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 Baranowska1*, 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
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 -70оC. 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).
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
REFERENCES
Abdel-Aziz F, 2016. Two new cheirosporous asexual taxa (Dictyosporiaceae, Pleosporales, Dothideomycetes) from freshwater habitats in Egypt. Mycosphere 7(4): 448-457. https://doi.org/10.5943/mycosphere/7/4/5.
Adachi H, Doi H, Kasahara Y, Sawa R, Nakajima K, Kubota Y, Hosokawa N, Tateishi K, Nomoto A, 2015. Asteltoxins from the entomopathogenic fungus Pochonia bulbillosa 8-H-28. J Nat Prod 78: 1730-1734. https://doi.org/10.1021/np500676j.
Akhtyamova N, Sattarova RK, 2013. Endophytic Yeast Rhodotorula rubra Strain TG-1: Antagonistic and Plant Protection Activities. Biochem Physiol 2: 104. https://doi.org/10.4172/2168-9652.1000104.
Alastruey-Izquierdo A, Hoffmann K, de Hoog GS, Rodriguez-Tudela JL, Voigt K, Bibashi E, Walther G, 2010. Species Recognition and Clinical Relevance of the Zygomycetous Genus Lichtheimia (syn. Absidia Pro Parte, Mycocladus). J Clin Microbiol 48(6): 2154-2170. https://doi.org/10.1128/JCM.01744-09.
Álvarez-Baz G, Fernández-Bravo M, Pajares J, Quesada-Moraga E, 2015. Potential of native Beauveria pseudobassiana strain for biological control of pine wood nematode vector Monochamus galloprovincialis. J Invertebr Pathol 132: 48-56. https://doi.org/10.1016/j.jip.2015.08.006.
Anderson JL, Marvanová L, 2020. Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genus Tetracladium. BioRxiv preprint. https://doi.org/10.1101/2020.04.06.027920.
Badali H, Gueidan C, Najafzadeh MJ, Bonifaz A, Gerrits van den Ende AHG, de Hoog GS, 2008. Biodiversity of the genus Cladophialophora. Stud Mycol 61: 175-191. https://doi.org/10.3114/sim.2008.61.18.
Baranowska M, Kartawik N, Panka S, Behnke-Borowczyk J, Grześkowiak P, 2023. The community of soil fungi associated with the western red cedar (Thuja plicata Donn ex D. Don, 1824). Fol Forest Pol 65(1): 23-33. https://doi.org/10.2478/ffp-2023-0003.
Barzdajn W, 2000. Strategia restytucji jodły pospolitej (Abies alba Mill.) w Sudetach. Sylwan 144(2): 63-77. [in Poland with English summary].
Barzdajn W, 2012. Restytucja jodły pospolitej w Sudetach. Program działania dla sudeckich nadleśnictw Regionalnej Dyrekcji Lasów Państwowych we Wrocławiu. 1st edn. Ośrodek Rozwojowo-Wdrożeniowy Lasów Państwowych, Bedoń, Polska, 92 p. [in Poland].
Barzdajn W, Kowalkowski W, 2012. Restytucja jodły pospolitej (Abies alba Mill.) w Sudetach. For Lett 103: 7-16. [in Poland with English summary].
Behnke-Borowczyk J, Kwaśna H, 2010. Grzyby gl-bowe i ich znaczenie. Sylwan 154(12): 846-850. [in Poland with English summary].
Behnke-Borowczyk J, Kowalkowski W, Kartawik N, Baranowska M, Barzdajn W, 2020. Soil fungal communities in nurseries producing Abies alba. Balt For 26(1): 426. https://doi.org/10.46490/BF426.
Behnke-Borowczyk J, Kwaśna H, Kulawinek BJ, 2019. Fungi associated with Cyclaneusma needle cast in Scots pine in the west of Poland. Forest Pathol 49(2): e12487. https://doi.org/10.1111/efp.12487.
Benítez T, Rincón AM, Limón AM, Codónet AC, 2004. Biocontrol Mechanisms of Trichoderma Strains. Int Microbiol 7(4): 249-260.
Bis R, Dobrowolska D, 2012. Silver fir (Abies alba Mill.) occurrence in south-eastern part of Iłżecka Forest. Forest Research Papers 73(4): 1-282. https://doi.org/10.2478/v10111-012-0026-0.
