Mycorrhizal associations of pine: Species, their characteristics, and role in forest ecosystems
ARTICLE PDF (Українська)

Keywords

mycorrhizal symbiosis
antagonists
tree resistance
mycorrhization мікоризний симбіоз
антагоністи
стійкість дерев
мікоризація

How to Cite

Дишко, В., Боровик, П., Ошако, Т., & Давиденко, К. (2024). Mycorrhizal associations of pine: Species, their characteristics, and role in forest ecosystems. Forestry and Forest Melioration, (145), 112–122. https://doi.org/10.33220/1026-3365.145.2024.112

Abstract

Introduction

Addressing the preservation and adaptation of key tree species to climate change is an urgent task. The ability of trees to survive under extreme conditions largely depends on their adaptability, particularly the development of robust root systems. Mycorrhizal symbiosis is crucial in enhancing plant growth, improving nutrient uptake, and protecting against toxic compounds and pathogens. Additionally, mycorrhizal fungi contribute to nutrient cycling and carbon sequestration in the soil, thereby supporting tree productivity, especially in nutrient-poor environments.

Impact of climate change on mycorrhizal fungi. Climate change significantly affects mycorrhizal associations, which are essential for maintaining plant health and ecosystem stability. Rising temperatures, shifts in precipitation patterns, and increased atmospheric CO2 levels pose new challenges for mycorrhizal fungi, influencing their symbiotic relationships with trees. For example, changes in soil moisture and temperature can promote the spread of pathogenic fungi, weakening the protective functions of mycorrhizae.

The role of mycorrhiza in forest ecosystems. Ectomycorrhizae (EM) play a vital role in forest ecosystems, particularly in nutrient-poor soils, by enhancing the uptake of nitrogen, phosphorus, and other essential minerals. This, in turn, improves tree growth and resilience to environmental stressors such as drought and extreme temperatures. Additionally, mycorrhizal fungi help protect trees against pathogens and toxic substances. In Ukraine, research on forest mycobiomes remains limited, primarily focusing on taxonomic descriptions. There is an urgent need for systematic studies to explore the functional roles of mycorrhizal fungi in nutrient cycling and forest stability. Furthermore, understanding the potential of mycorrhizal species for seedling inoculation could enhance reforestation efforts and improve forest resilience in the face of climate change.

Mycorrhizal companions of Scots pine. Pinus species rely on characteristic ectomycorrhizal (EM) associations with various soil fungi. Mycorrhizal networks in the soil and on tree roots enhance nutrient accessibility and create favourable conditions for tree growth and development. Research in Ukraine has demonstrated the positive effects of Suillus luteus and Amanita muscaria mycorrhizae on the survival of pine seedlings, especially after forest fires. Scots pine species depend on specific ectomycorrhizae formed by soil fungi, which enhance nutrient uptake and create favorable growth conditions. Mycorrhized seedlings with Thelephora terrestris, Suillus bovinus, and Scleroderma citrinum showed higher nitrogen assimilation rates and shoot-to-root ratios than non-mycorrhized seedlings but exhibited lower shoot growth rates. The mycelium of S. citrinum retains 32% of the nitrogen supplied to the plants, which resulted in reduced host plant growth rates. Another significant mycorrhizal partner of Scots pine is Imleria badia, which thrives in diverse environments, including areas contaminated with heavy metals. The symbiotic relationship between pines and ectomycorrhizal fungi, particularly species of the Suilloid genus, can support pine adaptation in various habitats.

Mycorrhiza and Disease Resistance in Pine. Mycorrhizal fungi play a vital role in the growth and survival of trees in nutrient-poor soils by protecting them from toxic substances and phytopathogens. By forming a biotrophic association with their host trees, these fungi receive carbohydrates while enhancing the trees’ resistance to environmental stress and pathogenic threats. Mycorrhizal symbiosis improves tree vitality by mitigating the effects of toxic compounds and harmful microorganisms, thereby contributing to overall forest health and stability.

