Root ectomycorrhizal status of oak trees symptomatic and asymptomatic for Acute Oak Decline in southern Britain
Barsoum, N., A'Hara, S. W., Cottrell, J. E., Forster, J., Garcia, M. S. J., Schonrogge, K. and Shaw, L.
(2021)
Root ectomycorrhizal status of oak trees symptomatic and asymptomatic for Acute Oak Decline in southern Britain.
Forest Ecology and Management, 482.
118800.
ISSN 0378-1127
It is advisable to refer to the publisher's version if you intend to cite from this work. See Guidance on citing. To link to this item DOI: 10.1016/j.foreco.2020.118800 Abstract/SummaryAcute Oak Decline (AOD) is a decline-disease that has distinctive symptoms and poses a serious threat to oak. Our understanding of the causal factors of AOD remains poor but it is likely that multiple biotic and abiotic factors contribute to a deterioration in oak condition. There is evidence that indications of above-ground tree health status are frequently reflected below-ground in roots and associated ectomycorrhizal (ECM) fungal communities. However, no study has yet explored these potential relationships specifically in AOD affected trees. In this study, we compare the composition and range of functional exploration types of ECM communities associated with AOD symptomatic oak trees and with AOD asymptomatic trees in three oak-dominated woodlands in southern England. We additionally assess the abundance of fine roots tips in surface soils beneath AOD symptomatic and asymptomatic trees and consider soil physico-chemical effects on ECM communities. The frequency of fine root tips was found to be significantly higher on asymptomatic compared with symptomatic trees in two of the three woodlands studied and long-distance ECM exploration types had a weak positive association with AOD asymptomatic trees. ECM diversity and composition were, however, unaffected by tree symptom status and were not related to the frequency of fine root tips. ECM diversity and compositional (but not exploration type) differences were evident only between the different woodlands and this was related to a small number of soil chemistry variables. This study revealed a relationship between the above-ground symptoms of AOD (i.e. stem lesions and Agrilus biguttatus exit holes) and the frequency of live root tips, providing a potential additional diagnostic tool of trees in decline and highlighting the importance of considering belowground rhizosphere microbiome communities. Item Type: | Article |
---|
Refereed: | Yes |
---|
Divisions: | Science > School of Archaeology, Geography and Environmental Science > Department of Geography and Environmental Science |
---|
ID Code: | 94793 |
---|
Additional Information: | References
Agerer, R., 2001. Exploration types of ectomycorrhizae – A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11, 107–114.
Agerer, R., 2006. Fungal relationships and structural identity of their ectomycorrhizae. Mycological Progress 5, 67–107.
Agerer, R., Rambold, G., 2020. DEEMY – An Information System for Characterization and Determination of Ectomycorrhizae. http://www.deemy.de/ (accessed 4 Sept 2020).
Averill, C., Hawkes, C. V., 2016. Ectomycorrhizal fungi slow soil carbon cycling. Ecology Letters 19(8), 937-947. https://onlinelibrary.wiley.com/doi/abs/10.1111/ele.12631
Bauce, E., Allen, D.C., 1992. Condition of the fine roots of sugar maple in different stages of decline. Canadian Journal of Forest Research 22 (2), 264-266. https://doi.org/10.1139/x92-034.
BCERN - British Columbia Ectomycorrhizal Research Network, 2020. http://forestrydev.org/biodiversity/bcern/profiles/profiles.shtml (accessed 4 Sept. 2020).
Blaschke, H., 1994. Decline symptoms on roots of Quercus robur. European Journal of Forest Pathology 24 (6‐7), 386-398. https://doi.org/10.1111/j.1439-0329.1994.tb00832.x
Branzanti, M.B., Rocca, E., Pisi, A., 1999. Effect of ectomycorrhizal fungi on chestnut ink disease. Mycorrhiza 9, 103–109.
Broberg, M., Doonan, J., Mundt, F., McDonald, J. 2018. Integrated multi-omic analysis of host-microbiota interactions in acute oak decline. Microbiome 6, 21.
