A New Lichenized Fungus, Lendemeriella luteoaurantia, with a Key to the Species of Lendemeriella

Abstract

Lendemeriella luteoaurantia B.G. Lee is described as a new lichen species from South Korea. The new species is identified by smaller, yellow-orange apothecia, larger ascospores with wider septum width, and the absence of Cinereorufa-green pigment and teloschistin, different from the closest species, L. aureopruinosa I.V. Frolov, Vondrák, Arup, Konoreva, S. Chesnokov, Yakovczenko and Davydov in morphology and chemistry. Molecular phylogeny employing internal transcribed spacer (nuITS), nuclear large subunit ribosomal RNA (nuLSU), and mitochondrial small subunit (mtSSU) sequences strongly supports the new species as nonidentical in the genus Lendemeriella. A preliminary key is provided to assist in the identification of all 10 species of Lendemeriella.

1. Introduction

The genus Lendemeriella S.Y. Kondr., previously the ‘Caloplaca’ exsecuta group, was defined recently from the mother genus Caloplaca Th. Fr. [1,2]. Lendemeriella is characterized by biatorine apothecia containing anthraquinones, i.e., chemosyndrome A such as parietin (major), emodin (minor), and traces of emodinal, emodic acid, parietinic acid, and fallacinal, golden brown episamma, ascospore septum width >3.5 μm, bacilliform pycnoconidia, Cinereorufa-green pigment in thallus or apothecia, and distribution in arctic-alpine to boreal-montane areas [1,2,3].

Lendemeriella is a genus in the subfamily Caloplacoideae and can be confused with similar genera in the subfamily, i.e., Bryoplaca Søchting, Frödén and Arup, Olegblumia S.Y. Kondr., Lőkös and Hur, Rufoplaca Arup, Søchting and Frödén, and Pyrenodesmia A. Massal. Vondrák et al. mentioned the similarity of Lendemeriella, Bryoplaca, and Parvoplaca Arup, Søchting and Frödén in the aspect of their habitat preference to humid alpine areas [1]. However, Lendemeriella differs from Bryoplaca by substrate preference mainly for rock or bark, biatorine apothecia, and the presence of parietin. Parvoplaca is easily distinguishable from Lendemeriella as the genus inhabits moss, plant debris, or bark with a poorly developed thallus and belongs to the subfamily Xanthorioideae [4]. Kondratyuk et al. compared Olegblumia as the most closely related genus to Lendemeriella in the introduction of Lendemeriella [2]. However, Lendemeriella quite differs from Olegblumia by the crustose thallus without lobes, the presence of the chemosyndrome A, and the narrow distribution limited to arctic-alpine and boreal-montane areas. Frolov et al. compared Lendemeriella with Rufoplaca because they have similar ecology [3]. However, Lendemeriella differs from Rufoplaca by an ascospore septum width of over 3.5 μm and the presence of episamma (the minute granules in epithecium). Pyrenodesmia, previously the Caloplaca xerica group, can be compared with Lendemeriella. The C. xerica group is similar to Rufoplaca, and Pyrenodemia s. lat. previously included Olegblumia, i.e., O. demissa (Flot. ex Körb.) S.Y. Kondr., Lőkös, Jung Kim, A.S. Kondr., S.O. Oh and Hur [3,4]. However, Lendemeriella differs from Pyrenodesmia by biatorine apothecia with an orange pigment other than Sedifolia-grey, bacilliform pycnoconidia, and the presence of the chemosyndrome A [4].

Lendemeriella comprised nine species. Eight species were transferred from Caloplaca, i.e., L. borealis (Vain.) S.Y. Kondr., L. dakotensis (Wetmore) S.Y. Kondr., L. exsecuta (Nyl.) S.Y. Kondr., L. lucifuga (G. Thor) S.Y. Kondr., L. nivalis (Körb.) S.Y. Kondr., L. reptans (Lendemer and B.P. Hodk.) S.Y. Kondr., L. sorocarpa (Vain.) S.Y. Kondr., and L. tornoensis (H. Magn.) S.Y. Kondr. [2]. An additional new species, L. aureopruinosa, was added by Frolov et al. [3]. Frolov et al. also suggested Caloplaca lacinulata (Hue) Zahlbr. and C. hexaspora (Hue) T. Okamoto as probable species for Lendemeriella [3].

