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Article

Gottschelia (Gottscheliaceae, Marchantiophyta) in Indochina

by
Vadim A. Bakalin
1,*,
Anna A. Vilnet
2,
Ksenia G. Klimova
1,
Van Sinh Nguyen
3 and
Seung Se Choi
4,*
1
Laboratory of Cryptogamic Biota, Botanical Garden-Institute of the Far Eastern Branch of the Russian Academy of Sciences, Makovskogo Street 142, Vladivostok 690024, Russia
2
Polar-Alpine Botanical Garden-Institute of the Russian Academy of Sciences, Akademgorodok 18A, Apatity 184209, Russia
3
Institute of Ecology and Biological Resources, Graduate University of Science and Technology, Vietnam Academy of Science and Technology, Hanoi 10072, Vietnam
4
Team of National Ecosystem Survey, National Institute of Ecology, Keumgangro 1210, Seocheon 33657, Republic of Korea
*
Authors to whom correspondence should be addressed.
Plants 2024, 13(16), 2198; https://doi.org/10.3390/plants13162198
Submission received: 5 July 2024 / Revised: 30 July 2024 / Accepted: 5 August 2024 / Published: 8 August 2024
(This article belongs to the Section Plant Systematics, Taxonomy, Nomenclature and Classification)
Browse Figures
Versions Notes

Abstract

:
Gottschelia, collected for the first time in Indochina, inspired an attempt to review the genus phylogeny to identify a more precise position of Indochinese plants. The genetic distance between African and Asian populations of G. schizopleura sensu lato was confirmed. The two groups should be treated as different species. A new combination, G. microphylla comb. nov., has been proposed for Asian plants. Aside from molecular genetics, distinguishing this species from the presumable strictly African G. schizopleura is also possible by morphological characteristics, as well as by its distribution. At the same time, at least three groups are distinguished among Asian haplotypes of G. microphylla, each of which can be interpreted as a species or, at least, subspecies. A morphological description, intravital photographs of the general habitat, and details of the morphological structures are provided. The position of Gottschelia in the phylogenetic schema of Jungermanniales does not allow us to attribute it to any of the known families and forces us to describe a new family, Gottscheliaceae, which is phylogenetically somewhat related to the Chaetophyllopsidaceae re-evaluated here and very different from Gottscheliaceae morphologically.

1. Introduction

Gottschelia is a bispecific paleotropic genus of liverworts, described more than 55 years ago by Grolle [1]. It was initially annotated by Grolle [1] as being morphologically similar to Anastrophyllum, Hattoria, Herzogobryum, and Jamesoniella. Even from these genera, the first two of which belong in the modern interpretation [2] to Anastrophyllaceae, the third to Cephaloziellaceae s.l. (in the ‘superfamily’ concept, following [3]), and the fourth to Adelanthaceae, it is clear that the position of the genus in the general phylogeny is at least debatable. In one of the early molecular phylogenetic studies, Gottschelia schizopleura (based on a specimen from Reunion) was found to have affinity for the genus Lophonardia [4]. A further precise study by Feldberg et al. [5] suggested that African and Asian accessions of Gottschelia schizopleura are sisters to Chaetophyllopsis whiteleggei, which belongs to its own morphologically distinctive family, Chaetophyllopsidaceae, with only two genera, Chaetophyllopsis and Herzogianthus [6]. The latter family, based on molecular studies, has been suggested to be polyphyletic: Chaetophyllopsis whiteleggei is phylogenetically related to some genera of Scapaniaceae sensu lato, and Herzogianthus vaginatus is placed in its own phylum, branched below Ptilidiales [7]. Later, Gottschelia and Chaetophyllopsis were classified in the family Scapaniaceae [8], and Herzogianthus vaginatus was segregated in its own family, Herzogianthaceae, in the order Ptilidiales [9]. Subsequent phylogenetic relationships of Gottschelia schizopleura with Chaetophyllopsis whiteleggei were demonstrated by Pazak et al. [10], who treated Gottschelia schizopleura as a member of Scapaniaceae, and by Katagiri and Inoue [11], who treated it within the complex family Cephaloziellaceae s.l. [3]. The relation of Gottschelia to the genus Andrewsianthus was determined by Feldberg et al. [12], and that to the genus Anastrophyllopsis was determined by Shaw et al. [13] (both genera are currently treated as members of Cephaloziellaceae s.l.). Subsequently, the affinities of Gottschelia and Chaetophyllopsis for Andrewsianthus and Anastrophyllopsis were shown by Bakalin et al. [14]. Therefore, to date, Gottschelia does not belong to the family Scapaniaceae sensu stricto. However, its placement in clearly polyphyletic and morphologically heterogeneous Cephaloziellaceae (as was also mentioned by Vana et al. [3]) is artificial as well. The present account provides a new attempt to identify the phylogenetic position of Gottschelia within the scope of currently available material.
It is worth mentioning that the controversial morphology of Gottschelia led to the description of two more taxa (Gottschelia grollei and G. patoniae) within the genus, and after molecular comparison, these taxa were subsequently transferred to the genus Solenostoma [5]. Therefore, to date, Gottschelia is regarded as a bispecific genus (the only species are Gottschelia schizopleura and G. maxima) with a rather unclear family placement. The genus Gottschelia was not previously reported from Indochina, so when we discovered plants belonging to this genus at the northern tip of the Annamite Range (an axial structure stretching 1200 km sub-meridionally across almost the entire Indochina Peninsula), we became interested in identifying the specific identity of the collected plants and attempted to analyze the phylogenetic relationships of this genus. The new input to solving both problems is the main goal of the present account.

