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13BRYOPHYTES - МОХООБРАЗНЫЕ
A rare moss Cynodontium suecicum (Rhabdoweisiaceae, Bryophyta) on the Barents Sea coast of the Kola Peninsula: morphological and molecular study
O. A. Belkina, A. A. Vilnet
Polar-Alpine Botanical Garden and Institute of the Kola Science Center of the Russian Academy of Sciences, Apatity, Murmansk Region, Russia Corresponding author. O. A. Belkina, olgabelk@yahoo.com
Abstract. Specimens of the rare species Cynodontium suecicum (Rhabdoweisiaceae, Bryophyta) were collected near Drozdovka Bay on the Barents Sea coast of the Kola Peninsula (Russia) in 2016. They were compared with samples of C. suecicum from the Teriberka area (also the coast of the Barents Sea) gathered in 1977 by R. N. Schljakov. The morphological features of both groups of samples were studied, and nucleotide sequence data for ITS1-2 nrDNA and trnL-F cpDNA were obtained. Molecular analysis suggested C. suecicum as a hybrid that inherited cytoplasmic DNA from C. tenellum and nuclear DNA from Kiaeria blyttii. Taking into account the rather clear morphological delimitation against other species, combined with the stability of genetic characters, we believe that S. suecicum should be retained as a species-level taxon.
Keywords: DNA, intergeneric hybridization, morphological variability, Murmansk Region, Russia.
Редкий мох Cynodontium suecicum (Rhabdoweisiaceae, Bryophyta) с побережья Баренцева моря Кольского полуострова: морфологические и молекулярные данные
О. А. Белкина, А. А. Вильнет
Полярно-альпийский ботанический сад-институт им. Н. А. Аврорина Кольского научного центра РАН, Апатиты, Мурманская область, Россия Автор для переписки: О. А. Белкина, olgabelk@yahoo.com
Резюме. В 2016 г. в районе губы Дроздовка (Баренцево море, Кольский п-ов) были собраны образцы редкого в мире мха Cynodontium suecicum (Rhabdoweisiaceae, Bryophyta). Проведено морфологическое и молекулярно-генетическое сравнение с образцами того же вида из района Териберки (Баренцево море), собранными в 1977 г. Р. Н. Шляковым. Приведены результаты изучения анатомо-морфологи-ческих признаков. Получены нуклеотидные последовательности ITS1-2 ядДНК и trnL-F хпДНК. Установлено сходство хлоропластного локуса с последовательностями C. tenellum, а ядерного - с последовательностями вида из другого рода, а именно Kiaeria blyttii. Таким образом, есть основания считать Cynodontium suecicum
https://doi.org/1031111/nsnr/2021.552.427
427
межродовым гибридом. Учитывая довольно четкие морфологические различия в сочетании с генетическими характеристиками, мы полагаем, что C. suecicum является таксоном видового уровня.
Ключевые слова: ДНК, межвидовая гибридизация, морфологическая изменчивость, Мурманская область, Россия.
Originally, Cynodontium suecicum (Arnell et C. E. O. Jensen) I. Hagen was collected in Sweden, from surroundings of Ostersund in 1870 and Hoting in 1894, and was described as a new species, Oncophorus suecicus, in 1895 (Arnell, Jensen, 1895). Later, Hagen transferred it to the genus Cynodontium (Hagen, 1899). To date, localities of this species have been recorded only within Fennoscandia (Sweden, Norway, and Finland; Hallingback et al, 2006) including the Kola Peninsula (Murmansk Region, Russia). For a long time, the single record of C. suecicum on the Kola Peninsula was known from the vicinity of the Teriberka village on the Barents Sea coast (Schljakov, Konstantinova, 1982). Later, several localities were discovered in the southern and east-southern coast of the Kola Peninsula (White Sea) — near Umba town and Cha-van'ga village, as well as on an island of the Porja Guba bay (Sofronova et al, 2017).
In August 2016 during fieldwork on the northeastern coast of the Kola Peninsula (Barents Sea), some specimens of C. suecicum were gathered in the area of Drozdovka Bay (Belkina, Likhachev, 2021; Fig. 1). Due to some variability of characters in our samples, we decided to compare them with the samples collected by R. N. Schljakov in 1977 in the surroundings of the Teriberka village, 170 km northwest of Drozdovka Bay. The northern and northeastern coasts of the Kola Peninsula belong to the Kola province of the subarctic (southern) tundra subzone (Aleksandrova, 1977), but birch stands can be found along river valleys and in moist protected depressions among the tundra. Natural conditions of the region are described in more details in Belkina and Likhachev (2021).
