Shift in fungal communities associated with Pinus sylvestris stands affected by root rot
ARTICLE PDF

Keywords

Scots pine
Heterobasidion annosum s.l. сосна звичайна
Heterobasidion annosum s.l.

How to Cite

Davydenko , K. V., & Ustsky, I. M. . (2023). Shift in fungal communities associated with Pinus sylvestris stands affected by root rot. Forestry and Forest Melioration, (142), 136–146. https://doi.org/10.33220/1026-3365.142.2023.136

Abstract

Introduction

Scots pine (Pinus sylvestris) covers large areas in European regions with significant economic importance to Ukrainian forest industry. Root rot caused by the wood-decay fungus Heterobasidion annosum damages both below- and above-ground parts of Scots pines. The disease progress is likely to be affected by reshaping in the forest such as soil properties, vegetation composition, and tree age. These changes are apparently followed up by paralleled shifts in fungal community composition on forest soil with potential feedback on ecosystem functioning.

The objective of the study was to screen fungal groups associated with the root system of P. sylvestris in stands affected by H.annosum s.s. to better understand the pathogenesis and development of root rot infection, as well as to recognize whether root size and disease severity affect diversity of fungi of the root system in the forest-steppe conditions of Ukraine. The additional object was to study other resident microflora of P. sylvestris root infested by H.annosum s.s. to find out whether the H. annosum s.s. impacts the overall diversity of other fungi.

Materials and Methods

The field study was carried out in 2018–2020. Field study sites were pure pine forest stands located in Kharkiv region (compartment 126, subcompartment 7, tract Bugri, Kharkiv Forest Research Station). Wood core and root samples from P. sylvestris were collected from the five infected (50–100 m apart from each other) and five non-infected trees (up to 500 m apart from the infested area and 50–100 m apart from each other). Wood and root samples were used for fungal culturing and direct sequencing using ITS1F and ITS4 primers.

Results

In the present study, we tried to evaluate fungal communities across diseased Pinus sylvestris stands and investigated correlations between taxonomic composition and forest health. Not surprisingly, root rot infestation had a significant effect on root-associated fungal abundance and diversity. During disease development, the root-associated fungal community shifted in composition from dominance by saprotrophic fungi to ectomycorrhizal and pathogenic fungal species. Our results suggested that maintenance of functional diversity in the root-associated fungal community may sustain long-term forest health or even root rot resistance to some extent by retaining a capacity for symbiosis-driven recycling of organic nutrients; however, this hypothesis is necessary to carefully examine and prove further.

Conclusions

Fungal culturing from 10 surface-sterilized wood cores resulted in 21 fungal cultures, 2.1 per wood segment. Direct sequencing from 40 surface-sterilized segments of lateral roots resulted in 247 fungal sequences or 6.2 per root segment on average. The most dominant fungi from the infested trees of Pinus sylvestris were Dactylonectria macrodidyma (4.98%), Acremonium sp (4.52%), Cladosporium cladosporioides (4.07%) from Ascomycota and Heterobasidion annosum s.s. (4.07%) from Basidiomycota, while for non-infested group Unidentified Ascomycota175244 (13.19%), Penicillium spinulosum (9.89%), Acremonium sp. (8.79%), Bionectriaceae sp. (8.79%) were the most common.

2 Figs., 2 Tables, 32 Refs.

https://doi.org/10.33220/1026-3365.142.2023.136
ARTICLE PDF

References

Altschul, S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990. Basic local alignment search tool. J Mol Biol, 215: 403–410.

Bailey, K. L., Pitt, W. M., Falk, S., Derby, J. 2011. The effects of Phoma macrostoma on nontarget plant and target weed species. Biological Control, 58(3): 379–386.

Colwell, R. K. and Coddington, J. A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 345(1311): 101–118. https://doi.org/10.1098/rstb.1994.0091

Dalya, L. B., Capretti, P., Ghelardini, L., Jankovsk?, L. 2019. Assessment of presence and distribution of Armillaria and Heterobasidion root rot fungi in the forest of Vallombrosa (Apennines Mountains, Italy) after severe windstorm damage. Forest-Biogeosciences and Forestry, 12(1): 118. https://doi.org/10.3832/ifor2929-012

Davydenko, K., Vysotska, N., Yushchyk, V., 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: 110–119. http://dspace.hnpu.edu.ua/handle/123456789/6751

Durant, H., T., de Rigo, D., Caudullo, G. 2016. Pinus sylvestris in Europe: Distribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Caudullo, G., Houston Durrant, T., and Mauri, A. (Eds.). European atlas of forest tree species. Publication Office of the European Union, Luxemburg, e016b94, pp. 132–135.

Garbelotto, M. and Gonthier, P. 2013. Biology, epidemiology, and control of Heterobasidion species worldwide. Annu. Rev. Phytopathol., 51: 39–59. https://doi.org/10.1146/annurev-phyto-082712-102225

Gardes, M. and Bruns, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol. Ecol., 2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x

Hagenbo, A., Kyaschenko, J., Clemmensen, K. E., Lindahl, B. D., Fransson, P. 2018. Fungal community shifts underpin declining mycelial production and turnover across a Pinus sylvestris chronosequence. Journal of Ecology, 106(2): 490–501. https://doi.org/10.1111/1365-2745.12917

Halleen, F., Fourie, P.H., Crous, P.W. 2006. A review of black foot disease of grapevine. Phytopatologia Mediterranea 45, 55–67 https://www.torrossa.com/en/resources/an/2211151#

Hammer, O., Harper, D. A. T., Ryan, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1–9.