2. Results

Molecular Phylogenetic Reconstruction

The nucleotide sequences of rbcL, trnL-F, and trnG-intron and the separately assembled ITS1 and ITS2 sequences were obtained for each of three tested Vietnamese Gottschelia specimens and deposited into GenBank, as well as the ITS2 sequence for Gottschelia schizopleura from Tanzania (#68). The produced and phylogenetically tested alignment of combined rbcL and trnL-F nucleotide sequence data included accessions from 59 specimens. The dataset includes 1830 positions, among which 1124 positions belong to rbcL and 706 to trnL-F. The arithmetic mean of log likelihood in the ML calculation was −17,028.831, and in the two runs of the BA analysis, the values were −16,789.51 and −16,791.55. The topologies from both estimations are congruent, and Figure 1 illustrates an ML tree with bootstrap support (BS) values from ML analyses and Bayesian posterior probabilities (PP) from BA. As expected, the constructed topology agreed with that previously obtained and did not contradict the commonly accepted leafy liverwort’s phylogeny [15].
The families combined into three lineages corresponding to three orders: Jungermanniales (clade A), Porellales (clade B), and Ptilidiales (clade C). Herzogianthus vaginatus was found in the clade Ptilidiales (C) but without support, which confirmed its segregation from Chaetophyllopsidaceae in the distinct family Herzogianthaceae in the order Ptilidiales [9]. Other taxa in focus were placed in the clade of the order Jungermanniales (A). The families Scapaniaceae, Anastrophyllaceae, and Obtusifoliaceae composed robustly supported clades (BS = 100% in ML and PP = 1.00 in BA or 100/1.00), and the clade of Lophoziaceae was supported by 97/0.94. The sister relation of Scapaniaceae and Lophoziaceae achieved the highest support at 100/1.00, whereas the affinity of Anastrophyllaceae with the recently described family Obtusifoliaceae received poor support only on ML estimation (70%). The position of Oleolophoziaceae was also poorly supported (70%). The family Cephaloziellaceae s.l. had clear polyphyly with four subsequently diverged linages. The first linage (99/-) was represented by the genus Cephaloziella, the second (99/-) by the genus Herzogobryum, the third (67/-) by the genus Nothogymnomitrion, and the fourth by sister-related clades (97/1.00) of the genera Andrewsianthus + Anastrophyllopsis (100/1.00) and Chaetophyllopsis + Gottschelia (98/1.00). The specimens of the genus Gottschelia (100/1.00) were distributed in two robustly supported subclades according to their geographical origin—Africa and Asia.
The nucleotide sequence divergence between the African and Asian subclades of the genus Gottschelia was 1.9–2.1% for rbcL (Table 1).
The specimens from Madagascar and Reunion were characterized by sequence identity, whereas in the Asian subclade, nucleotide sequences of rbcL varied by 0.3–0.9% between different localities. At the same time, all Vietnamese specimens possessed identity at all five sequenced loci, and the rbcL gene sequences of specimens from Malaysia and Sri Lanka were identical to those of specimens from Indonesia. The divergence in trnL-F (0.7%) was marked only between Vietnamese specimens and specimens from Malaysia (#36922). The divergence in trnG-intron between Vietnamese specimens and specimens from Reunion (#15883) was 6.0%. The difference in nuclear ITS2 between Vietnamese and Tanzanian (#68) specimens reached 11.0%.
The haplotype analysis of part of the rbcL gene revealed the presence of four haplotypes in the analyzed Gottschelia specimens (Figure 2). The Madagascar and Reunion specimens possessed a single haplotype. The Asian specimens were combined into three slightly diverged haplotypes that corresponded with geographical regions: Vietnam, Malaysia + Sri Lanka, and Indonesia. The distances between the African and three Asian haplotypes significantly exceeded the distances among the Asian haplotypes.
The p-distances calculated for the rbcL sequences of the specimens from the genus Gottschelia via ASAP analysis were divided into four groups, separated by three gaps (Figure 3). The two groups of p-distances that corresponded to the separation of African and Asian accessions were clearly different. The less pronounced segregation of p-distances from Asian accessions corresponded with lower sequence divergence within this geographical region.
Thus, Cephaloziellaceae, in its broad sense, suggested by Vana et al. [3], is polyphyletic (which also corresponds to previous papers), and its splitting into smaller entities is likely necessary to continue. Despite the fact that Chaetophyllopsis and Gottschelia are sisters among all of the variants of topologies, the morphological dissimilarity and high genetic distances did not allow a simple re-evaluation of Chaetophyllopsidaceae and embedding of Gottschelia. In contrast, we suggest the description of a new family for Gottschelia.
The second result of the analysis was the confirmed significant genetic distance between the African and Asian (in a broad sense, including Malesia and Melanesia) populations of Gottschelia schizopleura, which should be interpreted as different species. Moreover, within the Asian complex, there are at least three units that should be described as species; however, this is currently not possible due to limited data.

3. Discussion

3.1. Molecular-Genetic Estimations

Following the transfer of Gottschelia grollei and G. patoniae to Solenostoma s.l. by Feldberg et al. [5], the genus Gottschelia became bispecific, including G. maxima characterized by a crenulate leaf margin (and otherwise quite similar to G. schizopleura) and G. schizopleura sensu lato. The latter taxon was interpreted very broadly, as shown by our obtained results and as also noted by the authors of the mentioned paper [5]. Both studies noted high genetic dissimilarity between African and Asian–Melanesian populations. Feldberg et al. [5] (p. 249) wrote “The African and Asian accessions of G. schizopleura are separated [in phylogenetic trees] by long branches (Figure 2) [in l.c.], indicating a significant period of isolation of the respective populations”, and further, “The Madagascar and Reunion accessions of G. schizopleura are more robust than the accessions from Indonesia, Malaysia and Sri Lanka”.
The median age of Gottschelia origin was estimated to be 34.65 Ma by Laenen et al. [16]. These ages were similar for the genera Mylia (35.7 Ma), Liochlaena (32.54 Ma), and Hygrobiella (31.36 Ma) [16]. The sequence divergence between species of the genus Mylia was 4.1–6.0% for trnL-F [17], 0.7–0.9% for Liochlaena for trnL-F and 0.9–1.6% for trnG-intron [18], and 2.1–3.6% for Hygrobiella for trnL-F and 2.2–3.0% for trnG-intron [19]. The divergence between the Reunion and Vietnamese specimens from the trnG-intron was quite high (6.0%) and could be treated as an additional differentiated feature to recognize them as distinct species.