Material and Methods
Taxon sampling. In total, 11 samples were included in this study. The list with specimen vouchers and GenBank accession numbers are shown in Table 1. Three samples of C. suecicum from the surroundings of Drozdovka Bay and three Schljakov's specimens of C. suecicum from the vicinity of the Teriberka village (doublets) were studied. Five of these samples are stored in the herbarium of the Polar-Alpine Botanical Garden and Institute (KPABG) and one — in the Komarov Botanical Institute in St. Petersburg (LE).
In sample KPABG(M) 9391 (Table 1), along with the main species (C. suecicum), a small turf of C. tenellum with sporophytes was revealed. In specimen KPABG(M) 9392, the majority of the sample consisted of C. tenellum plants with or without sporophytes, while in another part of the sample, we found the plants of C. suecicum without capsules.
The morphological features and nucleotide sequences of ITS 1-2 nrDNA and trnL-F cpDNA were studied. For comparison, two representative samples of C. tenel-
Fig. 1. The map of Murmansk Region (Russia): 1 — Teriberka village, 2 — Drozdovka Bay.
lum (Schimp.) Limpr. from Teriberka area and from Pyhalampi Lake in southeastern part of the Murmansk Region were selected. For two Schljakov's samples [KPABG(M) 9391 and KPABG(M) 9392], analyses were undertaken both for individuals of C. sueci-cum and of C. tenellum. In addition, one questionable sample without sporophytes and similar to C. suecicum was examined (Table 1, #11). It was collected near the shore of widened Ivanovka River estuary, 10-13 km east of the Drozdovka moss populations.
For morphological study, the optical microscopes Mikmed 6 and Micromed MC-5-Zoom Led were used.
Molecular analysis. DNA extraction from dried moss tissue was carried out with DNeasy Plant Mini Kit (Qiagen, Germany). Amplification and sequencing reactions were done with primers suggested by White et al. (1990) for ITS1-2 and Taberlet et al. (1991) for trnL-F. PCR was carried out in 20 |il volumes with the following protocol: 3 min at 94°C, 30 cycles (30 s 94°C, 40 s 56°C, 60 s 72°C), 2 min of final extension at 72°C. Amplified fragments were visualized on 1% agarose TAE gels by EthBr staining, purified using the QIAquick Gel Extraction Kit (Qiagen, Germany), and used as a template in sequencing reactions with the ABI Prism BigDye Terminator v. 3.1 Ready Reaction Kit (Applied Biosystems, USA) following the standard protocol provided for 3730 DNA Analyzer (Applied Biosystems, USA).
Obtained sequences were assembled and aligned in BioEdit 7.0.1 (Hall, 1999). BLAST search (https://blast.ncbi.nlm.nih.gov/) was implemented to determine the
Table 1
The specimen's voucher information of the studied samples of Cynodontium suecicum, C. tenellum, Oncophorus wahlenbergii from the Murmansk Region.
## Herbarium number/ Field number Taxon or inferred taxon Description of the locality and habitat GenBank accession numbers, ITS1-2 nrDNA / iraL-F cpDNA
1 KPABG(M) 9391/542 Cynodontium suecicum About 69.10453°N, 35.04045°E; Teriberka River basin, left shore, to north of Dolgiy Creek, dry rock; 7 VIII 1977, Schljakov No data/ No data
2 C. tenellum MW996694/ MZ014505
3 KPABG(M) 9392/542a C. suecicum the same (doublet) MW996693/ MZ014504
4 C. tenellum MW996695/ MZ014506
5 LE/542 C. suecicum the same (doublet) MW996692/ MZ014503
6 KPABG(M) 121111/ B41-4-16 C. suecicum 68.29776°N, 38.44112°E; shore of the Drozdovka Bay in innermost part, 4 m a. s. l., low gentle coastal rocks near littoral zone, in a crevace; 10 VII 2016, Belkina MW996690/ MZ014501
7 KPABG(M) 124246/ B48-9-16 C. suecicum 68.27755°N, 38.45981°E, Drozdovka Bay surroundings, 48 m a. s. l., about 0.5 km west of Drozdovjavr Lake, southeast-facing rock cliffs in birch forest, on incline wall; 11 VII 2016, Belkina MW996689/ MZ014500
8 KPABG(M) 121154/ B48-18-16 C. suecicum ibid., in crevice in steep rock wall; 11 VII 2016, Belkina MW996691/ MZ014502
9 KPABG(M) 13917/ M572-77 C. tenellum About 69.15023°N, 35.10288°E; Teriberka River basin, left shore near Teriberka village, slope, turf on wet stone; 7 VIII 1977, Schljakov MW996696/ MZ014507
10 KPABG(M) 13941/ M262-72 C. tenellum About 66.77880°N, 29.84735°E; southwestern part of the Murmansk Region, near Pyhalampi Lake; 05 VII 1972, Schljakov MW996697/ MZ014508
11 KPABG(M) 121271/ B108-2-16 Oncophorus wahlenbergii Brid. (questionable sample) 68.26092°N, 38.72467°E; Ivanovskaya Bay surroundings (Barents Sea), southeastern shore of the Ivanovka River estuary, 8 m a. s. l., large rounded stones in the small stream, in cracks above the water; 20 VII 2016, Belkina MW996698/ MZ014509
similarity of newly generated sequences with data from allied moss species. The molecular variability of tested samples was estimated as the value of p-distances for both ITS1-2 and trnL-F in Mega 5.1 (Tamura et al, 2011) using the pairwise deletion option for counting gaps.