This study describes an additional new species of the genus. Field surveys of the lichen biodiversity in the main mountains of Korea, i.e., Baekdudaegan, were carried out during the summer of 2022, and 24 specimens in Lendemeriella were collected on a shaded scree of a valley and the summit of a mountain (Figure 1). The specimens were comprehensively analyzed and did not correspond to any previously known species. We describe them as a new species, Lendemeriella luteoaurantia, also providing a preliminary key for all Lendemeriella species.

2. Materials and Methods

2.1. Morphological and Chemical Analyses

Hand sections were prepared manually with a razor blade under a stereomicroscope (Leica LED2500; Leica, Wetzlar, Germany), scrutinized under a compound microscope (Nikon Eclipse E400; Nikon, Tokyo, Japan), and photographed using a software program (NIS-Elements D; Nikon, Tokyo, Japan) and a DS-Fi3 camera (Nikon, Tokyo, Japan) mounted on a Nikon Eclipse Ni-U microscope (Nikon, Tokyo, Japan). The ascospores were examined at 1000× magnification in water. The length and width of the ascospores were measured and the range of spore sizes was shown with average, standard deviation (SD), length-to-width ratio, and number of measured spores. Thin-layer chromatography (TLC) was performed using solvent systems A and C according to standard methods [5]. The specimens are used in the herbarium of the Baekdudaegan National Arboretum (KBA), South Korea.

2.2. Isolation, DNA Extraction, Amplification, and Sequencing

Hand-cut sections of 10 to 20 ascomata per collected specimen were prepared for DNA isolation and DNA was extracted with a NucleoSpin Plant II Kit in line with the manufacturer’s instructions (Macherey-Nagel, Düren, Germany). PCR amplification for the internal transcribed spacer region (ITS1-5.8S-ITS2 rDNA) and the nuclear large subunit ribosomal RNA genes was achieved using Bioneer’s AccuPower PCR Premix (Bioneer, Daejeon, Republic of Korea) in 20 μL tubes with 16 μL of distilled water, 2 μL of DNA extracts, and 2 μL of primers ITS5 and ITS4 [6] or LR0R and LR5 [7]. The PCR thermal cycling parameters used were 95 °C (15 s), followed by 35 cycles of 95 °C (45 s), 54 °C (45 s), and 72 °C (1 min), and a final extension at 72 °C (7 min) based on Ekman [8]. The annealing temperature was changed by ±1 degree for a better result. PCR purification and DNA sequencing were carried out by the Macrogen genomic research company (Seoul, Republic of Korea).

2.3. Phylogenetic Analyses

All nuITS, nuLSU, and mtSSU sequences were aligned and edited manually using ClustalW in Bioedit V7.7.1 [9]. All missing and ambiguously aligned data and phylogenetically uninformative positions were removed and only phylogenetically informative regions were finally analyzed. The final alignment comprised 1265 (nuITS), 2102 (nuLSU), and 965 (mtSSU) columns. In them, variable regions were 265 (nuITS), 532 (nuLSU), and 305 (mtSSU). The phylogenetically informative regions were 734 (nuITS), 638 (nuLSU), and 307 (mtSSU). A concatenation was carried out for combining all nuITS, nuLSU, and mtSSU gene loci. They were manually combined for the informative regions. Four problematic sequences were removed when conflicting results occurred in the internal branches with the bootstrap values ≥ 70% and the posterior probabilities ≥ 95% in the concatenated tree. Phylogenetic trees with bootstrap values were obtained in RAxML GUI 2.0.6 [10] using the maximum likelihood method with a rapid bootstrap with 1000 bootstrap replications and GTR GAMMA (SYM + I + G4) for the substitution matrix as the best models produced by the model test in the software. The posterior probabilities were obtained in BEAST 2.7.4 [11] using the GTR 123141 model as the appropriate model of nucleotide substitution produced by the Bayesian model averaging methods with bModelTest [12], empirical base frequencies, gamma for the site heterogeneity model, four categories for gamma, and a 10,000,000 Markov chain Monte Carlo chain length with a 10,000-echo state screening and 1000 log parameters. Then, a consensus tree was constructed in TreeAnnotator 2.7.4 [11] with no discard of burnin, no posterior probability limit, a maximum clade credibility tree for the target tree type, and median node heights. All trees were displayed in FigTree 1.4.4 [13] and edited in Microsoft Paint. Overall analyses in the materials and methods were accomplished based on Lee and Hur [14].

