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Original article / Оригинальная статья
УДК 582.28 : 581.95 (470+571)
DOI: 10.18470/1992-1098-2020-3-165-173
Species of Odontia and Tomentella (Thelephorales, Basidiomycota) new to Dagestan, Russia
Yuliya Yu. Ivanushenko1 and Sergey V. Volobuev2
'Dagestan State University, Makhachkala, Russia
2Komarov Botanical Institute, Russian Academy of Sciences, Saint Petersburg, Russia
Principal contact
Sergey V. Volobuev, Candidate of Sciences (Biology), Senior Researcher, Laboratory of Systematics and Geography of Fungi, Koma-rov Botanical Institute, Russian Academy of Sciences; 2 Professora Popova St, Saint Petersburg, Russia 197376. Tel. +7(812)3725469 Email sergvolobuev@binran.ru ORCID https://orcid.org/0000-0003-1217-5548
How to cite this article
Ivanushenko Yu.Yu., Volobuev S.V. Species of Odontia and Tomentella (Thelephorales, Basidiomycota) new to Dagestan, Russia. South of Russia: ecology, development. 2020, vol. 15, no. 3, pp. 165-173. DOI: 10.18470/1992-1098-2020-3-165-173
Received 27 April 2020 Revised 29 May 2020 Accepted 6 July 2020
Abstract
Aim. To obtain new data on the species diversity, phylogenetic structure, and ecological characteristics of thelephoroid fungi (Thelephorales, Basidiomycota) in the Republic of Dagestan.
Material and Methods. Both micromorphological and molecular analyses were used for studying of the fungal specimens collected by the authors in 2018-2019 in the Gunibsky and Magaramkentsky Districts of Dagestan. Additional specimens from the Mycological Herbarium of the Komarov Botanical Institute of the Russian Academy of Sciences (LE) were studied. The ITS region of nrDNA was amplified with two pairs of primers, ITS1F/ITS4 and ITS5/ITS4. Results. Sixteen ITS sequences belonging to eight species were obtained from the studied material. Of them, 14 sequences clustered in the Tomentella clade and two sequences nested within the Odontia clade. Four species - Odontia duemmeri, Tomentella lapida, T. radiosa, T. terrestris - were registered for the first time for Dagestan. Detailed information on the specimens studied is presented. Species identification of Odontia fibrosa, Tomentella badia, T. ferruginea, and T. stuposa was confirmed by ITS nrDNA analysis.
Conclusion. Data on the species richness of the genera Odontia and Tomentella in Dagestan is updated, and the species T. lilacinogrisea is excluded from the regional funga. To date the genera Odontia and Tomentella in the Republic of Dagestan are represented by three and fifteen species, respectively. Key Words
Biodiversity, basidiomycetes, distribution of fungi, ITS phylogeny, DNA barcodes, Tomentella, Dagestan, Caucasus.
© 2020 The authors. South of Russia: ecology, development. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Новые для Дагестана виды родов Odont¡a и ТотвШвИа (Thelephorales, Basidiomycota)
Юлия Ю. Иванушенко1, Сергей В. Волобуев2
'Дагестанский государственный университет, Махачкала, Россия 2Ботанический институт им. В.Л. Комарова РАН, Санкт-Петербург, Россия
Контактное лицо
Сергей В. Волобуев, кандидат биологических наук, старший научный сотрудник лаборатории систематики и географии грибов, Ботанический институт им. В.Л. Комарова РАН; 197376 Россия, г. Санкт-Петербург, ул. Профессора Попова, 2. Тел. +7(812)3725469 Email sergvolobuev@binran.ru ORCID https://orcid.org/0000-0003-1217-5548
Формат цитирования
Иванушенко Ю.Ю., Волобуев С.В. Новые для Дагестана виды родов Odontia и mentella (ТЬе!ерИога!е$, Ва$1^оту^а) // Юг России: экология, развитие. 2020. Т. 15, N 3. С. 165-173. 001: 10.18470/19921098-2020-3-165-173
Получена 27 апреля 2020 г.
Прошла рецензирование 29 мая 2020 г.
Принята 6 июля 2020 г.