3.2. Taxonomy

Our Vietnamese materials were genetically clearly placed within the broadly Asian macro-clade and, therefore, one cannot avoid discussing the question of the taxonomic status of Asian populations here. We studied the morphology of several specimens from Asian populations and only one specimen from Africa (see the Specimens Examined Section). In addition, we used the morphological data provided by Mufeed and Manju [20]. Overall, the materials reviewed supported the observations of Feldberg et al. [5]. All plants from Asia + Melanesia were characterized by the following: (1) rigid plants, versus soft and relatively lax plants in Africa; (2) smaller sizes, reaching only 1.5 mm (although it should be noted that materials from Vietnam were much larger than other Asian materials, up to 2.5 mm-wide and approaching the size of the African specimen); (3) the leaf sizes in Asian materials varied within 1.0–1.4 × 1.0–1.6 mm, except for Vietnamese materials, where they were the same size as African ones: 1.35–1.75 × 1.5–2.0 mm; (4) leaf cells in the mid-leaf in Asian materials were shortly oblong and varied near 20–30 × 20–25 µm, versus usually sub-isodiametric, 25–33 µm in diameter, in the African population; (5) the size of the cells in the lower part of the leaf in both groups overlapped, but were more elongated in Asian populations, 30–47 × 20–30 µm, versus 30–50 × 24–30 µm in African populations; (6) the cuticle was shortly papillose (not striolate) in the African population, versus mostly papillose-striolate in Asian populations; (7) the most clear difference was observed in the shape of the perianth, which was fusiform in Asian populations (that is, gradually becoming wider and then gradually narrowing), while in African plants, the perianth was rather cylindrical, rather abruptly narrowed toward the mouth; (8) a significant difference was also observed in the comparative length of the thin-walled cell zone in the upper part of the perianth, which constituted up to 1/4 of the perianth length in the Asian populations and only about 1/15–1/20 in African populations; (9) cells in the lower quarter of the perianth were shorter and wider in the African population, 30–50 (60) × 28–35 µm, and nearly thin-walled without intermediate thickenings, versus 50–75 × 12–18 µm with nearly thin walls, but with numerous intermediate thickenings in Asian populations; (10) the leaf insertion line in African populations was laterally merely oblique, while it was clearly transverse in Asian populations.
According to the available data, the Vietnamese populations represented the largest “phases” of the Asian taxonomic entity, which differed from the African taxon in a number of the above-listed characters. Considering its genetic differences, this Asian taxon should be considered an independent species and should be named Gottschelia microphylla comb. nov., described as Jungermannia colorata var. microphylla by Nees [21]. At the same time, it is worth mentioning that the Asian group itself may also split into several species, taking into account the genetic distances between the subclades, and the Vietnamese populations may well deserve to be treated as separate species characterized by larger sizes of plants, leaves, and cells. Other regional populations may also be different taxa; if not species, then subspecies. For example, a specimen from Papua New Guinea (Sleumer & Vink 4316) does not show purple–brown pigmentation, which is characteristic of other specimens (noticeably, purple pigmentation was mentioned as a generic characteristic in the original description of Grolle) [1]. In this paper, we currently accepted the species status of Asian populations but did not identify Vietnamese plants as a separate taxon, which requires an extensive study of not only fresh material using molecular genetic methods but also a restudy of type materials of at least the following names: Jamesoniella fleisherii Steph., Anastrophyllum cucullifolium Steph., and A. integerrimum Steph., listed by Grolle in the list of synonyms of Gottschelia schizopleura. The status of Gottschelia maxima also remains unresolved. Our attempt to obtain the sequence of the specimen of the latter species failed, as in [5]. The morphology of plants in the studied specimen of G. maxima (see the Specimens Examined Section) in terms of the size of leaf cells and the papillose cuticle feature was quite close to that of the African plant Gottschelia schizopleura, but there were clear differences in the nature of the leaf margin.
Below, we present a description of Gottschelia microphylla based entirely on materials from Vietnam and provide new combination proposals. In future research, the ‘Asian’ clade of Gottschelia, named here as G. microphylla, could be split into narrower taxa, and then the name G. microphylla could not be applied to Vietnamese plants. To avoid the artificial mixture of morphological features, we did not provide a unified description based on Gottschelia materials collected in various parts of Asia.
Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi comb. nov.
Basionym: Jungermannia colorata var. microphylla Nees Enumeratio Plantarum Cryptogamicarum Javae 27. 1830.
Description (based on Vietnamese materials). Plants were rigid, erect to ascending, in loose pure patches or mixed with other liverworts, brown–purple to wine–brown, 2.0–2.5 mm-wide (to 3 mm near perichaetia), 20–30 mm-long, with older parts decaying. Rhizoids were not seen. Stem brown to blackish brown, nearly straight, and branching was seen only as ventral sub-floral innovation. Cross-section was suborbicular to slightly transversely ellipsoidal, with 3 (–4)-stratose well-defined cortex composed by cells 12–18 µm in diameter, with strongly thickened walls (walls were sometimes so strongly thickened that the cell lumen collapsed), visible middle lamina, and outer wall papillose-striolate to nearly smooth. Inward cells suddenly became thin-walled or with only slightly thickened walls, 15–25 µm in diameter, 5–6-gonal, with small concave trigones. Leaves were obliquely spreading, somewhat or distinctly turned dorsally, distinctly canaliculate with margins turned inward (incurved adaxially), loosely sheathing the stem in the lower third, inserted transversely, with insertion lines turned up to the apex, both in dorsal and ventral ends. Flattened in the slide, commonly torn or plicate, ovate to widely ovate-triangular, 1350–1750 × 1500–2000 µm. Mid-leaf cells were sub-isodiametric to shortly oblong, 25–30 × 22–25 µm, with angular, very large trigones, abruptly turning to thin walls. Trigones had well-perceptible middle lamina with small transverse lines (similar to small plasmodesmata), and the cuticle was loosely to distinctly papillose. Cells along the leaf margin in the lower part of the leaf had a strongly thickened external wall, subquadrate to rectangular (then elongated perpendicularly to the leaf margin), 12–20 × 12–25 µm. Other walls were thin, but with very large angular trigones with well-visible middle lamina, which seemed never or very rarely confluent. Cells along the margin in the upper part of the leaf were similar to those in the lower margin, ca. 20–25 µm in diameter, with trigones sometimes confluent, and the cuticle loosely papillose. Cells in the lower 1/4 of the leaf length were oblong, 30–47 × 20–30 µm, with trigones similar to the mid-leaf, and the cuticle scarcely papillose. Under-leaves were absent. Dioicous (male plants not seen). Female bracteole were absent. Female bracts were widely ovate-triangular, 2200–2300 × 2200–2750 µm, with a margin entirely or somewhat crispate, with a sometimes-discolored distal margin. Perigynium was absent. Perianth fusiform, 3.0–4.0 × 1.0–1.2 mm, pluriplicate, except the lower third, gradually narrowed to narrow, but not beaked mouth. Mouth denticulate along the margin. Perianth cells were thin-walled with small concave trigones in the upper 1/4 of its length, then became thin-walled with angular and noticeable large trigones, similar to leaves in the perianth middle, and then became strongly oblong in the lower 1/4 of the perianth length, 50–75 × 12–18 µm, with nearly thin walls, but with numerous intermediate thickenings. Perianth unistratose. Archegonia 15–20 per perichaetium (always unfertilized in our specimens; Figure 4, Figure 5 and Figure 6).
Specimens examined:
Gottschelia maxima Papua New Guinea, Morobe Province, Kaindi Mt. (estimated coordinates 7.33229° S, 146.68166° E), 3000 m a.s.l., montane rainforest, 19 June 1984, B. Theirs 3299 (VBGI), originally identified as G. crenata Grolle.
Gottschelia microphylla Vietnam, North Central Vietnam, Nghệ An Province, Kỳ Sơn District, Na Ngoi Commune, Annamite Range (19.22636° N 104.11698° E), 1826 m a.s.l., the road across evergreen forest on steep slope, open moist cliff along the stream, 8 June 2023, V.A. Bakalin & M.H. Nguyễn V-87-3-23 (VBGI, HN); ibid. V.A. Bakalin & M.H. Nguyễn V-87-8-23 (VBGI, HN); ibid. (19.22826° N 104.11379° E), 1871 m a.s.l., the road across evergreen forest on steep slope, open moist cliff, 8 June 2023, V.A. Bakalin & M.H. Nguyễn V-88-6-23 (VBGI, HN); ibid. partly shaded moist cliff., 8 June 2023, V.A. Bakalin & M.H. Nguyễn V-88-7-23, V-88-15-23 (VBGI, HN); ibid. (19.22950° N 104.10697° E), 1838 m a.s.l., the road across evergreen forest on steep slope, open moist cliff, 8 June 2023, V.A. Bakalin & M.H. Nguyễn V-90-1-23 (VBGI, HN); ibid. (19.23096° N 104.11337° E), 1779 m a.s.l., the road across evergreen forest, open moist clayish road cut, 10 June 2023, V.A. Bakalin & M.H. Nguyễn V-100-3-23 (VBGI, HN)/.
Gottschelia schizopleura MALAYSIA, Pahang State, Titiwangsa Range, Cameron Highlands, Batu Brinchang Mt. (Gunung Batu Brinchang) (estimated coordinates 4.52096° N, 101.38249° E), 1950 m a.s.l., roadside bank, 19 October 1967, N. Kitagawa NY: 14,737 (VBGI); ibid. Genting Highlands, Ulu Kali Mt. (Gunung Ulu Kali) (3.41667° N 101.78333° E), 1700 m a.s.l., on soil bank of roadside, 8 November 1999, M. Higuchi, No.1221 in Bryophyta Selecta Exsiccata. Fasc. XXIX, Higuchi (2008) (VBGI); ibid. Mt. Brinchang, near Brinchang (4.51667° N 101.36667° E), 1550 m a.s.l., on bare soil at roadside bank, 29 July 2007, M. Higuchi No. 1443 in Bryophyta Selecta Exsiccata. Fasc. XXXVIII, Higuchi (2017) (VBGI); Tanzania, Moshi District, Kilimanjaro Mts., north of the village of Kibosho (3.23333° S 37.31667° E), 1950 m a.s.l., degraded montane rainforest above Osaki Forest Station, with scattered Macaranga, Agauria, Ocotea, and Myrica, on roadcut surface, 19 October 1967, T. Pocs, J.S. Miala & P.P. Maragesi 90066/D, No. 68 in Bryophyta Africana Selecta Series III, Ochyra, Pocs (1992) (VBGI); Indonesia, Western New Guinea, Pegunungan Arfak Regency, Arfac Mt., Pegunungan Arfak Nature Reserve (estimated coordinates 1.156295° S, 133.97962° E), 3000 m a.s.l., 1962, Sleumer & Vink 4316 (VBGI).