3. Results and Discussion

3.1. Phylogenetic Analyses

The new species is positioned in the Lendemeriella-clade in the concatenated tree. The tree describes L. luteoaurantia, the new species, being nested with L. aureopruinosa, supported by a bootstrap value of 100 and a posterior probability of 1.00 for the branch (Figure 2). Although neighboring L. aureopruinosa, L. luteoaurantia is located in another branch distant from L. aureopruinosa. The new species is included in the subfamily Caloplacoideae and positioned closer to the genera Bryoplaca, Pyrenodesmia, Rufoplaca and Usnochroma Søchting, Arup and Frödén than other genera such as Caloplaca s. str., Leproplaca (Nyl.) Nyl., and Seirophora Poelt in the subfamily. This result on the phylogeny for Lendemeriella and closely related genera corresponds to Frolov et al. [3]. Their phylogeny also describes Lendemeriella neighboring with Pyrenodesmia, Rufoplaca, and Usnochroma, and other genera such as Caloplaca s. str., Leproplaca, and Seirophora are located in a different clade.

3.2. Taxonomy

3.2.1. Lendemeriella luteoaurantia B.G. Lee sp. nov. (Figure 3)

MycoBank: MB 848800

Type: South Korea, North Chungcheong Province, Youngdong, Yonghwa-myeon, Mt. Gakho, a shaded scree slope, 36°04′03.6′′ N, 127°50′52.6′′ E, 900 m alt., on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001116, with Aspicilia pseudovulcanica S.Y. Kondr., Lőkös and Hur, Caloplaca sp., Porpidia albocaerulescens (Wulfen) Hertel and Knoph (holotype: KBA-L-0004045!; GenBank OQ981387 for ITS, and OQ981383 for LSU).

Figure 3. Lendemeriella luteoaurantia (KBA-L-0004045, holotype) in morphology. (A–C) habitus and apothecia. Black prothallus (red arrows) shown in (A). (D,E) apothecia section showing proper margin only and algal layer present at the base of hypothecium. (F) pycnidia. (G–K) clavate asci. (L) polarilocular ascospores. (M) bacilliform pycnoconidia. Scale bars: (A) = 2 mm, (B,C) = 500 μm, (D) = 100 μm, (E,F) = 50 μm, (G–M) = 10 μm.

Figure 3. Lendemeriella luteoaurantia (KBA-L-0004045, holotype) in morphology. (A–C) habitus and apothecia. Black prothallus (red arrows) shown in (A). (D,E) apothecia section showing proper margin only and algal layer present at the base of hypothecium. (F) pycnidia. (G–K) clavate asci. (L) polarilocular ascospores. (M) bacilliform pycnoconidia. Scale bars: (A) = 2 mm, (B,C) = 500 μm, (D) = 100 μm, (E,F) = 50 μm, (G–M) = 10 μm.

Description: thallus saxicolous, crustose, generally continuous but discontinuous or isolated locally, rarely rimose, smooth to slightly rugose, rarely with local thickenings, thin, brown-gray to olive-gray, the margin determinate, 70–150 μm thick; cortex indistinct, up to 10 μm thick; medulla mainly indistinct because of domination of algal layer and substrate-originated large rock crystals dispersed on and below algal layer, up to 150 μm thick; photobiont coccoid, cells globose to subglobose, 5–15 μm thick, algal layer 60–100 μm thick. Small crystals present between algal cells, dissolving in K. Prothallus black, endosubstratal.