Brown, N., Inward, D.J.G., Jeger, M., Denman, S., 2015. A review of Agrilus biguttatus
in UK forests and its relationship with acute oak decline. Forestry 88, 53–63.
Brown, N., Jeger, M., Kirk, S., Xu, X., Denman, S., 2016. Spatial and temporal patterns in symptom expression within eight woodlands affected by Acute Oak Decline. Forest Ecology Management 360, 97–109.
Brown, N., Vanguelova, E., Parnell, S., Broadmeadow, S., Denman, S., 2018. Predisposition of forests to biotic disturbance: Predicting the distribution of Acute Oak Decline using environmental factors. Forest Ecology Management 407, 145–154.
Bzdyk, R.M., Olchowik, J., Studnicki, M., Nowakowska, J.A., Oszako, T., Urban, A., Hilszczańska, D., 2019. Ectomycorrhizal colonisation in declining oak stands on the Krotoszyn Plateau, Poland. Forests 10, 30. https://doi.org/10.3390/f10010030.
Causin, R., Montecchio, L., Accordi, S., 1996. Probability of ectomycorrhizal infection in a declining stand of common oak. Annales des Sciences Forestières 53, 743-752.
Clarke, K.R., Warwick, R.M., 1998. A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35, 523–531.
Cools, N., De Vos, B., 2016. Part X: Sampling and Analysis of Soil, in: UNECE ICP Forests Programme Coordinating Centre (Ed.), Manual on methods and criteria for harmonized sampling, assessment, monitoring and analysis of the effects of air pollution on forests. Thünen Institute of Forest Ecosystems, Eberswalde, Germany, pp. 29. + Annex
Corcobado, T., Vivas, M., Moreno, G., Solla, A., 2014. Ectomycorrhizal symbiosis in declining and non-declining Quercus ilex trees infected with or free of Phytophthora cinnamomi. Forest Ecology and Management 324, 72–80. https://doi.org/10.1016/j.foreco.2014.03.040.
Corcobado, T., Moreno, G., Marisa Azul, A.M., Solla, A., 2015. Seasonal variations of ectomycorrhizal communities in declining Quercus ilex forests: interactions with topography, tree health status and Phytophthora cinnamomi infections. Forestry 88, 257–266.
Cox, F., Barsoum, N., Lilleskov, E. A., Bidartondo, M. I., 2010. Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecology Letters 13, 1103–1113.
Defrenne, C.E., Philpott, T.J., Guichon, S.H.A., Roach, W.J., Pickles, B.J., Simard, S.W., 2019. Shifts in ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior Douglas fir forests of western Canada. Front. Plant Sci. 10, 643.
Denman, S., Webber, J., 2009. Oak declines: new definitions and new episodes in Britain. Quarterly Journal of Forestry 103, 285–290.
Denman, S., Brown, N., Kirk, S., Jeger, M., Webber, J., 2014. A description of the symptoms of Acute Oak Decline in Britain and a comparative review on causes of similar disorders on oak in Europe. Forestry 87, 535–551.
Denman, S., Doonan, J., Ransom-Jones, E., Broberg, M., Plummer, S., Kirk, S., Scarlett, K., Griffiths, A.R., Kaczmarek, M., Forster, J., Peace, A., Golyshin, P.N., Hassard, F., Brown, N., Kenny, J.G., McDonald, J.E., 2018. Microbiome and infectivity studies reveal complex polyspecies tree disease in Acute Oak Decline. International Society Microbial Ecology Journal 12, 386–399.
Di Pietro, M., Churin, J.L., Garbaye, J., 2007. Differential ability of ectomycorrhizas to survive drying. Mycorrhiza 17, 547–550.
Duchesne, L.C., Peterson, R.L., Ellis, B.E., 1988a. Interaction between the ectomycorrhizal fungus Paxillus involutus and Pinus resinosa induces resistance to Fusarium oxysporum. Canadian Journal of Botany 66, 558–562.
Duchesne, L.C., Peterson, R.L., Ellis, B.E., 1988b. Pine root exudate stimulates the synthesis of antifungal compounds by the ectomycorrhizal fungus Paxillus involutus. New Phytol. 108, 471–476.
