Next Article in Journal
Changing Times at Cuban Universities: Looking into the Transition towards a Social, Entrepreneurial and Innovative Organization
Next Article in Special Issue
Diversity and Distribution Patterns of Endolichenic Fungi in Jeju Island, South Korea
Previous Article in Journal
Changes in Vegetation Growth Dynamics and Relations with Climate in Inner Mongolia under More Strict Multiple Pre-Processing (2000–2018)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 12
Issue 6
10.3390/su12062535
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Investigating Wood Decaying Fungi Diversity in Central Siberia, Russia Using ITS Sequence Analysis and Interaction with Host Trees

by
Ji-Hyun Park
1,
Igor N. Pavlov
2,3,
Min-Ji Kim
4,
Myung Soo Park
1,
Seung-Yoon Oh
5,
Ki Hyeong Park
1,
Jonathan J. Fong
6 and
Young Woon Lim
1,*
1
School of Biological Sciences and Institute of Microbiology, Seoul National University, Seoul 08826, Korea
2
Laboratory of Reforestation, Mycology and Plant Pathology, V. N. Sukachev Institute of Forest, Siberian Branch of Russian Academy of Sciences, 660036 Krasnoyarsk, Russia
3
Department of Chemical Technology of Wood and Biotechnology, Reshetnev Siberian State University of Science and Technology, 660049 Krasnoyarsk, Russia
4
Wood Utilization Division, Forest Products Department, National Institute of Forest Science, Seoul 02455, Korea
5
Department of Biology and Chemistry, Changwon National University, Changwon 51140, Korea
6
Science Unit, Lingnan University, Tuen Mun, Hong Kong
*
Author to whom correspondence should be addressed.
Sustainability 2020, 12(6), 2535; https://doi.org/10.3390/su12062535
Submission received: 27 February 2020 / Revised: 18 March 2020 / Accepted: 18 March 2020 / Published: 24 March 2020
(This article belongs to the Special Issue Fungal Diversity and Sustainability)
Browse Figures
Review Reports Versions Notes

Abstract

:
Wood-decay fungi (WDF) play a significant role in recycling nutrients, using enzymatic and mechanical processes to degrade wood. Designated as a biodiversity hot spot, Central Siberia is a geographically important region for understanding the spatial distribution and the evolutionary processes shaping biodiversity. There have been several studies of WDF diversity in Central Siberia, but identification of species was based on morphological characteristics, lacking detailed descriptions and molecular data. Thus, the aim of this study was to identify WDF in Central Siberia, regarding the degradation of host trees based on both morphological and molecular analyses. We collected 106 WDF samples from Krasnoyarsk and the Republic of Khakassia in 2014 and 2017, and identified a total of 52 fungal species from six main host tree genera. In order to assess the host preference of the WDF, we examined previous literature, and data from this study. We confirmed a division in host preference of WDF between gymnosperms and angiosperms. DNA-based identification and host preference assessment of the WDF provide preliminary data on WDF diversity and their role in nutrient cycles in the ecosystem of Central Siberia. To fully understand WDF diversity in Central Siberia, continuous long-term surveys, including DNA sequence data, are needed.

1. Introduction

Wood-decay fungi (WDF) decompose dead wood or attack living trees as a pathogen. Wood decomposition is a crucial biological process that breaks down complex molecules and recycles nutrients back to the soil [1,2]. Through the wood decay cycle, young trees grow and replace dead or decaying trees. As such, WDF are excellent ecosystem engineers that play a pivotal role in recycling nutrients in a forest ecosystem, and in providing a viable habitat for many other organisms [3,4].
Although WDF are not part of a natural taxonomic group, they form a number of well-defined groups within Ascomycota and Basidiomycota [5,6]. The majority of WDF typically form a fruitbody and belong to the class Agaricomycetes in Basidiomycota. Polypore decay fungi also form a polyphyletic group, with representatives in the orders Hymenochaetales, Polyporales, and Gloeophyllales. Gilled pleurotoid and corticoid decay fungi also form polyphyletic groups with representatives in orders Hymenochaetales, Corticiales, and Russulales [7,8]. WDF degrade wood using both enzymatic and mechanical processes, and based on the type of decay of the wood lingo-cellulose material, WDF fall into two groups: brown-rot fungi and white-rot fungi [3].
Russia, the largest country in the world, has a variety of environments and landforms such as arctic tundra, forest tundra, taiga, mixed and deciduous forests, broad-leaved forests, steppes, semi-deserts, and subtropics [9]. There are three biodiversity hotspots in Russia; the North Caucasus, South Siberia, and the Far East [10]. Recently, biologists from various backgrounds have shown a great interest in Central Siberia as a biodiversity hot spot [11,12]. As a geographic link between Europe and Asia, Central Siberia is an important region for understanding the spatial distribution and the evolutionary processes of a diversity of organisms, including WDF. WDF have been well-surveyed in the Western and Northern Siberian Plains [13,14,15,16], the Ural Mountains [17,18], the Altai-Sayan Mountains [19], and in several islands and peninsulas [20,21], but there is limited information from Central Siberia. Recent studies in Central Siberia consist of reports of WDF and their corresponding hosts without detailed descriptions or molecular data [15,22,23]
As many WDF produce a relatively rigid fruiting body, they are often identified based on morphological characteristics such as pileus color, pore size, basidiospore shape, cystidia shape, hyphal system, and type of rot [24,25]. However, species identification based on morphology alone has been shown to be inaccurate, due to morphological similarities and the tendency of morphological characters to undergo convergent evolution [26,27]. With an increase in available sequence data in public databases, sequence-based identification has become prevalent [28,29,30]. Sequence-based identification enables taxonomists to distinguish morphologically similar organisms, and to identify fruiting bodies that have no unique characteristics, are premature, or are fragmented in pieces. The internal transcribed spacer (ITS) region has been widely used as the primary fungal barcode [31] for sequence-based identification of fungi.
The majority of WDF are considered to have a broad range of hosts, but some species show close affinity and preference for specific host trees [32,33]. Investigating host preference is helpful in understanding the ecology of a particular area, because WDF contribute to the nutrient cycle by breaking down the host tree. The main objective of this study was to survey WDF in Central Siberia involved in the degradation of host tree species and identify them to species, based on their morphology and ITS sequence analysis. To investigate the major wood decayers in this area, we evaluated the WDF species lists from previous literature, along with the data from this study.

