaceae Juss., in Derev’ya i kustarniki SSSR (Trees and Shrubs of the USSR), Moscow, Leningrad: Akad. Nauk SSSR, 1958, vol. 4, pp. 659–727.

  57. Volkova, E.A., Isachenko, G.A., Khramtsov, V.N., Duderhofskie Vysoty – kompleksnyi pamyatnik prirody (Duderhof Heights Is a Complex Natural Monument), St. Petersburg, 2006.

  58. Walker, C., Gollotte, A., and Redecker, D., A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis), Mycorrhiza, 2018a, vol. 28, no. 3, pp. 213–219. https://doi.org/10.1007/s00572-017-0815-7

    Article  PubMed  Google Scholar 

  59. Walker, C., Harper, C.J., Brundrett, M.C., et al., Looking for arbuscular mycorrhizal fungi in the fossil record, in Transformative Paleobotany, Krings, M. et al., Eds., Academic Press, 2018b, pp. 481–517.

    Google Scholar 

  60. Wang, B. and Qiu, Y.L., Phylogenetic distribution and evolution of mycorrhizas in land plants, Mycorrhiza, 2006, vol. 16, pp. 299–363. https://doi.org/10.1007/s00572-005-0033-6

    Article  CAS  PubMed  Google Scholar 

  61. Weissenhorn, I., Mycorrhiza and Salt Tolerance of Trees, EU project Mycorem QLK3-1999-00097, 2002, p. 36.

  62. White, T.J., Bruns, T., Lee, S., et al., Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR Protocols: A Guide to Methods and Applications, Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J., Eds., San Diego: Academic Press, 1990, pp. 315–322.

    Google Scholar 

  63. Wickham, H., Ggplot2: Elegant Graphics for Data Analysis, New York: Springer-Verlag, 2009.

    Book  Google Scholar 

  64. Zhukova, E.A., Morozova, O.V., Volobuev, S.V., et al., Basidiomycetous macromycetes and their influence on the state of green spaces in the Gardens of the Russian Museum (St. Petersburg), Mikol. Fitopatol., 2017, vol. 51, no. 6, pp. 328–339.

    Google Scholar 

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ACKNOWLEDGMENTS

The authors thank Summer Garden employee O.V. Shalakitskaya for help in conducting research on the territory.

Funding

The study was carried out within the state task of BIN RAS 122011900032-7 on equipment of the Collective Use Center “Cellular and Molecular Technologies for the Study of Plants and Fungi” of the Komarov Botanical Institute RAS and with the financial support of the Russian Foundation for Basic Research (project no. 19-04-00024 A).

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  1. Komarov Botanical Institute, Russian Academy of Sciences, 197022, St. Petersburg, Russia

    V. A. Dudka, E. F. Malysheva & V. F. Malysheva

  2. Russian State Museum, 191186, St. Petersburg, Russia

    E. A. Zhukova

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Dudka, V.A., Malysheva, E.F., Malysheva, V.F. et al. Mycorrhiza of Linden (Tilia spp.) in Artificial Plantings in St. Petersburg. Biol Bull Rev 13 (Suppl 1), S17–S38 (2023). https://doi.org/10.1134/S2079086423070058

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