Results
Molecular estimation. ITS1-2 and trnL-F nucleotide sequences were obtained for ten samples — in total, twenty accessions were deposited into GenBank (Table 1). We were not able to obtain ITS1-2 for sample #1, despite two attempts, and it was excluded from the molecular analysis. Alignments were produced manually; all positions were taken in estimation; absent data were coded as missing. With exception of specimen #11, all studied samples possess quite similar sequences of the trnL-F region. BLAST search revealed their 99-100% similarity with accessions of Cynodon-tium tenellum from Sakhalin, Yamal, Taimyr (Russia), Norway, Austria, and with two samples of C. suecicum from the Kola Peninsula. Surprisingly, the two groups of highly distinct ITS1-2 sequences were obtained among Cynodontium specimens. For the first group (samples #2, 4, 9, 10), BLAST search resulted in 99% similarity to two samples of Cynodontium asperifolium, for the second (samples # 3, 5, 6, 7, 8) — 99-100% similarity to multiplied sampled Kiaeria blyttii (Bruch et Schimp.) Broth. Sample #11 is similar to Oncophorus wahlenbergii Brid. at 98% level for trnL-F and 99% for ITS1-2. The p-distance calculation (Table 2) revealed the presence of infraspecific variability in C. suecicum — 0.6% in ITS1-2 and 0.1% in trnL-F, whereas C. tenellum varied only in ITS1-2 (0.1%). The divergence between both species is absent for trnL-F and achieved 10.5% for ITS1-2. The specimen attended to O. wahlenbergii is distinct from both Cynodontium species at 27.5-30.3% level for ITS1-2 and at 7% for trnL-F.
Table 2
The value of ^-distances for studied specimens.
Taxon Infraspecific p-distances, ITSl-2/trnL-F, % p-distances among species, ITS1-2/ trnL-F, %
1 2 3
1 Cynodontium suecicum 0.6/0.1
2 C. tenellum 0.1/0.0 10.5/0.0
3 Oncophorus wahlenbergii n/c/n/c 30.3/15.7 27.5/15.7
Morphological features. We compared the descriptions of the diagnostic features of C. suecicum in the literature sources (Arnell, Jensen, 1895; Savicz-Ljubitzkaja, Smirnova, 1970; Nyholm, 1987; Hallingback et al, 2006). All authors indicate the following distinctive characteristics: 1) flat leaf margins throughout, 2) a more or less clearly differentiated group of cells at the angles of the leaf base, 3) a long excurrent nerve, 4) erect or almost erect, straight or hardly curved, furrowed capsule without struma, 5) an annulus composing of large cells, separating. Nyholm (1987) also poin-
ted at the width of cells in the upper part of leaf lamina — of 10-11 |im as a diagnostic feature. At the same time, some differences in the descriptions of the characters of this taxon can be found in the publications. Arnell and Jensen (1895) state that the nerve is weak, whereas Nyholm (1987) indicates a strong nerve and Hallingback et al. (2006) specifies that the nerve is widening towards the upper part of the leaf. Peristome teeth are split to 1/3 (Arnell, Jensen, 1895), to 1/2 (Savicz-Ljubitzkaja, Smirnova, 1970) or almost to the base (Nyholm, 1987; Hallingback et al., 2006).
The morphological features of mosses in our samples from Drozdovka Bay generally correspond to those of C. suecicum, though with slight variations (Supplement1). In particular, the narrowing of the leaf into a subula can be quite sudden (sample #8), the margins of the leaf lamina in the upper part can vary from entire to crenulate-ma-millose and even dentate-mamillose (the last — in specimens #7 and #8). Alar cell group can be indistinctly or clearly delimited from other cells of the lamina base and be inflated or not. A variable characteristic is the width of the cells in the upper part of the leaf, and it can differ even in the leaves of neighboring plants in the same turf. In the Barents Sea populations, these values may vary in range of 10-12 |im and up to 13.5 in sample #6. The nerve is quite strong in all populations and becomes wider by the middle of the leaf; it is always more or less long excurrent at the leaf apex. The appearance of the capsules is similar in all samples. In sample #6, some peristome teeth are divided into 3, significantly differing in size (i.e., not only split into 2 halves).
