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Taxonomic Reevaluation of Didymodon Nigrescens (Pottiaceae) in Japan

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Taxonomic Reevaluation of Didymodon Nigrescens (Pottiaceae) in Japan Hattoria 11: 61–75. 2020 Taxonomic reevaluation of Didymodon nigrescens (Pottiaceae) in Japan Yuya INOUE1, 2, Juan A. JIMÉNEZ3, Takumi SATO2, Hiromi TSUBOTA1 & Tomio YAMAGUCHI1 1 Program of Basic Biology, Graduate School of Integrated Sciences for Life, Hiroshima University, Kagamiyama 1–3–1, Higashihiroshima, Hiroshima 739–8526, Japan 2 Hattori Botanical Laboratory, Obi 6–1–26, Nichinan, Miyazaki 889–2535, Japan 3 Departamento de Biología Vegetal, Facultad de Biología, Universidad de Murcia, Campus de Espinardo 30100, Murcia, Spain Author for correspondence: Yuya INOUE, [email protected] Abstract Based on morphological investigation and molecular phylogenetic analysis, we find that the previous concept of Didymodon nigrescens (Mitt.) K.Saito sensu Saito in Japan includes D. nigrescens and D. subandreaeoides (Kindb.) R.H.Zander, the latter newly reported from Japan. Morphological and phylogenetic data from Japanese material clearly segregate these species from each other. In addition, Japanese D. nigrescens shows two groups, with morphological traits supporting the phylogeny, requiring further morpho-molecular evaluation based on broad sampling. Descriptions with analytical illustrations are provided based on Japanese material. Andreaea takakii Sakurai is proposed as a synonym of D. subandreaeoides. Introduction Didymodon nigrescens (Mitt.) K.Saito is a member of a group of Holarctic mosses whose range penetrates deeply into the tropics, including Central America and East Africa (Bednarek- Ochyra 2018). According to the monograph of Japanese Pottiaceae (Saito 1975), the species grows on calcareous rocks or cliffs in montane to subalpine zones, and was known from several localities from Central Honshu and Shikoku. Saito circumscribed the species by the following characters: (1) plants dark brown to blackish-green, (2) stems more or less branched, (3) basal cells of the leaves rhomboidal, sclerenchymatous near the costa, (4) seta moderately thick, strongly flattened when dry, and (5) perichaetial leaves about two times as long as the stem-leaves. The species was very variable and the extreme forms of variation superficially appear to be different species, based on Japanese and Chinese materials. In the course of floristic research in the Japanese Southern Alps in Central Honshu and Mt. Tsurugi in Shikoku, we collected several specimens of D. nigrescens (sensu Saito 1975) with variable morphological characters as discussed by Saito. After detailed morphological 61 and molecular investigation, using dried herbarium specimens, we found that his concept of D. nigrescens included two distinct species. One is D. nigrescens and the other D. subandreaeoides (Kindb.) R.H.Zander, the latter distributed in the Beringian part of Arctic Russia, northwestern North America, Central Europe, and also East Asia (e.g. Cao & Gao 1995; Kučera & Köckinger 2000), but has not been previously recognized for Japan. In the present paper, we newly report D. subandreaeoides from Japan and revised descriptions of these two species are provided based on Japanese material. The phylogenetic positions of the Japanese plants are inferred based on the nuclear ITS sequences with maximum likelihood and Bayesian inferences. Materials and Methods Morphological investigation The morphological investigation was made based on fresh samples included in the molecular phylogenetic analyses and additional dried herbarium specimens deposited in CBM, H, HIRO, KOCH, MAK, NUM, MUB, NICH, and S. Molecular phylogenetic analyses Nuclear internal transcribed spacers 1 and 2 including 5.8S (ITS) were selected for the present analyses. Total DNA was extracted from leaves or shoot tips following the method by Suzuki et al. (2013) or Doyle & Doyle (1987) with some minor modifications. At the first author’s laboratory, the conditions of PCR amplification followed Inoue & Tsubota (2014). Primers for PCR amplification and DNA sequencing followed Oguri et al. (2003). PCR products were purified by using NucleoSpin Gel and PCR Clean-up kit (Macherey-Nagel, Duren) following the manufacturer’s protocols. Purified PCR products were sequenced by Macrogen Japan (Kyoto, Japan). At the second author’s laboratory, the PCR amplification was performed in a 25 µl volume containing 1 µl Taq DNA Polymerase (1 U/µl; Biotools, Madrid, Spain), 2.5 µl of Mg2＋ buffer provided by the manufacturer, 2 µl of 2.5 mM dNTP mix, 1.5 µl of each primer (10 µM) and 1 µl of the DNA extract. Primers for PCR and sequencing followed Stech & Frahm (1999). PCR conditions were: 95°C for 4 min linked to 38 cycles at 94°C for 30 sec., 52°C for 30 sec., and 72°C for 1 min. with a final extension of 72°C for 10 min. After