2. Materials and Methods

2.1. Sampling Sites and Determining the Major Wood-Decaying Fungi

Wood-decay fungi were collected in Central Siberia: three sites near Krasnoyarsk in September 2014, and four sites at the Republic of Khakassia in August 2017 (Figure 1). A total of 106 fruiting bodies of WDF were sampled from six plant species: Abies sibirica (29 fruiting bodies), Betula pendula (59), Larix siberia (6), Pinus sylvestris (5), Populus tremula (3), and Salix alba var. sericea (4). All samples were dried in air-vented ovens at 55 °C for 3–4 days, then deposited at the Seoul National University Fungus Collection (SFC).
To investigate the major wood-decaying fungi in Central Siberia, we combined our data and the WDF lists from previous literature [15,22,23]. We investigated whether WDF species are host tree specific by categorizing species at the genus level of the host trees, focusing on the six main genera (Abies, Betula, Larix, Pinus, Populus, and Salix).

2.2. Morphological and Molecular Approaches to WDF Identification

The specimens were initially identified based on their macro- and micromorphological characters. For the microscopic structure observation, dried tissues were rehydrated in 3% (w/v) KOH, stained in 1% (w/v) phloxine and Melzer’s reagent (IKI), and then observed using a Nikon Eclipse 80i optical microscope (Nikon, Tokyo, Japan). Fungal nomenclature was based on the current information on Index Fungorum [34] to reflect the legitimate name.
Genomic DNA was extracted from the inner tissues of the fruiting body using a modified CTAB extraction protocol [35]. The ITS region was amplified using the primer set ITS1F/ITS4 [36]. PCR was performed in a C1000 thermal cycler (Bio-Rad, Richmond, CA, USA) using the Maxime PCR PreMix-StarTaq (Intron Biotechnology Inc., Seoul, Korea). The PCR conditions were slightly modified from the previously described method [37]: 95 °C for 5 min, followed by 35 cycles of 95 °C for 40 s, 55 °C for 40 s, and 72 °C for 1 min, and a final extension step at 72 °C for 10 min. The PCR products were electrophoresed on 1% agarose gel and purified for sequencing using the ExpinTM PCR Purification Kit (GeneAll Biotechnology, Seoul, Korea), according to the manufacturer’s instructions. DNA sequencing was performed in both forward and reverse directions using the PCR primers at Macrogen (Seoul, Korea), using an ABI Prism 3700 genetic analyzer (Life Technologies, Gaithersburg, MD). Sequences were assembled and proofread using MEGA 6 [38]. All consensus sequences were matched with a reference sequence using BLAST in the NCBI GenBank database.

3. Results

3.1. WDF Identification

WDF with obvious and distinct morphological characters were identified on the spot during the collection. In deciduous forests, identification of the following species was possible: Cerrena unicolor, Daedaleopsis tricolor, Fomes fomentarius, Fomitopsis betulina, Fomitopsis pinicola, Ganoderma applanatum, Innotus obliquus, Irpex lacteus, Phlebia tremellosa, Plicaturopsis crispa, Stereum subtomentosum, Trametes hirsuta, Trametes versicolor, and Trichaptum biforme. Species often found and identified in coniferous forests were as follows: Fomitopsis pinicola, Hymenochaete cruenta, Rhodofomes cajanderi, and Trichaptum abietinum. The remaining specimens could not be identified to the species-level based only on their macro- and micromorphologies, so they were identified based on the sequence analysis of the ITS region.
Based on the sequence analysis, the 106 WDF samples were identified to 52 species (Table 1). All BLAST searches, with two exceptions, showed over 98% similarity to the respective reference species. The two exceptions are as follows: SFC20170809-03 matched to Ph. igniarius with 96% similarity, and SFC20140922-07 matched to Postia sp. 3 with 96.7% similarity. Although 96% similarity is relatively low to distinguish a fungus at the species level, microscopic features of SFC20170809-03 corresponded to Ph. igniarius, the species identified in BLAST. Specimen SFC20140922-07 remained identified as Postia sp. due to an inconclusive morphological discrimination. Of the 52 species, 27 species were previously unrecorded from Central Siberia.