Entry, J.A., Cromack Jr., K., Susan G. Stafford, S.G., Castellano, M.A., 1987. The effect of pH and aluminum concentration on ectomycorrhizal formation in Abies balsamea. Canadian Journal of Forest Research 17, 865-871. https://doi.org/10.1139/x87-137
Fernandez, C.W., Kennedy, P.G., 2016. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytologist 209 (4), 1382-1394
Futai, K., Taniguchi, T., Kataoka, R., 2008. Chapter 11: Ectomycorrhizae and their importance in forest ecosystems, in: Siddiqui, Z.A. Akhtar, M.S., Futai, K. (Eds.), Mycorrhizae: Sustainable Agriculture and Forestry. Springer Science + Business Media B.V., pp. 241–285.
Gardes, M., Bruns, T.D., 1993. ITS primers with enhanced specificity for basidiomycetes —
application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113–118.
Harper, A.L., McKinney, L.V., Nielsen, L.R., Havlickova, L., Li, Y., Trick, M., Fraser, F., Wang, L., Fellgett, A., Sollars, E.S.A., Janacek, S.H., Downie, J.A., Buggs, R.J.A., Kjær, E.D., Bancroft, I., 2016. Molecular markers for tolerance of European ash (Fraxinus excelsior) to dieback disease identified using Associative Transcriptomics. Scientific Reports 6, 19335. http://dx.doi.org/10.1038/srep19335.
Hobbie, J.E., Hobbie E.A., 2006. N-15 in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87, 816–822.
Hobbie, E.A., Agerer, R., 2010. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil 327, 71–83. https://doi.org/10.1007/s11104-009-0032-z.
Jarvis, S., Woodward, S., Alexander, I.J., Taylor, A.F.S., 2013. Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine. Global Change Biology 19, 1688-1696.
Jones, M.D., Durall, D.M., Cairney, J.W.G., 2003. Ectomycorrhizal fungal communities in young forest stands regenerating after clear cut logging. New Phytologist 157, 399–422.
Jongbloed, R.H., Borst-Pauwels, G.W.F.H., 1992. Effects of aluminium and pH on growth and potassium uptake by three ectomycorrhizal fungi in liquid culture. Plant Soil 140, 157–16.5 https://doi.org/10.1007/BF00010593
Kjøller, R., Nilsson, L.O., Hansen, K., Schmidt, I.K., Vesterdal, L., Gundersen, P., 2012. Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytologist 194(1), 278-86.
Kovacs, G., Pausch, M. and Urban, A., 2000. Diversity of ectomycorrhizal morphotypes and oak decline. Phyton 40, 109–116.
Kuikka, K., Härmä, E., Markkola, A., Rautio, P., Roitto, M., Saikkonen, K. Ahonen-Jonnarth, U., Finlay, R., Tuomi, J., 2003. Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84, 2051–2061.
Lambers, H., Albornoz, F., Kotula, L., Laliberté, E., Ranathunge, K., Teste, F.P., Zemunik, G., 2018. How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyper-diverse ecosystems. Plant Soil 424, 11–33.
Lancellotti, E., Franceschini, A., 2013. Studies on the ectomycorrhizal community in a declining Quercus suber L. stand. Mycorrhiza 23, 533–542. https://doi.org/10.1007/s00572-013-0493-z.
Lilleskov, E.A., Kuyper, T.W., Bidartondo, M.I., Hobbie, E.A., 2019. Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review. Environmental Pollution 246, 148-162. https://doi.org/10.1016/j.envpol.2018.11.074
Maghnia, F.Z., Abbas, Y., Mahé, F., Kerdouh, B., Tournier, E., Ouadji, M., Tisseyre, P., Prin, Y., El Ghachtouli, N., Yakhlef, S.E.B., Duponnois, R., Sanguin, H., 2017. Habitat- and soil-related drivers of the root-associated fungal community of Quercus suber in the Northern Moroccan forest. PLoS ONE 12(11), e0187758. https://doi.org/10.1371/journal.pone.0187758.