3.3. Distribution and Ecology

The Asian–Australasian range of Gottschelia microphylla extends from South India and Sri Lanka through the Philippines, Malaysia, and Indonesia to the Moluccas and Papua New Guinea. The northernmost outpost of the species is in Taiwan [22]. Indochina is, therefore, considered the missing link in this list of regions, and the discovery of Gottschelia here should have been expected. This genus was discovered in Indochina in Vietnam on the Annamite Range, a little-studied system extending from the northern part of Laos and Vietnam (separating them) to almost the plain of the Mekong River in southern Vietnam.
The Annamite Range is widely known as the focus for the concentration of a unique and very rich flora and fauna in Indochina, in part due to its sub-meridional stretching, connecting the tropical rainforests of the southern tip of Indochina with the mountainous subtropical-temperature vegetation of the foothills of the Hengduan mountain system, including the Hoang Lien Son Range [23,24,25,26,27,28,29,30]. Little is known about the liverworts of the Annamite Range, although information has continued to accumulate in recent years, for example, due to efforts by Pocs et al. [31,32]. Bazzania asperrima Steph. was described from the Annamite Range in the past [33]. Gottschelia microphylla is another unique element of the Annamite Range biota, along with numerous other examples cited in the above literature sources.
As noted, when describing the genus [1], Gottschelia schizopleura s.l. grows mostly on bare soil and is found much less often on stones and tree trunks. The same habitat span was subsequently reported in the literature. All known locations of the species are restricted to the upper mountain belts. The species rarely descends even to rainforests at middle elevations. Apparently, the ecology of African Gottschelia schizopleura and Asian G. microphylla is similar, considering the studied specimens and literature data [1,20,22]. Interestingly, the northernmost record of G. microphylla in the world was made on the wet bark of a living tree in a mossy forest in Taiwan [22], but not on bare soil. All of our Vietnamese collections of the species were performed between 1779 and 1871 m a.s.l.; that is, in a rather narrow altitudinal range, not going lower (which is quite understandable, given that anthropogenically transformed habitats begin quite soon below), but not going higher either, although the altitudinal range in the study area extended to 2720 m a.s.l., as far as the top of Mt. Phu Xai Lai Leng, which we also studied. Moreover, most of the Vietnamese collections are associated with the open ground of anthropogenic origin (talus along roads), although the species is also found in the studied area on presumable granitic rocks along streams (but outside the zone of direct washing of flowing water). All collections were performed in open and temporarily moist, but likely often very dry places, so the xerophytic morphology of the species (papillose cuticle, large trigones in the leaf cells) appears very reasonable in this context. In terms of ecology, the species is somewhat reminiscent of Jackiella javanica and Plectocolea hasskarliana, which often grow together with Gottschelia microphylla in Vietnam, having not only a similar ecology but also a similar (albeit wider) range. Considering the neutral reaction of the sandstone rocks at the study site, the species can generally be characterized as a neutrophylous meso-xerophyte. The bioclimatic data (Table S1) showed the following: (1) a warm climate with an annual mean temperature of 16–17 °C, (2) seasonal temperature variation that is not strong and decreases to 12 °C in the coldest quarter but reaches 19–20 °C in the warmest quarter, (3) a distinct monsoon climate with strong precipitation variation across the year, with values of 260–270 mm in the wettest month and only 4–6 mm per driest month, and (4) a total amount of precipitation reaching 1800–1900 mm per year. A striking feature of the studied area is the high probability of sporadic snowfalls in winter. The referenced area (https://phapluatplus.vn/tuyet-phu-trang-o-chan-nui-phu-xai-lai-leng-12632.html (accessed on 22 June 2024)) shows the site slightly above the location where Gottschelia was collected. This phenomenon of snowfall at low altitudes far south of the Tropic of Cancer seems to be unique in Indochina.

3.4. The Position of Gottschelia within the Cephaloziellaceae–Scapaniaceae Superclade

Gottschelia specimens are rarely included in phylogenetic reconstructions, as reviewed in the Introduction. The first reliable phylogeny involving this genus was published by Feldberg et al. [5]. In the cited paper, Gottschelia has a sister position to Chaetophyllopsis, while Chaetophyllopsis first became involved in phylogenetic reconstructions by Hendry et al. [7], where it was also found in a sister position to Scapaniaceae s.l. The Chaetophyllopsis + Gottschelia pair is a remote sister to the Scapaniaceae s.l. superclade [5]. Based on the cited phylogeny, Váňa et al. [3] proposed that Scapaniaceae, Lophoziaceae, and Anastrophyllaceae should be considered in the traditional (=narrow) sense, while all genera ‘embedded’ between Scapaniaceae s.l. and Cephaloziellaceae s. str., including Chaetophyllopsis and Gottschelia, may be regarded as members of the ‘superfamily’ Cephaloziellaceae, which was distinctly polyphyletic in this case. The cited authors were fully aware that this position is partly artificial, and additional research is necessary to understand the system of the enormous clade of leafy liverworts Scapaniaceae s.l. + Cephaloziellaceae s.l. Later, a similar phylogeny was shown by Patzak et al. [10], but they interpreted it as distinctly different from that of Vana et al. [3] and treated Scapaniaceae in a very broad sense (then, it was graded to the ‘superfamily’) and maintained a narrower concept for Cephaloziellaceae.
We assume that both points of view are hardly convenient since either one or the other family (in this case, Scapaniaceae s.l. or Cephaloziellaceae s.l.) is also inconsistent in comparison with other accepted liverwort families. Our previous work described the small but genetically distinct families Obtusifoliaceae and Oleolophoziaceae [34,35]. This segregation process is clearly not complete, considering the large number of genera located between the finely defined clades, Cephaloziellaceae and Scapaniaceae–Lophoziaceae–Anastrophyllaceae, in known phylogenies. Since the assignment of Gottschelia to both Scapaniaceae and Cephaloziellaceae cannot be followed, it is necessary to find another family for this genus by restoring it from forgotten ones, if there are any, or by describing it as a new one.
Formally, the Gottschelia + Chaetophyllopsis clade has the name Chaetophyllopsidaceae for Chaetophyllopsis, and the simplest option is to restore the family Chaetophyllopsidaceae, which includes Gottschelia. However, this approach completely contradicts the morphology of both genera. It is difficult to imagine more morphologically dissimilar archetypes as Chaetophyllopsis and Gottschelia. Schuster [36] placed the isolated genus Herzogianthus morphologically close to Chaetophyllopsis (interpreted together with Chaetophyllopsis as representatives of the oligotypic Chaetophyllopsidaceae). Herzogianthus was later placed in its own family, Herzogianthaceae [9]. Both genera are characterized by leaf margins armed with stiff, hyaline, 1-celled setae (cilia), asymmetric succubous leaves and well-developed, basically bilobed under-leaves. Although there are several dissimilarities, e.g., in the presence of tetrahedrical 4–5-celled gemmae in Chaetophyllopsis (absent in Herzogianthus), leaves isomorphic, 3–4-lobed with some additional primary and several secondary lobes (versus leaves dimorphic, 3-lobed, without additional lobes and without secondary lobes), and rhizoids not confined to under-leaf bases (versus rhizoids confined to under-leaf bases). Several distinctions are also seen in the generative sphere, and they are perfectly described by Schuster [6]. Schuster [37] considered Chaetophyllopsis to be related to Ptilidiaceae and Lepidolaenaceae, but never expected the genus to be related to Scapaniaceae or something similar. In contrast, Gottschelia was suggested to be poorly related to Anastrophyllum [1]. Since Anastrophyllum in modern treatments belongs to the Scapaniaceae–Lophoziaceae–Anastrophyllaceae superclade, the suggestion by Grolle was relatively correct. Morphologically, Gottschelia and Chaetophyllopsis are strongly different in a number of features: unlobed versus lobed leaves (the same for female bracts) and absence versus the presence of under-leaves. However, some similarities may also be noted. They include the following: (1) brown to reddish-brown color of plants in both, (2) collenchymatous cell structure both in leaves and stem, (3) perianth fusiform with discolored mouth (although polystratose in the lower half in Chaetophyllopsis), and (4) 22 rows of outer cell walls in seta cross-section in both. Both genera also have stellate gemmae: unicellular in Gottschelia (not found in Vietnamese materials) versus 4-5-celled in Chaetophyllopsis. Chaetophyllopsis is an Australasian taxon, where the area of Gottschelia extends from Melanesia to the Southeast Asian mainland. Therefore, the two genera areas are somewhat in contact but not sympatric. Following the strong morphological dissimilarity below, we describe the new family to house Gottschelia.
Gottscheliaceae Bakalin, Vilnet, Klimova et S.S. Choi fam. nov.
Diagnosis. Plants were dioicous, rigid, and leaves were unlobed with entire or denticulate margin, concave-canaliculate, sheathing the stem at the base, and strongly interlocking dorsally. Under-leaves were absent. The cell network of leaves was pachydermous. Female bracteole were absent, and bracts were unlobed. Perigynium was absent. Perianth was fusiform, strongly exerted, pluriplicate near the mouth, and the upper part of the perianth was discolored, unistratose. Sub-floral innovation was present. Spores were verruculose. Elaters were bispiral. Gemmae were sometimes present, stellate, and unicellular.
Type genus: Gottschelia Grolle, J. Hattori Bot. Lab. 31: 13, 1968.
Included genera: The family is hitherto mono-generic.
The type species of the genus Gottschelia: Gottschelia schizopleura (Spruce) Grolle, J. Hattori Bot. Lab. 31: 16, 1968.
Basionym: Jungermannia schizopleura Spruce, Trans. & Proc. Bot. Soc. Edinburgh 15: 517, 1885.
The genus Gottschelia includes three species. Other included taxa are Gottschelia maxima (Steph.) Grolle and that evaluated above, Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova.