Conclusion

Given the critical role of mycorrhizal fungi in the restoration and conservation of temperate and boreal forests, further research and conservation measures are essential, particularly in the context of climate change. Preserving native and stress-tolerant mycorrhizal fungi strains offers a promising, eco-friendly strategy for enhancing forest ecosystem stability and mitigating the impacts of climate change.

76 Refs.

https://doi.org/10.33220/1026-3365.145.2024.112
ARTICLE PDF (Українська)

References

Agarwal, P. and Sah, P. (2009) ‘Ecological importance of ectomycorrhizae in world forest ecosystems’, Nature and Science, 7(2), pp. 107–116.

Agerer, R. (1996) ‘Characterization of ectomycorrhizae: A historical overview’, Descript Ectomycorrhizae, 1, pp. 1–22.

Alexopoulos, C.J., Mims, C.W. and Blackwell M. (1996) ‘Kingdom fungi – introduction to fungi and their significance to humans’ in Introductory Mycology. 4th edn. New York: John Wiley & Sons, Inc.

Banerjee, S., Schlaeppi, K. and van der Heijden, M. G. (2018) ‚Keystone taxa as drivers of microbiome structure and functioning’, Nature Reviews Microbiology, 16(9), pp. 567–576.

Bazilevskaya, N.A. and Maurin, A.M. (1984) Plant introduction: theories and practical approaches. Riga: Latvian University (in Russian).

Bever, J. D., Dickie, I. A., Facelli, E., Facelli, J. M., Klironomos, J., Moora, M., Rillig, M. C., Stock, W. D., Tibbett, M. and Zobel, M. (2010) ‘Rooting theories of plant community ecology in microbial interactions’, Trends in Ecology & Evolution, 25, pp. 468–478. https://doi.org/10.1016/j.tree.2010.05.004

Bonebrake, T. C., Brown, C. J., Bell, J. D., Blanchard, J. L., Chauvenet, A., Champion, C., ... and Pecl, G. T. (2018) ‘Managing consequences of climate?driven species redistribution requires integration of ecology, conservation and social science’, Biological Reviews, 93(1), pp. 284–305.

Brunner, I., Amiet, R., Zollinger, M. and Egli, S. (1992) ‘Ectomycorrhizal syntheses with Picea abies and three fungal species: A case study on the use of an in vitro technique to identify naturally occurring ectomycorrhizae’, Mycorrhiza, 2, pp. 89–96.

Canright, M. and Bruns, T. D. (2006) ‘The effects of heat treatments on ectomycorrhizal resistant propagules and their ability to colonize bioassay seedlings’, Mycological Research, 110(2), pp. 196–202.

Cardon, Z.G and Whitbeck, J.L. (2007) The rhizosphere. Elsevier Academic Press.

Claridge, A. W., Trappe, J. M. and Hansen, K. (2009) ’Do fungi have a role as soil stabilizers and remediators after forest fire?’, Forest Ecology and Management, 257(3), pp. 1063–1069.

Colpaert, J.V., Van Laere, A. and van Assche, J.A. (1996) ‘Carbon and nitrogen allocation in ectomycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings’, Tree Physiology, 16, pp. 787–793.

Compant, S., Van Der Heijden, M.G. and Sessitsch, A. (2010) ‘Climate change effects on beneficial plant-microorganism interactions’, FEMS Microbiology Ecology, 73, pp. 197–214.

Dahlberg, A. (2001) ‘Community ecology of ectomycorrhizal fungi: an advancing interdisciplinary field’, New Phytologist, 150(3), pp. 555–562.

Dahlberg, A. and Stenstr?m, E. (1991) ‚Dynamic changes in nursery and indigenous mycorrhiza of Pinus sylvestris seedlings planted out in forest and clearcuts’, Plant and Soil, 136, pp. 73–86.