Bosqueiro AS, Júnior RB, Rosa-Magri MM, 2020. Potential of Trichosporon asahii against Alternaria sp. and mechanisms of actions. Summa Phytopathol 46(1): 20-25. https://doi.org/10.1590/0100-5405/220861.
Brachaczek A, Kaczmarek J, Jedryczka M, 2016. Monitoring blackleg (Leptosphaeria spp.) ascospore release timing and quantity enables optimal fungicide application to improved oilseed rape yield and seed quality. Eur J Plant Pathol 145: 643-657. https://doi.org/10.1007/s10658-016-0922-x.
Burdekin DA, Phillips DH, 1992. Diseases of Forest and Ornamental Trees. 2nd edn. Springer, Palgrave Macmillan, London, UK, 581 p. https://doi.org/10.1007/978-1-349-10953-1.
Chen Q, Zhang K, Zhang GZ, Cai L, 2015. A polyphasic approach to characterize two novel species of Phoma (Didymellaceae) from China. Phytotaxa 197(4): 267-281. https://doi.org/10.11646/phytotaxa.197.4.4.
Chomicz-Zegar E, Niemtur S, Kapsa M, Ambroży S, 2016. Butt rot occurrence in plus trees of Silver fir Abies alba Mill. and Norway spruce Picea abies (L.) from the Carpathians. Forest Research Papers 77: 212-220. https://doi.org/10.1515/frp-2016-0023.
Coker TLR, Rozsypálek J, Edwards A, Harwood TP, Butfoy L, Buggs RJA, 2019. Estimating mortality rates of European ash (Fraxinus excelsior) under the ash dieback (Hymenoscyphus fraxineus) epidemic. Plants People Planet 1(1): 48-58. https://doi.org/10.1002/ppp3.11.
Comandini O, Pacioni G, Rinaldi AC, 2001. An assessment of belowground ectomycorrhizal diversity of Abies alba Miller in central Italy. Plant Biosyst 135(3): 337-350. https://doi.org/10.1080/11263500112331350960.
Cota LV, Maffia LA, Mizubuti ESG, Macedo PEF, 2009. Biological control by Clonostachys rosea as a key component in the integrated management of strawberry gray mold. Biol Control 50(3): 222-230. https://doi.org/10.1016/j.biocontrol.2009.04.017.
Crowther TW, Boddy L, Jones TH, 2012. Functional and ecological consequences of saprotrophic fungus-grazer interactions. ISME Journal 6(11): 1992-2001. https://doi.org/10.1038/ismej.2012.53.
Cui BK, Decock C, 2012. Phellinus castanopsidis sp. nov. (Hymenochaetaceae) from southern China, with preliminary phylogeny based on rDNA sequences. Mycol Prog 12: 341-351. https://doi.org/10.1007/s11557-012-0839-5.
Damm U, Fourie PH, Crous PW, 2010. Coniochaeta (Lecythophora), Collophora gen. nov. and Phaeomoniella species associated with wood necroses of Prunus trees. Persoonia 24: 60-80. https://doi.org/10.3767/003158510X500705.
DEEMY 2004-2020. An Information System for Characterization and DEtermination of EctoMYcorrhizae. Available online: http://www.deemy.de (19 August 2022).
Dernoeden PH, 2000. Creeping Bentgrass Management: Summer Stresses, Weeds and Selected Maladies. John Wiley & Sons, Inc., Hoboken, New Jersey, Canada, 133 p.
Desirò A, Hao Z, Liber JA, Benucci GMN, Lowry D, Roberson R, Bonito G, 2018. Mycoplasma - related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle. ISME J 12: 1743-1757. https://doi.org/10.1038/s41396-018-0053-9.
Doveri F, 2008. A bibliography of Podospora and Schizothecium, a key to the species, and a description of Podospora dasypogon newly recorded from Italy. Pagine di Micologia 29: 61-159.
Eberhardt U, Verbeken A, Rinaldi AC, Pacioni G, Comandini O, 2000. Lactarius ectomycorrhizae on Abies alba: morphological description, molecular characterization and taxonomic remarks. Mycologia 92(5): 860-873. https://doi.org/10.2307/3761582.