4. Materials and Methods

4.1. Materials and Nature Environment

The material used in this paper was collected during a survey of the northern end of the Annamite Range. The name Annam itself comes from the Vietnamese pronunciation of the Chinese ‘An Nan’, which has a literary meaning of ‘tranquil south’. This word was later used by the French during the colonial time of Vietnam, both to refer to the ridge and to the Vietnamese people in general. The Vietnamese themselves call the Annamite Range the Truong Son Range. This range, as noted above, has a sub-meridional strike of 1200 km and forms the orographic spine of all of Indochina. Administratively, the Annamite Range borders Laos and Cambodia from Vietnam. The highest point in the range is Mt. Phou Bia, which is located in Laos and reaches an altitude of 2819 m a.s.l. at its summit. The second highest mountain in the Annamite Range is Mt. Phu Xai Lai Leng, with a height of 2720 m a.s.l. This mountain is also located in the northern part of the range and is administratively divided in half between Laos and Vietnam. In Vietnam, it is administratively located in Vinh Province, which belongs to the North Central Vietnam group of provinces. This mountain was the object of our research in 2023, when Gottschelia was collected.
The Annamite Range is an ancient formation. The first and most powerful stage of uplift occurred during the Indonesian orogeny at the end of the Paleozoic–beginning of the Mesozoic era. At that time, a wide layer of marine sediments and underlying granitic intrusions were uplifted. At present, the study area consists of a few granite outcrops and mostly eroding sandstones dominating the mountains [30], while limestones are widespread at lower altitudes in the northern part of the Annam Range, but they are absent in the study area. The climate of the study area is a monsoon tropical climate associated with mountains, with annual precipitation varying between 2000 and 2500 mm per year [38]. The dominant type of vegetation is evergreen montane and highland forest on silicate rocks at 1000–3000 m a.s.l. Floristically, the study area belongs to the Northern Indochinese Floristic Province [30]. In phytogeographical terms, the northern part of the Annamite Range is interesting as an orographic route (or link) for mountain species common with the Sikang-Yunnan Floristic Province of the East Asian Floristic Region [39], sometimes treated as an East Asian Floristic Subkingdom or even kingdom [40] to the south, into subequatorial floras in southern Indochina.
The material for this work was collected during joint Russian–Vietnamese expeditions at the beginning of June 2023 to study the diversity of liverworts in the Annamite Range. When collecting specimens, geographic coordinates, altitude above sea level, type of vegetation community, and ecological habitat conditions, including moisture supply and illumination, were indicated. The specimens collected were studied at the Laboratory of Plant Ecology at the Institute of Ecology and Biological Resources of the Vietnam Academy of Science and Technology (Hanoi), where intravital Gottschelia photographs were taken using digital cameras mounted on Nikon SMZ800N and Olympus BX43 microscopes in the latter laboratory. During the initial study of the living material, some plants were stored in dry silica-gel-filled plastic zip lock bags for molecular genetic research. A detailed morphological description was subsequently compiled after the molecular genetic analysis.
Since the coordinates were known for all of our collected specimens in Vietnam, we obtained the bioclimates from WorldClim [41,42] (Table S1) for each point, which made it possible to compile the general climatic requirements for the obtained material. These data are listed in Table S1. To characterize each point, all 19 bioclimates were obtained, which could be determined with a maximum accuracy of 30″, and if the points were closer, then the parameters could be merged.

4.2. Molecular–Genetic Analysis

Three Vietnamese specimens morphologically identified as Gottschelia were included in the molecular phylogenetic estimation. The rbcL cpDNA was chosen as an appropriate molecular marker for the six sequenced accessions of Gottschelia schizopleura from [5], which were included in the current analysis. The trnL-F and trnG-intron were sequenced as additional markers to compare Vietnamese plants with specimens of Gottschelia from studies by Shaw et al. [13] and De Roo et al. [4]. The ITS1-2 nrDNA region was first sequenced in this study for specimens of Gottschelia schizopleura from Tanzania and three Vietnamese specimens to reveal the diversity in nuclear markers. The specimen vouchers and GenBank accession numbers for the specimens of Gottschelia sequenced in this study are listed in Table 2. For estimation, the accessions with different genetic regions of nine specimens of Gottschelia schizopleura were downloaded from GenBank. The unresolved relationship and questionable taxonomic position of the genus Gottschelia inspired us to analyze several key genera of Cephaloziellaceae s.l. previously estimated separately in different studies: Chaetophyllopsis, Andrewsianthus, Anastrophyllopsis, Herzogobryum, and Nothogymnomitrion. The dataset covered three orders: Jungermanniales, Porellales, and Ptilidiales, and Verdoornia succulenta from Metzgeriales was chosen as an outgroup following the general phylogeny in [15]. Additionally, 48 specimens, including those from recently segregated Obtusifoliaceae and Oleolophoziaceae, were downloaded from GenBank, 45 of which contained nucleotide sequence data for the rbcL and trnL-F loci. The list of downloaded specimens included in the molecular estimations with voucher details and GenBank accession numbers is provided in Table 3.