Davydenko, K., Vysotska, N., Yushchyk, V. and Markina, T. (2020) ‘Early effects of a forest fire on the diversity of fungal communities in pine forests in Left-Bank Ukraine with special emphasis on mycorrhizal fungi’, Forestry and Forest Melioration, 137, pp. 110–119.

Dickie, I. A., Bufford, J. L., Cobb, R. C., Desprez?Loustau, M. L., Grelet, G., Hulme, P. E., ... and Williams, N. M. (2017) ‘The emerging science of linked plant-fungal invasions’, New Phytologist, 215(4), pp. 1314–1332.

Dobo, B., Asefa, F. and Asfaw, Z. (2018) ‘Diversity and abundance of arbuscular mycorrhizal fungi under different plant and soil properties in Sidama, southern Ethiopia’, Agroforestry Systems, 92, pp. 91–101.

Du?abeitia, M.K., Hormilla, S., Salcedo, I. and Pe?a, J.I. (1996) ‘Ectomycorrhizae synthesized between Pinus radiata and eight fungi associated with Pinus spp.’, Mycologia, 88, pp. 897–908.

Dunstan, W. A., Malajczuk, N. and Dell, B. (1998) ‚Effects of bacteria on mycorrhizal development and growth of container grown Eucalyptus diversicolor F. Muell. Seedlings’, Plant and Soil, 201, pp. 241–249.

Dyderski, M. K., Pa?, S., Frelich, L. E. and Jagodzi?ski, A. M. (2018) ‘How much does climate change threaten European forest tree species distributions?’, Global Change Biology, 24(3), pp. 1150–1163.

Garrett, S.D. (1956) ‘Biology of root-infecting fungi’, Soil Science, 82(1), p. 97.

Godbout, C. and Fortin, J. (1983) ‘Morphological features of synthesized ectomycorrhizae of Alnus crispa and A. rugosa’, New Phytologist, 94, pp. 249–262.

Hagenbo, A., Hadden, D., Clemmensen, K. E., Grelle, A., Manzoni, S., M?lder, M., ... and Fransson, P. (2019) ‘Carbon use efficiency of mycorrhizal fungal mycelium increases during the growing season but decreases with forest age across a Pinus sylvestris chronosequence’, Journal of Ecology, 107(6), pp. 2808–2822.

Hawkins, H. J., Cargill, R. I., Van Nuland, M. E., Hagen, S. C., Field, K. J., Sheldrake, M., ... and Kiers, E. T. (2023) ‘Mycorrhizal mycelium as a global carbon pool’, Current Biology, 33(11), R560-R573.

Helgason, T., Merryweather, J.W., Denison, J., Wilson, P., Young, J.P.W. and Fitter, A.H. (2002) ‘Selectivity and functional diversity in arbuscular mycorrhizas of co?occurring fungi and plants from a temperate deciduous woodland’, Journal of Ecology, 90, pp. 371–384.

Hilszczanska, D. (2002) ‘Mycorrhizal fungi in Scots pine cultures after seedlings out planting on post-agricultural lands’, Folia forestalia Polonica. Serie A. Forestry, 44, pp. 97–102.

Hilszczanska, D. (2004) ‘Mycorrhizal status of Scots pine Pinus sylvestris L. seedlings grown in watered and non-watered nursery condition’, Dendrobiology, 52, pp. 23–28.

Hilszczanska, D. (2005) ‘Wplyw deszczowania siewek Pinus sylvestris L. na zmiany w zbiorowiskach grzybow mikoryzowych I glebowych’, Le?ne Prace Badawcze, 4, pp. 103–113 (in Polish).

Hilszczanska, D., Oszako, T. and Sierota, Z. (1999) ‘Influence of laser light on mycelial growth of Hebeloma mesophaeum and ectomycorrhizal development on Scots pine’, Mycorrhiza, 8, pp. 323–327.