3.2. Host Preference

In our research area, Abies sibirica and Betula pendula were the dominant host species, and most WDF were collected from these two species. Eighteen WDF species were collected from A. sibirica and 26 species were collected from B. pendula, while only two to four species were identified from each of the other four host plants (Table 1). A total of 23 WDF species were found on gymnosperms, with Fomitopsis pinicola, Phaeolus schweinitzii, and Trichaptum abietinum being the most commonly found species. F. pinicola and Pha. schweinitzii commonly occurred on both A. sibirica and Pin. sylvestris. In contrast, 30 WDF species were found on angiosperms. The dominant species collected were Fomes fomentarius, Fomitopsis betulinus, Ganoderma applanatum, Inonotus obliquus, Trametes versicolor, and Trichaptum biforme. Major species found on each host genus are represented in Figure 2.
To evaluate the host specificity, the records of WDF and their corresponding hosts from the previous literature (271 species), and the data from this study (52 species), were analyzed together (Figure 3a). A total of 130 WDF specifically grew on angiosperms, 143 on gymnosperms, and 20 grew on both (Figure 3b). There were no WDF species detected across all host plant species. Host preference of WDF was stronger on gymnosperms than on angiosperm trees; not many WDF found on a coniferous tree were found on other host genera. Fomitopsis pinicola and Trichaptum abietinum were the only species commonly found across all three genera of the gymnosperm (Figure 3c). On the other hand, a higher number of WDF species were found on two or more hosts among the deciduous tree genera. The following 11 WDF were confirmed to be involved in the decomposition of all angiosperms: Bjerkandera adusta, Cerrena unicolor, Fomes fomentarius, Ganoderma applanatum, Gloeoporus dichrous, Irex lacteus, Polyporus leptocephalus, Schizophyllum commune, Scopuloides rimosa, Trametes hirsuta, and Tra. versicolor (Figure 3d). The list of fungal species for each host plant is provided (See Supplementary Table S1).

4. Discussion

We identified 52 WDF species from six main host genera (Abies, Betula, Larix, Pinus, Populus, and Salix) located in Central Siberia [22,39]. Despite the large number of WDF reported from Central Siberia, very few have available sequence data. As the majority of WDF are macrofungi, many can be identified based on their morphological characters. However, some macrofungi can be difficult to identify when they are collected in an immature state or do not have distinguishing morphological characteristics. In addition, depending on the environment, the shape of many macrofungi within the same species can be different [37,40]. Thus, sequence-based identification can be an alternative approach for distinguishing morphologically similar species and reducing the rate of misidentification.
The community of WDF species collected from Central Siberia was largely consistent with those from all around the world. The reference ITS sequences used for identification were of specimens from Europe, North America, and East Asia (South Korea, China, and Japan), and a limited number from Russia. Considering the number of WDFs reported from Central Siberia, sequence information available from the public database is low (Table S1). A total of 25 WDF species matched with species that were described in previous records with only morphological characters [15,22,23], while 27 WDF species were identified as new records to Central Siberia. However, when looking at the identified species in several genera, our results differed from previous studies. Such discrepancy may be true differences based on different sampling sites or artifacts of misidentification. For example, Phellinus species are difficult to identify morphologically to the species level, and sequence data can be useful to confirm their identity to determine why there is a discrepancy. In addition, the provision of sequence data from this area is necessary to study the population genetics and phylogeography of these species.
There have been many studies focusing on host preference or host specialization of WDF to evaluate the distribution and the ecological impacts of plant-related fungi [41,42]. Since fungal host preference can affect spreading and population dynamics [33,43,44], understanding this aspect is important for studying the biological diversity of an ecosystem. Generally, WDF prefer either gymnosperm or angiosperm hosts [45], and this phenomenon has also been observed in Central Siberia. Brown-rot fungi were mainly found on gymnosperms, while most white-rot fungi were found on angiosperm, in accordance with previous studies [42,46]. Brown-rot fungi have an apparent preference for gymnosperm substrates and favor colder climates for survival and propagation [2]. Correspondingly, members of Antrodia, Gloeophyllum, and Postia likely play pivotal roles in degrading the Central Siberian coniferous forests. Heterobasidion annosum and Phaeolus schweinitzii are two well-known conifer pathogens [47,48] that might threaten the coniferous forests of Central Siberia. However, many other species found in this area are also known worldwide to cause a decay in gymnosperms [49,50,51,52], including Dichomitus squalens, Stereum sanguinolentum, Trichaptum abietinum, Trichaptum fuscoviolaceum, Tubulicrinis calothrix, and Tubulicrinis subulatus (Table 1; Table S1). For white-rot fungi, several species were exclusively found on angiosperms: Bjerkandera adusta, Cerrena unicolar, Fomes fomentarius, Irpex lacteus, Trametes hirsuta, and Tra. versicolor. These species are known to inhabit angiosperm branches and trunks [49,50].
Although Trichaptum abietinum is known as a powerful white-rotter, it was detected mostly on gymnosperms in this study (Table 1). This species overwhelmingly preferred gymnosperms and acted as a pine indicator species, growing on Picea, Pinus, and Abies [53]. In the case of Rhodofomes cajanderi, as reported to occur commonly on dead coniferous wood [54], it was frequently observed growing on a conifer, Larix siberia. However, for Hapalopilus rutilans, known to grow on most deciduous woods [55], it instead preferred to the host genus Abies in Siberia.
Three species frequently found in this survey (Fomitopsis betulina, Inonotus obliquus, and Phellinus laevigatus; Figure 2i–l) exhibited strong specialization on the host genus Betula. In support of this observation, the same results were found in previous studies in Central Siberia (Table S1). The generic name of Fomitopsis betulina was recently transferred from Piptoporus betulinus, based on its morphological characters and multi-gene analyses [56]. Tsuneda and Kennedy [57] confirmed that Piptoporus betulinus (current name Fomitopsis betulina) occurred only on Betula species as a typical host-specific fungus. For Fomes fomentarius and Stereum subtomentosum, which have been reported to occur on various hardwoods [51,52], Betula seems to be preferred in Central Siberia.
Fomitiporia punctate and Phellinus igniarius (Figure 2o,p) were frequently found on Salix in this region. Fomitiporia punctate, known as a harmful plant pathogen in regions growing Mediterranean vine, has been recorded as parasites of Salix, Sorbus, and Vitis in Europe and the USA [58]. Phellinus igniarius is also known to grow on Salix in Europe [59]. Apart from sharing the same host, Fomitiporia punctate and Phellinus laevigatus also have superficially similar morphology. The former, however, does not have setae and strongly dextrinoid and cyanophilous basidiospores [60], which distinguishes it from the latter.
In conclusion, WDF have been widely studied to monitor and assess biodiversity in forests [61]. It is known that a fruiting body of WDF is a better indicator compared to a non-fruiting mycelia, in that it reflects population persistence as a life-history stage [32]. Thus, our DNA-based identification of host preference of WDF in Central Siberia provides a good basis to further study the spatial distribution and the evolutionary process of WDF in Europe and Asia, and to understand the nutrient cycle in ecosystems. With that, a persistent long-term ecological investigation and survey of WDF in Central Siberia based on molecular data is necessary.