Apothecia numerous, scattered and not concentrated in center, solitary, rarely contiguous, emerging on the surface of thallus, adnate or sessile, slightly constricted at the base, 0.12–0.46 mm diam. (mean = 0.27; SD = 0.08; n = 108). Disc flat or slightly concave when young and flat or slightly convex when mature, with a yellow-orange pruina, yellow-orange to light orange or brownish yellow-orange, c. 200 μm thick; proper margin persistent, prominent, and wide when young and almost even and narrow when mature, entire or crenulate, concolorous with disc, more brownish laterally; thalline margin absent. Parathecium hyaline and brownish to periphery, 35–70 μm wide laterally with epinecral layer c. 10 μm. Epihymenium gold-brown, minutely granular (episamma), K+ wine red and episamma dissolving, 10–15 μm high. Hymenium hyaline, 50–70 μm high. Hypothecium hyaline or slightly yellowish, 70–120 μm high, with algal layer (up to 80 μm) at the base. Oil droplets absent. Paraphyses septate, simple, 1–1.5 μm wide, mainly simple or rarely branched at tips, tips not or slightly swollen, not pigmented, 1–2 μm wide. Asci clavate, 8-spored, 40–55 × 13–25 μm (mean = 50 × 17 μm; SD = 4.8 (L), 3.6 (W); n = 9). Ascospores ellipsoid to widely ellipsoid, 1-septate, polarilocular, permanently hyaline, 11–18 × 5–9.5 μm (mean = 14.7 × 7.6 μm; SD = 1.7 (L), 0.9 (W); L/W ratio 1.4–2.7, ratio mean = 2.0, ratio SD = 0.3; n = 106), septum width 4–6 μm (mean = 5; SD = 0.7; n = 26). Pycnidia dark brown to black, immersed at base and projecting with the upper 1/3, globose and sometimes widening, 135–210 μm high and 160–265 μm wide (SD = 32 (H), 49 (W); n = 5), with brownish wall, K–. Pycnoconidia hyaline, bacilliform, 2.7–4.2 × 0.8–1.4 μm (mean = 3.2 × 1.0 μm; SD = 0.2 (L), 0.1 (W); n = 50).

Chemistry: thallus K–, KC–, C–, Pd–. Apothecia K+ wine red. Epihymenium K+ wine red. Epihymenium and hymenium I+ blue. UV–. Parietin, parietinic acid, fallacinal and emodin were detected by TLC.

Distribution and ecology: The species occurs on siliceous rocks, mainly on the western scree slope shaded by deciduous trees (Acer pictum Thunb. var. mono (Maxim.) Maxim. ex Franch., Betula pendula Roth, Fraxinus mandshurica Rupr., F. rhynchophylla Hance, and Magnolia sieboldii K.Koch), herbs (Celastrus orbiculatus Thunb. and Urtica angustifolia Fisch. ex Hornem.), and a fern (Dryopteris crassirhizoma Nakai). The species is currently known from the shaded scree and the summit of Mt. Gakho (1176 m alt.), South Korea.

Etymology: the species epithet indicates the yellow-orange color of the apothecia.

Notes: the new species is similar to the saxicolous members of the genus, i.e., L. aureopruinosa, L. exsecuta, and L. reptans. However, the new species differs from L. aureopruinosa and L. exsecuta by pale, small apothecia, colorless hypothecium, little swollen tips of paraphyses, larger ascospores, and the absence of Cinereorufa-green pigment and teloschistin (Table 2).

The new species differs from L. reptans by the absence of soredia and thalline margin and the presence of emodin, fallacinal, parietin, and parietinic acid (Table 2).

Without regard to the substrate preference for rock, the new species is similar to the corticolous L. borealis in having yellow-orange and small (<0.5 mm diam.) apothecia, black prothallus, epihymenium with K+ red reaction, and the presence of emodin, fallacinal, parietin, and parietinic acid. However, the new species differs from L. borealis by darker and thicker thallus, higher hypothecium, larger ascospores with wider septum width, and the absence of teloschstin [15,16,17].

Caloplaca lacinulata is another comparable species that is a probable member of Lendemeriella and previously reported from South Korea [3,18]. However, the new species differs from C. lacinulata by continuous thallus, crystal-dominated medulla, presence of prothallus, smaller and paler apothecia, higher hypothecium, larger ascospores, larger pycnoconidia, and the absence of lacinules (vegetative propagules) [18,19].