Marx, D.H., 1972. Ectomycorrhizae as biological deterrents. Annual Review Phytopathology 10, 429–454.
Meinen, C., 2008. Fine root dynamics in broad-leaved deciduous forest stands differing in tree species diversity. PhD Dissertation, University of Göttingen, Germany.
Mosca, E., Montecchio, L., Sella, L., Garbaye, J., 2007. Short-term effect of removing tree competition on the ectomycorrhizal status of a declining pedunculate oak forest (Quercus robur L.). Forest Ecology and Management 244, 129–140.
Montecchio, L., Causin, R., Rossi, S., Accordi, S.M., 2004. Changes in ectomycorrhizal diversity in a declining Quercus ilex coastal forest. Phytopathologia Mediterranea 43 (1), 26-34.
Nechwatal, J., Oβwald, W., 2008. Comparative studies on the fine root status of healthy and declining spruce and beech trees in the Bavarian Alps and occurrence of Phytophthora and Pythium species. Forest Pathology 31(5), 257-273. https://doi.org/10.1046/j.1439-0329.2001.00244.x
Oksanen, J., Blanchet, F.G., Friendly., M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, H.M.H., Szoecs, E.,Wagner, H. 2019. vegan: Community Ecology Package. R package version 2.5-4. https://CRAN.R-project.org/package=vegan
Olsen, S. R., Cole, C. V., Watanabe, F. S., Dean. L. A., 1954. Estimation of available phosphorus in soils by extraction with NaHCO3. USDA Cir.939. U.S. Washington.
Parke, J. L., Lindeman, R. G., Black, C. H., 1983. The effect of ectomycorrhizas in drought tolerance of Douglas Fir seedlings. New Phytologist 95, 83-95.
Peay, K.G., Kennedy, P.G., Bruns, T.D., 2008. Fungal community ecology: A hybrid beast with a molecular master. BioScience 58(9), 799-810.
Pena, R., Offermann, C., Simon, J., Naumann, P. S. Geßler, A., Holst, J., Dannenmann, M., Mayer, H., Kögel-Knabner, I., Rennenberg, H., Polle, A., 2010. Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest. Applied and Environmental Microbiology 76, 1831–1841.
Power, A.S., Ashmore, M.R., 1996. Nutrient reelations and root mycorrhizal status of healthy and declining beech (Fagus sylvatica L.) in southern Britain. Water, Air and Soil Pollution 86, 317-333.
Przyby, K., Pukacka, S., 1995. Root characterization of declining Quercus robur L. trees. Phytopathologia Polonica 22, 125-132.
R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (accessed 4 Sept 2020).
Read, D. J., 1986. Non-nutritional effects of mycorrhizal infection, in Gianinazzi-Pearson, V., Gianinazzi, S. (Eds.), Physiological and Genetical Aspects of Mycorrihizae. 1st European Symposium on Mycorrhizae, 1-5 July, 1985, Dijon, pp. 169-176.
Reed, K., Denman, S., Leather, S.R., Forster, J., Inward, D.J.G., 2018. The lifecycle of Agrilus biguttatus: the role of temperature in its development and distribution, and implications for Acute Oak Decline. Agricultural and Forest Entomology 20(3), 334-346.
Rewald, B., Meinen, C., Trockenbrodt, M., Ephrath, J.E., Rachmilevitch, S., 2012. Root taxa identification in plant mixtures – current techniques and future challenges. Plant Soil 359, 165–182. https://doi.org/10.1007/s11104-012-1164-0
Rühling, A., Söderström, B. 1990. Changes in fruitbody production of mycorrhizal and litter decomposing macromycetes in heavy metal polluted coniferous forests in North Sweden. Water Air Soil Pollution 49, 375–387.
Saikkonen, K., Ahonen‐Jonnarth, U., Markkola, A.M., Helander, M., Tuomi, J., Roitto, M., Ranta, H., 1999. Defoliation and mycorrhizal symbiosis: a functional balance between carbon sources and below‐ground sinks. Ecology Letters 2(1), 19-26 https://doi.org/10.1046/j.1461-0248.1999.21042.x
Scattolin, L., Dal Maso, E., Mutto Accordi, S., Sella, L., Montecchio, L., 2012. Detecting asymptomatic ink-diseased chestnut trees by the composition of the ectomycorrhizal community. Forest Pathology 42, 501–509.