Supplementary Materials

The following are available online at https://www.mdpi.com/2071-1050/12/6/2535/s1, Table S1: The list of WDF from six main host tree genera in previous literature and current study.

Author Contributions

Conceptualization: Y.W.L. and I.N.P.; methodology: M.S.P. and S.-Y.O.; formal analysis: M.S.P. and S.-Y.O.; investigation: Y.W.L. and I.N.P.; writing–original draft preparation: J.-H.P., M.-J.K., Y.W.L.; writing–review and editing: J.-H.P., J.J.F., Y.W.L.; visualization: K.H.P.; supervision: Y.W.L.; funding acquisition: Y.W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the project on Korea Basidiomycota Resources Center of the National Research Foundation (NRF) funded by the Korean government, grant number NRF2015M3A9B8029237.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Harley, J.L. Fungi in ecosystems. J. Ecol. 1971, 59, 653–668. [Google Scholar] [CrossRef]
  2. Gilbertson, R.L. Wood-rotting fungi of North America. Mycologia 1980, 72, 1–49. [Google Scholar] [CrossRef]
  3. Deacon, J. Fungal Biology, 4th ed.; Wiley-Blackwell Publishing: Hoboken, NJ, USA, 2005; p. 384. ISBN 978-140-513-066-0. [Google Scholar]
  4. Lonsdale, D.; Pautasso, M.; Holdenrieder, O. Wood-decaying fungi in the forest: Conservation needs and management options. Eur. J. For. Res. 2008, 127, 1–22. [Google Scholar] [CrossRef]
  5. Ryvarden, L.; Johansen, I. A Preliminary Polypore Flora of East Africa; Fungiflora: Oslo, Norway, 1980; p. 636. ISBN 978-094-534-514-5. [Google Scholar]
  6. Lundell, T.K.; Mäkelä, M.R.; de Vries, R.P.; Hildén, K.S. Genomic, lifestyles and future prospects of wood-decay and litter-decomposing Basidiomycota. Adv. Bot. Res. 2014, 70, 329–370. [Google Scholar] [CrossRef] [Green Version]
  7. Miller, S.L.; McClean, T.M.; Walker, J.F.; Buyck, B.A. Molecular phylogeny of the Russulales including agaricoid, gasteroid and pleurotoid taxa. Mycologia 2001, 93, 344–354. [Google Scholar] [CrossRef]
  8. Wagner, T.; Fischer, M. Classification and phylogenetic relationships of Hymenochaete and allied genera of the Hymenochaetales, inferred from rDNA sequence data and nuclear behavior of vegetation mycelium. Mycol. Prog. 2002, 1, 93–104. [Google Scholar] [CrossRef]
  9. Mukhortova, L.; Schepaschenko, D.; Shvidenko, A.; McCallumm, I.; Kraxner, F. Soil contribution to carbon budget of Russian forests. Agric. For. Meteorol. 2015, 200, 97–108. [Google Scholar] [CrossRef] [Green Version]
  10. Venevsky, S.; Venevskaia, I. Hierarchical systematic conservation planning at the national level: Identifying national biodiversity hotspots using abiotic factors in Russia. Biol. Conserv. 2005, 124, 235–251. [Google Scholar] [CrossRef]
  11. Kamp, J.; Reinhard, A.; Frenzel, M.; Kämpfer, S.; Trappe, J.; Hölzel, N. Farmland bird responses to land abandonment in Western Siberia. Agric. Ecosyst. Environ. 2018, 268, 61–69. [Google Scholar] [CrossRef]
  12. Wu, C.; Wang, M.; Lu, C.; Venevsky, S.; Sorokina, V.; Kulygin, V.; Berdnikov, S. Climate-induced fire regimes in the Russian biodiversity hotspots. Glob. Ecol. Conserv. 2018, 16, e00495. [Google Scholar] [CrossRef]
  13. Mukhin, V.A.; Kotiranta, H. Wood-decaying fungi of northernmost forests in river Khatanga basin. Mikologiâ i Fitopatologiâ 2001, 35, 41–47. [Google Scholar]
  14. Ezhov, O.N.; Zmitrovich, I.V. Checklist of aphyllophoroid fungi (Agaricomycetes, Basidiomycota) in boreal forests of Pinega Reserve, north-east European Russia. Check List 2015, 11, 1495. [Google Scholar] [CrossRef]
  15. Kotiranta, H.; Shiryaev, A.G.; Spirin, V. Aphyllophoroid fungi (Basidiomycota) of Tuva Republic, Southern Siberia, Russia. Folia Cryptogam. Est. 2016, 53, 51–64. [Google Scholar] [CrossRef] [Green Version]
  16. Ezhov, O.; Zmitrovich, I.; Ruokolainen, A. Checklist of aphyllophoroid fungi (Agaricomycetes, Basidiomycota) in boreal forests of the Solovetsky Archipelago (Arkhangelsk Region, European Russia). Check List 2017, 13, 789–803. [Google Scholar] [CrossRef]
  17. Kotiranta, H.; Mukhin, V.A.; Ushakova, N.; Dai, Y.C. Polypore (Aphyllophorales, Basidiomycetes) studies in Russia 1. South Ural. Ann. Bot. Fenn. 2005, 42, 427–451. [Google Scholar]
  18. Kotiranta, H.; Ushakova, N.; Mukhin, V.A. Polypore (Aphyllophorales, Basidiomycetes) studies in Russia. 2. Central Ural. Ann. Bot. Fenn. 2007, 44, 103–127. [Google Scholar]
  19. Kotiranta, H.; Mukhin, V.A. Aphyllophorales (Basidiomycetes) of Tiksi, Republik of Sakha (Yakutia), Northeast Siberia. Karstenia 2000, 40, 65–69. [Google Scholar] [CrossRef]
  20. Parmasto, E. On the fungus-flora of kamtchatka. Issled. Prir. Daln. Vost. 1963, 1, 221–289. [Google Scholar]
  21. Kotiranta, H.; Mukhin, V.A. Polyporaceae and Corticiaceae of an isolated forest of Abies nephrolepis in Kamchatka, Russian Far East. Karstenia 1998, 38, 69–80. [Google Scholar] [CrossRef] [Green Version]
  22. Kotiranta, H.; Shiryaev, A.G. Aphyllophoroid fungi (Basidiomycota) in Tunguska River basin, central East Siberia, Russia. Karstenia 2016, 55, 25–42. [Google Scholar] [CrossRef] [Green Version]
  23. Shiryaev, A.G.; Kotiranta, H. Aphyllophoroid fungi (Basidiomycota) of the middle part of Yenisei River basin, East Siberia, Russia. Karstenia 2016, 55, 43–60. [Google Scholar] [CrossRef] [Green Version]