Резюме
Цель. Получить новые данные о видовом разнообразии, филогенетической структуре и экологических характеристиках телефоровых грибов (Thelephorales, Basidiomycota) Республики Дагестан.
Материал и методы. В работе были использованы микроморфологический и молекулярный анализы для изучения образцов грибов, собранных авторами в 2018-2019 гг. в Гунибском и Магарамкентском районах Дагестана. Были изучены дополнительные образцы из микологического гербария Ботанического института им. В.Л. Комарова Российской академии наук (LE). Участок внутреннего траскрибируемого спейсера (ITS) ярДНК был амплифи-цирован для исследованных образцов с использованием двух пар прайме-ров, ITS1F / ITS4 и ITS5 / ITS4.
Результаты. Впервые получены 16 ITS последовательностей, которые отнесены к восьми видам грибов. 14 нуклеотидных последовательностей оказались в пределах клады, сформированной видами рода Tomentella, а две других последовательности вошли в кладу, образованную видами рода Odontia. Четыре вида - Odontia duemmeri, Tomentella lapida, T. radiosa, T. terrestris - впервые отмечены в Дагестане. Находки видов Odontia fibrosa, Tomentella badia, T. ferruginea, T. stuposa, ранее известных для Дагестана, подтверждены на основе анализа ITS области ярДНК.
Заключение. Обновлены данные о видовом богатстве родов Odontia и Tomentella в Дагестане, при этом вид T. lilacinogrisea исключен из региональной микобиоты. К настоящему времени роды Odontia и Tomentella в Республике Дагестан представлены 3 и 15 видами соответственно. Ключевые слова
Биоразнообразие, базидиомицеты, распространение грибов, ITS-филогения, ДНК-штрихкодирование, Tomentella, Дагестан, Кавказ.
© 2020 Авторы. Юг России: экология, развитие. Это статья открытого доступа в соответствии с условиями Creative Commons Attribution License, которая разрешает использование, распространение и воспроизведение на любом носителе при условии правильного цитирования оригинальной работы.
INTRODUCTION
Despite rather detailed scientific research on the flora and fauna of Dagestan, mycological studies have not been given due attention; they have been episodic and unsystematic in nature. In general, the data on the diversity of aphyllopho-roid fungi are available for the protected natural territories [1-4]. This publication continues the series of works devoted to the inventory of species diversity and ecological characteristics of aphyllophoroid fungi in Dagestan [2-8], in particular of the genera Odontia and Tomentella [9].
To date fifteen species of the genus Tomentella s. lato are known for mycobiota of Dagestan: Tomentella atramentaria, T. badia, T. bryophila, T. cinerascens, T. crinalis (=Odontia ferruginea), T. ellisii, T. ferruginea, T. fibrosa (=Odontia fibrosa), T. lateritia, T. lilacinogrisea, T. pilosa, T. punicea, T. stuposa, T. subtestacea, and T. um-brinospora [7-10].
Taking into account the widespread use of molecular techniques in mycology both to describe new taxa and to study the modern species composition of regional my-cobiotas, we carried out a comparative study of the internal transcribed spacer (ITS) region of the nuclear ribosomal DNA (nrDNA) from the specimens of the genera Odontia and Tomentella, which allowed us to identify species new to Dagestan.
The aim of the study was to obtain new data on the species diversity, phylogenetic structure, and ecological characteristics of thelephoroid fungi (Thelephorales, Basi-diomycota) in Dagestan.
MATERIAL AND METHODS
Specimens of basidiomycetes were collected during a routine survey of forest ecosystems in the Gunibsky and Magaramkentsky Districts of the Republic of Dagestan
within the protected areas: the Upper Gunib Nature Park and the Samursky National Park in May and September-October 2018-2019. Additionally, specimens stored in the Mycological Herbarium of the Komarov Botanical Institute of the Russian Academy of Sciences (LE) were studied. Microscopy-based identification of fungi as well as re-examination of herbarium specimens was done at magnifications up to x1000 using LOMO Mikmed-6 optical microscope, Carl Zeiss AxioImager A1 microscope and a standard set of reagents (5% potassium hydroxide solution, Melzer's reagent).