Jackson, R. B., Banner, J. L., Jobb?gy, E. G., Pockman, W. T., and Wall, D. H. (2002) ‘Ecosystem carbon loss with woody plant invasion of grasslands’, Nature, 418, pp. 623–626. https://doi.org/10.1038/nature00910

Jo, I., Fei, S., Oswalt, C. M., Domke, G. M., and Phillips, R. P. (2019) ‘Shifts in dominant tree mycorrhizal associations in response to anthropogenic impacts’, Science Advances, 5(4), eaav6358.

Kopiy, L., Gonchar, V., Kopiy, S., Oliferchuk, V. and Kopiy, M. (2015) Influence of tree stand composition on the mycological structure of the soil’, Scientific Bulletin of UNFU, 25, p. 8–14 (in Ukrainian).

Kostikov, I. Yu., Dzhagan, V. V., Demchenko, E. M., Boyko, O. A., Boyko, V. R. and Romanenko, P. O. (2004) Botany. Algae and mushrooms. Kyiv (in Ukrainian).

Kottke, I. and Oberwinkler, F. (1986) ‘Mycorrhiza of forest trees – structure and function’, Trees, 1, pp. 1–24.

Kraigher, H., Grayling, A., Wang, T. L. and Hanke, D. E. (1991) ‘Cytokinin production by two ectomycorrhizal fungi in liquid culture’, Phytochemistry, 30(7), pp. 2249–2254.

Kumar, R., Reddy, B. and Mohan, V. (1999) ‘Distribution of ectomycorrhizal fungi in forest tree species of Andhra Pradesh, southern India – a new record’. Indian Forester, 125(5), pp. 496–502.

Kutorga, E., Adamonyt?, G., Ir??nait?, R., Juz?nas, S., Kasparavi?ius, J., Markovskaja, S., ... and Treigien?, A. (2012) ‘Wildfire and post-fire management effects on early fungal succession in Pinus mugo plantations, located in Curonian Spit (Lithuania)’, Geoderma, 191, pp. 70–79.

Kuznetsova, O. V. (2011) ‘The effect of growth stimulants on the development of the vegetative mycelium of Pleurotus ostreatus (Jacq: Fr.) Kumm’, Biotechnologia Acta, 4(3), pp. 082–089 (in Ukrainian).

Kuznetsova, O. and Vlasenko, E. (2020) ‘Effect of natural and synthetic phytohormones on growth and development of higher Basidiomycetes’, Biotechnol. Acta, 13, pp. 19–31.

Kyaschenko, J., Clemmensen, K. E., Karltun, E. and Lindahl, B. D. (2017) ‘Below?ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities’, Ecology Letters, 20(12), pp. 1546–1555.

Mach?n, P., Pajares, J., Diez, J. and Alves-Santos, F. (2009) ‘Influence of the ectomycorrhizal fungus Laccaria laccata on pre-emergence, post-emergence and late damping-off by Fusarium oxysporum and F. verticillioides on Stone pine seedlings’, Symbiosis, 49, pp. 101–109.

Malewski, T., Borowik, P., Olejarski, I., Berezovska, D., Dyshko, V., Behnke-Borowczyk, J., Pusz, W., Matic, S. and Oszako, T. (2023) ‘Mycobiome of post-agricultural soils 20 years after application of organic substrates and planting of pine seedlings’, Forests, 14, 36. https://doi.org/10.3390/f14010036

Mao, Z., Corrales, A., Zhu, K., Yuan, Z., Lin, F., Ye, J., Hao, Z. and Wang, X. (2019) ‘Tree mycorrhizal associations mediate soil fertility effects on forest community structure in a temperate forest’, New Phytologist, 223, pp. 475–486.

Milovi?, M., Kebert, M. and Orlovi?, S. (2021) ‘How mycorrhizas can help forests to cope with ongoing climate change?’, ?umarski List, 145(5–6), pp. 279–286.