Jurgensen, M. F., Harvey, A. E., Graham, R. T., Page-Dumroese, D. S., Tonn, J. R., Larsen, M. J., Jain, T. B. 1997. Impacts of timber harvesting on soil organic matter, nitrogen, productivity, and health of Inland Northwest forests. Forest Science, 43(2): 234–251. https://doi.org/10.1093/forestscience/43.2.234

Kyaschenko, J., Clemmensen, K. E., Hagenbo, A., Karltun, E., Lindahl, B. D. 2017. Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. The ISME journal, 11(4): 863–874. https://doi.org/10.1038/ismej.2016.184

Lygis, V., Vasiliauskas, R., Stenlid, J., Vasiliauskas, A. 2004. Silvicultural and pathological evaluation of Scots pine afforestations mixed with deciduous trees to reduce the infections by Heterobasidion annosum ss. Forest Ecology and Management, 201(2–3): 275–285. https://doi.org/10.1016/j.foreco.2004.07.013

Maggurran, A. M. 1998. Ecological diversity and its measurement. Princeton, Princeton University Press, 423 p.

Menkis, A., Vasiliauskas, R., Taylor, A. F., Stenlid, J., Finlay, R. 2005. Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation. Mycorrhiza, 16: 33–41. https://doi.org/10.1007/s00572-005-0011-z

Meshkova, V. 2022. Who, where, when, and how damages forest – challenges for prediction and control. Environmental Sciences Proceedings. 2022, 22, 71. https://doi.org/10.3390/ IECF2022-13044

Millberg, H., Hopkins, A. J. M., Boberg, J., Davydenko, K., Stenlid, J. 2006. Disease development of Dothistroma needle blight in seedlings of Pinus sylvestris and Pinus contorta under Nordic conditions. Forest Pathology, 46(5):

–521.

Mouillot, D. and Lepretre, A. 1999. A comparison of species diversity estimators. Researches on Population Ecology, 41(2): 203–215. https://doi.org/10.1007/s101440050024

Parkinson, L. E., Shivas, R. G., & Dann, E. K. 2017. Pathogenicity of nectriaceous fungi in Australia. Phytopathology, 107(12), 1479-1485. https://doi.org/10.1094/PHYTO-03-17-0084-R

Per?oh, D., Melcher, M., Flessa, F., Rambold, G. 2010. First fungal community analyses of endophytic ascomycetes associated with Viscum album ssp. austriacum and its host Pinus sylvestris. Fungal Biology, 114(7):

–596. https://doi.org/10.1016/j.funbio.2010.04.009

Piri, T., Vainio, E. J., Nuorteva, H., Hantula, J. 2021. High seedling mortality of Scots Pine caused by Heterobasidion annosum ss. Forests, 12(9): 1289. https://doi.org/10.3390/f12091289

Pitk?nen, T. P., Piri, T., Lehtonen, A., Peltoniemi, M. 2021. Detecting structural changes induced by Heterobasidion root rot on Scots pines using terrestrial laser scanning. Forest Ecology and Management, 492: 119239. https://doi.org/10.1016/j.foreco.2021.119239

Probst, C. M., Ridgway, H. J., Jaspers, M. V., Eirian Jones, E. 2019. Pathogenicity of Ilyonectria liriodendri and Dactylonectria macrodidyma propagules in grapevines. European Journal of Plant Pathology, 154: 405–421.

Oliva, J., Messal, M., Wendt, L., Elfstrand, M. 2017. Quantitative interactions between the biocontrol fungus Phlebiopsis gigantea, the forest pathogen Heterobasidion annosum and the fungal community inhabiting Norway spruce stumps. Forest Ecology and Management, 402: 253–264.

Stenstr?m, E., Ndobe, N. E., Jonsson, M., Stenlid, J., Menkis, A. 2014. Root-associated fungi of healthy-looking Pinus sylvestris and Picea abies seedlings in Swedish forest nurseries. Scandinavian Journal of Forest Research, 29(1): 12–21. https://doi.org/10.1080/02827581.2013.844850

Swedjemark, G. and Stenlid, J. 2001. A highly diverse population of Heterobasidion annosum in a single stump of Picea abies. Mycol. Res. 105(2): 183–189. https://doi.org/10.1017/S0953756200003270

Ustskyi, I. M. 2011. Soil features of pine plantations of the Right Bank Polissia affected by root rot fungus. Forestry and Forest Melioration, 118: 170–177. (in Ukrainian). http://dspace.nbuv.gov.ua/handle/123456789/72685

Ustskyi, I. M., Polyakova, L. V., Tkachuk, V. I. 2010. Secondary metabolites of sod-podzolic soils in stands affected chronic pine diseases in central Polissia. Forestry and Forest Melioration, 117: 271–277 (in Ukrainian). http://dspace.nbuv.gov.ua/handle/123456789/72683

Vasiliauskas, R. and Stenlid, J. 1998. Fungi inhabiting stems of Picea abies in a managed stand in Lithuania. Forest Ecology and Management, 109(1–3): 119–126. https://doi.org/10.1016/S0378-1127(98)00226-6

Vasaitis, R. 2013: Heart rots, sap rots and canker rots. In: Gonthier, P. & Nicolotti, G. (Eds.). Infectious forest diseases. Wallingford CAB International, p. 197–229.

Zhao, P. S., Guo, M. S., Gao, G. L., Zhang, Y., Ding, G. D., Ren, Y., Akhtar, M. 2020. Community structure and functional group of root-associated Fungi of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert. Ecology and Evolution, 10(6): 3032–3042. https://doi.org/10.1002/ece3.6119

Creative Commons License

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