Shannon, C.E., Weaver, A. 1949. The mathematical theory of communication. University of Illinois Press, Urbana IL, The University of Illinois Press, 1-117.
Sinclair, W. A., Sylvia, D. M., Larsen, A. O., 1982. Disease suppression and growth promotion in Douglas-fir seedlings by the ectomycorrhizal fungus Laccaria laccata. Forest Science 28 (2), 191–201.
Smith, S.E., Read, D.J., 2010. Mycorrhizal Symbiosis. Academic Press, London.
Spake, R., van der Linde, S., Newton, A.C., Suz, L.M., Bidartondo, M.I., Doncaster, C.P., 2016. Similar biodiversity of ectomycorrhizal fungi in set-aside plantations and ancient old-growth broadleaved forests. Biological Conservation 194: 71-79.
Suz, L.M., Barsoum, N., Benham, S., Dietrich, H.-P., Fetzer, K.D., Fischer, R., García, P., Gehrman, J., Kristöfel, F., Manninger, M., Neagu, S., Nicolas, M., Oldenburger, J., Raspe, S., Sánchez, G., Schröck, H.W., Schubert, A., Verheyen, K., Verstraeten, A., Bidartondo, M.I., 2014. Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Molecular Ecology 23, 5628–5644.
Swaty, R.L., Deckert, R.J., Whitham, T.G., Gehring, C.A., 2004. Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85 (4), 1072-1084.
Tedersoo, L., Bahram, M., Polme, S., Koljalg, U., Yorou, N.S., Wijesundera, R., et al., 2014. Global diversity and geography of soil fungi. Science 346(6213) 1256688 https://doi.org/10.1126/science.1256688
Thomas, F.M., Blank, R., Hartmann, G., 2002. Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. Forest Pathology 32, 277–307.
Thomas, F.M., 2008. Recent advances in cause–effect research on oak decline in Europe. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 3 (037), 1 – 12. http://dx.doi.org/10.1079/PAVSNNR20083037.
Treu, R., Karst, J., Randall, M., Pec, G.J., Cigan, P.W., Simard, S.W., Cooke, J.E.K., Erbilgin, N., Cahill, J.F., 2014. Decline of ectomycorrhizal fungi following a mountain pine beetle epidemic. Ecology 95, 1096–1103.
Van Driessche, I., Piérart, P., 1995. Ectomycorrhization and health of beeches and oaks in the forest of Soignes. Belgian Journal of Botany 128, 57-70.
Veselá, P.K., Vašutová, M., Hofmannová, K., Edwards-Jonášová, M., Cudlin, P. 2019. Ectomycorrhizal community on Norway spruce seedlings following bark beetle infestation. Forests 10, 740.
White, T.J., Bruns, T., Lee, S., Taylor, J.W., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press, Inc., New York, pp. 315-322. http://dx.doi.org/10.1016/B978-0-12-372180-8.50042-1.
Wang, Y., Mi, X., Rosa, G. J. M., Chen, Z., Lin, P., Wang, S., Bao, Z., 2018. Technical Note: An R package for fitting sparse neural networks with application in animal breeding. Journal of Animal Science 96(5), 2016–2026. https://doi.org/10.1093/jas/sky071
Wickham. H, 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.
Zhou, M., Sharik, T.L., Jurgensen, M.F., Richter, D.L., 1997. Ectomycorrhizal colonization of Quercus rubra seedlings in response to vegetation removals in oak and pine stands. Forest Ecology and Management 93 (1–2), 91-99. |
---|
Publisher: | Elsevier |
---|
Downloads per month over past year
Date Deposited: | 09 Dec 2020 14:25 | Date item deposited into CentAUR |
---|
Last Modified: | 09 Jun 2024 03:12 | Date item last modified |
---|
University Staff: Request a correction | Centaur Editors: Update this record
|