Farh ME, Kim YJ, Kim YJ, Yang DC, 2017. Cylindrocarpon destructans/Ilyonectria radicicola -species complex: Causative agent of ginseng root-rot disease and rusty symptoms. J Ginseng R 42(1): 9-15. https://doi.org/10.1016/j.jgr.2017.01.004.
Feng P, Klaassen CH, Meis JF, Najafzadeh MJ, Gerrits Van Den Ende AHG, Xi BL, de Hoog GS, 2013. Identification and typing of isolates of Cyphellophora and relatives by use of amplified fragment length polymorphism and rolling circle amplification. J Clin Microbiol 51(3): 931-937. https://doi.org/10.1128/JCM.02898-12.
González-Domínguez E, Armengol J, Rossi V, 2017. Biology and epidemiology of Venturia species affecting fruit crops: a review. Front Plant Sci 8: 1496. https://doi.org/10.3389/fpls.2017.01496.
Grantina-Ievina L, Kasparinskis R, Tabors G, Nikolajeva V, 2013. Features of saprophytic soil microorganism communities in conifer stands with or without Heterobasidion annosum sensu lato infection: a special emphasis on Penicillium spp. Environmental and Experimental Biology 11: 23-38.
Grantina-Ievina L, Berzina A, Nikolajeva V, Mekss P, Muiznieks I, 2014. Production of fatty acids by Mortierella and Umbelopsis species isolated from temperate climate soils. Environmental and Experimental Biology 12: 15-27.
Gramisci BR, Lutz MC, Lopes ChA, Sangorrín MP, 2018. Enhancing the efficacy of yeast biocontrol agents against postharvest pathogens through nutrient profiling and the use of other additives. Biol Control 121: 151-158. https://doi.org/10.1016/J.BIOCONTROL.2018.03.001.
Grünig CR, Duò A, Sieber TN, 2006. Population genetic analysis of Phialocephala fortinii s.l. and Acephala applanata in two undisturbed forests in Switzerland and evidence for new cryptic species. Fungal Genet Biol 43(6): 410-421. https://doi.org/10.1016/j.fgb.2006.01.007.
Gulden G, Stensrud Ø, Shalchian-Tabrizi K, Kauserud H, 2005. Galerina Earle: A polyphyletic genus in the consortium of dark-spored agarics. Mycologia 97(4): 823-837. https://doi.org/10.3852/mycologia.97.4.823.
Gumińska B, Wojewoda W, 1985. Grzyby i ich oznaczanie. Państwowe Wydawnictwo Rolnicze i Leśne. Warszawa, Poland, 506 p. [in Poland]
Hambleton S, Sigler L, 2005. Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (=Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53(1): 1-28. https://doi.org/10.3114/sim.53.1.1.
Han JG, Sung GH, Shin HD, 2014. Proliferodiscus inspersus var. magniascus and Rodwayella citrinula, two unrecorded taxa of Hyaloscyphaceae (tribe Arachnopezizeae) in Korea. Mycobiology 42(1): 86-91. https://doi.org/10.5941/MYCO.2014.42.1.86.
Hernández-Restrepo M, Gené J, Castañeda-Ruiz RF, Mena-Portales J, Crous PW, Guarro J, 2017. Phylogeny of saprobic microfungi from Southern Europe. Stud Mycol 86(1): 53-97. https://doi.org/10.1016/j.simyco.2017.05.002.
Hobbie EA, Weber NS, Trappe JM, 2001. Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence. New Phytol 150(3): 601-610. https://doi.org/10.1046/j.1469-8137.2001.00134.x.
Hustad VP, Miller AN, 2015. Maasoglossum, a basal genus in Geoglossomycetes. Mycoscience 56(6): 572-579. https://doi.org/10.1016/j.myc.2015.05.003.
Ishida TA, Nara K, Hogets T, 2007. Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174(2): 430-440. https://doi.org/10.1111/j.1469-8137.2007.02016.x.
Jankowiak R, Bilański P, Paluch J, Kołodziej Z, 2016. Fungi associated with dieback of Abies alba seedlings in naturally regenerating forest ecosystems. Fungal Ecol 24: 61-69. https://doi.org/10.1016/j.funeco.2016.08.013.
