SEEFOR – South-east European forestry - Vol. 14 No.2 - Baranowska et al - The Community of Fine Root Fungi of Silver Fir (Abies alba Mill.) Saplings

SEEFOR 14(2): 183-195
Article ID: 2313
DOI: https://doi.org/10.15177/seefor.23-13

ORIGINAL SCIENTIFIC PAPER

The Community of Fine Root Fungi of Silver Fir (Abies alba Mill.) Saplings

Marlena Baranowska^1*, Władysław Barzdajn¹, Robert Korzeniewicz¹, Wojciech Kowalkowski¹, Adrian Łukowski¹, Jolanta Behnke-Borowczyk², Mirzeta Memišević Hodžić³

(1) Poznań University of Life Sciences, Faculty of Forestry and Wood Technology, Department of Silviculture, Wojska Polskiego 71A, PL-60-625 Poznań, Poland;
(2) Poznań University of Life Sciences, Faculty of Forestry and Wood Technology, Department of Entomology and Forest Pathology, Wojska Polskiego 71C, PL-60-625 Poznań, Poland;
(3) University of Sarajevo, Faculty of Forestry, Department of Cultivation of Forests and Urban Greens, Zagrebačka 20, BA-71000 Sarajevo, Bosnia and Herzegovina

* Correspondence: e-mail:

Citation: Baranowska M, Barzdajn W, Korzeniewicz R, Kowalkowski W, Łukowski A, Behnke-Borowczyk J, Memišević Hodžić M, 2023. The Community of Fine Root Fungi of Silver Fir (Abies alba Mill.) Saplings. South-east Eur for 14(2): 183-195. https://doi.org/10.15177/seefor.23-13.

Received: 22 Feb 2022; Revised: 9 Apr 2023, 16 May 2023; Accepted: 22 May 2023; Published online: 2 Sep 2023

Cited by: Google Scholar

Abstract

This study aimed to assess the biodiversity of fungi colonizing the fine roots (diameter up to 2 mm) of 3-year-old silver fir saplings from areas of Międzylesie Forest District in Poland. It was hypothesized that quantitatively and qualitatively, mycorrhizal fungi would be the dominant fungi in root communities of silver fir. DNA extraction was performed using Plant Genomic DNA purification. The internal transcribed spacer1 (ITS1) rDNA region was amplified using specific primers, and the amplicons were purified and sequenced using sequencing by synthesis (SBS) Illumina technology. The obtained sequences were compared with reference sequences in the UNITE database (https://unite.ut.ee/) using the basic local alignment search tool (BLAST) algorithm to facilitate species identification. A total of 307,511 OTUs was obtained from each sample. There were 246,477 OTUs (80.15%) of fungi known from cultures. The genera Tuber spp. (7.51%) and Acephala spp. (3.23%) accounted for the largest share of the fungal communities on the fine roots of fir trees. Hence our results indicate the dominance of mycorrhizal fungi in these communities and reflect the excellent quality of the saplings that were assessed. Pathogenic fungi constituted a much smaller share of the fungal communities.

Keywords: Lower Silesia; Międzylesie Forest District; nursery; restoration; Sudeten Mountains

INTRODUCTION

The silver fir tree (Abies alba Mill.) used to be one of the most important forest-forming species in the mountainous and upland regions of forest stands in Poland, in which fir is the dominant species, occupying 2% of the forest area and having a 2.7% share in the volume in the forests managed by the State Forests (Bis and Dobrowolska 2012). However, since 1998, the share of fir trees in the forests of the Sudeten Mountains in Poland has fallen below 0.4%, and the species had already lost the possibility of continued existence and self-regeneration in the competitive environment of the forests of the region. For this reason, the State Forests (Poland) undertook a program to restore fir trees to forests of the Sudeten Mountains (Barzdajn 2000, 2012, Barzdajn and Kowalkowski 2012), but with time it was noticed that fungi-related issues should not be overlooked. The studies of fungal communities inhabiting fir roots have focused mainly on mycorrhizae (within and outside their natural occurrence) (Kowalski 1982, Comandini et al. 2001, Laganà et al. 2002, Rudawska et al. 2016) and pathogenic fungi that infect their root systems (Puddu et al. 2003, Oliva and Colinas 2007, Chomicz-Zegar et al. 2016). However, no research has been undertaken in the mountainous regions of Poland. In addition to pathogenic and mycorrhizal fungi, these communities are known to include antagonists of other microorganisms and neutral organisms. Root-associated fungal communities are essential components in ecosystem processes, impacting plant growth and vigour by influencing the quality, direction, and flow of nutrients and water between plants and fungi (Unuk et al. 2019). Hence, the aim of the current study was to assess the diversity of fungi occurring in the rhizosphere of the root systems of small cuttings and fir saplings. We tested the hypothesis that mycorrhizal fungi should dominate these communities