4.3. DNA Isolation, Amplification, and Sequencing

After being collected for molecular procedures, the liverwort plants were dried in silica gel. DNA was extracted with a DNeasy Plant Mini Kit (QIAGEN (Hilden, Germany)) following the manufacturer’s protocol. The pairs of primers suggested by Kress and Erickson [43] for rbcL, by Taberlet et al. [44] for trnL-F, by Shaw et al. [45] for trnG-intron, and by White et al. [46] for ITS1-2 were used for amplification and sequencing. PCR was carried out in 20 μL volumes with the following procedure: 3 min at 94 °C, 30 cycles (30 s at 94 °C, 40 s at 52 °C for rbcL, 56 °C for trnL-F and ITS1-2, 64 °C for trnG-intron, and 60 s at 72 °C), and 2 min for a final extension at 72 °C. The obtained amplicons were visualized on 1% agarose TAE gels by EthBr staining. Then, they were cleaned from agarose with a Cleanup Mini Kit (Evrogen, Moscow, Russia) and sequenced with an ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, Waltham, MA, USA) following the standard protocol provided for the 3730 DNA Analyzer (Applied Biosystems, Waltham, MA, USA) at the Genome Center of EIMB (Moscow, Russia).

4.4. Phylogenetic Analysis

The program BioEdit 7.0.1 [47] was used for sequence assembly and dataset alignment. The alignments of the rbcL and trnL-F datasets were automatically produced with the ClustalW tool and subsequently manually corrected. Preliminary estimations revealed a lack of incongruence from both DNA regions, and then rbcL and trnL-F were combined into a single dataset for subsequent analysis, with inclusion in the estimation of all positions and coding absent fragments as missing. Phylogeny was tested by maximum likelihood (ML) analyses with IQTree 1.6.12 [48] and the Bayesian approach with MrBayes v. 3.2.1 [49]. ModelFinder [50] selected TIM2 + F + I + G4 as the best-fit evolutionary model of nucleotide substitutions. The ultrafast bootstrapping procedure [51] included 1000 iterations. The ML tree topologies were visualized in NJplot [52]. The Bayesian calculation was run with the GTR + I+G model, as recommended by the developers of the program, with four rate categories of gamma distributions. Chains of two independent runs of the Metropolis-coupled ΜCMC were run for one million generations, and trees were sampled every 100th generation. The first 2500 trees in each run were discarded as burn-in, and 15,000 trees were sampled from both runs. The average standard deviation of the split frequencies between the two runs was 0.006454, and Bayesian posterior probabilities were calculated from the trees sampled after burn-in. The BA tree topologies were redrawn in FigTree v1.3.1 [53]. The level of nucleotide sequence variability among specimens of the genus Gottschelia from different geographical localities was estimated as average pairwise p-distances using the pairwise deletion option for counting gaps in Mega 11 [54]. The distribution of pairwise p-distances between rbcL sequences of the genus Gottschelia was determined by the ASAP program [55], with default settings and a p-distance model. The haplotype diversity of the genus Gottschelia was estimated in the TCS program [56] based on an analysis of rbcL alignment with a length of 451 base pairs common to all specimens.

5. Conclusions

As the present study showed, the genus Gottschelia was found in Indochina. This finding, considering the general distribution pattern of the genus, was quite expected. However, it did not concern the species name for the Vietnamese material, which is unclear. When considering the taxonomic position of the plants collected in Vietnam, it confirmed the earlier estimated high genetic and morphological differentiation of African and Asian+Papuasian plants, previously referred to as the same species (G. schizopleura). It was clearly shown that Asian plants cannot belong to the same species as African plants. Here, we were forced to search for a name for this taxon, which was carried out using a new combination of a previously existing name. However, this solution is somewhat preliminary, since the issue of genetic and, most importantly, morphological disunity between population groups in Asia, in the broad sense, and Melanesia remains unresolved. This issue must be left until more copious material collected in different areas of Asia appears, which would be studied by different methods, including the study of oil bodies in leaf cells. As it turned out over the course of the study, the genus Gottschelia could not be reliably assigned to any of the described families, and we proposed a new family to place this genus in the Cephaloziellaceae + Scapaniaceae macro-clade.
The geographical approach, widely used to describe the new-to-science species in the second half of the 19th and early 20th centuries, was undeservedly criticized in the middle of the 20th century. Since then, there has been a belief that liverworts have very wide species ranges. However, with the development of molecular genetic methods, it became necessary to admit that the use of a geographical approach in the taxonomy of liverworts is at times quite justified. The present account supports the effectiveness of the geographical approach, in which African populations represent one species and Asian populations represent another. There are many examples of species with admitted paleotropical ranges spanning from Africa to Melanesia. At the same time, it is not always reliably known whether this is actually one species or several. Further work on the interaction of genetic variability with geography will improve the understanding (and significance in general phytogeography) of a group of taxa with presumable paleotropical ranges.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants13162198/s1, Table S1: Bioclimatic data obtained for Gottschelia specimens collected in Vietnam.

Author Contributions

Conceptualization, V.A.B. and A.A.V.; methodology, A.A.V. and K.G.K.; software, A.A.V. and K.G.K.; validation, V.A.B., A.A.V. and S.S.C.; formal analysis, V.A.B., A.A.V. and K.G.K.; investigation, V.A.B., A.A.V., K.G.K. and V.S.N.; resources, A.A.V. and V.A.B.; data curation, A.A.V., K.G.K. and S.S.C.; writing—original draft preparation, V.A.B., A.A.V., K.G.K., V.S.N. and S.S.C.; writing—review and editing, V.A.B., A.A.V. and K.G.K.; visualization, A.A.V. and K.G.K.; supervision, V.A.B. and S.S.C.; project administration, V.A.B. and S.S.C.; funding acquisition, V.A.B., A.A.V., V.S.N. and S.S.C. All authors have read and agreed to the published version of the manuscript.

Funding

The studies of V.A.B. and K.G.K. were performed in the framework of the Botanical Garden Institute research project, “Bryophytes and lichens of Pacific Asia: taxonomy, floristic composition, patterns of species distribution” (No. 122040800088-5). The work of V.S.N. was supported by the Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology (Grant No. IEBR ĐT.5-24). The work of S.S.C. was partially supported by a grant from the National Eco-System Survey of the National Institute of Ecology (NIE-A-2023-01).

Data Availability Statement

All data are contained within the article and Supplementary Materials.