DNA was extracted from small pieces of dried ba-sidiocarps using the FitoSORB DNA extraction kit (Syntol, Russia) according to the manufacturer's instructions. PCR reactions were performed in 25 |L of reaction mixtures containing 5 |L of Fidelity Buffer (5X), 0.5 |L of KAPA HiFi HotStart DNA Polymerase, 0.75 |L of dNTPs, 0.5 |L of each PCR primer, 12.75 |L of deionized H2O, and 5 |L of template DNA. The ribosomal ITS1-5.8S-ITS2 region was amplified with two pairs of the primers: ITS1F and ITS4 or ITS5 and ITS4 [11; 12]. PCR products were visualized using agarose gel electrophoresis and GelRed staining, and subsequently purified with the Fermentas Genomic DNA Purification Kit (Thermo Fisher Scientific, Lithuania). Purified PCR products were sequenced on an ABI model 3130 Genetic Analyzer (Applied Biosystems, CA, USA). Raw data were edited and assembled in MEGA 6 [13]. Newly generated sequences were deposited in the GenBank. Additionally, 46 ITS sequences were retrieved from GenBank [14] and UNITE [15] (Table 1). Sequences were aligned with the MAFFT version 7 web tool [16; 17] using the E-INS-1 option. Maximum Likelihood (ML) analysis was performed in the IQ-TREE Web Server [18] with 1000 ultrafast bootstrap replicates.
Table 1. Specimens and sequences used in this study
Таблица 1. Образцы и нуклеотидные последовательности, использованные в данном исследовании
Species GenBank/ UNITE accessions Specimen voucher Origin
Odontia duemmeri UDB011121 KHL10605 Jamaica
Odontia duemmeri UDB018552 TU115185 Mexico: Municipality of Lazaro Cardenas
Odontia duemmeri UDB033701 TU115587 Germany: Bavaria
Odontia duemmeri MT981503 LE 314777 Russia: Dagestan
Odontia ferruginea UDB032228 TU111186 Estonia
Odontia fibrosa MK602775 TU115028 China
Odontia fibrosa MT981502 LE F-332368 Russia: Dagestan
Thelephora terrestris AF272921 JS17996(O) Unspecified
Thelephora terrestris AF272923 / UDB000215 TAA162083 Estonia
Tomentella alpina EF655702 IB20060231 (holotype) Austria
Tomentella atramentaria AF272904 TAA149211 Unspecified
Tomentella atramentaria EF644115 IB2004189 Austria
Tomentella atramentaria KT353045 GO-2009-248 Mexico: Mexico State
Tomentella badia AF272917 / UDB000239 TAA164600 Estonia
Tomentella badia AF272937 / UDB000238 TAA159022 Russia
Tomentella badia KJ140664 CFMR:DLL2011-166 United States: central Wisconsin
Tomentella badia UDB000961 NF.S103 (O) Norway
Tomentella badia MT981507 LE 299095 Russia: Kaluga Region
Tomentella badia MT981508 LE 299096 Russia: Kaluga Region
Tomentella badia MT981506 LE 313862 Russia: Lipetsk Region
Tomentella badia MT981495 LE 314772 Russia: Dagestan
Tomentella badia MT981499 LE 314775 Russia: Dagestan
Tomentella cinerascens UDB003309 TU100735 Finland
Tomentella cinerascens UDB016193 TU108037 Estonia
Tomentella cinerascens UDB016498 TU111378 Italy
Tomentella crinalis UDB032224 TU105627 Estonia
Tomentella ellisii UDB011603 TU115347 Finland
Tomentella ellisii UDB000226 TU123494 Germany
Tomentella ferruginea AF272909 TAAM166877 Estonia
Tomentella ferruginea MH310801 SS367B Unspecified
Tomentella ferruginea MT981504 LE 314778 Russia: Dagestan
Tomentella ferruginea MT981501 LE F-332319 Russia: Dagestan
Tomentella fuscocinerea DQ974776 src813 United States
Tomentella fuscocinerea GU214810 TU108229 Iran
Tomentella globosa MG136838 Yuan11618 Finland
Tomentella globosa MG136839 Yuan11603 Finland