visualization of PCR products with 1.5% agarose gel, successful amplicons were purified using the GenElute PCR Clean-Up kit (Sigma-Aldrich, St. Louis, Missouri), and sequenced at Macrogen Spain (Madrid, Spain). Sequences obtained in the present study have been submitted to the DNA Data Bank of Japan (DDBJ), a member of the International Nucleotide Sequence Database Collaboration (INSDC). Based on the results by Werner et al. (2005) and Kučera & Ignatov (2015), we selected published sequences of subsect. Fuscobryum (R.H.Zander) Jan Kučera as ingroup, and a species of sect. Didymodon as outgroup, using D. rigidulus Hedw. A total of 25 ITS sequences were examined in the present analyses, as shown in Appendix. Sequences were aligned using the program MAFFT ver. 7.463 (Katoh & Standley 2013) with some manual adjustment on the sequence editor of MEGA ver. 7.0.21 (Kumar et al. 2016). Gaps were treated as missing data. Prior to the phylogenetic reconstruction, the 62 software ModelTest-NG (Darriba et al. 2019) was used to determine the appropriate substitution model for our data based on corrected Akaike information criterion (AICc: Sugiura 1978). Phylogenetic analyses were performed based on maximum likelihood (ML) and Bayesian inference (BI) methods. RAxML-NG ver. 0.9.0 (Kozlov et al. 2019) was used for ML analysis using the TIM3ef＋I＋G4 model with a rapid bootstrap analysis with 10,000 replicates. MrBayes ver. 3.2.7a (Ronquist et al. 2012) was used for BI using the SYM＋I＋G4 model with 10,000,000 generations, sampling trees every 1,000 generations. Convergence was assessed using Tracer ver. 1.7.1 (Rambaut et al. 2018). A 50% majority-rule consensus tree was calculated after the convergence of the chains and discarding 25% of the sampled trees as burn-in. Results & Discussion Molecular phylogeny The data matrix had a total length of 746 bp, of which 94 (13%) were variable, and 70 (74% of the variable sites) were parsimony-informative. No topological conflict was detected between ML and BI trees which differed only at poorly supported nodes. Figure 1 shows the ML tree with supporting values from bootstrap and Bayesian posterior probabilities (BP/PP). The monophyly of subsect. Fuscobryum was well supported (100/1.00), and each analyzed species formed moderately to well supported clades as shown by Kučera & Ignatov (2015). The generic circumscription of Didymodon was recently reevaluated based on the macroevolutionary analysis using morphological data, and the genus were segregated into seven genera: Aithobryum R.H.Zander, Didymodon s.str., Exobryum R.H.Zander, Fuscobryum R.H.Zander, Geheebia Schimp., Trichostomopsis Cardot and Vinealobryum R.H.Zander (Zander 2013, 2019). If this were followed, all ingroup species of the present study would be treated as the genus Fuscobryum: F. nigrescens (Mitt.) R.H.Zander, F. perobtusum (Broth.) R.H.Zander and F. subandreaeoides (Kindb.) R.H.Zander. However, there are still not available comprehensive molecular data for evaluating this proposed systematic rearrangement, and here we use Didymodon in the broad sense. The Japanese samples were resolved as separate D. nigrescens and D. subandreaeoides clades, supporting the notion that both species occur in Japan. In D. nigrescens, two subclades were confirmed: Bhutan–Japan (93/0.98) and Nepal–China–Japan–U.S.A. (80/1.00), and Japanese samples showed different morphotypes corresponding to these subclades as discussed below. In D. subandreaeoides, Japanese samples were resolved in one clade and sister to the Russian sample (-/0.92). Taxonomic treatment Based on our investigation, the following taxonomic treatment is presented. Descriptions are based on Japanese materials, and synonyms of each species include only basionyms and heterotypic synonyms described from Japan. 63 Figure 1. Maximum likelihood tree based on ITS sequences, depicted by RAxML-NG. Supporting values more than 50% obtained by RAxML-NG for bootstrap probabilities (BP) and MrBayes for Bayesian posterior probabilities (PP) are shown on each branch (BP/PP). The root is arbitrarily placed on the branch leading to D. rigidulus. (A) indicates plants with acute to narrowly acuminate leaf apex and not spurred costa (Figs. 2A–B, 2E; 3), and (B) with rounded-obtuse to obtusely acute leaf apex and weakly spurred costa (Figs. 2F; 4). 1. Didymodon nigrescens (Mitt.) K.Saito, J. Hattori Bot. Lab. 39: 510. 1975. Figs. 2–4 ≡Barbula nigrescens Mitt., J. Proc. Linn. Soc., Bot. 1: 36. 1859. ＝Andreaea kai-alpina Sakurai & Takaki, J. Jap. Bot. 29: 111. 2. 1954. Type: Japan. Honshu, Mt. Kitadake, 3,100 m elev., 8 Aug. 1953, Takaki 14439 in herb. Sakurai 35073 (holotype: MAK!), Takaki 14439 ex herb. Noguchi 71417 (isotype: NICH- 182424!) For further synonyms, see Saito (1975), Cao & Gao (1995), Allen (2002), Zander (2007), Aziz & Vohra (2008), and Zhao et al. (2018). 64 Figure 2. Didymodon nigrescens
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