  24. Jülich, W. Notes on Subulicystidium longisporum (Pat.) Parm. Int. J. Mycol. Lichenol. 1984, 1, 281–282. [Google Scholar]
  25. Ryvarden, L.; Gilbertson, R.L. European polypores vol. 1. In Synopsis Fungorum; Fungiflora: Oslo, Norway, 1993; Volume 6, pp. 1–387. [Google Scholar]
  26. Hansen, L.; Knudsen, H. Nordic Macromycetes. Vol. 3: Heterobasidioid, Aphyllophoroid and Gastromycetoid Basidiomycetes; Nordsvamp: Copenhagen, Denmark, 1997; p. 444. ISBN 978-879-839-611-6. [Google Scholar]
  27. Yang, Z.H.; Rannala, B. Bayesian species delimitation using multilocus sequence data. Proc. Natl. Acad. Sci. USA 2010, 107, 9264–9269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Hebert, P.D.N.; Cywinska, A.; Ball, S.L.; de Waard, J.R. Biological identification through DNA barcodes. Proc. Biol. Sci. 2003, 270, 313–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Herr, J.R.; Öpik, M.; Hibbett, D. Towards the unification of sequenced-based classification and sequenced-based identification of host-associated microorganisms. New Phytol. 2015, 205, 27–31. [Google Scholar] [CrossRef] [PubMed]
  30. Hibbert, D.; Abarenkov, K.; Kõljalg, U.; Öpik, M.; Chai, B.; Cole, J.; Wang, Q.; Crous, P.; Robert, V.; Helgason, T.; et al. Sequence-based classification and identification of Fungi. Mycologia 2016, 108, 1049–1068. [Google Scholar] [CrossRef]
  31. Schoch, C.L.; Seifert, K.A.; Huhndorf, S.; Robert, V.; Spouge, J.L.; Levesque, C.A.; Chen, W.; Fungal Barcoding Consortium. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. USA 2012, 9, 6241–6246. [Google Scholar] [CrossRef] [Green Version]
  32. Yamashita, S.; Hattori, T.; Abe, H. Host preference and species richness of wood-inhabiting aphyllophoraceous fungi in a cool temperature area of Japan. Mycologia 2012, 102, 11–19. [Google Scholar] [CrossRef]
  33. Nogueria-Melo, G.; Santos, P.J.; Gibertoni, T.B. Host-exclusivity and host-recurrence by wood decay fungi (Basidiomycota-Agaricomycetes) in Brazilian mangroves. Acta Bot. Bras. 2017, 31, 556–570. [Google Scholar] [CrossRef] [Green Version]
  34. Index Fungorum. Available online: www.indexfungorum.org (accessed on 27 February 2020).
  35. Rogers, S.O.; Bendich, A.J. Extraction of total cellular DNA from plants, algae and fungi. In Plant Molecular Biology Manual; Gelvin, S.B., Schilperoort, R.A., Eds.; Springer: Dordrecht, The Netherlands, 1994; pp. 183–190. [Google Scholar]
  36. White, T.J.; Bruns, T.; Lee, S.; Taylor, J.L. Amplification and direct sequencing of fungal ribosomal RNAgenes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Academic Press: New York, NY, USA, 1990. [Google Scholar]
  37. Park, M.S.; Quan, Y.; Jung, P.E.; Oh, S.; Jang, Y.S.; Kim, J.; Lim, Y.W. Re-evaluation of the Genus Antrodia (Polyporales, Basidiomycota) in Korea. Mycobiology 2014, 42, 114–119. [Google Scholar] [CrossRef] [Green Version]
  38. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30, 2725–2729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Czerepanov, S.K. Vascular Plants of Russia and Adjacent States (The Former USSR); Cambridge University Press: Cambridge, UK, 2007; p. 532. ISBN 978-052-145-006-5. [Google Scholar]
  40. Grand, E.A.; Hughes, K.W.; Petersen, R.H. Relationships within Lentinus subg. Lentinus (Polyporales, Agaricomycetes), with emphasis on sects. Lentinus and Tigrini. Mycol. Prog. 2011, 10, 399–413. [Google Scholar] [CrossRef]
  41. Gilbert, G.S.; Gorospe, J.; Ryvarden, L. Host and habitat preferences of polypore fungi Micronesian tropical flooded forests. Mycol. Res. 2008, 112, 674–680. [Google Scholar] [CrossRef] [PubMed]
  42. Krah, F.; Bässler, C.; Heibl, C.; Soghigian, J.; Schaefer, H.; Hibbet, D.S. Evolutionary dynamics of host specialization in wood-decay fungi. BMC Evol. Biol. 2018, 18, 119. [Google Scholar] [CrossRef] [Green Version]
  43. Gilbert, G.S. Evolutionary ecology of plant diseases in natural ecosystems. Annu. Rev. Phytopathol. 2002, 40, 13–43. [Google Scholar] [CrossRef] [Green Version]
  44. Hattori, T.; Yamashita, S.; Lee, S.U. Diversity and conservation of wood-inhabiting polylores and other aphyllophoraceous fungi in Malaysia. Biodivers. Conserv. 2012, 21, 2375–2396. [Google Scholar] [CrossRef]
  45. Tuor, U.; Winterhalter, K.; Fiechter, A. Enzymes of white-rot fungi involved in lignin degradation and ecological determinants for wood decay. J. Biotechnol. 1995, 41, 1–17. [Google Scholar] [CrossRef]
  46. Rypacek, V. Chemical composition of hemicelluloses as a factor participating in the substrate specificity of wood-destroying fungi. Wood Sci. Technol. 1977, 11, 59–67. [Google Scholar] [CrossRef]
  47. Simpson, J.A.; May, T.W. Phaeolus schweinitzii in Australia. Australas. Plant Pathol. 2002, 31, 99–100. [Google Scholar] [CrossRef]
  48. Asiegbu, F.O.; Adomas, A.; Stenlid, J. Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. sl. Mol. Plant Pathol. 2005, 6, 395–409. [Google Scholar] [CrossRef]
  49. Breitenbach, J.; Kränzlin, F. Fungi of Switzerland, Vol. 2; Verlag Mykologia: Lucerne, Swizerland, 1986; p. 412. ISBN 978-385-604-220-2. [Google Scholar]