Acknowledgments

The authors are sincerely grateful to Matvey Bakalin for preparing line drawings of Gottschelia microphylla.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The phylogram for the Jungermanniidae obtained from the maximum likelihood approach based on rbcL + trnL-F cpDNA. Bootstrap support values and posterior probabilities more than 50% (0.50) are indicated. The branches stretched from nodes with 100% bootstrap support values and 1.00 posterior probabilities are in bold. A—order Jungermanniales, B—order Porellales, and C—order Ptilidiales.
Figure 1. The phylogram for the Jungermanniidae obtained from the maximum likelihood approach based on rbcL + trnL-F cpDNA. Bootstrap support values and posterior probabilities more than 50% (0.50) are indicated. The branches stretched from nodes with 100% bootstrap support values and 1.00 posterior probabilities are in bold. A—order Jungermanniales, B—order Porellales, and C—order Ptilidiales.
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Plants 13 02198 g002
Figure 2. Statistical parsimony network for the rbcL cpDNA (451 base pairs) for the genus Gottschelia. Solid points indicate missing haplotypes. The specimen vouchers, according to Table 2, are marked.
Figure 2. Statistical parsimony network for the rbcL cpDNA (451 base pairs) for the genus Gottschelia. Solid points indicate missing haplotypes. The specimen vouchers, according to Table 2, are marked.
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Plants 13 02198 g003
Figure 3. The distribution of pairwise p-distances between rbcL sequences (451 b.p.) of the genus Gottschelia specimens. Dist. Dt—distance value, and Nbr—number of runs.
Figure 3. The distribution of pairwise p-distances between rbcL sequences (451 b.p.) of the genus Gottschelia specimens. Dist. Dt—distance value, and Nbr—number of runs.
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Plants 13 02198 g004
Figure 4. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A) Perianthous shoot, dorsal view. (B) Part of shoot, dorsal view. (C) Part of shoot, ventral view. (D–I) Leaves, (J) perianth cross-section in its middle part, and (K,L) female bracts. Scales: a—2 mm for (A), b—2 mm for (B,C), c—1 mm for (D–I,K,L), and d—100 µm for (J). All from V-88-15-23 (VBGI, HN).
Figure 4. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A) Perianthous shoot, dorsal view. (B) Part of shoot, dorsal view. (C) Part of shoot, ventral view. (D–I) Leaves, (J) perianth cross-section in its middle part, and (K,L) female bracts. Scales: a—2 mm for (A), b—2 mm for (B,C), c—1 mm for (D–I,K,L), and d—100 µm for (J). All from V-88-15-23 (VBGI, HN).
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Plants 13 02198 g005
Figure 5. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A) Mat of Gottschelia microphylla covering rocks in natural conditions. (B) Mat with perianthous shoots in dry condition. (C) Shoots, dorsal view. (D) Fragment of perianthous shoot, dorsal view. (E) Perianthous shoots in a mat, dorsal view. Scales: 5 mm for (A,B) and 2 mm for (C–E). (B,D) From V-88-15-23, and (C,E) from V-88-7-23 (VBGI, NH).
Figure 5. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A) Mat of Gottschelia microphylla covering rocks in natural conditions. (B) Mat with perianthous shoots in dry condition. (C) Shoots, dorsal view. (D) Fragment of perianthous shoot, dorsal view. (E) Perianthous shoots in a mat, dorsal view. Scales: 5 mm for (A,B) and 2 mm for (C–E). (B,D) From V-88-15-23, and (C,E) from V-88-7-23 (VBGI, NH).
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Plants 13 02198 g006
Figure 6. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A–C) Leaves, curled up and torn under the slide. (D) Perianth mouth armature. (E) Perianth cells in lower part. (F) Stem cross-section, fragment. (G) Leaf cells along leaf margin. (H,I,L) Mid-leaf cells with oil bodies. (J) Papillose cuticle in lower part of the leaf. (K) Papillose cuticle in the mid-leaf. Scales: 1 mm for (A–C), 3 mm for (F), 100 µm for (D–K), and 50 µm for (L). (A–F,I–K) From V-88-15-23, and (G,H) from V-88-6-23 (VBGI, NH).
Figure 6. Gottschelia microphylla (Nees) Bakalin, Vilnet, Klimova et S.S. Choi: (A–C) Leaves, curled up and torn under the slide. (D) Perianth mouth armature. (E) Perianth cells in lower part. (F) Stem cross-section, fragment. (G) Leaf cells along leaf margin. (H,I,L) Mid-leaf cells with oil bodies. (J) Papillose cuticle in lower part of the leaf. (K) Papillose cuticle in the mid-leaf. Scales: 1 mm for (A–C), 3 mm for (F), 100 µm for (D–K), and 50 µm for (L). (A–F,I–K) From V-88-15-23, and (G,H) from V-88-6-23 (VBGI, NH).
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Table 1. The value of p-distances for specimens of the genus Gottschelia gathered in different geographical regions, %. “n/c”—Not calculated due to the presence of a single specimen, and “-”—Not calculated due to the absence of nucleotide sequence data.
Table 1. The value of p-distances for specimens of the genus Gottschelia gathered in different geographical regions, %. “n/c”—Not calculated due to the presence of a single specimen, and “-”—Not calculated due to the absence of nucleotide sequence data.
Geographical Origin of the Specimensp-Distances within
Region, rbcL/trnL-F/trnG-intron, ITS1, ITS2, %		p-Distances between Regions, rbcL/trnL-F/trnG-intron,
ITS1, ITS2, %
VietnamMalaysia–Sri LankaIndonesiaMadagascar–Reunion
Vietnam0.0/0.0/0.0/0.0/0.0
Malaysia–Sri Lanka0.0/n/c/-/-/-0.5/0.7/-
Indonesia0.0/-/-/-/-0.9/-/-0.3/-/-
Madagascar–Reunion0.0/-/n/c/-/-2.1/-/6.02.0/-/-1.9/-/-
Tanzania-/-/-/-/n/c-/-/-/-/11.0-/-/-/-/--/-/-/-/--/-/-/-/-
Table 2. The list of Gottschelia specimens sequenced in the current study with vouchers and GenBank accession numbers.
Table 2. The list of Gottschelia specimens sequenced in the current study with vouchers and GenBank accession numbers.
Specimen VoucherGenBank Accession Number
ITS1 nrDNAITS2 nrDNArbcL cpDNAtrnL-F cpDNAtrnG-intron cpDNA
Gottschelia microphylla Vietnam: Nghe An Prov., V. Bakalin & M.H. Nguyen, V-88-6-23, 206354 (VBGI)PP866642PP864427PP537608PP537614PP537611
Gottschelia microphylla Vietnam: Nghe An Prov., V. Bakalin & M.H. Nguyen, V-90-1-23, 206365 (VBGI)PP866643PP864428PP537609PP537615PP537612