Tomentella lammiensis MG136840 Yuan11617 Finland
Tomentella lammiensis MG136841 Yuan11597 Finland
Tomentella lapida UDB003322 TU100884 France: Vaucluse
Tomentella lapida UDB016346 TU115491 Estonia
Tomentella lapida UDB016370 TU115604 Estonia
Tomentella lapida MT981496 LE F-332369 Russia: Dagestan
Tomentella lilacinogrisea AF272910 TAA159499 Unspecified
Tomentella lilacinogrisea UDB016500 TU111381 Italy
Tomentella lilacinogrisea UDB018468 TU108189 Estonia
Tomentella longisterigmata MG136836 Yuan11610, holotype Finland
Tomentella longisterigmata MG136837 Yuan11602 Finland
Tomentella radiosa MT981500 LE 314776 Russia: Dagestan
Tomentella ramosissima U83480 LT19, Bruns Herbarium, UCB United States
Tomentella sp. UDB018564 TAAM150657 Estonia
Tomentella sp. UDB025528 TU116751 Morocco: Douar Tala Atia
Tomentella stuposa AF272944 JS20510 (O) Unspecified
Tomentella stuposa UDB000247 TAAM159822 Sweden
Tomentella stuposa MT981509 LE 286822 Russia: Oryol Region
Tomentella stuposa MT981505 LE 292220 Russia: Oryol Region
Tomentella stuposa MT981498 LE 314774 Russia: Dagestan
Tomentella stuposa MT981510 LE 314779 Russia: Dagestan
Tomentella terrestris AF272911 /
UDB000221 TAA159557 Estonia
Tomentella terrestris UDB003315 TU100886 France: Vaucluse
Tomentella terrestris MT981497 LE 314773 Russia: Dagestan
RESULTS AND DISCUSSION
The ITS dataset includes 16 newly generated sequences and 46 sequences of 19 species downloaded from public databases (GenBank, UNITE). The genus Odontia was used as an outgroup. The final ITS alignment contained 858 positions (including gaps). The ML tree is shown in Fig. 1. Our 16 sequenced specimens appeared in eight separate well-supported clades, which correspond to different species. Among them, 14 sequences clustered in the clade comprised of Tomentella species and two sequences nested within the Odontia clade.
The ITS nrDNA analysis confirmed the microscopy-based taxonomic assignment of the specimens from the Republic of Dagestan belonging to three species from the genus Tomentella (T. badia, T. ferruginea, T. stuposa) and one species from the genus Odontia (O. fibrosa) [7-10].
The first finding of Tomentella badia from Dagestan was recorded on a fallen trunk of Juniperus oblonga from the Gunib Plateau (Gunibsky District) as a result of the special study of juniper-associated aphyllophoroid fungi [7].
This fungus was also collected from fallen trunks of Betula sp. in the same area by Sergey Volobuev and Aziz Ismailov in October 2018 and these specimens (LE 314772, LE 314775) were sequenced now (Table 1).
The species Tomentella ferruginea was registered for Dagestan based on four specimens mentioned by U. Koljalg [10], one specimen (LE F-332319) from the Sa-mursky National Park (Magaramkentsky District) [8], and the specimen from the Gunib Plateau (Gunibsky District) collected from a fallen trunk of Betula sp. by Yuliya Iva-nushenko in May 2019 (LE 314778). The last two specimens mentioned were sequenced in this study.
T. stuposa, one of the most common species of the genus Tomentella, was reported for Dagestan [10], but the specimens from the Gunib Plateau (Gunibsky District) collected from fallen trunks of Betula sp. by Sergey Volobuev and Aziz Ismailov in October 2018 (LE 314774, LE 314779) were sequenced and included in the phylogenetic analysis for the first time (Table 1, Fig. 1).