Mohan, V., Nivea, R. and Menon, S. (2015) ‘Evaluation of ectomycorrhizal fungi as potential bio-control agents against selected plant pathogenic fungi’, Journal of Academia and Industrial Research, 3, pp. 408–412.

Mrak, T., K?hdorf, K., Grebenc, T., ?traus, I., M?nzenberger, B. and Kraigher, H. (2017) ‘Scleroderma areolatum ectomycorrhiza on Fagus sylvatica L.’, Mycorrhiza, 27, pp. 283–293.

Opoka, W., Ka?a, K., Kr??a?ek, R., Su?kowska-Ziaja, K., Ma?lanka, A. and Muszy?ska, B. (2018) ‘TLC-Densitometry analysis of indole compounds in mycelial culture of Imleria badia and Agaricus bisporus enriched with precursors – serine or anthranilic acid’, Acta Chromatographica, 30(4), pp. 236–242. https://doi.org/10.1556/1326.2017.00325

Pachlewski, R. and Pachlewska, J. (1974) Studies on symbiotic properties of mycorrhizal fungi of pine (Pinus silvestris L.) with the aid of the method of mycorrhizal synthesis in pure cultures on agar. Warsaw: Forest Research Institute.

Parlad?, J., Pera, J. and Alvarez, I.F. (1996) ’Inoculation of containerized Pseudotsuga menziesii and Pinus pinaster seedlings with spores of five species of ectomycorrhizal fungi’, Mycorrhiza, 6, pp. 237–245.

Peay, K. G., Kennedy, P. G. and Talbot, J. M. (2016) ‘Dimensions of biodiversity in the Earth mycobiome’, Nature Reviews Microbiology, 14(7), pp. 434–447.

Pecl, G.T., Ara?jo, M.B., Bell, J.D., Blanchard, J., Bonebrake, T.C., Chen, I.-C., et al. (2017). Biodiversity redistribution under climate change: impacts on ecosystems and human well-being’, Science, 355, eaai9214. https://doi.org/10.1126/science.aai9214

Pereima, I. V. and Ivanova, T. V. (2017) ‘Stimulation of growth of species of the fungus of the genus Pleurotus (Fr.) P. Kumm. at a glucose nutrition’, Biotechnologia Acta, 10(6), pp. 45–52 (in Ukrainian).

Py?ek, P., Jaro??k, V., Hulme, P.E., Pergl, J., Hejda, M., Schaffner, U. and Vil?, M. (2012) ‘A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment’, Global Change Biology, 18, pp. 1725–1737. https://doi.org/10.1111/j.1365-2486.2011.02636.x

Raidl, S. (1997) Studien zur Ontogenie an Rhizomorphen von Ektomykorrhizen. Berlin/Stuttgart: Cramer; Schweizerbart’sche Verlagsbuchhandlung, Bibliotheca Mycologica, Volume 169. ISBN 978-3-443-59071-0

Read, D.J. and Perez-Moreno, J. (2003) ‘Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance?’, New Phytologist, 157, pp. 475–492.

Richter, D.L. and Bruhn, J.N. (1990) ‘Scleroderma citrinum (Gasteromycetes, Sclerodermatales) and Larix decidua form ectomycorrhizae in pure culture’, Nova Hedwigia, 50, pp. 355–360.

Rybak, O. V. and Rybak, V. O. (2015) ‘Resistance of pine forests with understory crops of red oak to root fungus’, Ukrainian Journal of Forest and Wood Science, 216(1), pp. 146–154 (in Ukrainian).

Sirenko, O.G., Belova, N., Maltsov, I.Y., Marynyuk, M.M. and Sokol, V. (2011) ‘Mycorrhiza of Pinus sylvestris L. and Picea abies (L.) Karst. under natural and cultural conditions and the results of artificial mycorrhization of seedlings’, Newsletter of Precarpathian Natl. Univ. named after Vasyl Stefanyk. Ser. Biol., 15, pp. 224–234 (in Ukrainian).