In specimens #2 and #4, individuals of C. tenellum have nerve ending at the leaf apex, strongly recurved leaf margins and annulus of smaller cells, but at the same time, spores are large (20-25 |im). Some features of Cynodontium suecicum samples from Drozdovka Bay surroundings are presented on figures 2-5.
Discussion
Recent wide-scale phylogenetic reconstruction of the family Rhabdoweisiaceae based on cpDNA and mtDNA markers (Fedosov et al., 2021) elucidated great diversity within the family and revealed new and unexpected affinities among taxa traditionally associated with the same or different genera, resulting in numerous taxonomical rearrangements. The authors (l. c.) registered a high level of nucleotide markers similarity among C. suecicum and C. tenellum. Our multiplied sampling of both taxa, too, suggested an identity of trnL-F, but 10.5% divergence among ITS1-2 does not allow to include C. suecicum in synonymy with C. tenellum. We supposed that C. suecicum appears to be a hybrid between C. tenellum (cytoplasmic inheritance) and Kiaeria blyt-tii (nuclear inheritance) and could be treated as a species of a hybrid origin. Fedosov and coauthors deposited nucleotide sequences of ITS1-2 Kiaeria blyttii into GenBank, supporting this opinion (personal communication). Hybridization in mosses is possibly a frequent event that is registered among species of a single genus, among species of different genera in a single family, or even between genera from phylogenetically
1 The Supplement is available at the end of the article page on the journal website (https://doi.org/10.31111/nsnr/2021.55.2.427).
Fig. 2. Leaves of Cynodontium suecicum from Drozdovka Bay surroundings. 1, 2 — from KPABG(M)#121111; 3, 4 — from KPABG(M)#124246. Scale bar: 1 mm
remote families (cf.: Ignatov etal, 2019; Sawangproh, Cronberg, 2021). In our case, we discovered an example of intergeneric hybridization.
Considering the anatomical and morphological features, C. suecicum is a fairly well-defined species that is relatively easily identified in the presence of sporophytes. However, in the absence of mature capsules, plants can be confused with some other species. For example, on Ivanovka River shore, not far from Drozdovka Bay, we collected a specimen with sterile plants that were similar to gametophytes of the C. suecicum (leaves with slightly differentiated alar cells, elongate-rectangular incrassate cells in the lower part of leaf laminas, and mamillose excurrent nerves). By molecular data, it was associated with Oncophorus wahlenbergii (Table 1, #11). Nyholm (1987) wrote, that in habitus Cynodontium suecicum "may resemble Kiaeria blyttii" but "the latter is usually smaller and is easily recognized by its male inflorescences with several peri-gonial leaves". The inner perigonial leaves are wide, sheathing, suddenly narrowed to a short wide apiculus in Cynodontium suecicum vs. narrower, gradually tapering in Kiaeria blyttii.
In the Murmansk Region, C. suecicum is usually not very tall and is similar in height to C. tenellum. Sometimes it may be confused with the latter species, which can grow in adjacent or even in the same turf. In these cases, delimitation of them is difficult without preparing microscope slides. The main distinguishing features between these two species are flat leaf margins in the C. suecicum vs. recurved margins in the C. tenellum, nerve protruding from the leaf vs. apex-terminated nerve, and large cells of annulus
Fig. 3. Leaf lamina cells of Cynodontium suecicum. 1-3 — at the apex; 4, 5 — at the leaf middle, 6 — at the base; 7-9 — at the leaf angles; 1, 5-7 — from KPABG(M)#121111; 2-4, 8, 9 — from KPABG(M)#124246.
Scale bars: 100 |im.
Fig. 4. Cross sections of leaves at upper (1-3), middle (4-6) and lower (7, 8) parts in Cynodontium suecicum. 1 — from KPABG(M)#121111; 2-8 — from KPABG(M)#124246. Scale bar: 100 ^m.
(45-55 |im) vs. smaller cells (15-20 |im). The width of the upper leaf cells is not a reliable distinguishing characteristic.
Thus, we suggest, that C. suecicum can be considered as a species that originated from hybridization between C. tenellum and Kiaeria blyttii, but it has clear morphological differences and sufficient genetic stability.
Acknowledgments
We are grateful to the curator of the Herbarium of bryophytes of the Komarov Botanical Institute (LE) O. M. Afonina for providing of C. suecicum sample and to V. E. Fedosov for discussing the results.
Fig. 5. Annulus at the capsules before natural opening in Cynodontium suecicum [KPABG(M)#124246]. Scale bars: 50 |m.
This study was carried out in the framework of the State Research Program of the Polar-Alpine Botanical Garden and Institute of the KSC RAS (AAAA-A18-118050490088-0).
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Литература
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