Gottschelia microphylla Vietnam: Nghe An Prov., V. Bakalin & M.H. Nguyen, V-100-3-23, 206518 (VBGI)PP866644PP864429PP537610PP537616PP537613
Gottschelia schizopleura Tanzania, T. Pocs, J.S. Miala & P.P. Maragesi 90066/D No. 68 in BRYOPHYTA AFRICANA SELECTA Series III, Ochyra, Pocs (1992), 207901 (VBGI), 126285 (KPABG)no dataPP864430no datano datano data
Table 3. The list of specimens included in the molecular–phylogenetic analyses with voucher details and GenBank accession numbers.
Table 3. The list of specimens included in the molecular–phylogenetic analyses with voucher details and GenBank accession numbers.
TaxonSpecimen VoucherGenBank Accession Number
rbcL cpDNAtrnL-F/trnG-
intron cpDNA
Adelanthus bisetulusNew Zealand, Glenny 8858DQ026580DQ026614
Alobiellopsis dominicensisGuadeloupe: Basse Terre, Schaefer-Verwimp & Verwimp 22133 (M)KX098868KX098946
Anastrophyllopsis subcomplicataAustralia, D. Meagher & N. Klazenga 07-142 (F)KF943550KF942968
Anastrophyllum michauxiiUSA: North Carolina, M. Sargent s.n. (ABSH)AY507390AY507519
Andrewsianthus australisThailand, Schaefer-Verwimp & Verwimp 23734 (GOET)KC184706no data
Andrewsianthus perigonialisNew Zealand, J. Engel & M. von Konrat 27283 (GOET)KC184707no data
Calypogeia argutaJapan: Kagoshima, Yakushima Isl., N. Hayashida 743 (CBM)LC732076LC732078
Cephalozia hamatilobaMalaysia: Pahang, Schaefer-Verwimp & Verwimp 18559 (M)KX098890KX098968
Cephaloziella divaricataCzech Republic, P. Sova (DUKE)KF852399KJ802094
Cephaloziella hirtaAustralia, Streimann 59793 (NY)DQ439682KF943000
Chaetophyllopsis whiteleggeiAustralia, J. Curnow 4804 (F)KF852333AY463553
Cryptocolea imbricataNorway: Svalbard, A. Frisvoll 122667 (KPABG)OR604355OR604345
Eremonotus myriocarpusUnited Kingdom: Scotland, B. Buryova 165/93 (DUKE)KF852354KJ802082
Frullania longistipulaSao Tome and Principe: Sao Tome, Garcia 257,411 (LISU)KU310979KU310985
Gottschelia schizopleuraIndonesia, R. Gradstein 12065 (GOET)FJ984941no data
Gottschelia schizopleuraIndonesia, R. Gradstein 12064 (GOET)FJ984942no data
Gottschelia schizopleuraMalaysia: Pahang, D. Long 36922 (E)KF852362KJ802085
Gottschelia schizopleuraMalaysia, Schaefer-Verwimp 18695 (GOET)FJ984944no data
Gottschelia schizopleuraSri Lanka, Schaefer-Verwimp 5488/II (GOET)FJ984943no data
Gottschelia schizopleuraMadagascar, Ah-Peng R96 (GOET)FJ984940no data
Gottschelia schizopleuraReunion, Schaefer-Verwimp 19823 (GOET)FJ984938no data
Gottschelia schizopleuraReunion, Gradstein 12032 (GOET)FJ984939no data
Gottschelia schizopleuraReunion, T. Hedderson 15883 (BOL)no datano data/AM397736
Gymnocolea borealisRussia: West Siberian Arctic, Gydansky Peninsula, E. Troeva G1-138 (LE)MZ032229MZ353627
Gymnocolea fasciniferaUSA: Alaska, A. Potemkin, 92-9701 (LE)MZ298896MZ298895
Gymnomitrion concinnatumNorway: Svalbard, N. Konstantinova & A. Savchenko K158/8-07 (F)KF943557KF942980
Hattoria yakushimensisJapan: Kagoshima, Yakushima Island, T. Katagiri 4281 (NICH)LC376047LC376049
Herzogianthus vaginatusNew Zealand, Y. Qiu & J. Braggins NZ-03173 (AK)DQ787462no data
Herzogobryum vermiculareFrench Southern and Antarctic Lands: Iles Kerguelen, R. Ochyra 1011/06 (DUKE)KF943587KF943047
Jubula bogotensisMexico, R. Gradstein s.n.AY548100DQ987388
Jungermannia exsertifolia subsp. cordifoliaUSA: Alaska, B. Shaw F951/5 (DUKE)KF943592KF943051
Konstantinovia beringiiRussia: Kamchatka Terr., Commander Islands, Bering Isl., K. Klimova, Com-68-10-22 (VBGI)OR785039OR785035
Konstantinovia pulchraChina: Yunnan Prov., V. Bakalin & W.Z. Ma, C-77-2-18 (VBGI)OR785040MT476332
Lejeunea cocoesThailand, G. Lee 2496 (UKMB)ON646222ON646224
Lepidolaena clavigeraNew Zealand, Frahm 22-3 (GOET)EF545278EF545373
Liochlaena lanceolataRussia, 108000 (F)KF943558KF942981
Lophozia ventricosaFinland, 2003 He-Nygren & Piippo 1473AY462312AY463572
Marsupella sphacelataRussia, N. Konstantinova 29 June 2000 (F)KF943561KF942984
Mylia anomalaCanada: Alberta, D. Vitt s.n. (ABSH)KF852367KJ802088
Neotrichocolea bissetiiJapan, 1980 Inoue (5/03 200)AY462317AY463576
Nothogymnomitrion erosumAustralia, Streimann 53475 (JE), 1GQ900318GQ900216
Nothogymnomitrion erosumNew Zealand, J. Engel & M. von Konrat s.n. (F), 2KF852369KJ802089
Nowellia curvifoliaGermany: Bayern, Schaefer-Verwimp & Verwimp 28863 (M)KX098919KX099000
Obtusifolium obtusumSwitzerland: Canton of Valais, V. Bakalin, Sw-48-30-13 (VBGI)OR785041MT476337
Odontoschisma denudatumPortugal: Azores, Schaefer-Verwimp & Verwimp 29511 (M)KX098924KX099005
Oleolophozia perssoniiRussia: Magadan Prov., V. Bakalin, Mag-31-13-11 (VBGI)OR785042MT476335
Porella arboris-vitaePoland, J. Szweykowski 10429 (POZW)KR014902KR014871
Ptilidium pulcherrimumFinland, Ahonen Engblom 7 (H)AY302460AY251186
Scapania nemoreaUSA, Davis 124 (DUKE)AY608039AY608143
Scapania undulataFinland, 2000 He-Nygren & Piippo 1468AY149840AY149859
Schiffneria hyalinaJapan, 1992 Mizutani 15961AY462327AY463585
Solenostoma clavellatumButhan, D. Long 28,636 (E)KF943546KF942951
Southbya tophaceaRussia: Krasnodar Terr., N. Konstantinova & A. Savchenko K312-4-11, 122707 (KPABG)OR604354OR604344
Trilophozia quinquedentataFinland, 2003 He-Nygren & Piippo 1474AY462334AY463592
Verdoornia succulentaNew Zealand, Stotler & Crandall-Stotler 4602 (ABSH)AY507430AY507561
Vietnamiella epiphyticaVietnam: Lao Cai Prov., V. Bakalin & K. Klimova V-9-7-17 (VBGI, KPABG)MK290986MK290984
Wettsteinia inversaIndonesia, Gradstein 11014 (GOET)FJ984935GQ900275
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Bakalin, V.A.; Vilnet, A.A.; Klimova, K.G.; Nguyen, V.S.; Choi, S.S. Gottschelia (Gottscheliaceae, Marchantiophyta) in Indochina. Plants 2024, 13, 2198. https://doi.org/10.3390/plants13162198

AMA Style

Bakalin VA, Vilnet AA, Klimova KG, Nguyen VS, Choi SS. Gottschelia (Gottscheliaceae, Marchantiophyta) in Indochina. Plants. 2024; 13(16):2198. https://doi.org/10.3390/plants13162198

Chicago/Turabian Style

Bakalin, Vadim A., Anna A. Vilnet, Ksenia G. Klimova, Van Sinh Nguyen, and Seung Se Choi. 2024. "Gottschelia (Gottscheliaceae, Marchantiophyta) in Indochina" Plants 13, no. 16: 2198. https://doi.org/10.3390/plants13162198

APA Style

Bakalin, V. A., Vilnet, A. A., Klimova, K. G., Nguyen, V. S., & Choi, S. S. (2024). Gottschelia (Gottscheliaceae, Marchantiophyta) in Indochina. Plants, 13(16), 2198. https://doi.org/10.3390/plants13162198

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