Table 2. Comparison of the new species with closely related species in the genus Lendemeriella.

Species	Lendemeriella luteoaurantia	Lendemeriella aureopruinosa	Lendemeriella exsecuta	Lendemeriella reptans
Soredia	not observed	not observed	not observed	present
Apothecia color	yellow-orange to light orange	dark orange to orange-red	brown-yellow, orange-brown, or black	red-brown
Apothecia (mm in diam.)	0.1–0.4	0.3–0.6	0.2–0.7	immature
Thalline margin	absent	absent	absent	present (gray)
Hypothecium color	colorless to slightly yellowish	yellowish (upper), colorless (lower)	yellow to brown	–
Paraphysial tip width (μm)	1–2	3–4	1.5–4	–
Pigment in true exciple	not pigmented	Cinereorufa-green	Cinereorufa-green	–
Ascospores (μm)	11–18 × 5–9.5	11.5–15 × 6–7	12–16.5 × 6–7.5	–
Substance	emodin, parietin, parietinic acid, fallacinal	emodin, fallacinal parietin, parietinic acid, teloschistin	7-chloroemodin, emodin, fallacinal, fragilin, parietin, parietinic acid, teloschistin	no substance
Reference	KBA-L-0004040 (isotype), KBA-L-0004041 (isotype), KBA-L-0004045 (holotype), KBA-L-0004046 (isotype)	[3]	[20]	[21]

The morphological and ecological characteristics for the closely related species are referenced from the previous literature. All information on the new species is produced from selected types of specimens in this study.

Table 2. Comparison of the new species with closely related species in the genus Lendemeriella.

Species	Lendemeriella luteoaurantia	Lendemeriella aureopruinosa	Lendemeriella exsecuta	Lendemeriella reptans
Soredia	not observed	not observed	not observed	present
Apothecia color	yellow-orange to light orange	dark orange to orange-red	brown-yellow, orange-brown, or black	red-brown
Apothecia (mm in diam.)	0.1–0.4	0.3–0.6	0.2–0.7	immature
Thalline margin	absent	absent	absent	present (gray)
Hypothecium color	colorless to slightly yellowish	yellowish (upper), colorless (lower)	yellow to brown	–
Paraphysial tip width (μm)	1–2	3–4	1.5–4	–
Pigment in true exciple	not pigmented	Cinereorufa-green	Cinereorufa-green	–
Ascospores (μm)	11–18 × 5–9.5	11.5–15 × 6–7	12–16.5 × 6–7.5	–
Substance	emodin, parietin, parietinic acid, fallacinal	emodin, fallacinal parietin, parietinic acid, teloschistin	7-chloroemodin, emodin, fallacinal, fragilin, parietin, parietinic acid, teloschistin	no substance
Reference	KBA-L-0004040 (isotype), KBA-L-0004041 (isotype), KBA-L-0004045 (holotype), KBA-L-0004046 (isotype)	[3]	[20]	[21]

The morphological and ecological characteristics for the closely related species are referenced from the previous literature. All information on the new species is produced from selected types of specimens in this study.