Smith, F. A. and Smith, S. E. (1997a) ‘Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses’, New Phytologist, 137, pp. 373–388.

Smith, F. A. and Smith, S. E. (1997b) ‘Tansley review no. 96 structural diversity in (vesicular)–arbuscular mycorrhizal symbioses’, The New Phytologist, 137(3), pp. 373–388.

Smith, S. S. (1980) ‘Mycorrhizas of autotrophic higher plants’, Biological Reviews, 55(4), pp. 475–510.

Smith, S.E. and Read, D.J. (2010) Mycorrhizal Symbiosis. Cambridge: Academic Press.

Sterkenburg, E., Bahr, A., Brandstr?m Durling, M., Clemmensen, K. E. and Lindahl, B. D. (2015) ‘Changes in fungal communities along a boreal forest soil fertility gradient’, New Phytologist, 207(4), pp. 1145–1158.

Strzelczyk, E. and Pokojska-Burdziej, A. (1984) ‘Production of auxins and gibberellin-like substances by mycorrhizal fungi, bacteria and actinomycetes isolated from soil and the mycorrhizosphere of pine (Pinus silvestris L.)’, Plant and Soil, 81(2), pp. 185–194.

Suding, K.N., Gross, K.L. and Houseman, G.R. (2004) ‘Alternative states and positive feedbacks in restoration ecology’, Trends in Ecology & Evolution, 19, pp. 46–53. https://doi.org/10.1016/j.tree.2003.10.005

Tedersoo, L., Bahram, M., P?lme, S., K?ljalg, U., Yorou, N. S., Wijesundera, R., ... and Abarenkov, K. (2014) ‘Global diversity and geography of soil fungi’, Science, 346(6213), 1256688.

Tedersoo, L., Bahram, M. and Zobel, M. (2020) ‘How mycorrhizal associations drive plant population and community biology’, Science, 367.

Tripathi, S., Mishra, S.K., Varma, A. (2017). ‘Mycorrhizal fungi as control agents against plant pathogens’, in Varma, A., Prasad, R., Tuteja, N. (eds) Mycorrhiza – Nutrient Uptake, Biocontrol, Ecorestoration. Springer, Cham, pp. 161–178. https://doi.org/10.1007/978-3-319-68867-1_8

van Der Heijden, M.G., Martin, F.M., Selosse, M.A. and Sanders, I.R. (2015) ‘Mycorrhizal ecology and evolution: The past, the present, and the future’, New Phytologist, 205, pp. 1406–1423.

Vellinga, E.C., Wolfe, B.E. and Pringle, A. (2009) ‘Global patterns of ectomycorrhizal introductions’, New Phytologist, 181(4), pp. 960–973.

Veresoglou, S.D., Wulf, M. and Rillig, M.C. (2017) ‘Facilitation between woody and herbaceous plants that associate with arbuscular mycorrhizal fungi in temperate European forests’, Ecology and Evolution, 7(4), pp. 1181–1189.

Voiry, H. (1981) ‘Classification morphologique des ectomycorhizes du ch?ne et du h?tre dans le nord-est de la France’, European Journal of Plant Pathology, 11, pp. 284–299.

Waller, K., Raidl, S. and Agerer, R. (1993) ‘Ectomycorrhizae of Scleroderma citrinum’, Zeitschriff f?r Mykologie, 59(2), pp. 141–153 (in German).

Ugarov, V., Popov, O., Danilenko, O. and Nozhenko, N. (2013) ‘Influence of Pinus sylvestris L.seedlings preplanting mycorrhization on survival and growth of forest plantations on the burned areas’, Forestry and Forest Melioration, 123, 134–139.

Zhdanyuk, I. (2020) The effect of mycorrhizal preparation on the productivity of soybeans under Polissia conditions. Technical Report; Institutional Repository of Polissia National University: Zhytomyr, Ukraine (in Ukrainian).

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.