Johnson PR, 1986. Rhytismataceae in New Zealand 1. Some foliicolous species of Coccomyces de Notaris and Propolis (Fries) Corda. N Z J Bot 24(1): 89-124. https://doi.org/10.1080/0028825X.1986.10409723.
Jumpponen A, Mattson K, Trappe JM, Ohtonen R, 1998. Effects of established willows on primary succession on Lyman Glacie forefront, North Cascade Range, Washington, USA: evidence for simultaneous canopy inhibition and soil facilitation. Arctic Alpine Res 30(1): 31-39. https://doi.org/10.1080/00040851.1998.12002873.
Kaitera J, Henttonen HM, Müller MM, 2019. Fungal species associated with butt rot of mature Scots pine and Norway spruce in northern boreal forests of Northern Ostrobothnia and Kainuu in Finland. Eur J Plant Pathol 154: 541-554. https://doi.org/10.1007/s10658-019-01678-2.
Karim NFA, Mohd M, Nor NMIM, Zakaria L, 2016. Saprophytic and potentially pathogenic Fusarium species from peat soil in Perak and Pahang. Trop Life Sci Res 27(1): 1-20.
Kautmanová I, Adamčík S, Lizoň S, Jančovičová S, 2012. Revision of taxonomic concept and systematics position of some Clavariaceae species. Mycologia 104(2): 521-539. https://doi.org/10.3852/11-121.
Kirisits T, 2004. Untersuchungen über die Assoziierung von Bläuepilzen mit dem Lärchenbock (Tetropium gabrieli). Forstschutz Aktuell 32: 24-29. [in German].
Kotiranta H, Saarenoksa R, 2005. The genus Basidiodendron (Heterobasidiomycetes, Tremellales) in Finland. Ann Bot Fenn 42(1): 11-22.
Koukol O, 2011. New species of Chalara occupying coniferous needles. Fungal Divers 49(1): 75-91. https://doi.org/10.1007/s13225-011-0092-2.
Koukol O, 2012. A new species of Infundichalara from pine litter. Mycotaxon 120: 343-352. https://doi.org/10.5248/120.343.
Koukol O, 2019. Revision of root-associated microfungi of Pinus wallichiana in Kashmir Himalaya. Can J For Res 49(3): 326-329. https://doi.org/10.1139/cjfr-2018-0294.
Kowalski S, 1982. Role of mycorrhiza and soil fungi community in natural regeneration of fir (Abies alba Mill.) in Polish Carpathians and Sudetes. Eur J Plant Pathol 12(2): 107-112. https://doi.org/10.1111/J.1439-0329.1982.TB01380.X.
Kranabetter JM, Durall DM, MacKenzie WH, 2009. Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of southern boreal forest. Mycorrhiza 19: 99-111. https://doi.org/10.1007/s00572-008-0208-z.
Kryczyński S, Weber Z, 2010. Fitopatologia. Tom 1. Podstawy fitopatologii. Powszechne Wydawnictwo Rolnicze i Leśne. Poznań, Poland, 258 p. [in Poland].
Kuo M, 2012. Leotia lubrica. Retrieved from the MushroomExpert.Com Available online: http://www.mushroomexpert.com/leotia_lubrica.html (21 September 2022).
Laganà A, Agnolini C, Loppi S, Salerni E, Perini C, Barluzzi C, De Dominicis V, 2002. Periodicity, fluctuations of macrofungi in fir forests (Abies alba Mill.) in Tuscany, Italy. For Ecol Manag 169: 187-202. https://doi.org/10.1016/S0378-1127(01)00672-7.
Leal-Dutra CA, Griffith GW, Neves MA, McLaughlin EG, Clasen LA, Dentinger BTM, 2020. Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) introducing the ant-associated genus Myrmecopterula gen. nov., Phaeopterula Henn. and the corticioid Radulomycetaceae fam. nov. IMA Fungus 11(2): 1-24. https://doi.org/10.1186/s43008-019-0022-6.
Lee KK, Gloer JB, 1995. Petriellin AA Novel Antifungal Depsipeptide from the Coprophilous Fungus Petriella sordida. J Org Chem 60: 5384-5385. https://doi.org/10.1021/jo00122a010.