Additional specimens examined: South Korea, North Chungcheong Province, Youngdong, Yonghwa-myeon, Mt. Gakho, a shaded scree slope, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001111, with Porina leptalea (Durieu and Mont.) A.L. Sm. (isotype: KBA-L-0004040; GenBank OQ981385 for ITS, and OQ981381 for LSU); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-00112, with Aspicilia asteria Hue (isotype: KBA-L-0004041; GenBank OQ981386 for ITS and OQ981382 for LSU); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001114, with Caloplaca sp., Circinaria caesiocinerea (Nyl. ex Malbr.) A. Nordin, Savić and Tibell, Porina leptalea (isotype: KBA-L-0004043); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001115, with Aspicilia pseudovulcanica, Porpidia albocaerulescens (isotype: KBA-L-0004044); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001117, with Circinaria caesiocinerea, Porpidia albocaerulescens (isotype: KBA-L-0004046; GenBank OQ981388 for ITS and OQ981384 for LSU); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001119, with Aspicilia pseudovulcanica, Caloplaca sp., Lepraria sp. (isotype: KBA-L-0004048); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001122, with Aspicilia pseudovulcanica, Circinaria caesiocinerea, Porina leptalea (isotype: KBA-L-0004051); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001123 with Aspicilia sp., Porina leptalea (isotype: KBA-L-0004052); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001125, with Aspicilia pseudovulcanica, Porina leptalea, Rimularia geumodoensis (S.Y. Kondr., Lőkös and Hur) S.Y. Kondr., Lőkös, and Hur (isotype: KBA-L-0004054); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001129, with Caloplaca sp., Porpidia albocaerulescens, Pseudosagedia guentheri (Flot.) Hafellner and Kalb (isotype: KBA-L-0004058); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001137, with Aspicilia pseudovulcanica, Circinaria caesiocinerea, Porina leptalea (isotype: KBA-L-0004066); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001142, with Aspicilia pseudovulcanica, Porina leptalea (isotype: KBA-L-0004071); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001143, with Gyalolechia flavovirescens (Wulfen) Søchting, Frödén and Arup, Porina leptalea, Pseudosagedia guentheri, Rimularia geumodoensis, Verrucaria sp. (isotype: KBA-L-0004072); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001144, with Aspicilia pseudovulcanica, Caloplaca sp., Circinaria caesiocinerea, Porina leptalea, Rimularia geumodoensis (isotype: KBA-L-0004073); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001150, with Circinaria caesiocinerea, Ionaspis lacustris (With.) Lutzoni (isotype: KBA-L-0004079); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001151, with Aspicilia asteria, A. pseudovulcanica, Ionaspis lacustris, Porpidia albocaerulescens, Rimularia geumodoensis (isotype: KBA-L-0004080); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001152, with Caloplaca sp. (isotype: KBA-L-0004081); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001153, with Aspicilia pseudovulcanica, Caloplaca sp., Circinaria caesiocinerea, Pseudosagedia guentheri (isotype: KBA-L-0004082); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001154, with Porina leptalea, Rinodina oxydata (A. Massal.) A. Massal. (isotype: KBA-L-0004083); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001155, with Circinaria caesiocinerea, Gyalolechia flavovirescens, Porina leptalea (isotype: KBA-L-0004084); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001157, with Aspicilia pseudovulcanica, Circinaria caesiocinerea (isotype: KBA-L-0004086); same locality, on siliceous rock, 16 June 2022, B.G. Lee and J.M. Kim 2022-001158, with Circinaria caesiocinerea, Gyalolechia flavovirescens, Rinodina oxydata (isotype: KBA-L-0004087); South Korea, North Chungcheong Province, Youngdong, Yonghwa-myeon, Mt. Gakho (summit), 36°03′45.1′′ N, 127°50′46.4′′ E, 1176 m alt., on siliceous rock, 24 May 2022, B.G. Lee and H.W. Kim 2022-000173 with Acarospora badiofusca (Nyl.) Th. Fr., Aspicilia subgoettweigensis S.Y. Kondr., Lőkös and Hur, Buellia sp., Lecanora saxigena Lendemer and R.C. Harris, Micarea aff. peliocarpa (Anzi) Coppins and R. Sant., Scoliciosporum umbrinum (Ach.) Lojka (paratype: KBA-L-0003102).

3.2.2. Key to the Species of Lendemeriella (Table 3)

The key includes all 10 species in Lendemeriella. The genus Lendemeriella was defined by Kondratyuk et al. [2] with eight new combinations. Among them, L. dakotensis is doubtful for the genus, and the species was not supported with any proof for the new combination. The species differs from other Lendemeriella species by subsquamulose and lobed thallus, absence of proper margin in the apothecia, and no secondary metabolites, as well as no reaction to spot test. Lendemeriella dakotensis may not be in Lendemeriella at last but is included in the key at present.

Table 3. Key to the species of Lendemeriella.