MATERIALS AND METHODS

Fine roots of 6 saplings of silver fir from the forest nursery of Międzylesie Forest District (16°66'23"E, 50°14'86"N, south-west part of Poland) were randomly selected for the study. The samples were collected in June 2017. The research material comprised fine roots (roots up to three rows to identify all types of mycorrhizae) (McCormack et al. 2015). The fine roots were washed on sieves under running tap water and dried on sterile paper. After drying, the roots were ground in a mortar frozen to -70^оC. The DNA extracted from dried roots was separated under the microscope. We composited one sample from six trees. Environmental DNA was extracted with Plant Genomic DNA Purification Kit (Thermo Fisher Scientific). The internal transcribed spacer1 (ITS1), 5.8S rDNA region was used to identify the fungal species, and the analysis was carried out with primers ITS1FI2 5′-GAACCWGCGGARGGATCA-3′ (Schmidt et al. 2013) and 5.8S 5`-CGCTGCGTT CTTCATCG-3` (Vilgalys and Gonzalez 1990). Each amplification reaction was carried out in a final volume of 25.0 μl containing 2 ml of DNA, 0.2 ml of each primer, 10.1 ml of deionized water and 12.5 mL of 2X PCR MIX (A&A Biotechnology, Gdynia, Poland). The amplification reaction was carried out in a thermocycler. This included: initial denaturation (94°C, 5 min), 35 cycles of denaturation (94°C, 30 s), annealing (56°C, 30 s), elongation (72°C, 30 s) and final elongation (72°C, 7 min). The product was then checked on a 1% agarose gel stained with Midori Green Advance DNA (Genetics, Dueren, Germany). The obtained product was purified and sequenced using sequencing by synthesis (SBS) technology from Illumina (Genomed S.A. Warsaw, Poland). The results were subjected to bioinformatic and statistical analysis according to Behnke-Borowczyk et al. (2019). The resulting sequences were compared with the reference sequences deposited in the UNITE community database (Nilsson et al. 2018, UNITE community 2020) using the basic local alignment search tool (BLAST) algorithm.

The abundance of fungi was defined as the number of OTUs in a sample. A total amount of OTUs was obtained from six samples collected from each of the 3-year-old small roots of A. alba. The frequency of an individual taxon was defined as the percentage (%) of OTUs in the total number of OTUs. Diversity was defined as the number of species in a sample. The trophic role of the detected fungal species in the community was determined based on literature data and listed in Appendix (Table A1).

RESULTS

A total of 307 511 OTUs were obtained. There were 246 477 OTUs (80.15%) of fungi known from cultures, 1 876 OTUs (0.61%) of non-cultured fungi, 47 572 (15.47%) OTUs of non-fungal organisms (mainly plants, including silver fir), and 1 814 OTUs (0.59%) of organisms with no reference sequence in UNITE database. The total number of taxa obtained was 1612.

The community comprised taxa belonging to Ascomycota (46.27%), Basidiomycota (33.64%), Zygomycota (2.52%), Rozellomycota (0.65%), and we also obtained some sequences that are not represented in the UNITE database (0.59%) (Table A1).

The Thelephoraceae (8.22%), Tuber spp. (7.51%) and Acephala spp. (3.23%) had the largest share of fine roots of common fir trees, therefore accounting for the largest share of the fungal community (Table A1).