Łakomy P, Kwaśna H, 2008. Poradnik Leśnika. Atlas hub, Multico Oficyna Wydawnicza, Warszawa, Poland, 184 p. [in Poland].
Mańka K, 2005. Fitopatologia Leśna. Powszechne Wydawnictwo Rolnicze i Leśne Warszawa, Poland, 391 p. [in Poland].
Marcinkowska J, 2012. Oznaczanie rodzajów grzybów sensu lato ważnych w fitopatologii. Powszechne Wydawnictwo Rolnicze i Leśne, Warszawa, Poland, 508 p. [in Poland].
Martino E, Morin E, Grelet G, Kuo A, Kohler A, Daghino S, Barry K, Cichocki N, Clum A, Dockter R, Hainaut M, Kuo RC, LaButti K, Lindahl BD, Lindquist EA, Lipzen A, Khouja HR, Magnuson J, Murat C, Ohm RA, Singer SW, Spatafora JW, Wang M, Veneault‐Fourrey C, Henrissat B, Grigoriev IV, Martin FM, Perotto S, 2018. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol 217: 1213-1229. https://doi.org/10.1111/nph.14974.
Matouš J, Holec J, Koukol O, 2017. Ramariopsis robusta (Basidiomycota, Clavariaceae), a new European species similar to R. kunzei. Czech Mycol 69(1): 51-64. https://doi.org/10.33585/cmy.69104.
Matsuda Y, Hijii N, 1999. Ectomycorrhizal morphotypes of naturally grown Abies firma seedlings. Mycoscience 40(3): 217-226. https://doi.org/10.1007/BF02463958.
Matsuda Y, Hijii N, 2004. Ectomycorrhizal fungal communities in an Abies firma forest, with special reference to ectomycorrhizal associations between seedlings and mature trees. Can J Bot 82(6): 822-829. https://doi.org/10.1139/b04-065.
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M, 2015. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207(3): 505-518. https://doi.org/10.1111/nph.13363.
McGovern RJ, Horita H, Stiles CM, Seijo TE, 2006. Host range of Itersonilia perplexans and management of Itersonilia petal blight of China Aster. Plant Health Progress 7(1). https://doi.org/10.1094/PHP-2006-1018-02-RS.
Mehrabi M, Hemmati R, 2015. Two new records of Lopadostoma for mycobiota of Iran. Mycologia Iranica 2(1): 59-64. https://doi.org/10.22043/MI.2015.14225.
Münzenberger B, Bubner B, Wöllecke J, Sieber TN, Bauer R, Fladung M, Hüttl RF, 2009. The ectomycorrhizal morphotype Pinirhiza sclerotia is formed by Acephala macrosclerotiorum sp. nov., a close relative of Phialocephala fortinii. Mycorrhiza 19(7): 481-492. https://doi.org/10.1007/s00572-009-0239-0.
Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K, 2018. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47(D1): 259-264. https://doi.org/10.1093/nar/gky1022.
Noordeloos ME, 2011. Strophariaceae s.l. Fungi Europaei, Vol 13. Candusso Edizioni, Origgio, Italy, 648 p.
Oliva J, Colinas C, 2007. Decline of silver fir (Abies alba Mill.) stands in the Spanish Pyrenees: Role of management, historic dynamics and pathogens. For Ecol Manag 252(1): 84-97. https://doi.org/10.1016/j.foreco.2007.06.017.
Paz A, Bellanger J-M, Lavoise C, Molia A, Ławrynowicz M, Larsson E, Ibarguren IO, Jeppson M, Læssøe T, Sauve M, Richard F, Moreau P-A, 2017. The genus Elaphomyces (Ascomycota, Eurotiales): a ribosomal DNA-based phylogeny and revised systematics of European' deer truffles'. Persoonia 38: 197-239. https://doi.org/10.3767/003158517X697309.
Perry BA, 2002. A taxonomic investigation of Mycena in California. MS thesis, San Francisco State University, San Francisco, USA, 318 p.
Pitt JI, Samson RA, Frisvad JC, Samson RA, Pitt JI, 2000. List of accepted species and their synonyms in the family Trichocomaceae. In: Samson RA, Pitt JI (ed) Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Harwood Academic Publishers, Amsterdam Netherlands, pp 9-49.