Figure 1. The Maximum Likelihood tree illustrating the phylogeny of Odontia and Tomentella species, based on ITS sequence dataset. Ultrafast bootstrap values (%) not less than 70 are shown above the branches. Sequence accession numbers (GenBank or UNITE) of selected species are indicated before species names. The bold font shows the names of the sequences obtained in this study
Рисунок 1. Дерево, построенное методом максимального правдоподобия и иллюстрирующее филогению видов Odontia и Tomentella, на основе ITS-последовательностей. Значения ultrafast bootstrap (не менее 70%) показаны над ветвями. Номера последовательностей (в базах данных GenBank или UNITE) отобранных таксонов указаны перед видовыми названиями. Жирным шрифтом выделены названия нуклеотидных последовательностей, полученных в данном исследовании
The newly generated ITS sequence of Odontia fibrosa was obtained (Table 1) for the specimen from the Samursky National Park (Magaramkentsky District) [8], which is the second finding of the species besides the record in the Upper Gunib Nature Park (Gunibsky District) [9]. At the same time, four other species are new to Dagestan -Odontia duemmeri, Tomentella lapida, T. radiosa, and T. terrestris. Detailed annotations for specimens of these species and some taxonomic and distributional remarks are presented below.
Odontia duemmeri (Wakef.) Koljalg
Specimen examined: Russia, Republic of Dagestan, Gunibsky District, Gunib Plateau, 42.400873° N, 46.910158°
E, 1905 m a.s.l., herb-rich birch forest, on fallen trunk of Betula sp. (LE 314777), 1 October 2019, coll. and det. Sergey V. Volobuev and Yuliya Yu. Ivanushenko.
The second species of the Odontia genus, followed by O. fibrosa [9], which is reported for Dagestan. As stable isotope analyses showed, all representatives of Odontia possess a non-ectomycorrhizal lifestyle, but their nutrition differs from typical xylotrophic basidiomycetous fungi [19]. Micromorphology of O. duemmeri is carefully described and illustrated by E. Martini [20]. This species occurs both on deciduous (Quercus robur) and coniferous (Juniperus communis) trees, but it was not previously collected from the wood of birch. Our finding (Fig. 2) is the first one of the species on the Caucasus.
Figure 2. Basidiocarp of Odontia duemmeri (LE 314777): details of hymenophore with rhizomorphs Рисунок 2. Плодовое тело Odontia duemmeri (LE 314777): внешний вид гименофора с ризоморфами
Tomentella lapida (Pers.) Stalpers
Specimen examined: Russia, Republic of Dagestan, Magaramkentsky district, Samursky National Park, 41.845944° N, 48.560056° E, -9 m a.s.l., herb-rich mixed forest dominated by Carpinus betulus and Quercus robur subsp. pedunculiflora, on fallen trunk of Crataegus sp. (LE F-332369), 5 October 2019, coll. and det. Sergey V. Volo-buev.
This is a common species with a worldwide distribution. T. lapida is close to T. stuposa (Fig. 1), but it differs distinctly from the latter in its encrusted subicular hyphae and smaller basidiospores. At the same time, it was noted previously [10] that T. lapida is also close to T. lilacino-grisea. Apparently, the similarities in the incrustation of thick-walled and brown subicular hyphae as well as shape of basidiospores, which can be slightly globose in frontal
and lateral face in both species, were taken into account. The main differences between T. lapida and T. lilacino-grisea are in the size of spores (6-7 |im in T. lilacinogrisea and 7.5-9.5 |im in T. lapida) and the diameter of subicular hyphae. Our specimen (LE F-332369) has a smaller size of spores (6.5-7(7.5) |im). In a previous microscopic study [8], the specimen was incorrectly identified as T. lilacinogrisea. Based on the molecular analysis and additional examination of the micromorphology, the specimen was re-determined as T. lapida. The species was known previously in the Caucasus from Russia (Krasnodar Territory) and Armenia [10].
Tomentella radiosa (P. Karst.) Rick
Specimen examined: Russia, Republic of Dagestan, Gunibsky District, Gunib Plateau, 42.392758° N, 46.935123°
E, 1573 m a.s.l., herb-rich pine-dominated forest with birch and hornbeam, on fallen trunk of Betula sp. (LE 314776), 30 September 2019, coll. and det. Sergey V. Volobuev.
A widespread species in the Caucasus, in particular, in its north-western part (Karachay-Cherkessia Republic, Krasnodar Territory) and Transcaucasia (Armenia, Azerbaijan, Georgia) [10]. This species grouped together with sequences of Thelephora terrestris Ehrh. in our phylogenetic tree (Fig. 1) that supports the nomenclature combination of Thelephora terrestris f. radiosa (P. Karst.) Zmitr. [21] for this taxon.