Mycorrhizal fungi dominated the fungal community of the fine root (57,62%). The most common taxa identified among mycorrhizal fungi were: Hydnotrya spp., Tuber spp., Amphinema spp., Hymenogaster spp., Tylospora spp., endophytes including Acephala spp., Cadophora spp., pathogenic fungi including Ophiostoma spp. and saprotrophs Athelopsis lembospora, Archaeorhizomyces borealis and Mortierella spp. (Table 1, Table A1).

Table 1. Genus of ectomycorrhizal (ECM) fungi, whose frequency in the collection in fine roots of silver fir exceeded 0.03%. and which denotes the presence of a taxa in roots or soil in previous scientific reports.

Figure 1. Percentage share (%) of the most abundant types of fungi in the community (share > 0.5%).

DISCUSSION

The results of our analysis support our hypothesis that mycorrhizal fungi dominate the fungal communities on the fine root systems of silver fir saplings. Taxa, which belong to the fungi, forming mycorrhizal communities of silver fir, include Tuber spp. and Acephala spp., and these accounted for the largest share of the fungal communities on the fine root systems of fir saplings in our study. These results are slightly different from the studies of soil fungal communities in nurseries producing silver fir seedlings conducted by Behnke-Borowiczyk et al. (2020), where saprotrophic fungi dominated. However, Behnke-Borowczyk et al. (2020) also identified mycorrhizal fungi. We also identified some saprotrophs which accounted for just a small share of the fungal community (not exceeding 1.5%) on the roots of silver fir tree saplings in our study.

Smutek et al. (2010) obtained the following mycorrhizal families and species of fungi on old silver fir trees (90-105 years old): Cortinarius sertipes, Sebacina sp., Amphinema byssoides, Russula puellaris, Clavulina cristata, Cortinarius sp., Tomentella sublilacina, Russula fellea, Laccaria ametistina and Tylospora asteropcumum. Our results concur, confirming the occurrence of fungi belonging to all the taxa recorded by Smutek et al. (2010). Similarly, we have found the presence of some of the taxa detected by Wojewoda (2003) in the fungal community on fir trees, including Amanita, Amphinema, Boletus, Cenococcum, Clavulina, Cortinarius, Elaphomyces, Hydnotrya, Hydnum, Inocybe, Lactarius, Leotiomycetes, Piloderma, Pseudotomentella, Russula, Sebacina, Tomentella, Tuber, and Tylospora. However, unlike Ważny (2014) and Schirkonyer et al. (2013), the fungi genera Byssocorticium, Laccaria, Paxillus, Thelephora, Tomentellopsis and Xerocomus were not identified in our study. Ważny (2014) found that the mycorrhizal fungi which dominated on the youngest fir trees examined were: Clavulina cristata (25.2%), Tomentella sp. (10.5%), Tuber puberulum (8.9%), and Clavulina sp. (5.1%). While the genus Tuber accounted for a similar share (7.51%) of the community of fungi in our work, the presence of the other genera/species did not exceed 1%. Apart from Geopora sp. and Imleria sp., we identified similar taxa of fungi to those recorded by Rudawska et al. (2016), who studied mycorrhizal fungi of common fir trees outside their natural range, but from mature forest stands. To date, 13 species of ectomycorrhizal fungi (ECM) associated with the genus Abies have been included in DEEMY: Abierhiza fascicularis, A. tomentosa, Cortinarius odorifer, Lactarius caespitosus, L. deliciosus, L. intermedius, L. salmonicolor, L. subsericatus, Polyporoletus sublividus, Russula brevipes, R. ochroleuca, R silvicola, and Tricholoma bufonium, of which only R. ochroleuca was found in the sampled fungal community. The root community differs significantly from the fungal community associated with fir analyzed by Behnke-Borowczyk et all (2020), who isolated 13 taxa of ectomycorrhizal fungi (ECM) associated with the genus Abies.