Poelt J, Nash TH, 1993. Studies in the Umbilicaria vellea group (Umbilicariaceae) in North America. Bryologist 96(3): 422-430. https://doi.org/10.2307/3243872.
Puddu A, Luisi N, Capretti P, Santini A, 2003. Environmental factors related to damage by Heterobasidion abietinum in Abies alba forests in Southern Italy. For Ecol Manag 180: 37-44. https://doi.org/10.1016/S0378-1127(02)00607-2.
Quaedvlieg W, Verkley GJM, Shin H-D, Barreto RW, Alfenas AC, Swart WJ, Groenewald JZ, Crous PW, 2013. Sizing up Septoria. Stud Mycol 75(1): 307-390. https://doi.org/10.3114/sim0017.
Rice AV, Currah RS, 2006a. Oidiodendron maius: Saprobe in Sphagnum Peat, Mutualist in Ericaceous Roots? In: Schulz BJE, Boyle CJC, Sieber TN (ed) Microbial Root Endophytes. Soil Biology 9. Springer, Berlin, Heidelberg, Germany, pp 227-246. https://doi.org/10.1007/3-540-33526-9_13.
Rice AV, Currah RS, 2006b. Two new species of Pseudogymnoascus with Geomyces anamorphs and their phylogenetic relationship with Gymnostellatospora. Mycologia 98(2): 307-318. https://doi.org/10.3852/mycologia.98.2.307.
Richard F, Roy M, Shahin O, Sthultz Ch, Duchemin M, Joffre R, Selosse M-A, 2011. Ectomycorrhizal communities in a Mediterranean forest ecosystem dominated by Quercus ilex: seasonal dynamics and response to drought in the surface organic horizon. Ann For Sci 68(1): 57-68. https://doi.org/10.1007/s13595-010-0007-5.
Rudawska M, Pietras M, Smutek I, Strzeliński P, Leski T, 2016. Ectomycorrhizal fungal assemblages of Abies alba Mill. outside its native range in Poland. Mycorrhiza 26(1): 57-65. https://doi.org/10.1007/s00572-015-0646-3.
Sampaio JP, Gadanho M, Bauer R, Weiß M, 2003. Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiellagen. nov. and the new orders Leucosporidialesand Sporidiobolales. Mycol Prog 2(1): 53-68. https://doi.org/10.1007/s11557-006-0044-5.
Saunders CW, Scheynius A, Heitman J, 2012. Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog 8(6): e1002701. https://doi.org/10.1371/journal.ppat.1002701.
Schirkonyer U, Bauer Ch, Rothe GM, 2013. Ectomycorrhizal diversity at five different tree species in forests of the Taunus Mountains in Central Germany. Open J Ecol 3(1): 66-81. https://doi.org/10.4236/oje.2013.31009.
Schmidt P-A, Bálint M, Greshake B, Bandow C, Römbke J, Schmitt I, 2013. Illumina metabarcoding of a soil fungal community. Soil Biol Biochem 65: 128-132. https://doi.org/10.1016/j.soilbio.2013.05.014.
Sepúlveda-Chavera G, Salvatierra-Martínez R, Andía-Guardia R, 2013. The alternative control of powdery mildew complex (Leveillula Taurica and Erysiphe sp.) in tomato in the Azapa Valley, Chile. Cienc Inv Agr 40(1): 119-130. https://doi.org/10.4067/S0718-16202013000100010.
Shen M, Zhang JQ, Zhao LL, Groenewald JZ, Crous PW, Zhang Y, 2020. Venturiales. Stud Mycol 96: 185-308. https://doi.org/10.1016/j.simyco.2020.03.001.
Six DL, Bentz BJ, 2003. Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can J For Res 33(9): 1815-1820. https://doi.org/10.1139/x03-107.
Smutek I, Rudawska M, Leski T, 2010. Ektomikoryzy - ukryty potencjał w badaniach mikobioty drzew leśnych na przykładzie drzewostanów jodłowych. Available online: https://czlowiekiprzyroda.eu/wp-content/uploads/2017/07/74.pdf (13 September 2022)
Spatafora JW, Owensby CA, Douhan GW, Boehm EW, Schoch CL, 2012. Phylogenetic placement of the ectomycorrhizal genus Cenococcum in Gloniaceae (Dothideomycetes). Mycologia 104(3): 758-765. https://doi.org/10.3852/11-233.