Tomentella terrestris (Berk. et Broome) M.J. Larsen Specimens examined: Russia, Republic of Dagestan, Gunibsky District, Gunib Plateau, 42.409078° N, 46.901189° E, 1959 m a.s.l., herb-mosses pine forest, on fallen trunks of Betula sp. (LE 314790) and Pinus kochiana (LE 314791), 4 October 2018, coll. and det. Sergey V. Volobuev; 42.407591° N, 46.903117° E, 1920 m a.s.l., herb-mosses pine forest, on fallen trunk of Pinus kochiana (LE 314773), 6 October 2018, coll. Sergey V. Volobuev and Aziz B. Ismailov, det. Sergey V. Volobuev and Yuliya Yu. Ivanushenko; 42.396977° N, 46.922749° E, 1663 m a.s.l., herb-mosses pine-dominated forest with birch, on fallen trunk of Pinus kochiana (LE 314792) and on soil at the base of Pinus ko-chiana trunk (LE 314793), 28 September 2019, coll. and det. Sergey V. Volobuev and Yuliya Yu. Ivanushenko.
This is a remarkable species in the genus Tomentella due to the size of its basidia, which are up to 15-20 |im in diameter. This species is widely distributed in the Caucasus and is known from Russia (Karachay-Cherkessia Republic, Krasnodar Territory) and Azerbaijan [10]. The basidio-carps of T. terrestris were found during this study not only on well-decayed wood but also on soil.
CONCLUSION
Based on morphological and molecular evidence, four species of thelephoroid basidiomycetes - Odontia duemmeri, Tomentella lapida, T. radiosa, T. terrestris - were recorded for the first time to Dagestan. The data on the species richness of the genera Odontia and Tomentella in this region are updated and the species T. lilacinogrisea is excluded from the regional funga. Currently, the genera Odontia and Tomentella in the Republic of Dagestan are represented by three and fifteen species, respectively.
ACKNOWLEDGEMENTS
This study was funded by the RFBR according to research project №19-34-50111. The research was done using the equipment of the Core Facility Centre, Cell and Molecular Technologies in Plant Science at the Komarov Botanical Institute, Russian Academy of Sciences (St-Petersburg, Russia).
Morphological studies of LE specimens were carried out within the framework of the research project of the Komarov Botanical Institute RAS, Herbarium Funds of the BIN RAS (History, Conservation, Study and Supplementation) (АААА-А18-118022090078-2). БЛАГОДАРНОСТИ
Исследование выполнено при поддержке РФФИ в рамках научного проекта №19-34-50111 с использованием оборудования ЦКП «Клеточные и молекулярные технологии изучения растений и грибов» Ботанического ин-
ститута им. В.Л. Комарова РАН (Санкт-Петербург). Морфологическое изучение образцов из гербария 1-Е проведено в рамках госзадания БИН РАН по теме «Гербарные фонды БИН РАН: история, сохранение, изучение и пополнение» (АААА-А18-118022090078-2).
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http://mafft.cbrc.jp/alignment/server/ (дата обращения 20.04.2020)
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AUTHOR CONTRIBUTIONS
Both authors participated in the collection, morphological and molecular studies of the research materials, as well as in the preparation of the manuscript. Authors are equally responsible for plagiarism and self-plagiarism and other ethical transgressions.
NO CONFLICT OF INTEREST DECLARATION
The authors declare no conflict of interest.
КРИТЕРИИ АВТОРСТВА
Оба автора осуществляли сбор, морфологическое и молекулярное изучение материала, написание текста рукописи. Авторы в равной степени несут ответственность при обнаружении плагиата и других неэтических проблем.
КОНФЛИКТ ИНТЕРЕСОВ
Авторы заявляют об отсутствии конфликта интересов.
ORCID
Yuliya Yu. Ivanushenko / Юлия Ю. Иванушенко https://orcid.org/0000-0003-0197-4176 Sergey V. Volobuev / Сергей В. Волобуев https://orcid.org/0000-0003-1217-5548