The presence of Cenococcum geophilum and Thele-phora stuposa was insignificant in the study, which is in opposition to the research done by Rudawska et al. (2016). The list of mycorrhizal species detected in silver fir roots include Amphinema byssoides, Clavulina cristata, Lactarius aurantiacus, L. salmonicolor, Piloderma fallax, Tuber puberulum, T. asterophora, T. stuposa Boletus pruinatus, Cenococcum geophilum, and Laccaria amethystina, which have been confirmed in other studies (Eberhardt et al. 2000). In addition, C. geophilum, A. byssoides, T. stuposa, Amanita, Boletus, Cenococcum, Cortinarius, Inocybe, Laccaria, Lactarius, Russula, Sebacina, Tomentella, and Tuber also form mycorrhizal compounds with other fir species (Matsuda and Hijii 1999, 2004, Ishida et al. 2007, Kranabetter et al. 2009).

Acephala applanata, which we detected in fine roots of A. alba, was previously almost exclusively isolated from Picea abies (L.) H. Karst (Grünig et al. 2006). While second species from Acephala genus A. macrosclerotiorum formed ectomycorrhizas on Pinus sylvestris (Münzenberger et al. 2009) was detected in a study of the community of fungi on silver fir fine roots. These results are consistent with those obtained by Behnke-Borowczyk et al. (2020) in soil research related to nurseries producing silver fir seedlings. However, the share of Acephala spp. in the previously studied soil was lower than in the roots. The greater share of these fungi in the root community is not surprising, because both species inhabit the roots: A. applanata is included in the DSE (dark septate endopyhtes) (Stroheker et al. 2021), while A. macrosclerotiorum is classified as ectomycorrhizal fungi (Münzenberger et al. al. 2009).

For young silver fir trees, similarly to Unuk et all (2019), we detected endophytic root-associated fungal genera Oidiodendron, Phialocephala, and Rhizoscyphus. Some consider fungi of these genera to be mycorrhizal, and therefore they are treated as fungi in Appendix A. However, their role in the silver fir root community has not yet been clearly defined.

In fungal community of silver fir fine roots identified cosmopolitan fungi from the genera Trichoderma and Penicillium as well, which are antagonists of the pathogens Armillaria and Heterobasidion (Behnke-Borowczyk and Kwaśna 2010; Grantina-Ievina et al. 2013; Baranowska et al. 2023).

Our study also identified pathogenic fungi in the fine roots of silver fir tree saplings, namely Ophiostoma nigrocarpum, which, together with O. novo-ulmi and Ophiostoma sp., accounted for 1.11% of the fungal community. Fungi of the Ophiostoma genus are pathogens whose vectors are bark beetles on older trees (for example, Pissodes piceae), which cause white discolouration of fir’s wood, thus reducing its economic value (Six and Bentz 2003, Kirisits 2004).

CONCLUSIONS

This study led to recognizing the spectrum of mycorrhizal, saprotrophic, and pathogenic fungi characteristic for fine roots of the 3-year-old Abies alba. Relatively low proportion of pathogens in these fungal communities also supports the conclusion that they were healthy trees. To fully confirm the roles and functions of the identified taxa, further identification of communities should be carried out. Parallel to the analysis of the communities of fungi inhabiting silver fir fine roots, it is necessary to study the content of nutrients and soil pH and determine their impact on these communities. In addition, research should be continued at a later stage of tree development, i.e. in young forest stands, to determine the formation of these communities and the spectrum of specific species of fungi associated with young silver fir trees.

Author Contributions

WB, WK, JBB, MB conceived and designed the research, MB carried out the field measurements, JB performed laboratory analysis, JB and WB processed the data and performed the statistical analysis, WK, WB secured the research funding, AŁ, RK, JBB supervised the research and helped to draft the manuscript, MB wrote the manuscript. The main part of these results was presented at the international IUFRO Conference - Abies&Pinus 2022, “Fir and pine management in a changing environment: Risks and opportunities” held 19-22 September 2022 in Sarajevo, Bosnia and Herzegovina.

Funding

This study was financed by the State Forests National Forest Holding, General Directorate of the State Forests in Warsaw (Poland), as Program to Restore Resources in the Sudetes, part IV, (Project number OR.271.3.12.2017).

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Taxa occurring in the communities of fungi in the roots of fir trees, whose frequency in the collection exceeded 0.03%. The legend of colours in the "Frequency" column:

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