  50. Gilbertson, R.L.; Ryvarden, L. North American Polypores 1; Fungiflora: Oslo, Norway, 1986; p. 443. ISBN 978-094-564-506-0. [Google Scholar]
  51. Dai, Y.C.; Wei, Y.L.; Zhang, X.Q. An annotated checklist of non-poroid Aphyllophorales in China. Ann. Bot. Fenn. 2004, 41, 233–247. [Google Scholar]
  52. Dai, Y.C. Polypore diversity in China with an annotated checklist of Chinese polypores. Mycoscience 2012, 53, 49–80. [Google Scholar] [CrossRef]
  53. O’Hanlon, R.; Harrington, T.J. Macrofungal diversity and ecology in four Irish forest types. Fungal Ecol. 2012, 5, 449–508. [Google Scholar] [CrossRef]
  54. Carranza-Morse, J.; Gilbertson, R.L. Cultural studies on the Fomitopsis rosea complex. Mycologia 1989, 81, 85–97. [Google Scholar] [CrossRef]
  55. Murrill, W.A. The polyporaceae of North America-VIII. Hapalopilus, Pycnoporus, and new monotypic genera. Bull. Torrey Bot. Club 1904, 31, 145–428. [Google Scholar]
  56. Han, M.L.; Chen, Y.Y.; Shen, L.L.; Song, J.; Vlasák, J.; Dai, Y.; Cui, B. Taxonomy and phylogeny of the brown-rot fungi: Fomitopsis and its related genera. Fungal Divers. 2016, 80, 343–373. [Google Scholar] [CrossRef] [Green Version]
  57. Tsuneda, I.; Kennedy, L.L. Basidiospore germination and substrate preference in Fomes fomentarius and Fomitopsis cajanderi. Mycologia 1980, 72, 204–208. [Google Scholar] [CrossRef]
  58. Cortesi, P.; Fischer, M.; Milgroom, M.G. Identification and spread of Fomitiporia punctate associated with wood decay of grapevine showing symptoms of Esca. Phytopathology 2000, 90, 967–972. [Google Scholar] [CrossRef] [Green Version]
  59. Fischer, M. Phellinus igniarius and its closest relatives in Europe. Mycol. Res. 1995, 99, 735–744. [Google Scholar] [CrossRef]
  60. Fischer, M. Grapevine wood decay and lignicolous basidiomycetes. Phytopathol. Mediterr. 2000, 39, 100–106. [Google Scholar]
  61. Berglund, H.; Edman, M.; Ericson, L. Temporal variation of wood-fungi diversity in boreal old-growth forests: Implications for monitoring. Ecol. Appl. 2005, 15, 970–982. [Google Scholar] [CrossRef]
Sustainability 12 02535 g001 550
Figure 1. Location of the sampling sites in Central Siberia: open circles and squares - this study, closed circles and squares - previous literature. ●Central Siberia (Kotiranta and Shiryaev, 2016); ▲Tuva Republic, Southern Siberia (Kotiranta et al., 2016); ■Yenisein River basin, East Siberia (Shiryaev and Kotiranta, 2016); ○Krasnoyarsk, Central Siberia; □Republic of Khakassia.
Figure 1. Location of the sampling sites in Central Siberia: open circles and squares - this study, closed circles and squares - previous literature. ●Central Siberia (Kotiranta and Shiryaev, 2016); ▲Tuva Republic, Southern Siberia (Kotiranta et al., 2016); ■Yenisein River basin, East Siberia (Shiryaev and Kotiranta, 2016); ○Krasnoyarsk, Central Siberia; □Republic of Khakassia.
Sustainability 12 02535 g001
Sustainability 12 02535 g002 550
Figure 2. The major species found on each host genus in Central Siberia. a–c (Abies sibirica): (a) Antrodia gossypium, (b) Fomitopsis pinicola, (c) Hymenochaete cruenta; d,e (Larix siberia): (d) Laetiporus montanus, (e) Rhodofomes cajanderi; f–h (Pinus sylvestris): (f) Fomitopsis pinicola, (g) Phaeolus schweinitzii, (h) Trichaptum abietinum; i–l (Betula pendula): (i) Fomitopsis betulina, (j) Inonotus obliquus, (k) Phellinus laevigatus, (l) Phellinus lundellii; m,n (Populus tremula): (m) Ganderma applanatum, (n) Hypsizygus marmoreus; o,p (Salix alba var. sericea): (o) Fomitiporia punctate, (p) Phellinus igniarius.
Figure 2. The major species found on each host genus in Central Siberia. a–c (Abies sibirica): (a) Antrodia gossypium, (b) Fomitopsis pinicola, (c) Hymenochaete cruenta; d,e (Larix siberia): (d) Laetiporus montanus, (e) Rhodofomes cajanderi; f–h (Pinus sylvestris): (f) Fomitopsis pinicola, (g) Phaeolus schweinitzii, (h) Trichaptum abietinum; i–l (Betula pendula): (i) Fomitopsis betulina, (j) Inonotus obliquus, (k) Phellinus laevigatus, (l) Phellinus lundellii; m,n (Populus tremula): (m) Ganderma applanatum, (n) Hypsizygus marmoreus; o,p (Salix alba var. sericea): (o) Fomitiporia punctate, (p) Phellinus igniarius.
Sustainability 12 02535 g002
Sustainability 12 02535 g003 550
Figure 3. The number of wood-decay fungi (WDF) associated with different host tree species in Central Siberia. (a) Number of WDF species associated with six major host tree genera, combining data from this study with previous studies. (b) Venn diagram illustrating the number of WDF occurring on angiosperm and gymnosperm. (c) Venn diagram showing the number of WDF found on main host trees of gymnosperm (Abies spp., Larix spp., Pinus spp.). (d) Venn diagram showing the number of WDF found on main host trees of angiosperm (Betula spp., Populus spp., Salix spp.).
Figure 3. The number of wood-decay fungi (WDF) associated with different host tree species in Central Siberia. (a) Number of WDF species associated with six major host tree genera, combining data from this study with previous studies. (b) Venn diagram illustrating the number of WDF occurring on angiosperm and gymnosperm. (c) Venn diagram showing the number of WDF found on main host trees of gymnosperm (Abies spp., Larix spp., Pinus spp.). (d) Venn diagram showing the number of WDF found on main host trees of angiosperm (Betula spp., Populus spp., Salix spp.).