Springer DJ, Mohan R, Heitman J, 2017. Plants promote mating and dispersal of the human pathogenic fungus Cryptococcus. PloS One 12(2): e0171695. https://doi.org/10.1371/journal.pone.0171695.
Stielow B, Bratek Z, Orczán AKI, Rudnoy Sz, Hensel G, Hoffmann P, Klenk H-P, Göker M, 2011. Species delimitation in taxonomically difficult fungi: the case of Hymenogaster. PLoS One 6(1): e15614. https://doi.org/10.1371/journal.pone.0015614.
Stroheker S, Dubach V, Vögtli I, Sieber TN, 2021. Investigating host preference of root endophytes of three european tree species, with a focus on members of the Phialocephala fortinii-Acephala applanata species complex (PAC). J Fungi 7(4): 317. https://doi.org/10.3390/jof7040317.
Šutara J, 2008. Xerocomus s.l. in the light of the present state of knowledge. Czech Mycol 60(1): 29-62. https://doi.org/10.33585/CMY.60104.
Tedersoo L, May TW, Smith ME, 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-263. https://doi.org/10.1007/s00572-009-0274-x.
Unuk T, Martinović T, Finžgar D, Šibanc N, Grebenc T, Kraigher H, 2019. Root-Associated fungal communities from two phenologically contrasting Silver fir (Abies alba Mill.) Groups of Trees. Front Plant Sci 10: 214. https://doi.org/10.3389/fpls.2019.00214.
UNITE community 2020. rDNA ITS based identification of Eukaryotes and their communication via DOIs. Current version: 8.2. Available online: https://unite.ut.ee (12 April 2022).
Vilgalys R, Gonzalez D, 1990. Organization of ribosomal DNA in the basidiomycete Thanatephorus praticola. Curr Genet 18: 277-280. https://doi.org/10.1007/BF00318394.
Vanegas-León ML, Sulzbacher MA, Rinaldi AC, Roy M, Selosse M-A, Neves MA, 2019. Are Trechisporales ectomycorrhizal or non-mycorrhizal root endophytes? Mycol Prog 18(9): 1231-1240. https://doi.org/10.1007/s11557-019-01519-w.
Wang CJK, Zabel RA, 1990. Identification Manual for Fungi from Utility Poles in the Eastern United States. American Type Culture Collec, 356 p.
Warcup JH, 1990. Taxonomy, culture and mycorrhizal associations of some zygosporic Endogonaceae. Mycol Res 94(2): 173-178. https://doi.org/10.1016/S0953-7562(09)80609-6.
Ważny R, 2014. Ectomycorrhizal communities associated with silver fir seedlings (Abies alba Mill.) differ largely in mature silver fir stands and in Scots pine fore crops. Ann For Sci 71: 801-810. https://doi.org/10.1007/s13595-014-0378-0.
Wilson IM, 1951. Notes on some Marine Fungi. T Brit Mycol Soc 34(4): 540-543. https://doi.org/10.1016/S0007-1536(51)80039-1.
Wojewoda W, 2003. Checklist of Polish Larger Basidiomycetes. Biodiversity of Poland. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, Poland, 812 p.
Yakti W, Kovács GM, Franken P, 2019. Differential interaction of the dark septate endophyte Cadophora sp. and fungal pathogens in vitro and in planta. Microbiol Ecol 95(12): fiz164. https://doi.org/10.1093/femsec/fiz164.
Yang BY, 1962. Basidiobolus meristosporus of Taiwan. Taiwania 8: 17-27.
Yurkov AM., Kurtzman CP, 2019. Three new species of Tremellomycetes isolated from maize and northern wild rice. FEMS Yeast Research 19(2): foz004: https://doi.org/10.1093/femsyr/foz004.
Zettur I, Kullman B, 2011. Urnula hiemalis - a rare and interesting species of the Pezizales from Estonia. Folia Cryptog Estonica Fasc 48: 149-152.
© 2023 by the Croatian Forest Research Institute. This is an Open Access paper distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0).