1.	On rock or moss on rock	2
–	On bark	7
2.	Directly on rock	3
–	On moss	6
3.	Soredia present; apothecia immature; thalline margin gray; no substance	L. reptans
–	Soredia absent; apothecia developed; proper margin present only; emodin, fallacinal, parietin, parietinic acid present or other substance present	4
4.	Apothecia yellow-orange to light orange, less than 0.5 mm diam.; hypothecium entirely colorless; tips of paraphyses little swollen; ascospores 11–18 × 5–9.5 μm; Cinereorufa-green pigment absent; teloschistin absent	L. luteoaurantia
–	Apothecia brown-yellow, red-brown to black, 0.5–0.6 mm diam.; hypothecium yellowish to brownish; tips of paraphyses swollen; ascospores 12–17 × 6–7.5 μm; Cinereorufa-green pigment present in true exciple; teloschistin present	5
5.	Apothecia brownish or entirely black; 7-chloroemodin and fragilin present; arctic-alpine	L. exsecuta
–	Apothecia reddish; 7-chloroemodin and fragilin absent; boreal-montane	L. aureopruinosa
6.	On Racomitrium; thalline margin pale to dark gray; ascospores 25–30 × 3–5 μm; distributed in mid to high latitudes	L. nivalis
–	On Andreaea or Grimmia; thalline margin absent; ascospores 17–20 × 6–7.5 μm; limited to high latitudes	L. tornoensis
7.	Soredia present; apothecia extremely rare or absent	8
–	Soredia absent; apothecia generally present	9
8.	Soralia K+ purple	L. lucifuga
–	Soralia K–, C+ pale yellow	L. sorocarpa
9.	On deciduous trees (Alnus, Salix or Sorbus); thallus whitish, smooth to wrinkled; prothallus black; apothecia yellow, orange to reddish, 0.2–0.5 mm diam.; thalline margin absent; epihymenium K+ red; emodin, fallacinal, parietin, parietinic acid, and teloschistin present	L. borealis
–	On conifers; thallus gray-brown, subsquamulose, margin uplifted and lobed; prothallus absent; apothecia brown 0.5–0.8 mm diam.; thalline margin present; epihymenium K–; no substance	L. dakotensis

Table 3. Key to the species of Lendemeriella.

1.	On rock or moss on rock	2
–	On bark	7
2.	Directly on rock	3
–	On moss	6
3.	Soredia present; apothecia immature; thalline margin gray; no substance	L. reptans
–	Soredia absent; apothecia developed; proper margin present only; emodin, fallacinal, parietin, parietinic acid present or other substance present	4
4.	Apothecia yellow-orange to light orange, less than 0.5 mm diam.; hypothecium entirely colorless; tips of paraphyses little swollen; ascospores 11–18 × 5–9.5 μm; Cinereorufa-green pigment absent; teloschistin absent	L. luteoaurantia
–	Apothecia brown-yellow, red-brown to black, 0.5–0.6 mm diam.; hypothecium yellowish to brownish; tips of paraphyses swollen; ascospores 12–17 × 6–7.5 μm; Cinereorufa-green pigment present in true exciple; teloschistin present	5
5.	Apothecia brownish or entirely black; 7-chloroemodin and fragilin present; arctic-alpine	L. exsecuta
–	Apothecia reddish; 7-chloroemodin and fragilin absent; boreal-montane	L. aureopruinosa
6.	On Racomitrium; thalline margin pale to dark gray; ascospores 25–30 × 3–5 μm; distributed in mid to high latitudes	L. nivalis
–	On Andreaea or Grimmia; thalline margin absent; ascospores 17–20 × 6–7.5 μm; limited to high latitudes	L. tornoensis
7.	Soredia present; apothecia extremely rare or absent	8
–	Soredia absent; apothecia generally present	9
8.	Soralia K+ purple	L. lucifuga
–	Soralia K–, C+ pale yellow	L. sorocarpa
9.	On deciduous trees (Alnus, Salix or Sorbus); thallus whitish, smooth to wrinkled; prothallus black; apothecia yellow, orange to reddish, 0.2–0.5 mm diam.; thalline margin absent; epihymenium K+ red; emodin, fallacinal, parietin, parietinic acid, and teloschistin present	L. borealis
–	On conifers; thallus gray-brown, subsquamulose, margin uplifted and lobed; prothallus absent; apothecia brown 0.5–0.8 mm diam.; thalline margin present; epihymenium K–; no substance	L. dakotensis