Sustainability 12 02535 g003
Table
Table 1. List of wood-decay fungi collected from Krasnoyarsk and the Republic of Khakassia, Russia.
Table 1. List of wood-decay fungi collected from Krasnoyarsk and the Republic of Khakassia, Russia.
Fungal SpeciesKr1Kr2Kr3Kh1Kh2Kh3Kh4Specimen No.
(Acc No.)		Closest Match (Accession Number)Similarity (%)
Antrodia gossypium
(=Fibroporia gossypium)		 AbAbSFC20170811-08
(MT044421)		Fibroporia gossypium (HM590880)100
Antrodia hingganensis AbSFC20170811-04
(MT044428)		Antrodia hingganensis (KC595893)99.8
Antrodia xantha AbSFC20170811-17
(MT044427)		Antrodia xantha strain (DQ491424)100
Botryobasidium subcoronatum Be BeBe SFC20170809-07
(MT044390)		Botryobasidium subcoronatum (AJ389790)100
Cerrena unicolor Be Be SFC20140920-13
(MT044429)		Cerrena unicolor (KP135305)99.8
Climacodon pulcherrimus BeBeSFC20170810-20
(MT044416)		Climacodon pulcherrimus (KY948784)99.8
Coniophora puteana Ab Ab SFC20170809-26
(MT044400)		Coniophora puteana (AM293074)99.6
Daedaleopsis tricolor Be Be BeSFC20140920-08
(MT044430)		Daedaleopsis tricolor (MG696213)100
Fomes fomentarius Be BeBeBeSFC20170809-15
(MT044396)		Fomes fomentarius (EF155499)100
Fomitiporia punctata Sa Sa SFC20140922-20
(MT044431)		Fomitiporia punctata (KX639630)99.6
Fomitopsis betulina
(=Piptoporus betulinus)		 Be BeBeBeSFC20170809-09
(MT044392)		Piptoporus betulinus (JX109856)99
Fomitopsis pinicolaAb Pi Be AbSFC20140919-02
(MT044432)		Fomitopsis pinicola (KX524505)100
Ganoderma applanatumPo PoBe BeSFC20170809-27
(MT044401)		Ganoderma applanatum (KY364256)99.6
Gloeocystidiellum convolvens
(=Gloeopeniophorella convolvens)		 Be Be SFC20140920-19
(MT044433)		Gloeopeniophorella convolvens (KY848506)99.8
Gloiothele sp. Ab AbSFC20170811-07
(MT044420)		Gloiothele sp. (KJ713991)99.6
Hapalopilus rutilansAb Ab AbSFC20170811-05
(MT044419)		Hapalopilus rutilans (KX752625)98.9
Hericium coralloides Be SFC20170810-04
(MT044405)		Hericium coralloides (MG735348)99.8
Heterobasidion annosum Ab SFC20140922-17
(MT044434)		Heterobasidion annosum (MH859050)100
Hymenochaete cruenta Ab AbSFC20170811-12
(MT044423)		Hymenochaete cruenta (JQ279595)100
Hypsizygus marmoreus Po SFC20170809-28
(MT044402)		Hypsizygus tessulatus (KP192620)100
Inonotus leporinusAb SFC20140919-04
(MT044435)		Inonotus leporinus voucher (FJ775542)99.5
Inonotus obliquus Be BeBe SFC20140922-21
(MT044436)		Inonotus obliquus (KP004970)100
Irpex lacteus Sa Be SFC20170810-15
(MT044413)		Irpex lacteus strain (JX311924)100
Kuehneromyces mutabilis Ab SFC20170809-25
(MT044399)		Kuehneromyces mutabilis (AY354218)100
Laetiporus montanus La SFC20170809-01
(MT044387)		Laetiporus montanus (KX354466)99.8
Neolentinus lepideus Be SFC20170810-14
(MT044412)		Neolentinus lepideus (HM536098.1)99.5
Onnia tomentosa La SFC20170810-01
(MT044403)		Onnia tomentosa (KF996518)99.9
Phaeolus schweinitziiAb Pi SFC20170810-18
(MT044415)		Phaeolus schweinitzii (FR686570)99.6
Phellinus igniarius Sa SFC20170809-03
(MT044388)		Phellinus igniarius (GQ383711)96
Phellinus laricis
(=Porodaedalea laricis)		 LaAbSFC20170810-07
(MT044408)		Porodaedalea laricis (FJ775569)98.9
Phellinus cinereus BeSFC20170811-16
(MT044426)		Phellinus cinereus (AY340047)100
Phellinus laevigatus Be BeBe SFC20170809-14
(MT044395)		Phellinus laevigatus (AY340053)100
Phellinus lundellii Be Be BeSFC20170811-03
(MT044418)		Phellinus lundellii (AY340058)100
Phlebia tremellosa Be Be SFC20170809-08
(MT044391)		Phlebia tremellosa (LN611126)99.3
Pleurotus ostreatus
(=Pleurotus pulmonarius)		 Be BeBe SFC20170810-10
(MT044410)		Pleurotus pulmonarius (KP867918)100
Plicaturopsis crispa Be BeSFC20170811-10
(MT044422)		Plicaturopsis crispa (DQ494686)99
Postia balsamea La SFC20170810-11
(MT044411)		Postia balsamea (JF950570)99.1
Postia caesiosimulans AbSFC20170811-14
(MT044424)		Postia caesiosimulans (MG137061)99.2
Postia fragilis Ab SFC20170809-23
(MT044398)		Postia fragilis (JF950573)99.6
Postia lateritia AbSFC20170811-15
(MT044425)		Postia lateritia (JF950566)97.6
Postia sp. Pi SFC20140922-07
(MT044437)		Postia sp. (KJ668468)96.7
Rhodofomes cajanderi
(=Fomitopsis cajanderi)		 LaLa SFC20170810-06
(MT044407)		Fomitopsis cajanderi (DQ491413)100
Stereum hirsutum Be Be SFC20170809-10
(MT044393)		Stereum hirsutum (AY854063)99.8
Stereum subtomentosum Be BeBeSFC20140920-21
(MT044438)		Stereum subtomentosum ( KR673461)98.5
Trametes hirsuta BeBe SFC20170810-16
(MT044414)		Trametes hirsuta (KF573009)99.6
Trametes pubescens Be SFC20170810-09
(MT044409)		Trametes pubescens (JN164960)99.3
Trametes versicolor Be Be SFC20170809-05
(MT044389)		Trametes versicolor (JN164965)99.7
Trichaptum abietinumAbPiPi AbAbAbSFC20170809-22
(MT044397)		Trichaptum abietinum (AY781273)99.8
Trichaptum biforme Be BeBe SFC20170810-02
(MT044404)		Trichaptum biforme (MH245095)99.8
Vitreoporus dichrous
(=Gloeoporus dichrous)		 BeBe SFC20170810-21
(MT044417)		Gloeoporus dichrous (MG572751)100
Xylodon flaviporus Be SFC20170810-05
(MT044406)		Xylodon flaviporus (AF145585)100
Xylodon radula Ab AbSFC20170809-11
(MT044394)		Xylodon radula (KP814413)99.5
The number of samples63202292521

Share and Cite

MDPI and ACS Style

Park, J.-H.; Pavlov, I.N.; Kim, M.-J.; Park, M.S.; Oh, S.-Y.; Park, K.H.; Fong, J.J.; Lim, Y.W. Investigating Wood Decaying Fungi Diversity in Central Siberia, Russia Using ITS Sequence Analysis and Interaction with Host Trees. Sustainability 2020, 12, 2535. https://doi.org/10.3390/su12062535

AMA Style

Park J-H, Pavlov IN, Kim M-J, Park MS, Oh S-Y, Park KH, Fong JJ, Lim YW. Investigating Wood Decaying Fungi Diversity in Central Siberia, Russia Using ITS Sequence Analysis and Interaction with Host Trees. Sustainability. 2020; 12(6):2535. https://doi.org/10.3390/su12062535

Chicago/Turabian Style

Park, Ji-Hyun, Igor N. Pavlov, Min-Ji Kim, Myung Soo Park, Seung-Yoon Oh, Ki Hyeong Park, Jonathan J. Fong, and Young Woon Lim. 2020. "Investigating Wood Decaying Fungi Diversity in Central Siberia, Russia Using ITS Sequence Analysis and Interaction with Host Trees" Sustainability 12, no. 6: 2535. https://doi.org/10.3390/su12062535

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop